Comparative Parasitology 67(1) 2000 - Peru State College

January 2000 Number 1 

Comparative Parasitology 

Formerly the 

Journal of the Helminthological Society of Washington 

A semiannual journal of research devoted to 

Helminthology and all branches of Parasitology 

•> 

, 

BROOKS, D. R., AND"£. P. HOBERG. Triage for the Biosphere: Hie Need and Rationale 

for Taxonomic Inventories and Phylogenetic Studies of Parasites/ 

MARCOGLIESE, D. J., J. RODRIGUE, M. OUELLET, AND L. CHAMPOUX. Natural 

Occurrence of Diplostomum sp. (Digenea: Diplostomatidae) in Adult Mudpiippiesand 

Bullfrog Tadpoles from the St. Lawrence River, Quebec __ 

COADY, N. R., AND B. B. NICKOL. Assessment of Parenteral P/agior/iyncûs cylindraceus 

(Acatithocephala) Infections in Shrews „ . . ___. 

AMIN, O. M., R. A. HECKMANN, V H. NGUYEN, V L. PHAM, AND N. D. PHAM. Revision of 

the Genus Pallisedtis (Acanthocephala: Quadrigyridae) with the Erection of Three 

New Subgenera, the Description of Pallisentis (Brevitritospinus) ^vietnamensis 

subgen. et sp. n., a Key to Species of Pallisentis, and the Description of ,a'New 

QuadrigyridGenus,Pararaosentis gen. n. . , ..... '. _. ... ,- 

SMALES, L. R.^ Two New Species of Popovastrongylns Mawson, 1977 (Nematoda: 

Gloacinidae) from Macropodid Marsupials in Australia ."_ ^.1 . . 

BURSEY, C.,R., AND S. R. GOLDBERG. Angiostoma onychodactyla sp. n. (Nematoda: 

Angiostomatidae) and'Other Intestinal Hehninths of the Japanese Clawed Salamander,^ 

Onychodactylns japonicus (Caudata: Hynobiidae), from Japan „„ „..„. 

DURETTE-DESSET, M-CL., AND A. SANTOS HI. Carolinensis tuffi sp. n. (Nematoda: TrichostrongyUna: 

Heligmosomoidea) from the White-Ankled Mouse, Peromyscuspectaralis 

Osgood (Rodentia:1 Cricetidae) from Texas, U.S.A. . 

AMIN, O. M., W. S. EIDELMAN, W. DOMKE, J. BAILEY, AND G. PFEIFER. An Unusual 

^ Case of Anisakiasis in California, U.S.A. 1 

KRITSKY, D. C., E. F. MENDOZA-FRANCO, AND T. SCHOLZ. Neotropical Mpnogenoidea. 

36. Dactylogyrids from the Gills of Rhamdia guatemalensis (Siluriformes: 

Pimelodidae) from Cenotes of the Yucatan Peninsula, Mexico, with Proposal of 

Ameloblastella gen. n. and Aphanoblastella gen. ,n. (Dactylogyridae: 

Ancyrocephalinae) , : __. • • •"' . . • ' - . ; • . ' ,-.' 

MENDOZA-FRANCO, p., V. VIDAL-MARTINEZ, L.'AGUIRRE-MACEDO, R. RODR!GUEZ- 

CANUL, AND T. SCHOLZ. Species of Sciadicleithrum (Dactylogyridae: 

.Ancyrocephalinae) of Cichlid Fishes from Southeastern Mexico and Guatemala: 

New Morphological Data and Host and Geographical Records _^ ;: . ;/. • -~ ___^ 

(Continued on Outside Back Cover) 

Copyright © 2011, The Helminthological Society of Washington 

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THE SOCIETY meets approximately five times per year for the presentation and discussion of papers 

in any and all branches of parasitology or related sciences. All interested persons are invited to attend. 

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OFFICERS OF THE SOCIETY FOR 2000 

President: - DENNIS J. RICHARDSON 

Vice President-. LYNN K. CARTA 

Corresponding Secretary-Treasurer'. NANCY D. PACHECO 

Recording Secretary: W. PATRICK CARNEY 

Archivist/Librarian: PATRICIA A. PILOT 

Custodian of Back Issues: J.RALPH LICHTENFELS 

Representative to the American Society of Parasitologists: ERIC P. HOBERG 

Executive Committee Members-at-Large: RALPH P. ECKERLIN, 2000 

WILLIAM E. MOSER, 2000 

ALLEN L. RICHARDS, 2001 

BENJAMIN M." ROSENTHAL; 2001 

Immediate Past President: ERIC P, HOBERG , - _ 

COMPARATIVE PARASITOLOGY is published semiannually at Lawrence, Kansas by the 

Helminthological Society of Washington. Papers need not be; presented at a meeting to be published in 

the journal. Publication of COMPARATIVE PARASITOLOCjY is supported in part by the Brayton H. 

Ransom Memorial Trust Eund. . . 

:MANUSCRIPTS should be sent to the EDITORS,; Drs. Willis

Comp. Parasitol. 

67(1). 2000 pp. 1-25 

Triage for the Biosphere: The Need and Rationale for Taxoiiomic 

Inventories and Phylogeiietic Studies of Parasites 

DANIEL R. BROOKS' AND ERIC P. HoBERG2 ^ 

1 Department of Zoology, University of Toronto, Toronto, Ontario M5S 3G5, Canada 

(e-mail: dbrooks@zoo.utoronto.ca) and 

2 Biosystematics and National Parasite Collection Unit, U.S. Department of Agriculture, Agricultural Research 

Service, BARC East No. 1 180, 10300 Baltimore Avenue, Beltsville, Maryland 20715, U.S.A. 

(e-mail: ehoberg@lpsi.barc.usda.gov). 

ABSTRACT: A parasitological perspective in biodiversity survey and inventory provides powerful insights into 

the history, structure, and maintenance of the biosphere. Parasitology contributes a powerful conceptual paradigm 

or landscape that links ecology, systematics, evolution, biogeography, behavior, and an array of biological 

phenomena from the molecular to the organismal level across the continuum of microparasites to macroparasites 

and their vertebrate and invertebrate hosts. Effective survey and inventory can be strategically focused or can 

take a synoptic approach, such as that represented by the All Taxa Biodiversity Inventory. We argue that 

parasitology should be an integral component of any programs for biodiversity assessment on local, regional, or 

global scales. Taxonomists, who constitute the global taxasphere, hold the key to the development of effective 

surveys and inventories and eventual linkage to significant environmental and socioeconomic issues. The taxasphere 

is like a triage team. The "battlefield" is the biosphere, and the "war" is human activities that degrade 

the biosphere. Sadly, at the point in time that we reali/,e we have documented only a tiny portion of the world's 

diversity, and want to document more, we find that one of the most rare and declining groups of biologists is 

the taxasphere. This taxonomic impediment, or critical lack of global taxonomic expertise recognized by Systematics 

Agenda 2000 and DIVERSITAS, prevents initiation and completion of biodiversity research programs 

at a critical juncture, where substantial components of global diversity are threatened. The Convention for 

Biological Diversity mandates that we document the biosphere more fully, and as a consequence, it is necessary 

to revitalize the taxasphere. One foundation for development of laxonomic expertise and knowledge is the Global 

Taxonomy Initiative and its 3 structural components: (1) systematic inventory, (2) predictive classifications, and 

(3) systematic knowledge bases. We argue that inclusion of parasites is critical to the success of the Global 

Taxonomy Initiative. Predictive databases that integrate ecological and phylogenetic knowledge from the study 

of parasites are synergistic, adding substantially greater ecological, historical, and biogeographic context for the 

study of the biosphere than that derived from data on free-living organisms alone. 

KEY WORDS: biodiversity, biosphere. Global Taxonomy Initiative, inventory, parasites, phylogeny, survey, 

taxonomy. 

A Biodiversity Perspective knowledge. They can (1) focus on local, region- 

Biodiversity represents a continuum across a al> or §lobal scales^ (2> emphasize a specific taxvariety 

of scales, encompassing numerical, eco- on (e-g- host or parasite) or ecosystem; (3) be 

logical, and phylogenetic components within a oriented in strategic or problem-based perspectemporal-spatial 

framework or fabric (Ricklefs, tives; or (4) be broadly synoptic, such as the 

1987; Barrowclough, 1992; Eldredge, 1992; approaches linked to the concept of the All Taxa 

Hoberg, 1997a). Any definition of biodiversity, Biodiversity Inventory (ATBI) (Janzen, 1993). 

then, must parallel this continuum across scales Further continua are circumscribed within the 

driven by habitats, ecosystems, and communi- sphere of strictly curiosity-based acquisition of 

ties, genetic diversity in populations and species, knowledge, with eventual affiliation to economic 

genealogy and taxonomy, and history and ge- and societal concerns. The scope of the problem 

ography. Different definitions are associated may help determine the appropriate approach, 

with an array of research programs for survey but there is little question that the state of the 

and inventory that seek different kinds of biosphere should be a profound concern for science 

and society (Ehrlich and Wilson, 1991; 

1 Corresponding author. Senior authorship designat- Wilson, 1992; Smith et al., 1993; Savage, 1995). 

ed arbitrarily. We explore this intricate web to examine the 

Copyright © 2011, The Helminthological Society of Washington

2 COMPARATIVE PARASITOLOGY, 67(1), JANUARY 2000 

critical contributions that emanate from an integrative 

and comparative approach that emphasizes 

a parasitological perspective. Parasitology 

is arguably the most integrative of all biological 

disciplines. Parasitology provides a powerful 

conceptual paradigm or landscape that links 

ecology, systematics, evolution, biogeography, 

behavior, and an array of biological phenomena 

from the molecular to the organismal level 

across the continuum of microparasites to macroparasites 

and their vertebrate and invertebrate 

hosts. Information from the study of parasites is 

synergistic, adding substantially greater ecological, 

historical, and biogeographic context for 

the study of the biosphere than information derived 

from free-living organisms alone. 

Valuing Biodiversity 

Humans work hard to preserve what they value 

and replace or ignore what they do not. This 

is true of furniture and gardens and should be 

true of biodiversity. This leads to a deceptively 

simple conclusion: the more species we value, 

the more species we will preserve. But value is 

a difficult concept to apply to biodiversity. 

Equating value with market price does not necessarily 

lead to sustainable use of resources, although 

this equation is a necessary component 

of socioeconomic development, especially in the 

biodiverse regions of the world. Attempting to 

define an intrinsic value for biodiversity underscores 

the fact that different groups of humans 

have different sets of values about biodiversity 

and have different degrees of biophilia (Wilson, 

1984, 1988, 1992; Takacs, 1996; Brooks, 1998). 

Biodiversity is valued in many different ways, 

not all of them mutually reinforcing (Ehrlich and 

Wilson, 1991; Pimentel et al., 1997). Concomitant 

with recognition of value is the necessity to 

develop a basic or baseline understanding of the 

components of biodiversity within the framework 

of a maximally informative system that focuses 

attention on the following: (1) societal, 

aesthetic, and intrinsic values (i.e., biophilia); 

(2) economic benefits and beneficial components 

(both historical and future); (3) ecosystem services 

and the value of information; and (4) patterns, 

processes, and distribution of pathogens 

and disease (Ehrlich and Wilson, 1991). 

An appeal to the intrinsic value of biodiversity, 

for example, does not necessarily put food 

in people's stomachs or decrease infant mortality 

rates, the issues of most immediate importance 


for many people. Some species have value because 

they produce direct economic benefit, providing 

marketable products such as ecotourism 

and the raw materials for research and breeding 

stock (sourcing drugs and biocontrol agents 

from wildlands is familiar in many sectors, but 

the idea of paying wildlands, or the governments 

that administer them, for this service is a novel 

concept). Other species have value because they 

maintain ecosystem services, such as biodegradation 

of agricultural wastes and sequestration 

of carbon. Still other species have value because 

they provide the recreation—intellectual and 

physical—that contributes to a happy and adjusted 

populace. No one looks forward to living 

in a country congested with forest fire smoke or 

with oil-coated beaches, but in the absence of 

ecological alternatives that are also economical, 

people will choose to feed their families even if 

it means having to deal with massive local degradation 

of the biosphere. Using the resources 

provided by biodiversity or the application of a 

refined knowledge of the biosphere could provide 

these ecological and economically sound 

alternatives. Finally, many species have value 

because they are essential for the well-being and 

persistence of other species that have greater direct 

value. 

Although economic and societal issues highlight 

the necessity to fully define the scope and 

depth of biodiversity within urban, agricultural, 

and natural ecosystems, elucidation of faunal 

structure and processes is also a prerequisite for 

understanding significant interactions at the interfaces 

of such systems, including the distribution 

of pathogens and emergence of disease 

(e.g., Davis, 1995, 1996; Epstein, 1997, 1999; 

Hoberg, 1997b; Brooks et al., 2000; Brooks, 

Leon-Regagnon, and Perez-Ponce de Leon, 

2000; Hoberg, Gardner, and Campbell, 1999; 

Hoberg et al., 1999). Pathogens and parasites 

have direct implications for human health, agriculture, 

natural systems, conservation practices, 

and the global economy through continued 

introductions and dissemination and our often 

limited knowledge of mechanisms that control 

distribution and emergence (Hoberg, 1997b). 

Humans are concentrated in the world's most 

biodiverse regions, where they often live in conditions 

of poverty, poor education, and poor 

health. These people currently preserve only 

those species and ecosystems that enhance the 

immediate quality of their lives or those of their

children. This means, to most of them, domestic 

species and the habitats they occupy rather than 

wildlands. We are led to a deceptively straightforward 

proposition: link economic development 

to the preservation of wildlands and the 

species they contain, encouraging people to understand 

that the plant and animal species in the 

wildlands are as valuable as the more familiar 

domestic species. In this way, some wildlands 

may survive, not as the agroscape, but as another 

kind of cropland interdigitated with the agroscape. 

This proposition implies developing the 

economic and social potential of species living 

in wildlands, thus reducing demand for economic 

development of wildlands, into still more impoverished 

agroscape, which partly sustains yet 

more often starves people. Such a proposition 

assumes that at least some societies will conserve 

biodiversity on some portion of their landscape, 

if the wildlands generate intellectual and 

economic benefits that pay for their maintenance 

and contribute to national economic growth and 

sustainability. The preservation of biodiversity is 

thus driven, at present, more by social and economic 

development than technical expertise 

(Janzen, 1992; Brooks, 1998). 

People interested in economic and social development 

of conserved wildlands can benefit 

from forming partnerships with the scientific 

community. Such partnerships are required to 

meld what scientists have long known and are 

still discovering through basic research with the 

pragmatic efforts of developing the wildlands as 

a third kind of major land use, alongside the 

urban and agricultural landscape. Being able to 

determine the multiple uses of species and their 

combinations requires technical and scientific 

expertise and social will (Parma, 1998). 

If preservation is to be true and long-lasting, 

biodiversity conservation can occur only 

through nondestructive use of that biodiversity 

by a wide array of social sectors. Effective conservation 

efforts will simultaneously encompass 

biodiversity development and conservation projects 

(Soule, 1991). This occurs by designating 

areas for wildland status, finding out what is in 

them, and putting that biodiversity to work. In 

this regard, a critical element of the scientific 

community is the taxasphere (Janzen, 1993), the 

global population of taxonomists and systematists. 

These issues highlight the critical importance 

and rationale for biodiversity survey and inven- 

BROOKS AND HOBERG—PARASITE BIODIVERSITY 

tory. Although inventory work is fundamentally 

important, we must remember that it is only a 

means to an end. Names attached to species revealed 

through intensive field and laboratory investigations 

must represent a significant amount 

of natural history, especially ecological, information 

for the stakeholders in national socioeconomic 

development to be able to assess the value 

of each species. The taxasphere may be likened 

to a triage team. The "battlefield" is the 

biosphere, and the "war" is human activities 

that tend to degrade the biosphere. In this war, 

every species is affected to a greater or lesser 

extent. Some are attacked directly through overexploitation 

and others indirectly through neglect. 

The triage teams survey parts of the battlefield 

as completely as possible, looking for 

"wounded" participants. They must be able to 

recognize all possible participants and the degree 

to which each has been affected (e.g., critical 

habitat requirements that are gone or going). 

The teams must then pass that information on to 

the decision makers, who are responsible for the 

optimal deployment of resources to save the 

maximum number of participants possible. Taxonomists 

communicate such information most 

efficiently through predictive classifications and 

electronic management of information. 

Valuing Taxonomy 

We already know much—and are learning 

more each day—about the importance of the 

documented portions of the biosphere. However, 

we have not documented, and thus do not understand, 

more than a fraction of that diversity, 

with only 1.7 million of an estimated 13 million 

to 14 million existing species currently described 

(Hawksworth, 1995). Consequently, we 

often have no idea what we might be losing and 

have only incomplete information on how to 

preserve what remains. Faced with our ignorance 

and gaps in knowledge, biologists react in 

a way that seems paradoxical. They often advocate 

extreme caution in development projects, 

simply because our ignorance may lead us to 

make mistakes and lose habitat and diversity 

both in the short- and long-term. At the same 

time, biologists understand that caution cannot 

impose stasis or inaction. We cannot be satisfied 

with slowing the rate at which species are lost 

or habitat is destroyed, because extinction is an 

irreversible process. We can never bring a species 

back once it is lost, and its potential to play 



a role in the survival of our species is gone forever. 

Moreover, each species that becomes extinct 

may represent an irreversible loss of socioeconomic 

potential and may restrict our survival 

options for the future. Each species lost represents 

an irreversible loss of evolutionary potential, 

the very potential that has been the source 

of biotic recovery from past global ecological 

perturbations and environmental disasters (Jablonski, 

1991). Many biologists, therefore, advocate 

immediate action to document the 

world's biodiversity. Sadly, at the point in time 

that we have realized that we have documented 

only a tiny portion of the world's diversity and 

want to document more, we find that one of the 

rarest and fastest declining groups of biologists 

is the taxasphere. 

The fundamental units of biodiversity are genealogical 

information systems called species, 

which store and transmit information that leads 

to the emergence of ecosystems with their complex 

interactions. Who is trained to find and distinguish 

among those units? Taxonomists. 

Where do we find that information? In the descriptions, 

surveys, and revisions of taxonomists. 

The predictable parts of biological systems 

are the stable biological elements, both 

form and function, autecological and synecological, 

that have persisted through evolutionary 

time (Brooks, 1985a; Brooks and McLennan, 

1991, 1993a; Brooks et al., 1995). This predictive 

power of taxonomy is embodied in the phylogenetic 

classifications of taxonomists (Simpson 

and Cracraft, 1995). The taxasphere includes 

some of the best-trained bioprospectors in the 

world, who are often highly skilled at finding 

particular species. Taxonomists are also versatile 

and opportunistic in the field because of their 

ability to recognize novelty. Their ability to determine 

evolutionary relationships and add value 

by making predictions based on those relationships 

can minimize the time and cost in research 

and development and planning and prioritization 

(Brooks et al., 1992). 

Parasites in Biodiversity and Conservation 

Biology 

In the realm of conservation biology, parasites 

have dual and conflicting significances. Pathogenic 

parasites can represent threats to the success 

of programs for management and recovery 

of threatened or endangered species (Dobson 

and May, 1986b; Scott, 1988; Lyles and Dobson, 


1993; Holmes, 1996). Alternatively, parasites 

can control host populations, and they can play 

a central role in maintenance of genetic diversity 

and structuring of vertebrate and invertebrate 

communities (Windsor, 1995, 1996); in this latter 

role, parasites are significant and vital components 

of the biosphere. Additionally, it has 

been suggested that under special conditions 

(such as on islands) introduction of parasites and 

pathogens may be a viable method of controlling 

introduced mammals (Dobson, 1988). 

The significance of biodiversity surveys and 

inventories in a phylogenetic—ecological context 

is apparent in documenting the abundance and 

species composition of faunas in protected host 

species and habitats. For example, in endangered 

Attwater's prairie chickens (Tympanchus cupido 

attwateri), the potential for interspecific interactions 

and sharing of pathogenic parasites with 

related species of grouse provided the rationale 

for comparative baseline studies of parasite diversity 

(Peterson, 1996). Definition of the parasite 

fauna, including recognition of new cryptic 

species, in Holarctic ruminants was necessary to 

identify the potential for impacts from circulation 

of endemic and exotic parasites among cervids 

and bovids in North America (Hoberg, Kocan, 

and Rickard, 2000). For wild ungulates, 

translocation and either introduction of parasites 

or exposure to novel pathogens remain major 

considerations in management decisions (Lankester 

and Fong, 1989; Samuel et al., 1992; 

Woodford and Rossiter, 1994; Hoberg, 1997b). 

Parasites must be regarded as integral components 

of biodiversity; thus, there should be 

concerns about the ramifications of extinction 

both locally and globally (Wilson, 1984; Rosza, 

1992; Windsor, 1995; Durden and Keirans, 

1996). Coming full circle, the importance of accurate 

documentation for biodiversity and the 

world's parasite faunas is based on the intrinsic 

and extrinsic importance of parasites in healthy 

ecosystems, as agents of human disease, and at 

the nexi of natural and domestic, terrestrial, 

aquatic, and marine environments. 

Parasites as Contemporary Ecological Indicators. 

At a higher level than the communities 

of parasites themselves, we recall that parasites 

track broadly and predictably through ecosystems. 

Parasites inform us of a myriad of interesting 

things about host ecology, behavior, 

and trophic interactions (Hoberg, 1996; Marcog-

liese, 1995; Marcogliese and Cone, 1997). Complex 

life cycles are integrated within intricate 

food webs, so parasites can be valuable indicators 

of trophic ecology, structure of food webs, 

food preferences, and foraging mode of hosts 

(Bartoli, 1989; Williams et al., 1992; Hoberg, 

1996; Marcogliese and Cone, 1997). Within this 

ecological-trophic context, parasites can tell us 

the following: (1) trophic positions in food webs 

(what hosts eat and what eats them); (2) use of 

and time spent in different microhabitats (e.g., 

even though Termpene Carolina is mainly a terrestrial 

turtle, it hosts the digenean Telorchis robustus, 

which uses tadpoles as second intermediate 

hosts); (3) whether hosts are picking up 

parasites via host switching, and if so, which 

hosts might be in potential competition (e.g., 

guild associations were recognized in the Sea of 

Okhotsk based on examining parasites (Belogurov, 

1966)); (4) whether any host harbors parasites 

that are likely to cause disease problems; 

(5) whether the host changes diet during its lifetime, 

including seasonally or regionally denned 

changes in food habits or prey availability 

(Bush, 1990; Hoberg, 1996); and (6) which 

hosts are residents and which are colonizers in 

the community. Because such a wide range of 

information can be gleaned from relatively little 

effort, parasites should be highly useful in all 

biodiversity studies. Additional special cases for 

the application of parasitological data are related 

to their use as contemporary biogcographic indicators. 

Analysis of parasite biogeography has 

been a powerful approach for identification of 

stocks or populations in fisheries management 

(Williams et al., 1992) and among marine mammals 

(Dailey and Vogelbein, 1991; Balbuena and 

Raga, 1994; Balbuena et al., 1995). 

We can maximize the use of this information 

if we begin to think of parasites as biodiversity 

probes par excellence and as libraries of natural 

and geological history (Brooks et al., 1992; 

Gardner and Campbell, 1992; Hoberg, 1996). 

Parasites are admirably suited to augment the 

development of conservation strategies through 

the recognition of regions of critical diversity 

and evolutionary significance (Gardner and 

Campbell, 1992; Hoberg, 1997a). 

The predictive power of parasitology in a 

phylogenetic context becomes increasingly important 

when attempts are made to elucidate impacts 

from natural and anthropogenic perturbations 

of faunas and ecosystems. In marine sys- 

BROOKS AND HOBHRG—PARASITE BIODIVERSITY 

tems, climatological forcing, such as that linked to 

the El Nino-Southern Oscillation or to cyclical 

changes in atmospheric circulation, dramatically 

influences patterns of oceanic upwelling and water 

masses, which are reflected in food web 

structure and ultimately in parasite faunas. In 

such situations, parasites should be well suited 

to tracking variation in trophic dynamics and 

host distributions on the global scale (Hoberg, 

1996). Knowledge of the evolution of a hostparasite 

assemblage can provide direct estimates 

of the history of ecological associations and can 

indicate the continuity of trophic assemblages 

through time. 

Parasites as Historical Indicators. Manter 

(1966) made the most eloquent statement about 

the significance of parasites for understanding 

evolutionary and ecological phenomena: 

Parasites . . . furnish information about present-day 

habits and ecology of their individual hosts. These 

same parasites also hold promise of telling us something 

about host and geographical connections of 

long ago. They are simultaneously the products of 

an immediate environment and of a long ancestry 

reflecting associations of millions of years. The 

messages they carry are thus always bilingual and 

usually garbled. As our knowledge grows, studies 

based on adequate collections, correctly classified 

and correlated with knowledge of the hosts and life 

cycles involved should lead to a deciphering of the 

message now so obscure. Eventually there may be 

enough pieces to form a meaningful language which 

could be called parascript—the language of parasites 

which tells of themselves and their hosts both 

of today and yesteryear. (Manter, 1966) 

Phylogenetic systematics provided the Rosetta 

stone for what are now called parascript studies 

(Brooks and McLennan, 1993a). In the past 2 

decades, since formalization of the parascript 

concept (Brooks, 1977), the number of such 

studies has increased dramatically (see reviews 

in Brooks and McLennan, 1993a; Hoberg, 

1997a). Today there is virtually no area of modern 

comparative evolutionary biology and historical 

ecology that has not been enriched by at 

least one parascript study. 

The concept of parascript was based on the 

contention by Manter (1966) that parasites are 

powerful biological indicators of recent and ancient 

ecological associations and geographic distributions. 

Parasites tell stories about themselves 

and their hosts that involve evolutionary emergence 

of complex ecological associations 

throughout immense periods. These ideas dra- 



matically influenced the development of a research 

program for comparative evolutionary biology 

of parasites (Brooks and McLennan, 

1993a). Extending from the seminal study by 

Brooks (1977), this program has led to elaboration 

of methods for analyzing cospeciation, 

extinction, dispersal, and host switching in the 

evolution of parasite biotas (Brooks, 1979, 1981, 

1990; Hoberg, Brooks, and Siegel-Causey, 

1997), with the emergence of historical ecology 

(Brooks, 1985a; Brooks and McLennan, 1991) 

as the foundation for parascript investigations 

(Brooks and McLennan, 1993a, 1993b, 1993c). 

Because their geographic distributions are limited 

to those areas in which all obligate hosts are 

sympatric and synchronic, parasites are excellent 

systems for historical biogeographic studies. 

Thus, parasites, particularly those with complex 

life cycles, provide the linkage for examining 

the interaction of coevolution, colonization, and 

extinction on faunal structures and ecological 

continuity across deep temporal and broad geographic 

scales (Hoberg, 1997a; Hoberg, Gardner, 

and Campbell, 1999; Hoberg, Jones, and 

Bray, 1999). 

The significance of historical reconstruction 

for current approaches in the assessment of biodiversity 

resides in the concept of the past as the 

key to the present (Hoberg, 1997a). Historical 

reconstruction allows identification of important 

centers for diversification (ancestral areas) and 

promotes a predictive framework to assess the 

importance of specific habitats, geographic regions, 

and biotas and recognition of areas of 

critical genealogical and ecological diversity. 

These are the realms of historical ecology 

(Brooks, 1985a; Brooks and McLennan, 1991) 

and historical biogeography. Although we have 

much to learn about the biosphere, historical 

studies of helminth parasite systems in piscine, 

amphibian, mammalian, and avian hosts have 

contributed context for understanding faunal 

structure across terrestrial (Platt, 1984; Gardner 

and Campbell, 1992; Hoberg and Lichtenfels, 

1994), aquatic (Brooks et al., 1981; Klassen and 

Beverley-Burton, 1987, 1988; Kritsky et al., 

1993), and marine environments (Klassen, 1992; 

Hoberg, 1995; Hoberg et al., 1998) (further reviewed 

in Brooks and McLennan, 1993a; Hoberg, 

1997a). A historical ecological context, in 

conjunction with developing understanding of 

contemporary systems, is the basis for using par- 


asites to illuminate local, regional, and global 

ecological perturbations. 

Parasites as Mine Canaries Through Ecological 

and Evolutionary Time. Parasites 

track broadly and predictably through ecosystems, 

highlighting major trophic interactions 

among hosts that occupy multiple niches. As 

such, parasites may be sensitive indicators of 

subtle changes within ecosystems. This is especially 

true for parasites with heteroxenous life 

cycles. Severe reduction or disappearance of a 

population of only 1 of several obligate hosts 

will cause the parasite to disappear. Environmental 

pollution of benthic invertebrate faunas 

has resulted in elimination of many digeneans in 

fishes in some localities (Caballero y Rodriguez 

et al., 1992; Overstreet, 1997; Overstreet et al., 

1996). Conversely, increased and detrimental 

levels of parasitism in molluscan intermediate 

hosts may result from changes in behavioral patterns 

and population density of seabirds, such as 

larids, that concentrate near areas of human activity 

in coastal zones (Bustnes and Galaktionov, 

1999). 

At the extreme, parasite extinction may precede 

host extinction, i.e., the sudden loss of a 

particular species of parasite in a given vertebrate 

host may result from degradation of faunal 

structure or from changes in host population 

density (Dogiel, 1961; Hoberg and McGee, 

1982; Bush and Kennedy, 1994). As some hosts 

go extinct, some parasites will go extinct as 

well. Alternatively, some surviving parasites 

may be brought into contact with novel hosts as 

a result of ecological release. This new contact 

may produce disease, which is maladaptive for 

host and parasite, but given the alternative of 

extinction, from the parasite's standpoint it may 

represent a viable "strategy" to avoid extinction. 

From the host's standpoint, the cost of exposure 

to novel pathogens may be offset by the 

benefit of surviving a major environmental disaster. 

In the longer-term, revolutionary dynamics 

might ameliorate, if not eliminate, the 

negative impacts of these once novel host-parasite 

associations, although we understand that 

reduction in virulence may not be correlated 

with length of association of pathogen and host 

(Ewald, 1995). 

Thus, parasites can serve as indicators of ecosystem 

integrity and can be used to measure 

contemporary environmental perturbations. Nat-

ural and human alterations of ecosystems may 

be reflected in increases or decreases in abundance 

of a certain spectrum of the parasite fauna 

(Marcogliese, 1995). A particularly elegant 

study showing this was a documentation of the 

impact of acidification in riparian habitats on 

parasites of eels (Anguilla rostrata) in Nova 

Scotia (Cone et al., 1993; Marcogliese and 

Cone, 1996). 

Aside from the effects of pollution, we predict 

substantial impacts on host-parasite systems and 

on changes in the distribution and emergence of 

pathogens and parasites from global climate 

change and global warming (Dobson and Carper, 

1992; Epstein, 1997, 1999). Contemporary 

changes in distribution caused by global climate 

change have already been documented for anisakine 

nematodes in seals and fishes (Marcogliese 

et al., 1996). Disease outbreaks of elaphostrongyline 

nematodes in reindeer have been 

correlated with variation in summer temperatures 

(Handeland and Slettbakk, 1994). Historical 

studies of parasites can illuminate the influence 

of past climate variation on the distribution 

and diversification of parasites and their hosts 

(Hoberg, 1986, 1992, 1995). 

Continued surveys and inventories of parasites 

become important components in documenting 

the impact of environmental change. As 

indicated by Marcogliese and Price (1997), 

"Parasitism is simply a reflection of the natural 

state of ecosystems, and healthy populations of 

organisms will play host to healthy populations 

of parasites." 

Parasites and Assessing the Risk of Emerging 

Diseases. Parasites may act as agents of 

population control by causing acute or chronic 

disease in hosts (Scott, 1988; Gulland, 1995). 

Comprehensive inventories permit us to assess 

risk, to make predictions (for wildlife and game, 

agriculture and livestock, or public health), and 

to recognize endemic and introduced faunal elements 

(Hoberg, 1997b; Hoberg et al., 1999; 

Hoberg, Kocan, and Rickard, 2000). We are interested 

in interfaces between natural, agricultural, 

and urban ecosystems and the barriers that 

inhibit or the paths that promote introduction 

and dissemination of pathogens and parasites. 

Inventories within a historical-phylogenetic 

context focus the range of questions to be examined. 

We can consider whether the same or 

related parasites occur only in related hosts or 


whether they occur in distantly related hosts 

with similar ecological habits. This is an ecological 

and evolutionary question with implications 

for emerging diseases. On the ecological side, 

we will find out which parasites are limited by 

host or geographic associations and which parasites 

are likely to disperse or colonize. On the 

evolutionary side, we can ask which groups 

have persisted through major environmental 

changes, either because their hosts survived or 

because the parasites successfully switched to 

alternative hosts. We might predict increasing 

host switching as hosts or host groups go extinct, 

i.e., the extinction of certain hosts might 

accelerate the emergence of pathogens and diseases 

rather than simply eliminating disease organisms. 

Mechanisms for emergence have been well 

documented and generally are linked in some 

way to the breakdown of isolating barriers 

(Rausch, 1972; Dobson and May, 1986a, 1986b; 

Hoberg, 1997b). Factors that contribute to disease 

emergence include the following: (1) translocation, 

introduction, and dissemination of 

pathogens; (2) faunal disruption and ecological 

release (new hosts or new ecological situations); 

(3) increasing host population density (stress and 

reduced abilities for adaptation); and (4) amplification 

of parasite populations linked to environmental 

change, such as global warming. 

When dealing with complex systems, however, 

cause and effect are often difficult to distinguish. 

Limb deformities and mortality in anurans have 

been linked to infections by a species of Ribeiroia, 

a psilostomid digenean, which may be indicative 

of environmental pollution and its effect 

on populations of the snail intermediate hosts 

(Johnson et al., 1999). The ongoing reduction in 

anuran populations may further indicate the pervasive 

nature of emergence and the continued 

translocation and introduction of wildlife parasites 

on a global scale (Morell, 1999). 

Introduction of parasites and pathogens with 

either wild or domesticated hosts is a major 

source of disease emergence. Establishment of 

introduced parasites has been documented for 

the following: (1) nematode faunas in ruminants 

across the Holarctic (Hoberg and Lichtenfels, 

1994; Hoberg et al., 1999; Hoberg, Kocan, and 

Rickard, 2000); (2) parasites in freshwater and 

marine fishes (Kennedy, 1993; Scholz and Cappellaro, 

1993; Barse and Secor, 1999); and (3) 

helminths in some avian hosts such as ratites 



(Hoberg, Lloyd, and Omar, 1995). Many local 

parasite faunas are now mosaics of endemic and 

introduced species. A principal role for taxonomic 

inventories in such situations is to provide 

baseline information on the patterns of distribution 

for hosts, parasites, and pathogens as 

the foundation for prediction and prevention. 

Knowledge of the diversity and distribution of 

pathogens and parasites is important in limiting 

economic, societal, and biotic impacts and liability 

in management of endemic or exotic organisms 

(Hoberg, 1997b). 

International Initiatives in Systematics and 

Biodiversity: Getting Parasitology Involved 

The Convention on Biological Diversity 

(CBD) (Glowka et al., 1994) designated ecosystems 

management and sustainable development 

as the fundamental organizing principles for 

managing global biodiversity. Biologists and 

managers quickly realized that the current inventory 

of the world's species was far too limited 

to implement the mandate properly and that 

a critical shortage of trained taxonomists contributed 

directly to the problem. The United Nations 

Environment Program in biodiversity, 

called DIVERSITAS, coined the term the taxonornic 

impediment to refer to this critical lack of 

global taxonomic expertise, which prevents initiation 

and completion of biodiversity research 

programs (SA2000, 1994; Hoagland, 1996; 

Blackmore, 1996; PCAST, 1998). In North 

America, this concern led to Systematics Agenda 

2000 (SA2000), an intensive professional inventory 

of the value of taxonomic expertise to 

this planet, and a set of recommendations for 

revitalizing the taxasphere and justifying the allocation 

of resources necessary to carry out such 

a revitalization (SA2000, 1994). In 1998, the 

Conference of the Parties to the CBD endorsed 

a Global Taxonomy Initiative (GTI) to improve 

taxonomic knowledge and capacity to further 

country needs and activities for the conservation, 

sustainable use, and equitable sharing of 

benefits and knowledge of biodiversity (GTI, 

1999; http : //research . amnh . org/biodiversity / 

acrobat/gti2.pdf). It appears that the solution to 

removing the taxonomic impediment in biodiversity 

planning is the revitalization of the taxasphere, 

and the rationale for revitalizing the 

taxasphere is the potential of taxonomic contributions 

for managing the biodiversity crisis. A 

foundation for development of taxonomic ex- 


pertise and knowledge is the GTI and its 3 components: 

(1) systematic inventory, (2) predictive 

classifications, and (3) systematic knowledge bases, 

including collections. 

GTI Component 1: Systematic Inventory— 

Discovering and Naming the World's Species. 

Assessments by DIVERSITAS indicate 

that there are no more than 2,000 full-time professional 

taxonomists and perhaps an additional 

5,000 people with some degree of taxonomic expertise 

on the planet. Furthermore, that population 

has a median age of 55 years. Concurrently, 

less than 10% of the terrestrial species and perhaps 

1% of the world's marine species have 

been discovered and named. These factors act 

synergistically as the foundation of the taxonomic 

impediment (SA2000, 1994). Biodiversity inventories, 

as envisioned by the CBD, are biodiversity 

development and conservation projects, 

a means for restoring global taxonomic capacity, 

and opportunities to study the health, 

reproductive, and nutritional requirements and 

the ecology and evolution of a large number of 

wild species in natural, yet protected, environments. 

What information should inventories provide? 

For each species, the following should be provided: 

(1) what is it (and how to distinguish it 

from others); (2) where does it occur; (3) what 

is its natural history; and (4) how do you get it 

when desired? 

To what purposes should this information be 

put? (1) Monitoring global environmental 

health; (2) promoting socioeconomic development 

through sustainable use and equitable sharing 

of benefits and knowledge derived from diverse 

biological resources, including forestry, 

fisheries, and some components of agriculture; 

(3) developing of new products and ecotourism; 

and (4) providing risk assessment about the impact 

of introduced species and the source and 

impact of emergent diseases. Potential user 

groups for the information gathered include ecotourism, 

agricultural, pharmaceutical, and biotechnology 

prospecting companies; educational 

and scientific institutions; human, veterinary, 

and agricultural health experts; environmental 

monitoring and restoration programs; economists; 

and development agencies. 

What general criteria do we follow in choosing 

particular inventory projects? They should 

(1) have high public visibility and approval in-

ternationally and locally; (2) be international in 

scope; (3) have high scientific value in both basic 

and applied terms; and (4) encourage group 

cohesion and cooperation, leading to the engagement 

of as many stakeholders as possible. 

The CBD has mandated that each country embark 

on some form of national biodiversity inventory. 

National socioeconomic planners will 

determine the form of such an inventory. Once 

such a decision has been made, an immediate 

concern will be coordinating efforts. Every 

country in the world is now a debtor nation with 

respect to taxonomic expertise. As mentioned 

herein, the taxasphere sees the removal of the 

taxonomic impediment as an opportunity for the 

survival of the taxasphere and the biosphere. But 

because the taxasphere today consists of a relatively 

small, generally poorly funded and globally 

dispersed population of scientists, any national 

inventory project will require a multinational 

effort. Furthermore, most members of the 

taxasphere work in academia or museums, 

which represents an additional layer of cultural 

distinction. Academic and museum naturalists 

have a long history of self-motivated and selfdirected, 

essentially solitary pursuit of knowledge. 

Specialists on the same groups of organisms 

may see each other as professional competitors 

rather than collaborators. Encouraging 

such people, representing different institutions 

and different countries, each with different personal 

career agendas, to collaborate is difficult 

but not impossible (Janzen and Hallwachs, 

1994; Hoberg, Gardner, and Campbell, 1997). A 

1993 National Science Foundation-sponsored conference 

in Philadelphia, Pennsylvania, U.S.A., 

brought leading taxonomists together to consider 

the feasibility of their cooperating to document 

those species useful to humans before they become 

extinct and to stave off the loss of a science 

of specialists who could identify them and 

learn about their natural histories. Faced with the 

immediacy of the crisis, the taxonomists present 

were able to cooperate strategically, even though 

there were and still are differences of opinion 

about tactics, primarily in the realm of inventory 

projects (Janzen and Hallwachs, 1994). Inventories 

can represent synoptic examinations of 

complex ecosystems or well-circumscribed, 

problem-driven projects. Synoptic examinations 

include the concept of the ATBI, documenting 

all species in a large conserved wildland site 

(Janzen, 1993; Janzen et al., 1993). 

BROOKS AND HOBHRG—PARASITE BIODIVERSITY 

The ATBI concept was originally conceived 

to serve 2 functions. First, the most biodiverse 

terrestrial ecosystems in the world occur in tropical 

developing countries. Great diversity, many 

unknown species, and generally untapped biodiversity 

resources characterize tropical ecosystems. 

In such situations, recognizing that biodiversity 

programs may be simultaneously biodiversity 

development and conservation projects is 

critical. They can create a mechanism to preserve 

wildlands, build scientific infrastructure, 

and promote sustainable use of environmental 

resources. Socioeconomic development stemming 

from an ATBI is achieved by giving the 

neighbors of a conservation area a stake in preserving 

the local diversity; the more species that 

can be shown to be valuable, the more such opportunities 

exist, and the more species will be 

conserved. 

Second, each site where an ATBI is carried 

out becomes a gigantic mine canary, where the 

effects of global environmental change could be 

monitored across significant numbers of species 

and large sectors of integrated ecosystems, giving 

us a true picture of the overall large-scale 

effects of such phenomena as global warming, 

biotic invasions, and habitat perturbation (Janzen, 

1996, 1997; Janzen and Hallwachs, 1994). 

The information generated by an ATBI could be 

valuable for conservationists and land use planners, 

where conserved wildland choice is critical 

in the following ways: (1) Observing that a conserved 

wildland can be useful and used, national 

policy makers will be able to consider conserving 

wildland as an appropriate form of land use, 

on a par with agricultural and urban landscapes. 

Conservationists and economic development 

programs will become partners rather than adversaries. 

(2) An ATBI will aid conservationists 

who make site choices elsewhere, because it will 

generate a complete picture of a biodiverse landscape, 

a "known universe," by which biodiversity 

and ecosystem sampling schemes can be 

calibrated. (3) The data from an ATBI may enable 

us to answer difficult conservation questions 

based on correlations between the diversity 

of 2 or more taxa in a site or habitat array. (4) 

By accomplishing a project with high social approval, 

the taxasphere and biodiversity managers 

will feel more confident in making new partnerships 

with conservationists. (5) An ATBI will be 

a campus for people representing many stakeholders 

in biodiversity, many of those involved 



directly in conservation site selection and biodiversity 

development in other places. 

Inventories conducted to facilitate the use of 

wildland biodiversity by societies simultaneously 

benefit the taxasphere and those who desperately 

need food, shelter, education, and health 

care. The ATBI approach is not the only model 

for undertaking inventories, and many members 

of the taxasphere do not believe it represents the 

best use of limited taxonomic resources. The 

major selling points of an ATBI are the immediate 

socioeconomic benefits to local residents 

of a conserved wildland and the exciting 

"moonshot" nature of such a large-scale project. 

In addition, although there is currently a lack of 

funds for any ATBI, such a project could become 

important in the future. 

Some doubt, given the state of the taxasphere, 

that it is in our best interests to concentrate a 

disproportionate amount of effort on a single 

site. They argue that the best way to revitalize 

the taxasphere globally is to initiate multiple inventory 

projects simultaneously throughout the 

world using available expertise. This emphasizes 

the concept of working locally and thinking 

globally. Furthermore, given that the goal of an 

ATBI may be national socioeconomic development, 

how can the taxasphere, especially 

through a GTI, give preference to one country's 

socioeconomic aspirations over another's? 

Wouldn't it be preferable to give individual 

countries a means of prioritizing their limited 

human and economic resources to make national 

inventories of priority taxa? 

Critics of the more disseminated inventory 

approach suggest that it tends to reinforce taxonomic 

expertise in taxa for which there are already 

many taxonomists, and risks excluding interested 

taxonomists who do not happen to study 

one of the priority groups in one of the priority 

places. Advocates of the ATBI concept argue 

that the choice of which country to prefer will 

simply be a first-come, first-served phenomenon 

and that the expertise generated from the first 

ATBI will permit the second and succeeding 

ATBIs to be done faster and more cost-effectively. 

They also argue that, in contrast to an 

ATBI, which is focused within a single country, 

targeted inventories of selected taxa over wide 

geographic ranges will involve international and 

intranational planning and cooperation, something 

that is not guaranteed to happen in all parts 

of the world at any given time. 


Clearly, there are good points made by people 

of goodwill on both sides of this issue. All agree 

that taxonomic inventories are fundamental to 

the future of biodiversity preservation and development 

(GTI, 1999), and that if we had unlimited 

funds, complete inventories of all targeted 

areas throughout the world would be ideal. 

This is what we refer to as strategic agreement. 

The realities of the situation, however, are that 

there will be only limited amounts of money 

available for national inventories and for revitalizing 

the taxasphere, even if the taxonomic 

impediment is regarded as a critical national priority 

or imperative such as that recently outlined 

for the United States (PCAST, 1998). We urge 

all parties to listen to each other, learn from each 

other, work together as much as possible, and 

take proactive stances that are environmentally, 

scientifically, and politically relevant. 

PARASITES IN BIODIVERSITY SURVEYS AND IN- 

VENTORIES: It is clear from the variety of research 

programs supported by parasitological 

studies that parasites represent significant components 

of global biodiversity. Continued survey 

and inventory of the world's parasite faunas remain 

requisite for understanding basic issues in 

evolutionary biology, ecology, and biogeography. 

Documentation of parasite biodiversity is 

significant in an "applied" sense for elucidating 

solutions to ecological problems, examining 

emergence and re-emergence of pathogens, understanding 

interactions at the interface of ecosystems, 

and recognizing the impacts of global 

change. We will examine later 2 models for pursuing 

studies of parasite diversity in tropical and 

high-latitude boreal and arctic systems. Different 

strategies for acquiring biodiversity knowledge 

are dictated by prevailing social and economic 

situations. 

Those who argue for inventories that focus on 

priority taxa suggest the following selection criteria: 

taxa should (1) be intrinsically important 

to humans, such as insect groups known to include 

important pollinators, biocontrol agents, or 

disease vectors; (2) be intrinsically important to 

ecosystems that humans want to preserve; (3) 

provide efficient means of learning something of 

importance; (4) be geographically widespread; 

and (5) provide opportunities for international 

networking of professionals, collaborative research, 

and training. In our opinion, it is easy to

justify the inclusion of parasites in any inventory 

project under all these guidelines. 

Taxa should be intrinsically important to humans: 

Parasites are agents of disease in humans, 

livestock, and wildlife, with attendant socioeconomic 

significance. Parasites are significant 

components for assessing the risk of loss of 

biocontainment by introduced species, whether 

because of parasites of introduced species moving 

into the agricultural landscape or wildlands 

and switching to native hosts or because of parasites 

of native species moving out of the agricultural 

landscape or wildlands and infecting introduced, 

economically important host species. 

A special case involves the possibility of local 

residents and tourists sharing parasites and parasitic 

diseases between themselves and between 

humans and nonhuman hosts. Some parasite 

species may provide revenue as model systems 

for pharmaceutical companies or as biocontrol 

agents. Additionally, we must understand parasite 

biodiversity within the context of global 

change (Dobson and Carper, 1992; Hoberg, 

1997b; Brooks et al., 2000; Brooks, Leon-Regagnon, 

and G. Perez-Ponce de Leon, 2000; 

Hoberg, Kocan, and Rickard, 2000). 

Taxa should be intrinsically important to ecosystems 

that humans want to preserve: Parasites 

are significant regulators of host populations 

(Scott, 1988; Gulland, 1995) and are potent 

agents that maintain ecosystems' integrity and 

stability (Minchella and Scott, 1991; Dobson 

and Hudson, 1986; Hudson et al., 1998). Complex 

feedback loops that involve parasites, herbivores, 

and habitat structure in ruminant grazing 

systems further indicate the significance of 

parasites as determinants of community structure 

(Grenfell, 1992). Parasites can also be important 

mediators of host behavior (Holmes and 

Bethel, 1972). Introduced parasites may have 

unpredictable and deleterious impacts on native 

species of hosts (Dobson and May, 1986a, 

1986b; Woodford and Rossiter, 1994; Vitousek 

et al., 1996). It is, therefore, important to be able 

to quickly distinguish native from introduced 

parasite species (Hoberg, 1997b; Brooks, Leon- 

Regagnon, and Perez-Ponce de Leon, 2000; 

Hoberg et al., 1999; Hoberg, Kocan, and Rickard, 

2000). 

Taxa should provide efficient means of learning 

something of importance: Parasites, espe- 


cially those having complex life cycles involving 

more than 1 obligate host, are indicators of 

stable trophic structure in ecosystems (Marcogliese 

and Cone, 1997). This is because all the 

biotic components necessary for completion of 

the life cycle must co-occur regularly to maintain 

any given parasite species. Knowing the 

complement of parasite species inhabiting any 

given host thus provides a means of rapid assessment 

of the breadth and form of trophic interactions 

of host species. 

Taxa should be geographically widespread: 

Many parasite taxa are widespread geographically. 

At the same time, they are highly localized 

with respect to infecting particular hosts, which 

themselves may be the focus of particular inventory 

activities. 

Taxa should provide opportunity for international 

networking of professionals, collaborative 

research, and training: Parasite systematics is 

in serious trouble worldwide. Laboratory closures 

in the United Kingdom and elsewhere 

have eroded the infrastructure for taxonomy and 

systematics at a critical time. New survey opportunities 

and recognition of the importance of 

parasites may stimulate international collaboration 

and revitalization. 

Parasites, therefore, fit a set of extrinsic criteria, 

indicating the importance of their inclusion 

as basic elements of surveys and inventories. 

Parasites are critically important as (1) ecological-trophic 

indicators (Marcogliese and Cone, 

1997; Overstreet, 1997); (2) historical indicators 

of phylogeny, ecology, and biogeography 

(Brooks, 1985a; Brooks and McLennan, 1993a, 

and references therein; Perez-Ponce de Leon, 

1997; Perez-Ponce de Leon, Leon-Regagnon, 

and Garcia-Prieto, 1997; Brooks et al., 2000; 

Brooks, Leon-Regagnon, and Perez-Ponce de 

Leon, 2000); (3) contemporary and historical 

probes for biodiversity research (Brooks et al., 

1992; Brooks et al., 2000; Brooks, Leon-Regagnon, 

and Perez-Ponce de Leon, 2000; Gardner 

and Campbell, 1992; Hoberg, 1996, 1997a, and 

references therein; Perez-Ponce de Leon, 1997; 

Perez-Ponce de Leon, Leon-Regagnon, and Garcia-Prieto, 

1997); and (4) model systems to explore 

theoretical issues and generalities in evolutionary 

biology, ecosystem and community 

structure, biogeography, adaptation and radiation, 

modes of speciation, and life history within 

a comparative framework (Price, 1980, 1986; 


12 COMPARATIVE PARASITOLOGY. 67(1), JANUARY 2000 

Esch, Bush, and Aho, 1990; Esch, Shostak et al., 

1990; Brooks and McLennan, 1991, 1993a, 

1993b, 1993c; Brooks et al., 2000; Brooks, 


2000; Ewald, 1995; Huxham et al., 1995; Poulin, 

1995a, 1995b, 1997a, 1997b; Perez-Ponce 

de Leon, 1997; Perez-Ponce de Leon, Leon-Regagnon, 

and Garcia-Prieto, 1997). Substantial 

contributions by parasitological research to biodiversity 

inventories extend from the accretion 

of novel information from standard surveys established 

during the past 200 years to sophisticated 

research programs for systematics, ecology, 

biogeography, and evolutionary biology 

based on organismal and molecular approaches. 

The ultimate value and comparability of these 

often disparate areas of research will be increased 

by standardized protocols and methods 

of collection, documentation, and reporting of 

information (Walther et al., 1995; Bush et al., 

1997; Doster and Goater, 1997; Clayton and 

Walther, 1997; Hoberg, Kocan, and Rickard, 

2000). Standardization will also emphasize the 

interdisciplinary linkages of parasitology within 

the biological sciences. 

TROPICAL AND ARCTIC PARASITOLOGY—THE 

POWER OF INTEGRATED PARASITOLOGICAL RE- 

SEARCH: 

The ATBI Model in the Tropics: The Area 

de Conservacion Guanacaste (ACG) in northwestern 

Costa Rica (http://acguanacaste.ac.cr) is 

a biodiversity development area. Its purpose is 

to provide information about preserving species 

living within Costa Rica through sustainable use 

of at least some of them, while simultaneously 

representing a significant portion of national preserved 

wildlands (Janzen, 1992, 1993; Janzen et 

al., 1993). The ACG provides economic opportunity, 

involving local employment and training 

through various biodiversity-related activities, 

including taxonomic inventories. Equally, national 

and international socioeconomic development 

results from the findings of such inventories. 

The valuation of sustained use of biodiversity 

requires that the best technical and scientific 

knowledge be brought to bear on such 

inventories to make the findings of the inventory 

itself useful to as wide a range of stakeholders 

as possible. Moreover, local taxonomists must 

be trained for Costa Rica to be as self-sustaining 

as possible with respect to taxonomic expertise. 

An inventory of eukaryotic parasites inhabiting 


the 940 species of vertebrates living in the ACG 

began in 1997 (Brooks et al., 1999; Desser, 

1997; Hoberg et al., 1998; Marques et al., 1997; 

Monks et al., 1997; Perez-Ponce de Leon et al., 

1998). 

An ATBI assesses biotic resources synoptically 

and exhaustively. Strategically focused inventories, 

such as the one discussed next, are 

better for addressing specific environmental issues. 

The Arctic Consortium Model: Large mammals, 

particularly ruminants, including muskoxen 

(Ovibos moschatus), caribou, and reindeer 

(Rangifer tarandus), represent keystone species 

for subsistence and maintenance of remote communities 

across the Holarctic. Parasite faunas, 

largely nematodes, of these ruminants had been 

considered to be well known. Since 1995, however, 

a new genus and 2 new species have been 

described from the central Canadian Arctic 

(Hoberg, Lloyd, and Omar, 1995; Hoberg et al., 

1999). These projects highlight the importance 

of molecular data in the recognition of cryptic 

species (Anderson et al., 1998) but also demonstrate 

our poor level of knowledge about these 

systems, which is insufficient to understand the 

ecological control mechanisms for dissemination 

and host range. Additionally, poor documentation 

of faunal diversity, host distribution, and 

geographic range hinders development of predictions 

about impacts of global climate change 

and management practices, such as translocation 

and linkages to emergence of parasites (Hoberg, 

Kocan, and Rickard, 2000). 

An initial step in the process of defining the 

fauna involved consolidating information in the 

form of comprehensive checklists and inventory 

for parasites in Holarctic Bovidae and Cervidae 

(Neilsen and Neiland, 1974; Hoberg, Kocan, and 

Rickard, 2000). These form the basis for strategic 

survey and inventory or targeted projects 

to examine the distribution of parasites and to 

assess the potential for parasitic disease emergence. 

Comprehensive collections from specific 

hosts or geographic localities during the past 20 

to 30 years, such as those for Dall's sheep (Ovis 

dalli) (Neilsen and Neiland, 1974) and other 

northern ruminants, are baselines for comparison 

with contemporary surveys to document alteration 

in parasite distribution and abundance on 

local and regional scales. In this process, the 

utility of systematics and historical biogeogra-

phy to understand faunal structure is evident 

(Hoberg et al., 1999). 

Studies of parasite diversity among large ruminants 

in the Arctic are consequential, because 

environmental perturbations attributable to global 

warming may be pronounced in that region. 

Synoptic data for parasite distribution in conjunction 

with studies of the intricacies of parasite 

biology contribute to the development of 

model systems to predict the biotic responses to 

ameliorating climatic conditions in the Arctic 

(Kutz et al., 2000). 

The need to understand even relatively simple 

Arctic systems has led to development of a partnership 

for discovery that seeks to build a synergistic, 

complementary, and interdisciplinary 

linkage for parasitology, wildlife biology, and 

the dynamics of wildlife diseases with systematics 

and biogeography. An informal consortium 

links the University of Saskatchewan, the Department 

of Wildlife, Resources and Economic 

Development (Government of the Northwest 

Territories), the University of Alaska, and the 

Biosystematics and National Parasite Collection 

Unit of the Agricultural Research Service, U.S. 

Department of Agriculture, in studies of Arcticparasite 

biodiversity. Success of this approach 

depends on substantial input and approval from 

local communities in the North. The consortium 

is a powerful model for involvement and collaboration 

among academic scientists, government 

agencies, and native Inuit in the Arctic and also 

represents a general means of integrating the efforts 

of ecologists and systematists to treat a specific 

problem. 

GTI Component 2: Predictive Classifications—What's 

in a Name? A crucial element 

in preserving biodiversity within the context of 

the CBD is managing information about the 1.7 

million species currently known and the millions 

yet to be discovered and described. The framework 

for such information systems must include 

the capability of making predictions about the 

characteristics of species based on what we 

know about the biology of close relatives. Making 

such predictions requires knowledge of phylogenetic 

relationships. Phylogenetic classification 

systems are the most effective framework 

for predictive information systems about organisms 

and their place in the biosphere (Erwin, 

1991; Brooks and McLennan, 1991, 1993a; 

SA2000, 1994; Humphries et al., 1995; Simpson 

BROOKS AND HOBKRG—PARASITE BIODIVKRSITY 

and Cracraft, 1995; Brooks et al., 2000; Brooks, 


2000). Although systematists have made major 

strides in understanding the interrelationships of 

life, corroborated phylogenetic hypotheses are 

still lacking for many groups. DIVERSITAS and 

SA2000 propose to coordinate international research 

to achieve a phylogenetic framework for 

all life, resolved to the family level, by the year 

2010. 

The past decade has seen the integration of 

phylogenetic information in virtually all areas of 

evolutionary research (Brooks and McLennan, 

1991; Harvey and Pagel, 1991), including historical 

ecology (Brooks, 1985a). Historical ecology 

is an interesting and important component 

of basic research in evolutionary biology and 

may also provide a means for placing a variety 

of important biodiversity information in a predictive 

framework. As a framework within 

which information from systematics and ecology 

can be integrated, historical ecology represents 

common ground that can serve the professional 

agendas of taxonomists and ecologists involved 

in biodiversity initiatives, while providing relevant 

data to conservation managers. For example, 

when plant taxonomists suggested that the 

sister species of the American yew tree might 

well have a compound similar to taxol, Taxotene 

was discovered. The interface of systematics and 

biodiversity has also been vital for the successful 

development of agriculture in this century 

(Miller and Rossman, 1995). The advent of such 

predictive applications for integrative data from 

systematics clearly drives the development of efficient 

and accessible systems for the storage, 

maintenance, and retrieval of such information. 

PARASITKS—A MAJOR COMPONENT OF BIO-COM- 

PLHXITY: Since the advent of modern phylogenetic 

studies of parasites (Brooks, 1977), examination 

of these complex systems has included 

an assessment of the degree of congruence 

between host and parasite phylogeny as an indication 

of the form and duration of historical 

association between the host and parasite group. 

Interpretation of the current database (Brooks 

and McLennan, 1993a) suggests that about 50% 

of the host—parasite associations examined have 

resulted from cospeciation (Brooks, 1979), in 

which the ancestors of the host and the parasite 

were associated and have inherited (metaphorically 

speaking) their present ecological associa- 



tion. The remainder can be attributed to speciation 

by host switching or colonization (Brooks, 

1979). Significantly, in these systems, whether 

they were derived through cospeciation or colonization, 

there is no correlation between the degree 

of host specificity with definitive hosts and 

the age of coevolutionary associations (Brooks, 

1979, 1981; Hoberg, 1986; Poulin, 1992; Brooks 

and McLennan, 1991, 1993a, 1993b, 1993c). 

These studies have emphasized that for parasitic 

helminths and their hosts, cospeciation is not a 

universal driving force behind diversification 

(Brooks and McLennan, 1993a and references 

therein; Perez-Ponce de Leon and Brooks, 

1995a, 1995b; Leon-Regagnon, 1998; Leon-Regagnon 

et al., 1996, 1998; Boeger and Kritsky, 

1997; Hoberg, Brooks, and Siegel-Causey, 

1997; Perez-Ponce de Leon, Leon-Regagnon, 

and Mendoza-Garfias, 1997). Entire faunas have 

apparently originated by host switching and subsequent 

coevolution, e.g., the tetrabothriidean 

tapeworms among seabirds and marine mammals 

(Hoberg, 1997; Hoberg, Gardner, and 

Campbell, 1999; Hoberg, Jones, and Bray, 

1999), and major taxa of eucestodes among terrestrial 

and aquatic vertebrates (Hoberg, Gardner, 

and Campbell, 1999; Hoberg, Jones, and 

Bray, 1999), the mazocraeidean monogenoideans 

among primary marine fishes (Boeger 

and Kritsky, 1997), and the absence of members 

of the Oligonchoinea (monogenoideans) in 

freshwater fishes (Boeger and Kritsky, 1997). 

Indeed, the importance of host switching has recently 

been emphasized in hypotheses for multiple 

origins of parasitism among the nematodes 

(Blaxter et al., 1998). 

The discovery that there are no general patterns 

of host specificity correlated with patterns 

of speciation in parasitic groups supports the hypothesis 

that speciation and adaptation are always 

phylogenetically correlated, but neither is 

causally dependent on the other. This conclusion 

was also reached using studies of free-living organisms 

(Brooks and McLennan, 1991). The degree 

of host specificity shows no macroevolutionary 

regularities, i.e., one cannot estimate the 

degree of phylogenetic congruence between host 

and parasite phylogenies or the length of time 

hosts and parasites have been associated from 

observations of host specificity. Similar conclusions 

have been derived from investigations on 

the interaction of herbivores and plants in tropical 

systems (Janzen, 1973, 1980, 1985). 

Phylogenetic approaches are thus requisite for 

elucidation of the complex histories of host-parasite 

assemblages and evaluation of a range of 

alternative hypotheses and predictions in the 

evolution of complex systems (Brooks et al., 

2000; Brooks, Leon-Regagnon, and Perez-Ponce 

de Leon, 2000). A diversity of model systems is 

necessary to resolve the intricacies of processes 

associated with cospeciation, particularly processes 

associated with host switching (Hoberg, 

Brooks, and Siegel-Causey, 1997, and references 

therein). In the future, we may be able to 

compare macroevolutionary patterns of association 

and search for generalities between hostparasite 

and other coevolutionary associations, 

such as phytophagous insects and their host 

plants or pollinators and their host plants. Comparative 

phylogenetic approaches are also a 

foundation for detailed studies in evolution and 

community structure. Next, we briefly review 

applications of parasitological data to these 

broader areas of biology. 

PARASITES AND COMPARATIVE BIOLOGY: 


Parasites are excellent systems for macroevolutionary 

studies of character evolution: Parasites 

are neither unusually simplified nor unusually 

adaptively plastic in their morphological 

traits (Brooks and McLennan, 1993a; Perez- 

Ponce de Leon and Brooks, 1995a, 1995b; 

Perez-Ponce de Leon, Leon-Regagnon, and 

Mendoza-Garfias, 1997; Leon-Regagnon, 1998; 

Leon-Regagnon et al., 1996, 1998). Parasite 

evolution has not been characterized by widespread 

loss of traits that would indicate that parasites 

have given up much evolutionary independence 

to their hosts or by widespread homoplasy, 

indicating that parasites are so simplified 

that their options for morphological 

innovation are limited evolutionarily. 

Parasites are not degenerate, overspecialized, 

host-dependent creatures on the periphery of 

evolution (Brooks and McLennan, 1993a; Poulin, 

1995b). They are successful, innovative 

creatures, many of which have persisted for a 

long time on this planet. This contention is supported 

by phylogenetically based estimates for 

the origins and age of the major groups of parasitic 

platyhelminths. Divergence of the common 

ancestor of the Aspidobothriidea and the 

Digenea, of the major lineages of monogenoideans, 

and of the common ancestor of the Gyrocotylidea 

and the Cestoidea (Amphilinidea +

Eucestoda) coincided with the divergence of the 

common ancestor of the Chondrichthyes and the 

common ancestor of the rest of the gnathostomous 

vertebrates (Brooks, 1985b). Complementary 

independent assessments within the eucestodes 

(Hoberg, Gardner, and Campbell, 1999; 

Hoberg, Jones, and Bray, 1999; Hoberg, Mariaux, 

and Brooks, 2000) and monogenoideans 

(Boeger and Kritsky, 1997) suggest origins extending 

to the Devonian from 350 million to 420 

million or more years ago. 

Other studies (Brooks et al., 1985, 1989) indicated 

that parasite ontogenies evolve as coherent 

units and that larval and adult morphological 

traits are phylogenetically congruent. 

The degree of adaptive response by each life cycle 

stage is thus constrained by common evolutionary 

history. Finally, although molecular 

systematics is in its infancy within parasitology, 

studies to date show that there is a high degree 

of concordance between phylogenies based on 

molecular and morphological traits, when proper 

phylogenetic methods are used and careful character 

analysis is performed (e.g., for ordinal-level 

relationships among the eucestodes, Hoberg 

et al., 1997; Hoberg, Mariaux, and Brooks, 

2000; Mariaux, 1998). The merits of studies 

based on "total evidence" that combine morphological 

and molecular databases (Kluge, 

1989, 1997, 1998a, 1998b; de Queiroz et al., 

1995; Huelsenbeck et al., 1996; Sanderson et al., 

1998) are also apparent (Hoberg, Mariaux, and 

Brooks, 2000). Leon-Regagnon et al. (1999) 

have recently emphasized this point, showing 

that a combination of molecular and morphological 

data could help resolve outstanding specieslevel 

taxonomic problems within a group of frog 

digeneans. 

Parasites and the evolution of life history 

traits: The extent to which the individual components 

of reproductive biology, development, 

and ecology, as well as their complex interactions, 

can be highlighted and examined in parasite-host 

systems is impressive. Phylogenetic 

analysis also allows us to examine phylogenetically 

associated changes in reproductive and 

nonreproductive male and female characters. We 

can then ask questions, such as what are the 

costs and benefits of different reproductive strategies? 

Do male and female characters covary in 

either their origin or their loss (digeneans, monogenoideans)? 

What is the relationship between 

BROOKS AND HOBERG—PARASITE BIODIVERSITY 15 

reproductive conservatism and reproductive 

flexibility in male or female characters (digeneans, 

monogenoideans)? What is the relationship 

between sexual reproduction and the appearance 

of character novelty (eucestodes)? And if asexual 

reproduction is good and sex is better, is sex 

combined with asexual reproduction the best (digeneans)? 

How does dioecy evolve in monoecious 

lineages (Platt and Brooks, 1997)? Recent 

studies (Morand, 1996a, 1996b; Poulin, 1992, 

1995a, 1995b, 1997a, 1997b; Sasal et al., 1997, 

1998; Sasal and Morand, 1998) confirm the suitability 

of parasite systems for studies of the evolution 

of life history strategies. Their results 

confirmed the assertion by Brooks and Mc- 

Lennan (1993a) that parasites show the same 

kinds of life history evolution as their closest 

free-living relatives. 

Parasites as model systems for studying adaptive 

radiations: Parasites have not experienced 

unusually high degrees of adaptive radiation but 

do show interesting patterns. Within the parasitic 

flatworms, the monogenoideans appear to have 

undergone adaptive radiation, whereas the digeneans 

and the eucestodes appear to have experienced 

evolutionary radiation that may or 

may not have been adaptive (Brooks and Mc- 

Lennan, 1993b, 1993c). It is important to realize, 

however, that a relatively species-poor sister 

group balances each species-rich group, so it is 

inaccurate to speak of parasites in general as 

having experienced high levels of adaptive radiations. 

The question of the relative extent of 

parasite adaptive radiations cannot be answered 

until we have comparable databases for free-living 

groups. At the moment, we can say that the 

monogenoideans, digeneans, and eucestodes, not 

unlike ostariophysan and percomorph fishes and 

passerine birds, provide a wealth of information 

about radiations, adaptive or not. This information, 

in turn, supports the hypothesis that such 

radiations were primarily a function of diversification 

of life cycle components. For example, 

4 putative key innovations were identified during 

examination of the database for the parasitic 

flatworms (Brooks and McLennan, 1993a, 

1993c): (1) the evolution of a direct life cycle (a 

developmental change, possibly caused by peramoiphosis, 

with an ecological outcome); (2) 

the appearance of additional larval stages (a developmental 

change); (3) the appearance of 

asexual amplification of larval stages (a devel- 


16 COMPARATIVH PARASITOLOGY, 67(1), JANUARY 2000 

opmental change); and (4) the appearance of 

sexual amplification of reproductive output 

(again, a developmental change, this time involving 

the repetitious production of segments). 

The success of these key innovations was based 

on an interaction between the environment and 

populations, tempered by a background of substantial 

inherited constraints. Since both parasites 

and hosts have evolutionary tendencies and 

capabilities, parasite evolution will be historically 

correlated in some way with host evolution 

but will not necessarily be caused by it. Adaptive 

radiations, therefore, result from active interaction 

between parasite and environmental 

(host) characteristics rather than just from evolutionarily 

passive parasite responses to host 

characteristics. 

The evolution of life cycles is the key element 

in the phylogenetic diversification and adaptive 

radiation of parasites. Life cycle patterns show 

a rich mosaic of diversification in reproductive, 

developmental, and ecological characteristics in 

a strongly phylogenetic context. Evolutionary 

radiations of parasite groups appear to involve, 

first, ontogenetic innovations, second, changes 

in adult reproductive structures, and third, ecological 

components of life cycles. The evolution 

of changes in the biology of the parasites dictates 

the changes in life cycle patterns, including 

patterns of host utilization, rather than the reverse. 

Species richness, therefore, is correlated 

with different phenomena in different groups of 

parasites. These phenomena include changes in 

ecological components of life cycles, production 

or amplification of dispersing larval or juvenile 

stages, and amplification of sexual reproductive 

output. 

Parasites as systems for examining the modes 

of speciation: Price (1980) proposed that the 

evolution of many new parasite-host relationships 

occurred through colonization of new 

hosts. He interpreted this as an example of sympatric 

speciation, because the hosts had to overlap 

geographically for the switch to occur. This 

host-biased perspective changes when we view 

the speciation process from the perspective of 

the organism that is actually speciating. Brooks 

and McLennan (1993a) suggested that if one 

takes a worm's-eye view, different host species 

are like different island archipelagos, and speciation 

by host switching is better explained as 

a form of peripheral isolates, i.e., allopatric spe- 


ciation, than as sympatric speciation. Recently, 

Funk (1998) has shown that if we consider speciation 

by host switching in the manner suggested 

by Brooks and McLennan (1993a), it is 

easier to understand how natural selection can 

play a role in producing isolating mechanisms 

in the populations living on or in different hosts. 

By this logic, true sympatric speciation in parasitic 

platyhelminths can be identified by finding 

sister species restricted to different parts of the 

same host. Rohde (1979) used similar reasoning 

to suggest that natural selection might play a 

role in determining the high degree of site specificity 

exhibited by many parasites. 

The evidence collected to date suggests that 

vicariant and peripheral isolates speciation via 

host switching have played the dominant roles 

in the speciation of parasitic platyhelminths, including 

crocodilians and their digeneans, freshwater 

stingrays and their eucestodes, frogs and 

their digeneans, freshwater and marine turtles 

and their digeneans, marine fish and their digeneans 

and monogenoideans, and seabirds and 

pinnipeds and their eucestodes (see refs. in 

Brooks and McLennan, 1993a; also Hoberg, 

1992, 1995; Hoberg and Adams, 1992; Perez- 

Ponce de Leon and Brooks, 1995a, 1995b; Boeger 

and Kritsky, 1997; Leon-Regagnon, 1998; 

Leon-Regagnon et al., 1996, 1998). Tantalizing 

possibilities of sympatric speciation suggested 

by, for instance, ochetosomatid digeneans in 

snakes, some monogenoideans, and many oxyurid 

nematodes remain to be investigated phylogenetically. 

Host isolation, and particularly isolation for 

definitive hosts, therefore drives speciation. Current 

evidence suggests that intermediate hosts 

are evolutionarily neutral. This seems to be a 

general pattern, emerging from phylogenetic 

studies of cestodes in avian and mammalian 

hosts in either terrestrial or marine environments 

(Hoberg, 1986, 1992, 1995; Hoberg and Adams, 

1992; Hoberg et al., 2000). For example, among 

tapeworms of the genus Taenia (a group where 

detailed information is available for the life cycles 

of most species), speciation appears to be 

driven by host switching among definitive hosts 

exploiting prey within guild associations. A prediction 

that might follow from these findings 

suggests that ecological continuity and predictability 

are limited by transmission dynamics 

linked to intermediate hosts but that diversification 

is driven by predator—prey associations

(Hoberg et al., 2000). These studies indicate the 

necessity for having detailed phylogenetic and 

ecological data as the basis for examining patterns 

and process in speciation for hosts and parasites 

and at a higher level for evaluation of faunal 

and community history. 

Parasites—paradigm systems for studies of 

community structure and evolution: 

One major advantage of parasite communities 

over others is that the habitat they live in, the 

host, has such a well defined structure. . .The host 

microcosm is replicated through time and space 

much more so than habitats for most other organisms. 

Therefore, the study of comparative 

community structure is very powerful. (Price, 

1986) 

There is, as yet, little overlap between parasite 

groups for which we have extensive community 

ecological information and groups for which we 

have extensive phylogenetic information (Poulin, 

1995a, 1997b). In addition, differences in 

understanding between systematists and ecologists 

about the use of phylogenetic methods and 

the possible forms of phylogenetic components 

in community structure have led to unproductive 

and inappropriate polarization of perspectives 

(Bush et al., 1990). Perspectives on the primacy 

of ecological versus phylogenetic-historical determinants 

of faunal structure are changing, 

however, as researchers begin to recognize that 

communities are mosaics of species that evolved 

elsewhere and dispersed into the area (colonizers) 

and species that evolved in situ (residents 

or endemics) (Aho and Bush, 1993). Each parasite 

community represents a historically unique 

combination of colonizers and endemic species, 

in terms of both geographic dispersal and host 

switching (Brooks and McLennan, 1991, 1993a, 

1993b, 1993c; Hoberg, 1997a). Because parasite 

communities are so well defined and so easily 

studied, parasitologists have an opportunity to 

assume a leadership role in the study of community 

evolution. 

Parasites are developmentally and ecologically 

complex organisms subject to and constrained 

by the same rules that govern the evolution of 

all biological systems (Poulin, 1995b). This is 

the key to their value in predictive studies. Ernst 

Mayr (1957) recognized nearly half a century 

ago that the study of parasites "is not only valuable 

for the parasitologist, but is also a potential 

gold-mine for the evolutionist and general biologist." 


Here at the end of the twentieth century, and 

in the midst of the biodiversity crisis, those sentiments 

are truer than ever. The ability to distinguish 

evolutionary colonizers from residents 

will permit us to recognize introduced species 

and to assess the risk that they may cause emergent 

diseases. The ability to distinguish evolutionary 

generalists from specialists will enable 

us to assess more fully the extent of biocontainment 

for any parasite being used as a biocontrol 

agent. Finally, the ability to distinguish the old 

from the recent components of ecosystem structure 

will help us assess what species are likely 

to respond to anthropogenic changes, in what 

order, in what ways, and to what extent. 

GTI Component 3—Management of Systematic 

Knowledge Bases: Getting the Information 

to Those Who Can Use it Effectively. 

DIVERSITAS estimates that within 5 years 

electronic data handling and interlinked knowledge 

systems will become the principal medium 

for all activities associated with applying systematic 

information to biodiversity studies and 

policies. These efforts will require large databases 

on taxonomic information, specimens, and 

data in collections. 

The taxasphere can contribute substantially in 

this area by developing 2 types of home pages: 

(1) phylogenetic home pages, providing the 

most up-to-date phylogenetic trees for all groups 

of parasites, interconnected in such a way that 

anyone can move from one taxonomic level to 

another (this will provide the predictive framework 

within which a variety of specialists can 

operate), and (2) species home pages, providing 

the following information for each targeted species: 

(i) what is it (and how to distinguish it from 

others), (ii) where is it, and (iii) what is its natural 

history. This process has been termed the 

creation of a biodiversity Yellow Pages for the 

Internet (Janzen and Hallwachs, 1994). These 

home pages will include electronic images, 

which can be used for other purposes, such as 

taxonomic descriptions and revisions or identification 

guides. These home pages would also 

include information about the known natural history 

of each species. Species home pages should 

be cross-linked to phylogenetics home pages so 

that we will eventually have a complete listing 

of the phylogenetic relationships of all species 

linked to their natural histories. Biodiversity information, 

irrespective of format, must eventu- 



ally be linked back to a specimen-based reference 

system or biological collection. 

GTI AND COLLECTIONS AS FUNDAMENTAL 

FOUNDATIONS FOR BIODIVERSITY: Biological 

collections are essential elements in the development 

of biodiversity information (Davis, 

1996; GTI, 1999). Collections developed from 

inventory activities represent "a permanent, 

documentable record of specimen-based information" 

(GTI, 1999) that provides historical, 

contemporary, and predictive baselines for understanding 

the patterns and distribution of organisms 

in the biosphere. Collections are vital 

in defining the continuity of ecosystem or community 

structure and integrity. Collections allow 

detailed examination of spatial and temporal 

variation from local to global scales, directly 

linked to specimens and data for populations and 

species, and such biologically significant parameters 

as reproductive phenology, ecology, behavior, 

biogeography, and host associations. Biological 

collections are the context for developing 

and applying biodiversity information efficiently 

and effectively. Thus, the infrastructure for collections 

must be regarded as an integral facet of 

any developing programs for survey, inventory, 

and documentation of global biodiversity resources 

(GTI, 1999). 

Conclusions 

Both the taxasphere and the biosphere may 

be facing imminent extinction. We have insufficient 

taxonomic expertise across all components 

of diversity to address global needs for 

survey and inventory in a timely manner. Survival 

of the taxasphere depends in large part on 

making the cultural change from seeing ourselves 

in the traditional mode of collectors of 

things to being managers of information. It is no 

longer important, or even relevant, to have more 

specimens of a particular species in a collection 

than are found in any other collection; rather, it 

is important to know how much information is 

available about each species. Just as society is 

no longer willing to invest huge sums of money 

in classic set-aside conservation projects, neither 

is it willing to invest in ever-expanding museum 

collections that serve only as repositories of material 

accessible to an ever-decreasing number of 

specialists (Davis, 1996). Neither is society willing 

to invest enormous amounts of money in a 

taxasphere whose only concern is esoteric research. 

The ongoing internal conflict among sys- 


tematic biologists about whether we should be 

seen as a service discipline or as an independent 

research discipline threatens to weaken the taxasphere 

in its efforts to make a significant contribution 

to society and thereby ensure its own 

survival. 

Already too many ecologists and biodiversity 

managers believe that systematists are good only 

for providing names; at the same time, too many 

systematists believe that their only function 

should be generating phylogenies and cuttingedge 

comparative evolutionary studies. We must 

fully internalize the belief that the fundamental 

importance of systematic biology stems from its 

being both an essential service profession and 

an essential element of evolutionary biology. 

Ecologists have successfully grappled with similar 

issues (Lubchenco et al., 1991) 

The call for more inventory work in biodiversity 

thus represents a tremendous opportunity 

and challenge for the taxasphere. Members of 

the taxasphere must understand that biodiversity 

preservation is based on such issues as economic 

development, conservation, solving major environmental 

challenges, and limiting the impacts 

of emerging pathogens and parasites. Inventories 

that seek to identity the critical components of 

biodiversity are necessary to achieve these 

goals, which are mutually beneficial and can be 

synergistic for the scientific community and the 

general population. They are an essential part of 

helping to save the biosphere by helping improve 

the socioeconomic status of as many people 

as possible. 

The taxasphere has long assumed the responsibility 

of naming and classifying the species on 

this planet, and modern phylogenetic methods 

have produced maximally efficient modes of 

storing and transmitting information through 

classifications. The Internet gives us a powerful 

mechanism for disseminating enormous amounts 

of information quickly and widely. All those interested 

in preserving, managing, and sustainably 

using biodiversity should have a vested interest 

in supporting a strong taxasphere. Within 

the scientific community, however, taxonomists 

do not have a history of close and cordial interactions 

with other specialists. There are many 

reasons for this, some of which have been discussed 

(Brooks and McLennan, 1991), but we 

must overcome the historical constraints of sectarian 

competition for academic positions and 

prestige. The scientific community can help pre-

serve biodiversity effectively if each participant 

can give up something of his or her own immediate 

personal agenda to help achieve a greater 

good. 

We return to the analogy of the taxasphere as 

a triage team, the biosphere as a "battlefield," 

and the "war" as human activities that degrade 

global biotic resources. The triage teams survey 

parts of the battlefield as completely as possible 

looking for "wounded" participants. All possible 

participants and the degree to which each has 

been affected must be recognized, and the taxasphere 

has the role of passing that information 

on to the decision makers who are responsible 

for the optimal deployment of resources. Names 

and critical life history and ecological information 

provided by taxonomists constitute the 

foundation for bringing a broad array of stakeholders 

in the national and international arena to 

understand the value of biodiversity. 

DIVERSITAS has designated 2001 as the International 

Biodiversity Observation Year, which 

will, among other things, focus attention on the 

value of the taxasphere and promote a successful 

launch of the GTI. With an emphasis on involving 

local people in a variety of initiatives associated 

with this observation, the International 

Biodiversity Observation Year is an excellent 

opportunity for coalitions of international, national, 

and local political, social development, 

and environmental agencies to join together to 

provide a fuller inventory of the species on this 

planet. 

One should never change a winning game and 

always change a losing game. So far we have 

been playing a losing game. On a global basis, 

people's lives are not improving, and we continue 

to lose large parts of the planet's biota. The 

3-pronged action plan of the GTI represents a 

bold and assertive effort to change a losing game 

into a winning one. The comparative parasitelogical 

perspective using historical, ecological, 

and biogeographic information offers the potential 

for contributions toward recognizing, defining, 

and solving challenges to global biodiversity. 

Acknowledgments 

We would like to express our deepest thanks 

to all those who participated in planning efforts 

for the ATBI in the ACG, in particular, ACG 

administrative and scientific personnel: Sigifrcdo 

Marin, Roger Blanco, Alejandro Masis, Guil- 


lermo Jimenez, Maria Marta Chavarria, and Felipe 

Chavarria; parataxonomists: Calixto Moraga, 

Carolina Cano, Elda Araya, Fredy Quesada, 

Dunia Garcia, Roberto Espinoza, Elba Lopez, 

and Petrona Rios; scientific advisers: Dan Janzen 

and Winnie Hallwachs; and international 

collaborators: Sherwin Desser, Anindo Choudhury, 

Derek Zelmer, Odd Sandlund, Rita Hartvigsen-Daverdin, 

Tom Platt, Greg Klassen, Ramon 

Carreno, Fernando Marques, Scott Monks, 

and Gerardo Perez-Ponce de Leon. We also 

thank members of the developing consortium for 

research on Arctic parasites: Susan Kutz and 

Lydden Polley of the University of Saskatchewan; 

Anne Gunn, Alasdair Veitch, and Brett 

Elkin of the Department of Wildlife, Resources 

and Economic Development, Government of the 

Northwest Territories. Daniel R. Brooks has 

been supported in these efforts by operating 

grant A7696 from the Natural Sciences and Engineering 

Research Council of Canada. 

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67(1), 2000 pp. 26-31 

Natural Occurrence of Diplostomum sp. (Digenea: Diplostomatidae) 

in Adult Mudpuppies and Bullfrog Tadpoles from the 

St. Lawrence River, Quebec 

DAVID J. MARCOGLiESE,1'4 JEAN RooRiGUE,2 MARTIN OuELLET,3 AND LOUISE CHAMPOUX2 

1 St. Lawrence Centre, Environment Canada, 105 McGill Street, 7th Floor, Montreal, Quebec, 

Canada H2Y 2E7 (e-mail: david.marcogliese@ec.gc.ca), 

2 Canadian Wildlife Service, Environment Canada, Quebec Region, 1141 Route de LEglise, P.O. Box 10100, 

Ste. Foy, Quebec, Canada G1V 4H5 (e-mail: jean.rodrigue@ec.gc.ca; louise.champoux@ec.gc.ca), and 

3 Redpath Museum, McGill University, 859 Sherbrooke Street West, Montreal, Quebec, Canada H3A 2K6 

(e-mail: mouell9@po-box.mcgill.ca) 

ABSTRACT: Adult mudpuppies (Necturus maculosus) and bullfrog tadpoles (Rana catesbeiana) infected with 

the eyefluke Diplostomum sp. in the lenses were collected from the St. Lawrence River, Quebec, Canada. 

Respective prevalence and mean abundance of Diplostomum sp. were 100% and 3.1 ± 1.7 in Lake St. Franfois, 

58.3% and 1.5 ± 1.8 in Lake St. Louis, and 53.8% and 0.7 ± 0.8 in Lake St. Pierre. No eyeflukes were observed 

in mudpuppies from the Richelieu River. Prevalence and mean abundance of Diplostomum sp. were significantly 

higher in mudpuppies from Lake St. Fran£ois than in those from other sites. The high prevalence and abundance 

in Lake St. Frangois may be because the regulated water levels may enhance snail intermediate host habitats. 

There was a significant negative correlation between mudpuppy length and number of eyeflukes per host when 

samples were pooled from the 3 sites where Diplostomum sp. was found. Mean length of infected mudpuppies 

from those 3 sites was significantly smaller than uninfected ones. Twenty-four (28%) of 86 mudpuppies had 

cataracts associated with infections of eyeflukes. Prevalence and mean abundance of Diplostomum sp. in bullfrog 

tadpoles collected from Lake St. Pierre were 14.3% and 0.1 ± 0.4 parasite per animal, much lower than observed 

for mudpuppies from the same lake. Higher occurrence of eyeflukes in mudpuppies compared with tadpoles is 

attributed to the greater age and more sedentary benthic nature of mudpuppies. This is the first report of 

amphibians naturally infected with Diplostomum sp. and only the second with eyeflukes in general. 

KEY WORDS: Diplostomum sp., eyefluke, Necturus maculosus, mudpuppy, Rana catesbeiana, tadpole, amphibians, 

prevalence, abundance, St. Lawrence River, Canada. 

The eyefluke Diplostomum spathaceum (Ru- worms from frogs were administered to chicks 

dolphi, 1819) (Digenea: Diplostomatidae) is (Ferguson, 1943), indicating that amphibians 

among the most common parasites of freshwater and reptiles may be able to function as interfishes 

worldwide (Chappell et al., 1994) and in- mediate hosts. Sweeting (1974) successfully esfects 

more than 100 species of fish belonging to tablished infections of D. spathaceum in the Afdiverse 

taxa (Chappell, 1995). Diplostome meta- rican clawed frog, Xenopus laevis (Daudin, 

cercariae are the most important pathogens of 1802), and observed what appeared to be normal 

the eyes of fish, cause blindness, and lead to development of metacercariae. 

poor growth, emaciation, and death (Williams The occurrence of D. spathaceum in natural 

and Jones, 1994; Chappell, 1995). amphibian populations is not known. However, 

While the host spectrum of D. spathaceum is in Mountain Lake, Virginia, U.S.A., the redwithout 

question diverse, its actual extent be- spotted newt Notophthalmus viridescens (Rafyond 

fishes is not clear. For example, Ferguson inesque; 1820), is naturally infected with the fish 

(1943) successfully infected tadpoles and adults 

of the northern leopard frog, Rana pipiens 

eyefluke Tyiodeiphys scheuringl (Hughes, 1929) 

in it§ humors (Etg£S 1961) NQ frogs Qr Qther 

Schreber, 1782, in addition to painted turtles salamanders were found infected5 and experi_ 

(Chrysemys picta (Schneider, 1783)), with meta- mental infections of tadpoles and adult frogs 

cercariae of D. spathaceum. Morphologically, ,, , /rr. ioî\ l ° 

worms appeared normal in these "abnormal' 

_ , , , , , , 

hosts. Development to adulthood occurred when 

T ,. . , , ,, ,. , . , „ . 

Infection levels of diplostomatid eyeflukes in 

- . -. , O T r.- "Li- j 

fish from the St. Lawrence River are believed to 

be high, given the frequency of cataracts and 

4 Corresponding author. blindness in fish from the river (Fournier et al., 


26

MARCOGLIESE ET AL.—DIPLOSTOMUM SP. IN MUDPUPPIES AND BULLFROGS 27 

Figure 1. Map of the St. Lawrence River, Quebec, Canada, depicting sampling localities and areas 

mentioned in the text. Adult mudpuppies (Necturus maculosus) were collected from Port Lewis, lies de la 

Paix, Sainte-Anne-de-Sorel, and the Richelieu River during winter 1998. Bullfrog tadpoles (Rana catesbeiana) 

were collected from lie aux Ours in August 1998. Insert: Location of the sampling region is 

indicated on the map of Canada by a rectangle encompassing Montreal and the St. Lawrence River. 

1996; Lair and Martineau, 1997; Mikaelian and 

Martineau, 1997). During a population study of 

mudpuppies, Necturus maculosus (Rafinesque, 

1818), from the St. Lawrence River, we observed 

an individual with cataracts, and subsequently, 

an infection of Diplostomum sp. We 

then examined adult mudpuppies from 4 areas 

in the St. Lawrence River and 1 of its tributaries 

for eyeflukes. The mudpuppy is a long-lived, 

bottom-feeding, and strictly aquatic salamander, 

studied as a bioindicator of the St. Lawrence 

River (Bonin et al., 1995; Gendron et al., 1997). 

In addition, a single sample of bullfrog tadpoles 

(Rana catesbeiana Shaw, 1802) was collected 

from an area of high diplostome intensity (Marcogliese 

and Compagna, 1999) and examined 

for eyeflukes. 

Materials and Methods 

Mudpuppies were collected during a live trapping 

program with a small hoop net baited with dead fish 

placed at a depth of 1.5-2.5 m (Bonin et al., 1994) 

between the end of January and March 1998 from Port 

Lewis in Lake St. Francois (45°10'N; 74°17'W), lies 

de la Paix in Lake St. Louis (45°20'N; 73°50'W), 

Sainte-Anne-de-Sorel in Lake St. Pierre (46°04'N; 

73°03'W), and the Richelieu River (45°53'N; 

73°09'W). The 3 lakes are formed from expansions of 

the St. Lawrence River, and the Richelieu River composes 

1 of its tributaries (Fig. 1). Animals collected 

from Lake St. Francois (N = 36), Lake St. Louis (N 

= 27), and the Richelieu River (N = 23) were examined 

live for cataracts. Subsamples from these collections 

were examined directly for eyefllukes as follows. 

Animals from Lake St. Francois (N = 13) and the Richelieu 

River (N = 10) were transported live to the 

laboratory, where they were euthanized by cervical 

dislocation. The eyes were removed from the freshly 

killed animals, dissected, and examined with a stereomicroscope 

for parasites. Animals from Lake St. Louis 

(N = 12) were euthanized by cervical dislocation, 

fixed, and stored in 10% neutral buffered formalin, and 

their eyes removed, dissected, and examined with a 

stereomicroscope for parasites. No animals from Lake 

St. Pierre were examined for cataracts, but a sample 



Table 1. Number (N), prevalence (P), and mean abundance (A ± SE) of Diplostomum sp. in the lenses 

of adult mudpuppies (Necturus maculosus) and bullfrog tadpoles (Rana catcsheiana) collected from localities 

in the St. Lawrence River and 1 of its tributaries in 1998. 

Necturus macula sus 

Lake St. Francois 

N P (

MARCOGLIESE HT f^L.—DIPLOSTOMUM SP. IN MUDPUPPIHS AND BULLFROGS 29 

0.0003). Mean total length of infected hosts 

(246.0 ±11.3 mm) was smaller than that of uninfected 

ones (306.2 ± 17.8 mm) (x2 = 6.88; df 

= 1; P — 0.0087) when mudpuppies were 

pooled from the same 3 sites. 

Five of 35 bullfrog tadpoles from Lake St. 

Pierre were infected, each with a single worm, 

giving a mean abundance of 0.1 ± 0.4 and a 

prevalence of 14.3% (Table 1). 

Discussion 

This is only the second report of amphibians 

from North American waters naturally infected 

with eyeflukes. Previously, red-spotted newts 

from Mountain Lake, Virginia, were found infected 

with Tylodelphys scheuringi at a prevalence 

of 100% (Etges, 1961). Adult mudpuppies 

and bullfrog tadpoles were infected with Diplostomum 

sp. at various localities in the St. 

Lawrence River. Mudpuppies were infected to a 

much greater degree than were tadpoles, probably 

due to their more sedentary benthic nature 

and their greater age. All mudpuppies collected 

were reproductive, making them at least 5 yr of 

age for males and 6 yr for females (Bonin et al., 

1994). Among fishes, benthic species tend to be 

more heavily infected than pelagic ones. Cataracts 

are more prevalent in benthic fishes in the 

St. Lawrence River compared with pelagic foragers 

(Lair and Martineau, 1997). In addition, 

D. spathaceum metacercariae accumulate from 

year to year in hosts (Chappell et al., 1994), so 

older hosts tend to be more heavily infected. 

Benthic fish in the St. Lawrence River are more 

heavily infected than mudpuppies. Mean abundance 

of Diplostomum sp. in the white sucker 

(Catostomus commersoni (Lacepede, 1803)) 

aged 2-6 yr was 69.5 in Lake St. Louis and 22.0 

in Lake St. Pierre, whereas in fish aged 7 yr or 

older, it was 167.0 and 62.9 in the 2 lakes, respectively 

(Marcogliese, unpubl.). 

There is little information on geographic variation 

in infection levels within the St. Lawrence 

River system. In a survey of young-of-the-year 

fishes, no significant differences were found 

among sites (Marcogliese and Compagna, 

1999), but among older fishes, infection levels 

were much higher in those from Lake St. Louis 

compared with Lake St. Pierre and near Quebec 

City (Marcogliese, unpubl.). Data presented 

herein demonstrate that infection levels in mudpuppies 

from Lake St. Francois were significantly 

higher than in lakes St. Louis and St. 

Pierre. Moreover, there is a gradient in abundance 

declining downstream from west to east 

in the river. This cannot be directly correlated to 

the distribution of the definitive hosts, gulls and 

terns, as a large colony of ring-billed gulls consisting 

of 6156 pairs in 1997 is located near the 

sampling site in Lake St. Louis, but 3 larger colonies 

of ring-billed gulls, each consisting of 

more than 10,000 pairs, are situated downstream 

east of Lake St. Louis (P. Brousseau, Canadian 

Wildlife Service, pers. comm.). In addition, 

small colonies of common terns (Sterna hirundo 

Linnaeus, 1758), totaling 85 pairs in 1989, 108 

pairs in 1997, and 138 pairs in 1997, as well as 

colonies of black terns (Chlidonias niger (Linnaeus, 

1758)) occur in Lake St. Francois, Lake 

St. Louis, and Lake St. Pierre, respectively 

(Chapdelaine et al., 1999). Habitat in Lake St. 

Francois may be more suitable for the first intermediate 

hosts, lymnaeid snails. One important 

difference between Lake St. Francois and the 

other lakes is that water levels in this lake are 

heavily regulated, and do not fluctuate as much 

as in the other lakes. This stability may enhance 

snail populations and productivity. No worms 

were found in mudpuppies from the Richelieu 

River, although 1 mudpuppy was observed with 

cataracts. There is no information available on 

whether fish are infected with Diplostomum sp. 

in that river, Characteristics of that river may 

make it particularly unsuitable for the completion 

of the parasite's life cycle, in that definitive 

hosts or snail intermediate hosts are rare. There 

are no colonies of gulls or terns located on the 

river. 

There was no relationship between body 

length and number of parasites among mudpuppies 

at any of the sites. When data were pooled 

from the 3 sites where Diplostomum sp. was 

found, there was a significant negative correlation 

between mudpuppy length and the number 

of parasites per host. Moreover, mean length of 

uninfected mudpuppies from those 3 sites was 

significantly greater than that of infected ones. 

These observations suggest that infections with 

Diplostomum sp. may be detrimental to mudpuppy 

growth, as was observed with infections 

in fish (Williams and Jones, 1994; Chappell, 

1995). However, this conclusion may be premature. 

Our sample sizes are small. In addition, 

size of mudpuppies may be affected by pollution 

levels. For example, concentration of contaminants 

in mudpuppies varies with location in the 



St. Lawrence River watershed (Bonin et al., 

1995). Differences in mudpuppy size also could 

reflect some other aspect of habitat quality or 

age differences among the populations. 

Prevalence of cataracts was high in Lake St. 

Frangois, but extremely low in Lake St. Louis 

and the Richelieu River. This can be attributed 

to the higher prevalence and abundance of Diplostotnum 

sp. in Lake St. FranQois compared 

with the other sites. Yet, in both Lake St. Fran- 

Qois and Lake St. Louis, the prevalence of cataracts 

was much lower than the prevalence of 

eyeflukes. Thus, the presence of cataracts is not 

a reliable indicator of infection with eyeflukes, 

at least in mudpuppies. It is not known if the 

single mudpuppy possessing cataracts in the Richelieu 

River was infected with eyeflukes, or 

whether the cataracts resulted from another 

cause. Cataracts are caused by metacercariae, by 

dietary deficiency or excess, or by excessive exposure 

to sunlight, cold, or injury (Ferguson, 

1989). In any case, the possibility of the presence 

of Diplostomum sp. in the Richelieu River 

cannot be dismissed. 

The results demonstrate that animals other 

than fish become infected with metacercariae of 

Diplostomum sp. Given that amphibians develop 

cataracts (Ferguson, 1943; this study), concern 

for the health of aquatic fauna susceptible to 

blindness resulting from infection with eyeflukes 

must be extended beyond fish to include amphibians, 

especially in areas where Diplostomum 

sp. levels are high. 


We thank Sacha Compagna, Emmanuelle Bergeron, 

Michel Arseneau, Paul Messier, and Robert 

Angers for technical assistance. Thanks go to 

Francois Boudreault for preparing the figure. 

Drs. Don McAlpine and Tim Goater provided 

keys and assistance for the identification of the 

tadpoles. Dr. J. D. McLaughlin is gratefully acknowledged 

for sharing his unpublished information 

on experimental infections of gulls with 

Diplostomum spp. metacercariae from the St. 

Lawrence River. 


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(lies, 1959) Shigin, 1977 (Digenea, Diplostomidae) 

and its larval stages—a new record from Poland. 

Acta Parasitologica Polonica 31:199-210. 

SAS Institute. 1997. JMP® Statistical Discovery Software, 

Version 3.2.1. Cary, North Carolina. 

Sweeting, R. A. 1974. Investigations into natural and 

experimental infections of freshwater fish by the 

common eye-fluke Diplostomum spathaceum 

Rud. Parasitology 69:291-300. 

Williams, H., and A. Jones. 1994. Parasitic Worms 

of Fish. Taylor & Francis Ltd., London. 593 pp. 

Executive Committee Member at Large, 1977-1979 

Anniversary Award Recipient, 1987 

Elected Life Member, 1991 




Assessment of Parenteral Plagiorhynchus cylindraceus (Acanthocephala) 

Infections in Shrews 

NATHANIEL R. COADY' AND BRENT B. NiCKOL2 

School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska 68588-0118, U.S.A. 

(e-mail: bnickol@unlinfo.unl.edu) 

ABSTRACT: Plagiorhynchus cylindraceus, a common acanthocephalan parasite of passerine birds, does not require 

a paratenic host for completion of the life cycle, but extraintestinal (parenteral) infections do occur in 

short-tailed shrews (Blarina brevicauda). Examination of wild mammals trapped at 13 sites in and around 

Lincoln, Nebraska, U.S.A., revealed infections in short-tailed shrews and a masked shrew (Sorex cinereus) but 

not in any other species of mammals collected. Laboratory exposures of B. brevicauda and 5 other mammalian 

species that co-occur with short-tailed shrews at sites where shrews harbor extraintestinal P. cylindraceus infections 

resulted in infections only in short-tailed shrews and a single deer mouse (Peromyscus maniculatiis). A 

cystacanth obtained from the mesentery of 1 of these shrews was infective when fed to a robin (Turdus migratorius), 

the usual definitive host. Intestinal histology and susceptibility of P. maniculatiis to laboratory infections 

suggest that the absence of parenteral infections in mammals other than shrews is due to ecological 

circumstances rather than physiological or anatomical constraints. Laboratory exposures of 3 species of isopods 

and a survey of isopods collected from a site where infected shrews occur failed to reveal any species susceptible 

to P. cylindraceus other than the only known intermediate host, the terrestrial isopod Armadillidium vulgare. 

An analysis of the literature regarding diets and the fact that deer mice did not prey on A. vulgare in laboratory 

feeding trials suggest that other mammals co-occurring with shrews are unlikely to consume the intermediate 

host of P. cylindraceus. 

KEY WORDS: Plagiorhynchus cylindraceus, Acanthocephala, cystacanths, shrews, Blarina brevicauda, extraintestinal 

infection, experimental infection, robin, Turdus migratorius, Nebraska, U.S.A. 

As adults, acanthocephalans occur in the intestinal 

lumen of vertebrate definitive hosts; larvae 

develop in the hemocoel of arthropod intermediate 

hosts. Ingestion of the infected intermediate 

host by the definitive host completes the 

life cycle. Larval acanthocephalans of many 

species also occur as parenteral (extraintestinal) 

infections in the viscera of vertebrate hosts, but 

sexual maturity is not attained in these paratenic 

hosts. Paratenic hosts facilitate distribution 

across gaps in trophic levels between the intermediate 

host and predatory definitive hosts high 

in the food chain. Ewald et al. (1991) implicated 

2 species of Sorex in the life cycle of Centrorhynchus 

aluconis (Miiller, 1780) Luhe, 1911, 

which attains maturity in owls. Elkins and Nickol 

(1983) demonstrated that infection of raccoons, 

Procyon lotor (Linnaeus, 1758) Storr, 

1780, with Macracanthorhynchus ingens (Linstow, 

1789) Meyer, 1932, can be accomplished 

by ingestion of cystacanths occurring in mesenteries 

of green water snakes, Nerodia cyclo- 

1 Present address: Department of Zoology, Michigan 

State University, East Lansing, Michigan 48824, 

U.S.A. 

2 Corresponding author. 


32 

pion (Dumeril, Bibron, and Dumeril, 1854) 

Rossman and Eberle, 1977. Several instances of 

paratenic hosts being incorporated into life cycles 

of acanthocephalans that infect piscivorous 

fish have been documented (Hasan and Qasim, 

1960; Paperna and Zwerner, 1976). 

Although it is clear that paratenic hosts play 

an important role in transmission of many acanthocephalans, 

the role of parenteral infections 

often is not explained easily by predator-prey 

relationships. Cystacanths frequently occur in 

hosts from which transmission is unlikely or impossible. 

For example, M. ingens occurs extraintestinally 

in armadillos (Radomski et al., 1991), 

in addition to water snakes, and Mediorhynchus 

grandis Van Cleave, 1916, a parasite of nonpredatory 

birds (usually icterids), can occur parenterally 

in shrews (Collins, 1971). 

Adults of the acanthocephalan species Plagiorhynchus 

cylindraceus (Goeze, 1782) Schmidt 

and Kuntz, 1966, occur in passerine birds, especially 

robins (Turdus migratorius Linnaeus, 

1766) and starlings (Sturnus vulgaris Linnaeus, 

1758). Isopods are infected by ingesting parasite 

eggs passed from birds, and infective larvae develop 

in the hemocoel of Armadillidium vulgare

(Latreille, 1804) Brandt and Ratzeburg, 1831, a 

terrestrial isopod (Schmidt and Olsen, 1964; 

Nickol and Dappen, 1982). Cystacanths of this 

acanthocephalan species also have been reported 

(Nickol and Oetinger, 1968) from the mesenteries 

of short-tailed shrews, Blarina brevicauda 

(Say, 1823) Baird, 1858, in New York state. 

When cystacanths of P. cylindraceus were 

discovered in the viscera of short-tailed shrews 

of eastern Nebraska, a study to assess the significance 

of these parenteral forms was undertaken. 

The distribution of extra-intestinal forms 

among shrews and other co-occurring mammals 

was determined, infectivity of isopod-borne cystacanths 

to shrews and other co-occurring mammals 

was studied, and infectivity of mammalborne 

cystacanths to robins was tested. 


Acquisition and maintenance of P. cylindraceus 

Gravid female worms obtained from robins and starlings 

in Lancaster County, Nebraska, were stored a 

maximum of 3 mo in tap water at 4 C. To infect isopods, 

egg suspensions were prepared by pulverizing 

stored worms in tap water. Each suspension was examined 

microscopically to ensure the presence of fully 

developed eggs. 

A laboratory colony of isopods (A. vulgare) was 

maintained in covered plastic containers (32.5 X 17.5 

X 9.0 cm) provided with 2 to 3 cm of soil, pieces of 

broken clay pots for shelter, a sponge moistened regularly 

to maintain humidity, and potato slices for food. 

Large pieces of potato were used to maintain humidity 

in some containers in place of the moistened sponge. 

These pieces of potato were allowed to sprout, and 

isopods were observed feeding regularly on the shoots 

as well as the potato itself. 

To obtain laboratory-reared cystacanths, isopods 

less than 9.5 mm long (see Nickol and Dappen, 1982) 

were removed from the colony and held without food 

for 36 hr, after which they were allowed to feed on 

potato slices over which a suspension of P. cylindraceus 

eggs in water had been spread. Exposure was in 

covered wells (3.5 cm diameter X 1.() cm deep) imprinted 

on a plastic plate. Fresh egg suspension was 

added to the potato slices after 24 hr. Except to add 

egg suspension, isopods were left undisturbed in the 

dark. After 36 to 48 hr of exposure, isopods were removed 

and isolated in a separate culture. Before use, 

cystacanths were allowed to develop at least 70 days 

in the isopods to ensure infectivity (Schmidt and Olsen, 

1964). 

Survey of mammals 

Mammals at 13 sites located within 4 townships 

(North Bluff, Oak, West Lincoln, and Yankee Hill) in 

and around Lincoln, Nebraska, were surveyed to determine 

locations at which parenteral infections occur 

and to determine which species harbor cystacanths in 

nature. Mammals were trapped with medium-sized 

COADY AND NICKOL—PLAGIORHYNCHUS CYLINDRACEUS IN SHREWS 33 

Sherman live traps baited with a mixture of peanut 

butter and oats, and all mammals caught were examined 

for P. cylindraceus cystacanths. 

Laboratory exposure of mammals 

To determine susceptibility to P. cylindraceus cystacanths, 

mammals of 6 species, collected at sites from 

which P. cylindraceus was absent in previous surveys, 

were administered cystacanths orally. The mammal 

species exposed were short-tailed shrews; European 

mice, Mus musculus Linnaeus, 1758; hispid pocket 

mice, Perognathus hispidus Baird, 1858; wood mice, 

Peromyscus leucopus (Rafinesque, 1818) Thomas, 

1895; deer mice, Peromyscus maniculatus (Wagner, 

1845) Bangs, 1898; and 13-lined ground squirrels, 

Spermophilus tridecemlineatus Mitchill, 1821. 

To expose mammals, laboratory-reared cystacanths 

were pipetted to the back of the throat of lightly anesthetized 

(methoxyflurane) animals. Following exposure, 

each animal was placed into a receptacle lined 

with clean, Ian-colored paper toweling for observation 

and recovery. After the animal recovered from anesthesia, 

it was returned to its normal housing. The recovery 

receptacle then was examined for cystacanths 

that were not ingested by the animal. The white cystacanths 

were highly visible on the paper towels, making 

possible an accurate determination of the number 

administered. 

Mammals were housed in standard mouse cages fitted 

with wire tops, water bottles, paper towels for nesting 

and shelter, and wood shavings. All nonsoricids 

were fed commercial hamster and gerbil food and observed 

to ensure that they were eating. Short-tailed 

shrews were provided additionally with a block of untreated 

wood (5 X 10 X 15-25 mm) and a small clay 

flower pot. The wood absorbed excess oil from the 

shrew's fur and provided shelter. The shrews deposited 

feces regularly within the flower pots, which were removed 

easily and cleaned. Shrews were fed 5 adult 

cockroaches, Periplaneta americana (Linnaeus, 1758) 

Burmeister, 1838, from a laboratory colony at each of 

3 daily feedings. 

Survey and susceptibility of isopods 

A survey was conducted to determine what isopod 

species inhabit sites from which the infection was determined 

to be present in shrews. Isopods were collected 

by hand for 1 hr at night by flashlight, identified, 

and examined for cystacanths. 

To investigate the extent of intermediate host specificity, 

isopods of 3 terrestrial species (Armadillidium 

nasatuin Budde-Lund, 1885, A. vulgare, and Metoponorthus 

pruinosus (Brandt, 1833) Budde-Lund, 1879) 

were exposed to eggs of P. cylindraceus. All of these 

isopods were collected within Lancaster County, Nebraska. 

Peromyscus feeding trials 

Deer mice (P. maniculatus) were offered isopods (A. 

vulgare) as prey to determine the likelihood of their 

consuming an intermediate host in nature. After having 

food withheld for 4 hr, each of 6 deer mice was presented 

20 isopods of assorted sizes for a period of 2 

hr in 10-gallon aquaria. The bottom of each aquarium 



Table 1. Number (N) of wild-caught mammals examined and prevalence (percentage infected [% Inf]) 

and mean intensity (Mean int)* of parenteral infections by Plagiorhynchus cylindraceus. 

Species examined 

Lipotyphyla 

Blarina brevicauda 

Sorex cinercus 

Rodentia 

Microtus ochrogaster 

Microtus pennsylvanicus 

Mus musculus 

Perognathus flavescens 

Peromyscus leucopus 

Perotnyscus maniculatus 

Reithrodontomys rnegalotis 

Spermophilus tridecemlineatus 

Carnivora 

Mustela nivalis 

N 

27 

9 

16 

48 

25 

3 

72 

55 

10 

4 

* Number of worms/number of infected shrews. 

6 

All sites 

surveyed 

was covered by heavy paper with all edges taped down 

to prevent isopods from hiding. Water was available 

to the mice for the duration of the trial. The room 

housing the aquaria was left undisturbed in the dark 

for 2 hr, after which the deer mice were removed and 

the remaining isopods counted. 

% Inf 

Measurements of external muscularis 

To determine whether thickness of intestinal muscle 

could account for differences in susceptibility, the duodenum 

of each of 3 short-tailed shrews, meadow 

voles (Microtus pennsylvanicus (Ord, 1815) Rhoads, 

1895), and deer mice was removed and fixed in neutral 

buffered 10% formalin. Tissues were imbedded in paraffin, 

cut in 6-(jim cross-sections, stained with hematoxylin 

and eosin, and examined with light microscopy. 

The thickness of the external muscularis was measured 

in micrometers at 4 points along the intestine, 

with 2 measurements taken directly opposite on the 

cross-section at each point. Differences in thickness 

among species were sought by 1-way analysis of variance 

(ANOVA) of the resulting 24 measurements for 

each species. 

Infectivity of mammal-borne cystacanths 

The infectivity of mammal-borne cystacanths was 

tested with laboratory exposures to robins. Robins 

were collected with mist nets (U.S. permit PRT- 

694828 and Nebraska permit 96-2) and housed in the 

laboratory where they were given food (Blankespoor, 

1970) and water ad libitum. The robins were held for 

3 wk for acclimation to captivity and to ensure that 

any worms naturally present would be old enough to 

distinguish from those fed in the trial. Cystacanths obtained 

from extraintestinal sites in mammals were pipetted 

directly into the esophagus of each bird to be 

exposed. 

37 

11 

0 

0 

0 

0 

0 

0 

0 

0 

0 

Infection-free 

sites 

N 

10 

4 

8 

10 

4 

3 

40 

34 

6 

3 

3 

N 

17 

5 

8 

38 

21 

0 

32 

21 

4 

1 


3 

Results 

Infection-present 

sites 

% Inf Mean int 

59 3.8 

20 2.0 

0 — 

0 

0 

— — 

0 — 

0 

0 

0 

0 — 

Two hundred seventy-five mammals were collected 

at the 13 sites surveyed. Parenteral infections 

of P. cylindraceus occurred in 11 animals 

of 2 species. All infected animals were collected 

at either of 2 sites. Ten mammalian species were 

examined from these 2 sites, but P. cylindraceus 

was present only in short-tailed shrews and a 

masked shrew (Table 1). Ten of 17 short-tailed 

shrews were infected with 1 to 11 (mean intensity 

3.8) extraintestinal cystacanths. The cystacanths 

were not found consistently in any specific 

location within the abdominal cavity; however, 

several had migrated through the peritoneal 

cavity and had extended their proboscides into 

abdominal muscle tissue. Some of these worms 

appeared vital and little changed from infective 

cystacanths found in isopods. Others were 

heavily encapsulated and appeared moribund. 

One of 5 masked shrews harbored 2 cystacanths, 

1 encysted in the mesentery of the small intestine 

and the other unattached in the lumen of the 

small intestine. 

Each of 27 mammals of 6 species was fed 5 

to 16 cystacanths in the laboratory. Of the 12 

short-tailed shrews fed, 7 cystacanths were recovered 

from the viscera of 3 (Fig. 1); 1 cystacanth 

was recovered from 1 of 7 deer mice (Fig. 

2); and no other animal became infected (Table 

2).

COADY AND N]CKOL—PLAGIORHYNCHUS CYLINDRACEUS IN SHREWS 

1 

Figures 1, 2. Photographs of Plagiorhynchiis cylindraceus 

cystacanths in viscera of laboratory-infected 

mammals. 1. Cystacanth (arrow) 3 days after 

infection in a short-tailed shrew, Blarina brevicauda. 

2. Cystacanth (arrow) 14 days after infection in 

a deer mouse, Peromyscus maniculatus. 

Two species of terrestrial isopods, Trachelipus 

rathkei (Brandt, 1833) Buddie-Lund, 1908 

(n = 62) and A. vulgare (n = 2), were collected 

at a site from which infected shrews were obtained. 

None of the isopods was infected. To 

learn more about the susceptibility of isopods, 3 

species of terrestrial isopod were exposed to P. 

cylindraceus eggs in the laboratory. Eighty percent 

of the exposed A. vulgare became infected 

(mean intensity = 2.98), but cystacanths were 

absent from all isopods of the other 2 species 

(Table 3). None of the isopods (A. vulgare) offered 

to 6 deer mice as food was consumed. 

Measurement of the external muscularis of the 

duodenum revealed a mean thickness of 80 u,m 

for short-tailed shrews, 72 u,m for meadow 

voles, and 42 u,m for deer mice (Table 4). 

Two days after exposure, 1 of 3 robins that 

were fed cystacanths (4, 2, and 1 cystacanths) 

obtained from parenteral sites in laboratory-infected 

shrews harbored a 6-mm-long P. cylindraceus 

cystacanth. The other birds were uninfected. 

Discussion 

Presence at only 2 of 13 sites surveyed suggests 

that distribution of parenteral P. cylindraceus 

infections in mammals is highly localized 

within a broader geographical range of occurrence. 

The type of habitat does not appear to be 

the restricting factor, as the locations at which 

infections were present resembled infection-free 

sites more closely than each other. One of the 

infection sites is dry with thin cover and a flat 

terrain. The second infection site has moist soil 

with a thick cover of lush vegetation and a steep 

grade. The infection was absent from other sites 

surveyed that were similar to the infection sites. 

In addition to having localized occurrence, 

parenteral P. cylindraceus infections appear to 

be restricted to certain individuals of the susceptible 

species. The laboratory infection of a deer 

mouse suggests that mammals other than shrews 

are susceptible. However, natural infections 

were found only in shrews even though mammals 

of other species, including deer mice, at the 

infection sites were examined. The thickness of 

the intestinal wall to be penetrated by a cystacanth 

for establishment of an extraintestinal infection 

does not seem to explain the restriction 

of hosts. Our measurements contained considerable 

variation and were from wild-caught animals, 

leaving several unaccountable variables, 

e.g., age and distention with chyme. Nevertheless, 

the 8 measurements from each of 3 animals 

of each of 3 species form a consistent pattern 

and ANOVA revealed a significant difference (P 

< 0.01) among the species. If our measurements 

are properly representative, short-tailed shrews 

possess a thicker external muscularis than do 

some uninfected species, e.g., deer mice and 

meadow voles. 



Table 2. Occurrence of Plagiorhynchus cylindraceus in laboratory-exposed mammals. 

Species exposed 

Lipotyphla 


Rodentia 

Mus muscidus 

Perognathus hispidus 


Perornyscus maniculatiis 

Spermaphilus tridecemlineatus 

* Number of animals receiving the dose. 

Number of cystacanths 

administered 

16 

11 

9 

7 

5 

10 

10 

10 

7 

10 

The restriction of infections to certain individuals 

is more likely because of interactions 

among birds, isopods, and these mammals than 

to inherent susceptibility or anatomical obstacles. 

Voles rarely use arthropods as prey (Rose 

and Birney, 1985). Deer mice and wood mice 

do so slightly more frequently (Hamilton, 1941; 

Whitaker and Ferraro, 1963). Because of the inclusion 

of arthropods, albeit rarely, in the diet of 

these animals, an occasional infection might be 

expected. Shrews, however, consume arthropods 

more commonly (Table 5) and, therefore, probably 

are exposed to infective cystacanths more 

frequently. 

Interspecific differences among mammals that 

consume isopods might play a role in further 

limiting the distribution of P. cylindraceus. Apparently, 

A. vulgare is the only intermediate host 

for P. cylindraceus. It is the only species of iso- 

1 

4 

1 

4 

2 

3 

1 

6 

3 

2 

Number of cystacanths 

recovered 

0 

0, 0, 0, 5 

0 

0, 0, 0, 1 

o, 1 

0, 0. 0 

0 

0 0, 0, 0, 0, 0 

0, 0, 1 

0, 0 

pod known to be infected in nature (Schmidt and 

Olsen, 1964), and examination of 62 T. rathkei 

collected from a site at which shrews were infected 

revealed no infection. Laboratory exposures 

of isopods of 2 additional local species (A. 

nasatum and M. pruinosus) failed to produce 

any cystacanths, whereas isopods of the species 

A. vulgare were infected readily. Porcellionid 

isopods are soft bodied and, according to Sutton 

(1980), cannot roll into a protective ball, whereas 

the exoskeleton of isopods belonging to the 

family Armadillidiidae is harder, and according 

to Sutton (1980), these isopods do roll up into a 

protective ball. Even after having food withheld 

for 2 hr, deer mice did not eat isopods (A. vulgare) 

offered in the laboratory feeding trial. This 

suggests that the isopod materials identified in 

dietary studies (Table 5) were not remains of 

infected isopods. 

Table 3. Occurrence of Plagiorhynchus cylindaceus cystacanths in laboratory-exposed isopods. 

Species exposed 

Armadillidium vulgarac 

Trial 1 

Trial 2 

Combined 

A nnadillidium nasatum 

Trial 1 

Trial 2 

Combined 

Metoponorthus pruinosus 

Trial 1 

Trial 2 

Combined 

Number examined 

50 

20 

70 

22 

16 

38 

7 

10 

17 

Number (%) infected Mean 

38 (76) 3.03 

18 (90) 2.89 

56 (80) 2.98 

0 — 

0 — 

0 

0 — 

o 

0 — 


Intensity 

Maximum 

10 

7 

10 

— 

— 

— 

— 

— 

—

COADY AND NICKOL—PLAGIORHYNCHUS CYLJNDRACEUS IN SHREWS 37 

Table 4. Thickness (micrometers) of external muscularis of 3 mammalian species.* 

Species 


Peromyscus maniculatus 

. 

1 

89 37 

66.13 

38.10 

Animal 

2 

58 12 

59.06 

32.50 

3 

92 50 

91.94 

54.00 

Mean (SD) 

xn no 1 1 7 xn*) 

72.38 (17.30) 

41.53 (11.15) 

* Measurements were made for 3 animals of each species. For each animal, the thickness given is the mean of 8 measurements 

(2 measurements directly opposite each other at 4 points along the duodenum). Differences among species were significant (P 

< 0.01) by 1-way analysis of variance of the 24 individual measurements for each species. 

The establishment in the intestine of a robin 

by a cystacanth removed from the viscera of a 

laboratory-exposed shrew demonstrates that parenteral 

cystacanths from mammals can be infective 

to definitive hosts. An infective cystacanth 

from an intermediate host is 3.0 to 4.4 mm long 

(Schmidt and Olsen, 1964), and parenteral cystacanths 

from our laboratory-infected shrews 

were 3.5 to 4.2 mm long. The worm recovered 

from the laboratory-infected robin measured 6.0 

mm in length. Such growth during 2 days in the 

bird's intestine indicates successful establishment. 

Despite the infectivity of extraintestinal cystacanths 

and occasional reports of passerine 

birds eating shrews and other small mammals 

(Powers, 1973; Penny and Knapton, 1977) we 

conclude that paratenic hosts are not important 

to P. cylindraceus populations. Comprehensive 

studies fail to identify small mammals as an important, 

or even minor, part of these birds' diets 

(Paszkowski, 1982; Wheelwright, 1986). Likewise, 

there is little evidence that paratenic hosts 

have played any meaningful role in facilitating 

wider host distribution for P. cylindraceus. 

There is little question that raptors and other 

flesh-eating birds could consume P. cylindraceus 

cystacanths (see Audubon, 1937, Plate 

374). Dollfus and Golvan (1961) listed Buteo 

buteo Linnaeus, 1758, as a host for P. cylindraceus, 

and Ewald and Crompton (1993) found it 

in Strix aluco Linnaeus, 1758. Neither report, 

however, gives an indication of whether the 

worms reach maturity and produce eggs in those 

birds. Additionally, P. cylindraceus has been reported 

from several species of Corvidae. Rutkowska 

(1973) described eggs from females harbored 

by 1 of 500 jackdaws, Coloeus monedula 

= Corvus monedula Linnaeus, 1758, examined 

in Poland, but the other 8 records from corvids 

(Jones, 1928; Pemberton, 1961; Williams, 1961; 

Threlfall, 1965; Todd et al., 1967; Hendricks et 

Table 5. Inclusion of isopods as prey by mammals that co-occurred at collection sites where Plagiorhynchus 

cylindraceus was present. 

Species 

Lipotyphyla 


Cryptolis parva 

Sorex cinereus 

Rodentia 

Microtus ochrogastor 


Mas musculus 


Peromyscus maniculatus 

Frequency* 

3.7 

6.7 

1.6 

2.8 

4.0 

().() 

().() 

().() 

1.6 

0.0 

2.0 

0.0 

Percentage of animals with isopods present in diet. 

Volume of diet (%) 

No report 

1.4 

1.6 

1.9 

2.1 

— 

— 

— 

1.7 

— 

No report 

— 


Reference 

Hamilton, 1941 

Whitaker and Ferraro, 1963 

Whitaker and Mumford, 1972 



Zimmerman, 1965 

Zimmerman, 1965 

Whitaker, 1966 

Whitaker and Ferraro, 1963 

Whitaker, 1966 

Hamilton, 1941 

Whitaker, 1966


al., 1969; Andrews and Threlfall, 1975; Lisitsyna, 

1993) either report juveniles or give no 

indication of maturity. 

Acanthocephalans belonging to all taxonomic 

classes and 6 of the 8 orders of the phylum have 

been reported as extraintestinal infections in vertebrates. 

Such parenteral infections are results of 

either specific adaptations serving to enhance 

transmission or historical events not currently 

maintained by natural selection. It is probable 

that this trait in P. cylindraceus, and perhaps in 

other species that occur parenterally in hosts 

from which transmission to a definitive host is 

impossible or unlikely, is a result of inheritance 

from an ancestor in which it might have had a 

selective advantage, rather than being an adaptation 

shaped by current selective forces. 


Russell A. Benedict, School of Biological Sciences, 

University of Nebraska-Lincoln, assisted 

with trapping of mammals, and Patricia W. Freeman, 

curator of zoology, University of Nebraska 

State Museum, loaned traps. The study was supported, 

in part, by an Ashton C. Cuckler Fellowship 

(to N.R.C.). 


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COADY AND NICKOL—PLAGIORHYNCHUS CYLINDRACEUS IN SHREWS 39 

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Revision of the Genus Pallisentis (Acanthocephala: Quadrigyridae) 

with the Erection of Three New Subgenera, the Description of 

Pallisentis (Brevitritospinus} vietnamensis subgen. et sp. n., a Key to 

Species of Pallisentis, and the Description of a New Quadrigyrid 

Genus, Pararaosentis gen. n. 

OMAR M. AivnN,1-4 RICHARD A. HecKMANN,2 NGUYEN VAN HA,3 PHAM VAN Luc,3 AND 

PHAM NGOC DoANH3 

1 Institute of Parasitic Diseases, P.O. Box 28372, Tempe, Arizona 85285, U.S.A., and Department of Zoology, 

Arizona State University, Tempe, Arizona 85287, U.S.A. (e-mail: omaramin@aol.com), 

2 Department of Zoology, Brigham Young University, Provo, Utah 84602, U.S.A. 

(e-mail: richard_heckmann@email.byu.edu), and 

3 Institute of Ecology and Biological Resources, Nghiado, Caugiay, Hanoi, Vietnam 

ABSTRACT: The genus Pallisentis is revised. Golvan's 3 subgenera (Farzandia, Neosentis, Pallisentis) were 

distinguished solely by the number of hooks in proboscis hook circles, which proved to be a variable trait. Three 

new subgenera are erected based on the relative size of hooks in subsequent circles, the size of cement glands, 

and the number of their giant nuclei. A new species of Pallisentis is described from the snake head mullet, 

Ophicephalus maculatus, in Vietnam. A key to all 26 species of the genus Pallisentis accepted as valid and 

following our classification is included. A new quadrigyrid genus Pararaosentis is erected. 

KEY WORDS: revision of Pallisentis; Acanthocephala, Quadrigyridae, new taxa, Pallisentis (Brevitritospinus) 

vietnamensis subgen. et sp. n., taxonomic key, Pararaosentis gen. n., snake head mullet, Vietnam. 

The discovery of new species of the genus 

Pallisentis Van Cleave, 1928, from a Vietnamese 

mullet, Ophicephalus maculatus (Lacepede, 

1802) (Channidae) necessitated the review of the 

current status of the genus and its component 

species. The confused taxonomic state was compounded 

by Golvan's (1959, 1994) subgeneric 

designations and assignments based on the variable 

character of the number of hooks in proboscis 

hook circles. Other problems of omissions, 

inconsistent assignments, and improper 

generic relegations necessitated the revision of 

the entire group, the creation of 3 new subgenera 

based on naturally consistent characters, and the 

creation of a key to all 26 species of Pallisentis. 


Fifteen snake head mullets, O. maculatus, measuring 

26-48 (mean, 36) cm in total length were examined 

for parasit.es. The fish were collected from waters 

around Hanoi, Vietnam, and purchased alive in a Hanoi 

fish market on 25 May 1998. Two fish were infected 

with about 20 worms, of which 9 were made 

available and described in this paper as a new species. 

These thin cylindrical worms were easily located in 

the pathologically enlarged upper intestine because of 

the apparent reddish inflammation at attachment sites. 



40 

The worms were removed, extended in water, and 

fixed and shipped in 70% ethanol. Worms were stained 

in Mayer's acid carmine, dehydrated in ascending concentrations 

of ethanol, and whole-mounted in Canada 

balsam. Measurements are in micrometers unless otherwise 

stated. The range is followed by mean values 

(in parentheses). Width measurements refer to maximum 

width. Body ( = trunk) length does not include 

neck, proboscis, or male bursa. Specimens have been 

deposited in the United States National Parasite Collection 

(USNPC), Beltsville, Maryland, U.S.A. 

Results and Discussion 

The Genus Pallisentis Van Cleave, 1928 

Van Cleave (1928) created the genus Pallisentis 

in his new family Pallisentidae to accommodate 

Pallisentis umbellatus Van Cleave, 

1928. Baylis (1933) synonymized the genera 

Farzandia Thapar, 1930, and Neosentis Van 

Cleave, 1928, despite Meyer's (1932) retention 

of Farzandia as an independent genus in a different 

family, Acanthogyridae. Petrochenko 

(1956) followed Meyer (1932). Baylis' (1933) 

synonymies were accepted by Harada (1935) 

and Yamaguti (1963) and currently remain valid; 

the genus Pallisentis was recognized in the family 

Quadrigyridae Van Cleave 1920, subfamily 

Pallisentinae Van Cleave, 1928. 

In his generic diagnosis, Van Cleave used re-

strictive traits that were basically descriptive of 

specific features of P. umbellatus. These included 

the number of proboscis hooks, collar and 

trunk spines, and giant nuclei of the cement 

gland, as well as the extent of distribution of the 

trunk spines, and the position of the testes. 

These same traits were used by subsequent 

workers, e.g., Petrochenko (1956) and Yamaguti 

(1963), despite the addition of more species adding 

more variability to the diagnostic criteria of 

the genus over the years. A new diagnosis of the 

genus Pallisentis is provided below. 

Pallisentis Van Cleave, 1928, sensu lato 

DIAGNOSIS: Quadrigyridae, Pallisentinae. 

Trunk slender, small-medium in length, with an 

anterior set of collar spines and a posterior set 

of trunk spines separated by region lacking 

spines. Collar spines arranged in a few closely 

set circles; circles of trunk spines more widely 

spaced and may extend to posterior end of males 

or females. Giant hypodermal nuclei may be 

present. Proboscis short, cylindroid-spheroid 

with 4 circles of 6-12 hooks each. Proboscis receptacle 

single-walled, with large cerebral ganglion 

near its base. Lemnisci long, cylindrical, 

equal or unequal. Testes ovoid-cylindrical, contiguous. 

Cement gland syncytial, medium-long, 

with few to many giant nuclei. Cement reservoir 

present. Saefftigen's pouch present or absent. 

Parasites of freshwater fishes in Asia. 

The Subgenera of Pallisentis 

Based on the number of hooks in each of the 

proboscis hook circles, Golvan (1959) erected 3 

subgenera of Pallisentis: Farzandia Thapar, 

1931, with 10 hooks per circle, Neosentis Van 

Cleave, 1928, with 8 hooks per circle, and Pallisentis 

Van Cleave, 1928, with 6 hooks per circle. 

Some species were not assigned to a subgenus, 

and others could be relegated to more 

than 1 subgenus or not to any. By 1994 a greater 

number of species had been described and the 

number of nonassignments and exceptions increased 

disproportionately. Golvan (1994) additionally 

did not include 4 other species described 

earlier (footnote, Table 1). The character (number 

of hooks per circle) used by Golvan (1959) 

is inconsistent and showed variations even within 

the same species and, thus, should not be used 

for subgeneric assignment of species. Yamaguti 

(1963), Tadros (1966), Gupta and Verma (1980), 

Soota and Bhattacharya (1982), Gupta and Fat- 

AMIN ET AL.—REVISION OF THE GENUS PALLISENTIS 41 

ma (1986), and Chowhan et al. (1987) also rejected 

Golvan's (1959) system. Tadros (1966) 

and Soota and Bhattacharya (1982) also agreed 

with the above authors and evaluated other taxonomic 

characters of Pallisentis. We found the 

most consistent character to be the difference in 

the size of proboscis hooks in subsequent circles. 

Other characters of considerable consistency 

included the size of the cement gland and the 

number of its giant nuclei, the shape and distribution 

of trunk spines, and the presence or absence 

of Saefftigen's pouch. Based on the first 3 

characters listed above, we designate herein 3 

new subgenera. All characters (above) are used 

to construct the subsequent key to species. 

Demidueterospinus subgen. n. 

DIAGNOSIS: With the characters of the genus 

Pallisentis provided herein. Proboscis hooks in 

circle 2 about half as long as hooks in circle 1. 

Cement gland usually small, with few giant nuclei. 

Taxonomic summary 

TYPE SPECIES: Pallisentis (D.) ophiocephali 

(Thapar, 1931) Baylis, 1933. 

OTHER SPECIES: Pallisentis (£>.) basiri Farooqi, 

1958; Pallisentis (£>.) panadei Rai, 1967. 

Remarks 

Pallisentis basiri and P. panadei were synonymized 

with Pallisentis colisai Sarkar, 1954, 

by Soota and Bhattacharya (1982). We consider 

these species to be valid. These and other synonymies 

made by Soota and Bhattacharya 

(1982) did not acknowledge the species-specific 

differences that we outline in our key. Further, 

their tabulated data often did not match the narrative 

and were occasionally misplaced. These 

synonymies were also not accepted by Khan and 

Bilqees (1987) and were not followed by other 

workers. The redescription of P. basiri by Gupta 

and Fatma (1986) is inconsistent with the characteristics 

of that species and appears to be of 

another species. Pallisentis ophiocephali of Moravec 

and Sey (1989) from Vietnam is conspecific 

with our material from the same location 

and is described herein as a new species. 

Brevitritospinus subgen. n. 


Pallisentis provided herein. Proboscis hooks in 

circle 3 about half as long as hooks in circle 2. 


Table 1. Present status of the subgenera and species of the genus Pallisentis according to Golvan (1959) 

number of proboscis hooks per circle in species assigned to each subgenus. 

No. of proboscis 

hooks/circle 

Species and subgenera'' 

Thapar (1931) established genus 

(=Echinorhynchus gaboes MacC 

(1963), and Yamaguti (1954) 

Synonymized with P. ophioceph 

Kennedy 1989 

Baylis (1933) Synonymized the 

Type species of Neosentis', redes 

P. ophiocephali of Moravec and 

Nominal subgenus of genus Pal 


and Gupta (1979) 

Needs a new subgenus (Tadros, 

charya (1982) 

Improper assignment; included i 

with P. colisai by Soota and 

Gupta (1979) 

Also agrees with subgenera Far 

Improper assignment; fits subge 

Also fits subgenera Farzandia a 

Not a species of the genus Palli 

Improper assignment; fits subge 

Improper assignment; Synonymi 




Originally described as P. golva 

Type species of Pallisentis Van 

As per Golvan (1959, 1994) 

Originally reported as Farzandia 

Belongs in the genus Acanthocep 

( = Devendrosentis garuai Sahay 

Agrees with subgenus Neosentis 

Agrees with subgenus Farzandia 

Agrees with subgenus Farzandia 


Agrees with subgenus Neosentis 

Subgenus Farzandia Thapar, 1931 (10) 

P. (F.) gaboes (MacCallum, 1918) Van Cleave, 1928 (10) 

P. (F.) nagpurensis (Bhalerao, 1931) Baylis, 1933 (8-10) 

Subgenus Neosentis Van Cleave, 1928 (8) 

P. (N.) celatus (Van Cleave, 1928) Baylis, 1933 (8) 

P. (N.) ophiocephali (Thapar, 1931) Baylis, 1933 (8-10) 

Subgenus Pallisentis Van Cleave, 1928 (6) 

P. {P.) allahabadi Agarwal, 1958 8-10 

P. (P.) basiri Farooqi, 1958 9 

P. (P.) buckleyi Tadros, 1966 10 

P. (P.) cavasii Gupta and Verma, 1980 6-10 

P. (P.) colisai Sarkar, 1954 (10-12) 

P. (P.)fasciata Gupta and Verma, 1980 6-10 

P. (P.) golvani Troncy and Vassiliades, 1973 6 

P. (P.) gomtii Gupta and Verma, 1980 8-10 

P. (P.) guntei Sahay, Nath, and Sinha, 1967 8-10 

P. (P.) magnum Saeed and Bilqees, 1971 8-10 

P. (P.) nandai Sarkar, 1953 8-10 

P. (P.) panadei Rai, 1967 10 

P. (P.) tetraodonlae Troncy, 1978 6 

P. (P.) umbellatus Van Cleave, 1928 (6) 

Subgenus not assigned 6-12 

Pallisentis sp. Pearse, 1933 10 

P. cholodkowskyi (Kostylew, 1928) Amin, 1985 3 

P. gamai (Sahay, Sinha, and Ghosh, 1971) Jain and Gupta, 1979 6 

P. guptai Gupta and Fatma, 1986 8 

P. kalriai Khan and Bilqees, 1985 10 

P. mehrai Gupta and Fatma, 1986 10-12 

P. nandai Sarkar, 1953 (8-10) 

P. sindensis Khan and Bilqees, 1987 8 

* Golvan (1994) did not include P. chipei Gupta and Gupta 1979 (8 hooks per circle), P. croftoni Mital and Lai, 1981 (10), 

and Ip, 1989 (10). He correctly reassigned "P. (?) ussuriensis" (Kostylew, 1941) Golvan, 1959 (= Acanthocephalorhynchoides 

Meyer, 1932. 


Cement gland usually small with few giant nuclei. 


TYPE SPECIES: Pallisentis (B.) allahabadi 

Agarwal, 1958. 

OTHER SPECIES: Pallisentis (B.) cavasii Gupta 

and Verma, 1980; Pallisentis (B.) croftoni Mital 

and Lai, 1981; Pallisentis (B.)fasciata Gupta 

and Verma, 1980; Pallisentis (B.) guntei Sahay, 

Nath, Sinha, 1967; Pallisentis (B.) indica Mital 

and Lai, 1981; Pallisentis (B.) tnehrai Gupta and 

Fatma, 1986; Pallisentis (B.) vietnamensis sp. n. 

(this report). 

Remarks 

Pallisentis allahabadi and P. guntei were synonymized 

with P. ophiocephala and P. colisai, 

respectively, by Soota and Bhattacharya (1982). 

These synonymies did not acknowledge speciesspecific 

differences outlined in our key. The redescription 

of P. allahabadi by Jain and Gupta 

(1979) and their synonymization of P. buckleyi 

Tadros, 1966, with it are considered sound and 

are accepted; the key taxonomic characters are 

in agreement. 

Pallisentis subgen. n. Van Cleave, 1928, 

sensu stricto 


Pallisentis provided herein. Proboscis hooks 

gradually declining in size posteriorly; cement 

glands usually long with many giant nuclei. 


TYPE SPECIES: Pallisentis (P.) umbellatus 

van Cleave, 1928. 

OTHER SPECIES: Pallisentis (P.) celatus (Van 

Cleave, 1928) Baylis, 1933; Pallisentis (P.) colisai 

Sarkar, 1954; Pallisentis (P.) clupei Gupta 

and Gupta, 1979; Pallisentis (P.) gaboes 

(MacCallum, 1918) Van Cleave, 1928; Pallisentis 

(P.) garuei (Sahay, Sinha, and Ghosh, 1971) 

Jain and Gupta, 1979; Pallisentis (P.) gomtii 

Gupta and Verma, 1980; Pallisentis (P.) guptai 

Gupta and Fatma, 1986; Pallisentis (P.) kalriai 

Khan and Bilqees, 1985; Pallisentis (P.) magnum 

Saeed and Bilqees, 1971; Pallisentis (P.) 

nandai Sarkar, 1953; Pallisentis (P.) nagpurensis 

(Bhalero, 1931) Baylis, 1931; Pallisentis (P.) 

pesteri (Tadros, 1966) Chowhan, Gupta, and 

Khera, 1987; Pallisentis (P.) sindensis Khan and 


Bilqees, 1987; Pallisentis (P.) singaporensis 

Khan and Ip, 1989. 

Remarks 

Pallisentis celatus was redescribed by Moravec 

and Sey (1989) from Vietnamese specimens. 

Pallisentis gaboes was provisionally and incompletely 

redescribed by Yamaguti (1954) and 

briefly referenced by Fernando and Furtado 

(1963). Khan and Ip (1988) referred to the proboscis 

armature of P. gaboes as similar to that 

of P. singaporensis. The synonymization of the 

genus Devendrosentis Sahay, Sinha, and Ghosh, 

1971, with the genus Pallisentis and the assignment 

of D. garuai Sahay, Sinha, and Gosh, 

1971, to the genus Pallisentis are accepted; the 

descriptions of the new genera are identical. 

Since none of their accounts was sufficiently 

similar to the original description, the incomplete 

redescription of P. nagpurensis by Jain and 

Gupta (1979) is considered questionable, that of 

Chowhan et al. (1987) uncertain, and that of 

Kennedy (1981) not of the same species. Based 

on comparability of cement gland structure, we 

accept the synonymy of the genus Saccosentis 

Tadros, 1966, with Pallisentis as proposed by 

Chowhan et al. (1987), and Saccosentis pesteri 

Tadros, 1966, is assigned to the genus Pallisentis. 

The synonymization of P. magnum, P. nandai, 

and P. nagpurensis with P. ophiocephali by 

Soota and Bhattacharya (1982) is not accepted, 

since these synonymies did not acknowledge the 

species-specific differences outlined in our key. 

Other Taxonomic Assignments 

Pallisentis cholodkowskyi (Kostylew, 1928) 

Amin, 1985 ( = Quadrigyrus cholodkowskyi Kostylew, 

1928) is assigned to the genus Acanthocephalorhynchoides 

Kostylew, 1941, based on 

proboscis and trunk spination patterns (see Williams 

et al. [1980] for additional information). 

Golvan (1994) made a similar assignment regarding 

Acanthocephalorhynchoides ussuriensis 

Kostylew, 1941. 

Pallisentis tetraodontae Troncy, 1978, was 

described by Troncy (1978) as a subspecies of 

Pallisentis golvani Troncy and Vassiliadis, 1973. 

Golvan (1994) elevated it to species rank without 

justification. We have determined that P. 

golvani does not belong to the genus Pallisentis 

or any other known genus of the family Quadrigyridae 

Van Cleave, 1920 (see remarks). A 



new genus is described below to accommodate 

P. golvani. 

Pararaosentis n. gen. 

DIAGNOSIS: Quadrigyridae, Pallisentinae. 

Trunk short with hypodermal nuclei and anterior 

constriction containing 1 set of minute spines 

arranged in a few complete circles, most anteriorly. 

Proboscis short, with 4 circles of small 

hooks gradually decreasing in length posteriorly. 

Proboscis receptacle single-walled, with large 

cerebral ganglion at its base. Male reproductive 

system compacted in posterior region. Testes 

short, robust, contiguous. Cement gland syncytial, 

small with few giant nuclei. Cement reservoir 

and Saefftigen's pouch present. Parasites of 

freshwater fishes in Africa. 


TYPE SPECIES: Pararaosentis golvani (Troncy 

and Vassiliades, 1973) n. comb. (=Pallisentis 

golvani Troncy and Vassiliades, 1973; Pallisentis 

tetraodontae Troncy, 1978). 

Remarks 

The type species does not belong in the genus 

Pallisentis because of its anterior trunk constriction, 

the presence of only 1 set of spines anteriorly, 

the noncylindrical form of its testes and 

cement gland, and its occurrence in African, not 

Asian, fishes. Furthermore, the trunk is short and 

lacks the anterior swelling of the long slender 

specimens of Pallisentis. The new genus is closest 

to the genus Raosentis Datta, 1947. In Raosentis, 

however, the trunk is not constricted anteriorly, 

and the proboscis hooks in the anterior 

2 circles are longer and stouter than the hooks 

in posterior 2 circles and are separated from 

them by an unarmed area. 

The characters on which Troncy (1978) based 

his assignment of P. tetraodontae as a subspecies 

of P. golvani are not significant enough to 

justify a subspecific status, and P. tetraodontae 

is herein relegated to a synonym of P. golvani. 

Pallisentis (Brevitritospinus) vietnamensis sp. n. 

(Figs. 1-9) 

Description 

GENERAL: Shared characters (proboscis and 

hooks, proboscis receptable, trunk, and lemnisci) 

larger in females than in males (see Table 2 for 

measurements). Trunk curved ventrad, medium 

in length, slender, cylindrical with anterior 


swelling (Figs. 1, 5) and 83-137 long X 21-62 

wide hypodermic nuclei in anterior half of trunk 

(0—5), posterior half (1—4), and in apical organ 

of proboscis (3). Proboscis truncated, wider than 

long, with conspicuous apical organ (Fig. 3). 

Proboscis hooks with shallow pluglike roots, in 

4 circles of 10 hooks each. Hooks in first circle 

largest, hooks in second circle slightly smaller, 

hooks in third circle about half as long as hooks 

in second circle, hooks in fourth circle smallest 

(Figs. 3, 4). Neck very short (Figs. 3, 5, 9). Proboscis 

receptacle 5-6 times as long as proboscis, 

single-walled, with cerebral ganglion near its 

base (Figs. 1, 5). Lemnisci long, tubular, unequal, 

and with 1 giant nucleus each (Figs. 1, 

5). Collar spines triangular, in 18—22 closely 

spaced circles beginning just behind a spineless 

area on anterior trunk (often interpreted as the 

neck) and overlapping and extending slightly 

posterior to the posterior half of the proboscis 

receptacle (Figs. 1, 5). Trunk spines triangular 

(Figs. 7, 8), in considerably more widely spaced 

circles extending to posterior end of females and 

to testes in males. Anterior trunk swelling covered 

by 17-20 circles of trunk spines. An unspined 

area separating trunk spines from collar 

spines (Figs. 1, 5). Unspined areas often occurring 

in posterior 2-3 circles of collar spines, and 

up to 5 or 6 times involving 2-6 circles of trunk 

spines throughout (Figs. 1, 5). Number of trunk 

spines decreasing to 1 or 2 in posteriormost circles 

where their size slightly decreases. 

MALE: Based on 4 specimens. Reproductive 

system at posterior end of trunk. Testes oblong, 

contiguous; anterior testis larger than posterior. 

Cement gland rectangular, syncytial with 7-8 giant 

nuclei. Cement reservoir branching posteriorly 

into 2 ducts (Figs. 1, 2). 

FEMALE: Based on 5 specimens. Reproductive 

system short, robust with the vaginal complex, 

uterus, and uterine bell of almost equal 

length; gonopore subterminal (Fig. 6). Eggs 

ovoid with concentric shells. 


TYPE HOST: Snake head fish (mullet), Ophiocephalus 

maculatus (Lacepede, 1802) (Channidae). 

OTHER HOST: ca the be (Vietnamese name) 

Acanthorhodeus fortunensis (Cyprinidae) (only 

1 juvenile found by Moravec and Sey, 1989). 

SITE OF INFECTION: Upper intestine.


Figures 1-8. Pallisentis vietnamensis sp. n. 1. Holotype male (note gaps in distribution of trunk spines). 

2. Reproductive system of holotype male. 3. Proboscis of a paratype female (note 3 giant nuclei in apical 

organ). 4. One row of proboscis hooks from proboscis in Fig. 3. 5. Anterior end of a paratype female 

(note gaps in the distribution of collar and trunk spines). 6. Reproductive system of allotype female (note 

balloon-shaped vaginal gland and unripe egg). 7-8. Side and en face views of trunk spines from paratype 

in Fig. 5. 



Figure 9. Pallisentis vietnamensis sp. n. Anterior 

end of trunk of paratype female in Fig. 5, showing 

clear line of demarcation between the naked anterior 

end of the trunk and the very short neck at the 

base of the proboscis. 

TYPE LOCALITY: Lakes and Red River near 

Hanoi, Vietnam. 

SPECIMENS DEPOSITED: USNPC No. 88635 

(holotype male); No. 88636 (allotype female); 

No. 88637 (paratypes). 

ETYMOLOGY: The new species is named for 

its geographical location in Vietnam. 

Remarks 

The identification of P. vietnamensis sp. n. as 

P. ophiocephali by Moravec and Sey (1989) 

overlooked the difference in proboscis hook size 

(these species belong to 2 different subgenera) 

and the fact that trunk spines of the latter species 

extend to the posterior ends of individuals of 

both sexes. Specimens believed to be conspecific 

with the new species by Moravec and Sey 

(1989) were previously reported by Ha (1969) 

from O. maculatus. 

Of the 26 species of Pallisentis recognized as 

valid, P. vietnamensis sp. n. has the largest number 

of trunk spine circles in males (57-88) and 

females (120-149). The largest number of trunk 


spine circles in other species are 52 in P. ophiocephali 

males, 30-66 in P. nagpurensis males 

and females, and 28-32 and 36-76 in P. garuei 

males and females, repectively. The new species 

also has giant nuclei in the apical organ of the 

proboscis, a feature not reported in any other 

species of Pallisentis (Fig. 3). The female reproductive 

system is similar to that of P. colisai 

except that the uterus in the latter species is considerably 

longer. 

The reference to Pallisentis sp. from threadfin 

shad, Dorosoma petenense (Giinther, 1867), in 

Louisiana, U.S.A. by Arnold et al. (1968) is 

clearly in error, since Pallisentis occurs only in 

Asia. 

Further differentiation between P. vietnamensis 

and the other 25 species of the genus Pallisentis 

is presented in the following key. 

Key to Species of the Genus Pallisentis 

sensu lato 

1. Proboscis hooks in second or third circle 

declining abruptly in size; cement gland 

usually small, with few giant nuclei ... 2 

Proboscis hooks gradually declining in 

size posteriorly; cement glands usually 

long, with many giant nuclei 

Subgenus Pallisentis subgen. n. 12 

2. Proboscis hooks in second circle about half 

as long as hooks in first circle 

.. Subgenus Demidueterospinus subgen. n. 3 

Proboscis hooks in third circle about half 

as long as hooks in second circle 

Subgenus Brevitritospinus subgen. n. 5 

3. Trunk spines conical and extending to posterior 

end of males and females; Saefftigen's 

pouch absent Pallisentis (D.) 

ophiocephali (Thapar, 1931) Baylis, 1933 

Trunk spines Y-shaped not extending to 

posterior end of males; Saefftigen's 

pouch present 4 

4. Proboscis hooks in first circle 70-80 

long; hook roots recurved, simple; lemnisci 

equal; testes equatorial, 580-620 

(anterior) and 510-560 (posterior) 

long; cement gland 470—630 long; 

Saefftigen's pouch 320-390 long; female 

gonopore terminal 

Pallisentis (D.) panadei Rai, 1967 

Proboscis hooks in first circle 100 long; 

hook roots stubby knobs; lemnisci unequal; 

testes pre-equatorial, 950 (ante-

AMIN ET AL.—REVISION OF THE GENUS PALL1SENTIS 47 

Table 2. Morphometric characteristics of Pallisentis (B.) vietnamensis (measurements are in micrometers 

unless otherwise noted). 

Males 

Trunk (mm) 

Hypodermal/nuclei 

Proboscis 

First circle hooks 

Second circle hooks 

Third circle hooks 

Fourth circle hooks 

Neck 

Proboscis receptacle 

Brain 

Anterior spineless area 

Lemniscus 

Long (mm) 

Short (mm) 

Collar spines 

Circles/no, per circle 

Length 

Trunk spines 


Length 

Anterior testis 

Posterior testis 

Cement gland 

No. nuclei 

Cement reservoir 

Cement duct 

Bursa 

Females 

Trunk (mm) 

Subcuticular nuclei 

Proboscis 

First circle hooks 

Second circle hooks 

Third circle hooks 

Fourth circle hooks 

Neck 

Proboscis receptacle 

Brain 

Anterior spineless area 

Lemniscus 

Long (mm) 

Short (mm) 

Collar spines 


Length 

Trunk spines 


Length 

Reproductive system 

Gonopore 

Eggs 

* NG = not given. 

t Range (mean). 

Moravec and Sey (1989) 

(9 males, 5 females) 

6.74-14.6 X 0.408-0.503 

NG* 

163-177 X 204-245 

81-84 

72-75 

36-42 

30 

NG 

340-517 X NG 

NG 

272-367 X 177-204 (called neck) 

1.06-1.90 X NG 

Only 1 measurement given 

18-21/20-22 

27-30 

Extend to testes 

57-86/NG 

21-30 

449_767 X 218-313 

449-721 X 218-313 

NG (550 X 180, Fig. 2C) 

8 

NG (370 X 180, Fig. 2C) 

NG (400, Fig. 2C) 

NG X 258 

14.42-20.54 X 0.54-0.57 

NG 

177_204 X 218-258 

87-99 

75-94 

39 

30 

NG 

NG 

NG 

258-422 X 190-218 (called "neck") 

NG 

NG 

21/22-24 

24-30 

Extend to posterior end 

120/NG 

24-30 

NG (Fig. 21 of another species) 

Subterminal 

75-84 X 30-33 (ripe) 

50 X 25 (Fig. 2J) 

Present paper 

(4 males, 5 females) 

7.04-14.20 (9.03) X 0.29-0.42 (0.37)t 

3 (apical organ), 0-5 (anterior), 3-4 (posterior) 

130-145 (135) X 167-187 (178) 

80-88 (85) 

75 (75) 

32-38 (35) 

25-28 (26) 

22-32 (29) X 112-135 (123) 

458-728 (855) X 146-156 (152) 

100-137 (120) X 50-75 (64) 

187-312 (236) X 135-156 (146) 

2.49 X 0.04-0.06 

1.87 X 0.03-0.05 

20-21/10-22 

17-25 (21) (anterior), 20-32 (26) (posterior) 

Extend to testes 

75-88 (82)/l-16 


406-988 (616) X 146-198 (161) 

333-551 (424) X 125-166 (148) 

395-728 (504) X 94-156 (119) 

7-8 (usually 8) 

187-499 (304) X 83-187 (117) 

364-572 (455) 

238 X 135 (n = 1) 

11.02-19.40 (15.81) X 0.32-0.47 (0.38) 

3 (apical organ), 0-2 (anterior), 1-3 (posterior) 

142-175 (156) X 177-210 (197) 

75-95 (85) 

70-87 (77) 

33-45 (38) 

25-32 (28) 

25-32 (28) X 130-145 (135) 

655-728 (699) X 135-187 (168) 

125-150 (135) X 45-80 (61) 

228-260 (239) X 146-187 (169) 

2.08-2.67(2.50) X 0.04-0.07 (0.05) 

1.56-2.50 (2.13) X 0.04-0.06 (0.05) 


19-22/6-23 


Extend to posterior end 

125-149 (138)/1-17 


364-458 (410) 

Subterminal 

42-57 (50) X 18-22 (20) (unripe)


rior) and 700 (posterior) long; cement 

gland 900 long; Saefftigen's pouch 770 

long; female gonopore subterminal 

Pallisentis (D.) basiri Farooqi, 1958 

5. Trunk spines conical 6 

Trunk spines Y-shaped 9 

6. Trunk spines in many circles, 57-88 in 

males and 120-149 in females; Saefftigen's 

pouch absent Pallisentis 

(B.) vietnamensis sp. n. 

Trunk spines in fewer circles, up to 27 in 

males and 36 in females; Saefftigen's 

pouch present 7 

7. Trunk small, up to 2.0 mm long in males 

and 4.5 mm long in females; proboscis 

hooks in anterior 2 circles similar in size; 

trunk with 14-18 circles of spines each 

with 17—24 spines; cement gland less 

than 200 long Pallisentis (B.) guntei 

Sahay, Nath, and Sinha 1967 

Trunk larger, 3.4-6.9 mm long in males 

and 7.3—15.6 mm long in females; proboscis 

hooks in second circle slightly 

smaller that hooks in first circle; trunk 

with 20-27 circles of spines each with 

up to 12 spines; cement gland 400-973 

long 8 

8. Female gonopore terminal; length of testes 

733-910 (anterior), 785-925 (posterior); 

cement gland 863-973, and cement reservoir 

580-816 Pallisentis (B.) 

croftoni Mital and Lai, 1981 

Female gonopore subterminal; length of 

testes 475 (anterior), 437 (posterior), 

cement gland 400, and cement reservoir 

361 Pallisentis (B.) allahabadi 

Agarwal, 1958 

9. Trunk spines extending to posterior end 

of males and females; proboscis hooks 

10—12 per circle; hooks in anterior circle 

larger than 100 Pallisentis (B.) 

mehrai Gupta and Fatma, 1986 

Trunk spines not extending to posterior 

end of males or females; proboscis 

hooks 6-10 per circle; hooks in anterior 

circle shorter than 100 10 

10. Females less than 4.0 mm long; lemnisci 

ending well above anterior testis, testis 

small, up to 225 (anterior) and 200 

(posterior) long; cement gland small, 

200-230 long, with 6-8 giant nuclei 

Pallisentis (B.) cavasii Gupta and 

Verma, 1980 


Females longer than 4.0 mm long; lemnisci 

may reach anterior testis; testes 

between 200 and 910 long; cement 

glands between 172 and 926 long, with 

10—18 giant nuclei each 11 

11. Proboscis hooks 10 per circle; female proboscis 

receptacle more than 700 mm 

long; lemnisci ending well above anterior 

testis Pallisentis (B.) indica 

Mital and Lai, 1981 

Proboscis hooks 6-10 per circle; female 

proboscis receptacle less than 400 long; 

lemnisci extending to mid-anterior testis 

Pallisentis (B.) fasciata 

Gupta and Verma, 1980 

12. Trunk spines conical or Y-shaped, extending 

to posterior end of at least 1 

sex 13 

Trunk spines only conical, not extending 

to posterior end of either sex 16 

13. Trunk spines conical, extending to posterior 

end in females only; testes postequatorial 

14 

Trunk spines conical or Y-shaped, extending 

to posterior end of both males 

and females; testes equatorial 15 

14. Proboscis hooks in first circle less than 

100 long; proboscis receptacle less than 

500 long; cement gland with 20—30 giant 

nuclei; female gonopore subterminal 

Pallisentis (P.) nagpurensis 

(Bhalero, 1931) Baylis, 1933 

Proboscis hooks in first circle 100 or 

more long; proboscis receptacle more 

than 800 long; cement gland with 9-16 

giant nuclei; female gonopore terminal 

Pallisentis (P.) clupei 

Gupta and Gupta, 1979 

15. Trunk spines conical, in 28-32 circles in 

males and 36-76 circles in females; 

neck separated from proboscis by transverse 

circular muscle band; cement 

gland longer than 1.6 mm Pallisentis 

(P.) garuei (Sahay, Sinha and Ghosh, 

1971) Jain and Gupta, 1979 

Trunk spines Y-shaped, in 16-20 circles 

in males and 25-30 circles in females; 

no muscle band between neck and proboscis; 

cement gland less than 0.6 mm 

long Pallisentis (P.) guptai 

Gupta and Fatma, 1986 

16. Males with Saefftigen's pouch 17 

Males lacking Saefftigen's pouch 21

17. Trunk spines appearing continuous with 

collar spines Pallisentis (P.) magnum 

Saeed and Bilqees, 1971 

Trunk spines well separated from collar 

spines 18 

18. Proboscis hooks 10 per circle, each embedded 

in thickened cuticular rim; 

trunk spines with cuticular comblike 

thickening; males with additional circles 

of posttesticular trunk spines; testes 

preequatorial Pallisentis 

(P.) kalriai Khan and Bilqees, 1985 

Proboscis hooks 8-10 per circle; no cuticular 

thickening at base of proboscis 

hooks or trunk spines; no posttesticular 

trunk spines; testes not preequatorial 19 

19. Female trunk spines in 36-73 circles, extending 

to just anterior to posterior end; 

lemnisci unequal; testes small, less 

than 0.5 mm long Pallisentis 

(P.) gomtii Gupta and Verma, 1980 

Female trunk spines in 10-20 circles, extending 

only to anterior third of trunk; 

lemnisci equal; testes large, more than 

1.0 mm long 20 

20. Proboscis hooks 8 per circle; testes equatorial; 

cement gland 2.2-3.0 mm long 

Pallisentis (P.) sindensis Khan and 

Bilqees, 1987 

Proboscis hooks 10 per circle; testes 

postequatorial; cement gland short, 

0.7—1.6 long Pallisentis (P.) gaboes 

(MacCallum, 1918) Van Cleave, 1928 

21. Proboscis hooks 6-7 per circle 22 

Proboscis hooks 8-12 per circle 23 

22. Proboscis hooks 6 per circle; anterior 

hooks 89-119 long; cement gland with 

16 giant nuclei Pallisentis 

(P.) umbellatus Van Cleave, 1928 

Proboscis hooks 7 per circle; anterior 

hooks 60-70 long; cement gland with 

10—12 nuclei Pallisentis pesteri 

(Tadros, 1966) Showhan, Gupta, 

and Khera, 1987 

23. Cement gland with 12-14 giant nuclei; 

lemnisci equal 24 

Cement gland with 23-25 giant nuclei; 

lemnisci unequal 25 

24. Proboscis hooks 8 per circle; collar 

spines in 6-7 circles each with 29—40 

spines; trunk spines in 8—13 circles 

each with 30—41 spines with sclerotized, 

large, variably shaped beds; tes- 


tes longer than 0.7 mm Pallisentis 

(P.) celatus Van Cleave, 1928 

Proboscis hooks 10—12 per circle; collar 

spines in 15-17 circles each with 18- 

20 spines; trunk spines in 21-22 

(males), 67 (females) circles each with 

16-20 simple triangular spines; testes 

0.28-0.42 long 

- Pallisentis (P.) colisai Sakkar, 1954 

25. Proboscis hooks 93, 80, 60, 33 long 

(from anterior); trunk spines in 44-55 

circles, each with 16-20 spines; female 

gonopore posteroventral 

Pallisentis (P.) nandai Sarkar, 1953 

Proboscis hooks 62-64, 49-54, 36-46, 

24-28 long (from anterior); trunk 

spines in 25-26 circles, each with 10 

spines; female gonopore terminal 

Pallisentis (P.) singaporensis Khan 

and Ip, 1988 


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pp.



Two New Species of Popovastrongylus Mawson, 1977 (Nematoda: 

Cloacinidae) from Macropodid Marsupials in Australia 

L. R. SMALES 

School of Biological and Environmental Sciences, Central Queensland University, Rockhampton, 

Queensland 4702, Australia (e-mail: l.warner@cqu.edu.au) 

ABSTRACT: The cephalic anatomy of Popovastrongylus wallabiae (Johnson and Mawson) is described, giving 

additional morphological details. New species of Popovastrongylus (Nematoda: Cloacinidae: Cloacininae) are 

described. Popovastrongylus tasmaniensis sp. n. from Thylogale billardierii (Desmarest) from Tasmania, Australia, 

has an oval mouth opening and buccal capsule, and the intestinal wall extends anteriorly to surround the 

esophageal bulb. Popovastrongylus pluteus sp. n. from Macropus robust us Gould from New South Wales, 

Australia, is similar to Popovastrongylus pearsoni (Johnson and Mawson) in having, among other characters, a 

shelf-like projection in the buccal capsule. It differs from P. pearsoni in having a circular mouth opening and 

buccal capsule rather than a quadrangular mouth opening and slightly oval buccal capsule. Species of Popovastrongylus 

infect mainly pademelons, Thylogale spp., and the smaller wallabies, Macropus rufogriseus Desmarest, 

Macropus irma (Desmarest), and Macropus eugenii (Desmarest). It also occurs in the larger kangaroos, 

Macropus rufus (Desmarest), Macropus giganteus Shaw, and M. robustus, in northern Australia where it is 

uncommon. In southern Australia the only kangaroo hosts known are Macropus fuliginosus (Desmarest) on 

Kangaroo Island, off the shore of South Australia, M. robustus in New South Wales, and an accidental infection 

of M. robustus in the Australian Capital Territory. 

KEY WORDS: Nematoda, marsupials, macropodids, Popovastrongylus wallabiae, Popovastrongylus tasmaniensis 

sp. n., Popovastrongylus pluteus sp. n., Macropus robustus, Thylogale billardierii, taxonomy, Australia. 

More than 40 genera of the strongylid family 

Cloacinidae (Stossich, 1899) are found in the 

large herbivorous marsupials, kangaroos, wallabies, 

and wombats of Australia, Irian Jaya, and 

Papua New Guinea (Beveridge, 1987). Popovastrongylus 

Mawson, 1977, was erected to contain 

those species occurring in the stomachs of 

macropodid marsupials (kangaroos and wallabies) 

that had, among other characters, 4 submedian 

papillae and 2 amphids borne on a cephalic 

collar, a circular to oval mouth opening, 

and a cylindrical to oval buccal capsule with a 

thick transparent inner layer that may form a 

shelf-like structure in the lumen. Mawson 

(1977) included 3 species, Popovastrongylus 

wallabiae (Johnston and Mawson, 1939), the 

type species, Popovastrongylus pearsoni (Johnston 

and Mawson, 1940), and Popovastrongylus 

irma Mawson, 1977, in the new genus. Subsequently 

Beveridge (1986) revised the group, expanding 

the generic definition to encompass a 

quadrilateral, triangular, or small and triradiate 

mouth opening and to include a labial collar, internal 

to the cephalic collar, the buccal capsule 

sclerotized, often with annular thickening, and 

the lining inflated and/or forming a shelf. He 

redescribed P. pearsoni, indicating additional 

features not given in the earlier descriptions by 

51 

Johnston and Mawson (1939) and Mawson 

(1971, 1977) and described 2 new species, Popovastrongylus 

macropodis Beveridge, 1986, 

and Popovastrongylus thylogale Beveridge, 

1986. 

Known hosts for species of Popovastrongylus 

are Macropus rufogriseus (Desmarest, 1817) 

(the red-necked wallaby); Macropus fuliginosus 

(Desmarest, 1817) (the western grey kangaroo); 

Macropus eugenii (Desmarest, 1817) (the tammar 

wallaby); Macropus irma (Jourdan, 1837) 

(the western brush wallaby); Macropus rufus 

(Desmarest, 1822) (the red kangaroo); Macropus 

giganteus Shaw, 1790 (the eastern grey kangaroo); 

Macropus robustus Gould, 1841 (the common 

wallaroo); Thylogale stigmatica Gould, 

1860 (the red-legged pademelon); Thylogale 

brunii (Schreber, 1778) (the dusky pademelon); 

Thylogale thetis (Lesson, 1827) (the red-necked 

pademelon); and Petrogale persephone Maynes, 

1982 (the Proserpine rock-wallaby). 

Collections of material from M. robustus and 

Thylogale billardierii (Desmarest, 1822) in the 

South Australian Museum, Adelaide (SAMA), 

were found to have 2 new species of Popovastrongylus, 

which are described in this paper. 

The cephalic anatomy of P. wallabiae, examined 

for comparative puiposes, is also described in 

greater detail than previously given. 




No details of hosts, beyond those given below, are 

known, and there is no record of host bodies having 

been deposited in any museum. All the parasite material 

studied had been deposited in the SAMA. Its 

preservation history is not known, but probably it was 

fixed in 5%—10% formalin before being stored in 70% 

ethanol. Specimens were cleared for study in temporary 

wet mounts in lactophcnol prior to examination 

with the aid of interference contrast light microscopy. 

Measurements were made with the aid of an ocular 

micrometer or drawing tube and map measurer. Unless 

otherwise stated, measurements are given in micrometers 

as a range followed by the mean in parentheses. 

Drawings were prepared with the aid of a drawing 

tube. Terminology used follows that of Beveridge 

(1986). 

Results 

Popovastrongylus wallabiae (Johnston and 

Mawson, 1939) Mawson, 1977 

(Figs. 1-6) 

SYNONYMS: Macropostrongylus wallabiae 

Johnson and Mawson, 1939; Gelanostrongylus 

wallabiae Popova, 1952. 

GENERAL: Cloacinidae: Cloacininae. With 

characters of the genus Popovastrongylus as described 

by Johnston and Mawson (1939) and 

Mawson (1977) and redefined by Beveridge 

(1986). Comparative measurements of specimens 

from New South Wales and Tasmania are 

given in Table 1. 

DESCRIPTION OF CEPHALIC END: Mouth opening 

quadrangular in apical view, surrounded by 

elevated, finely striated labial collar, indented at 

corners on external margin by submedian papillae; 

amphids on lateral projections external to 

labial collar; submedian papillae each with 2 

short, medially directed setae; cephalic collar 

present posterior to labial collar, bearing papillae 

and amphids. Buccal capsule approximately cylindrical, 

longer than wide, thickened anteriorly; 

internal lining of buccal capsule thick, transparent, 

almost occluding lumen anteriorly but not 

forming shelf-like projection; outer wall of buccal 

capsule sclerotized, refractile, thickened in 

mid region, nonstriated; buccal capsule circular 

in cross section. 

TYPE SPECIMENS: Holotype male, allotype female, 

SAMA AHC V2832. 

TYPE HOST: Macropus rufogriseus (Desmarest, 

1817). 

SITE OF INFECTION: Stomach. 

LOCALITY: Bathurst District, New South 

Wales. 

SPECIMENS STUDIED: Types from M. rufogriseus: 

Southern Queensland: 3 female, 1 male, no 

other collection data, SAMA AHC 6004; from 

Tasmania: 3 male, 2 female from Launceston, 18 

April 1973, SAMA AHC 6006; 3 male, 1 female 

from Pipers River, collector D. Obendorf 26 January 

1982, SAMA AHC 16410. 

REMARKS: This species was clearly differentiated 

from P. pearsoni, the other species of 

Popovastrongylus occurring in M. rufogriseus, 

by Mawson (1977). Furthermore, Beveridge 

(1986, pp. 263-264, Fig. 3A, B), in his redescription 

of the cephalic end of P. pearsoni, noted 

and figured a shelf-like projection of the inner 

lining of the buccal capsule. Mawson (1977) described 

a narrow shelf toward the anterior end 

of the buccal capsule of the type, but not other 

specimens of P. wallabiae. Careful examination 

of specimens of P. wallabiae in this study has 

shown that a shelf-like projection is not present, 

but the inner lining of the buccal capsule is 

thickest at the anterior end. 

Mawson (1977) listed Macropostrongylus 

wallabiae Johnston and Mawson, 1939 p. 526 

from Wallabia bicolor Desmarest, 1804, as a 

synonym of P. wallabiae. This is in error, as M. 

wallabiae was described by Johnston and Mawson 

(1939) from Macropus ruficollis (=M. rufogriseus). 

The material from Macropus ualabatus 

( = W. bicolor), originally described as Macropostrongylus 

dissimilis Johnston and Mawson, 

1939, was subsequently identified as 

Arundelia dissimilis (Johnston and Mawson, 

1939) by Mawson (1977). Wallabia bicolor 

therefore is not a host for P. wallabiae. 

Popovastrongylus tasmaniensis sp. n. 

(Figs. 7-21) 

Description 


GENERAL DESCRIPTION: Small worms, body 

covered with numerous fine transverse striations; 

mouth opening oval; surrounded by elevated, 

finely striated collar, indented on external margin; 

cephalic collar present, posterior to labial 

collar, bearing 2 amphids and 4 cephalic papillae, 

each with 2 prominent setae. Buccal capsule 

cylindrical, oval in cross-section, slightly longer 

than wide; walls sclerotized, refractile internal 

lining thick, transparent, expanded anteriorly. 

Esophageal corpus long, cylindrical; isthmus 

short; bulb ovoid; deirids anterior to nerve ring, 

excretory pore in mid-esophageal position, pos-

SMALES—POPOVASTRONGYLUS FROM MARSUPIALS 53 

Figures 1-8. Popovastrongylus wallabiae from Macropus rufogriseus. 1. Cephalic end, optical section 

(ventral view). 2. Cephalic end, optical section (lateral view). 3. Cephalic collar (lateral view). 4. Cephalic 

collar (ventral view). 5. Mouth opening (apical view). 6. Buccal capsule, optical transverse section showing 

thickened internal lining. 7, 8. Popovastrongylus tasmaniensis sp. n. from Thylogale billardierii. 1. Ovejector 

(lateral view). 8. Female tail (lateral view). Scale bars: Figures 1-4 = 25 urn; Figures 5, 6 = 10 u.m; 

Figure 7 = 50 (xm; Figure 8 = 200 u.m. 

terior to nerve ring. Intestinal wall extending anteriorly, 

surrounding esophageal bulb. 

MALES (measurements of 10 specimens): 

Length 6.5-9.0 (7.5) mm; width 310-460 (385); 

buccal capsule 50-60 (53) long by 23-43 (38) 

wide; esophagus 1.04-1.75 (1.61) mm long; 

nerve ring 535-740 (655), deirids 210-300 

(265), excretory pore 690-920 (800) from anterior 

end; spicules 1.16-1.45 (1.33) mm. Dorsal 

and lateral lobes of bursa about equal in length; 

ventral lobes shorter. Ventral rays apposed, 

reaching margin of bursa; externolateral ray divergent, 

shorter, almost reaching margin of bursa; 

mediolateral and posterolateral rays apposed, 

reaching margin of bursa; externodorsal ray arising 

close to lateral trunk, not reaching margin of 

bursa; dorsal ray long, slender at origin, dividing 

at midlength into 2 arcuate branches that reach 

margin of bursa; lateral branchlets short, arising 

soon after bifurcation, terminating in small ele- 


Table 1. Comparative measurements (mm) of Popovastrongylus wallabiae from Macropus rufogiseus 

Mawson, 1939), and from Launceston and Pipers River, Tasmania. 

New South Wales 

Female 

Male 

(« = 5) 

6.0-9.5 (7.7) 

0.22-0.40 (0.33) 

Male 

11.4 

— 

8.4 

— 

0.025-0.045 

0.80 

Popovastrongylus tasmaniensis sp. n. is readily 

distinguished from its congeners by its oval 

mouth opening and buccal capsule, in having the 

intestinal wall extending anteriorly to surround 

the esophageal bulb, and spicules longer than 

1150 (Jim. Popovastrongylus pearsoni, which 

also occurs in M. rufogriseus from Tasmania 

(Mawson, 1977), has a distinct shelf-like projec- 

0.025-0.03 (0.025) X 0.048-0 

1.00-1.09 (1.04) 

0.23-0.33 (0.27) 

0.40-0.48 (0.44) 

0.48-0.64 (0.56) 

0.84-0.97 (0.92) 

— 

— 

— 

— 

— 

— 

— 

— 

— 

0.80 

0.30 

— 

0.25 

— 

— 

0.80 

— 

— 

— 

Remarks 

TYPE SPECIMENS: Holotype male SAMA 

AHC 31310; allotype female SAMA AHC 

31311; paratypes 5 male, 10 female SAMA 

AHC 19844. 

TYPE HOST: Thylogale billardierii (Desmarest, 

1822). 

TYPE LOCALITY: Launceston, Tasmania. 


SPECIMENS STUDIED: Types from T. billardierii, 

from Tasmania; 10 male, 14 female from 

Launceston, collectors D. Obendorf, I. B everidge, 

20 February 1990, 18 November 1991, 

SAMA AHC 19844, AHC 19791, AHC 26578; 

3 male, 4 female from Piper's River, collector 

D. Obendorf, 26 January 1983, SAMA AHC 

16373, AHC 31312; 1 female from Georgetown, 

collector D. Obendorf, 28 June 1982, SAMA 

AHC 16398; 2 female from Golconda, collector 

I. Beveridge, April 1977, SAMA AHC 13925. 

ETYMOLOGY: The name of the new species 

refers to its type locality. 

— 0.13 X 0.07 — 

Length 

Width 

Buccal capsule: 

Width X depth 

Esophagus 

Deirids 

Nerve ring 

Excretory pore (from anterior end) 

Spicules 

Vulva to posterior 

Tail 

Vagina 

Eggs 

I t!J j 


vations on internal surface of bursa. Anterior lip

tion in a circular buccal capsule. The nerve ring 

is in the mid-esophageal position in P. tasmaniensis 

but is posterior and surrounds the isthmus 

in P. pearsoni. Popovastrongylus wallabiae, the 

other species occuring in Tasmania (Mawson, 

1977), has a quadrangular mouth opening and a 

buccal capsule circular in cross-section. The 

submedian papillae of P. wallabiae are short, 

and the setae are not easily seen at low magnifications, 

while P. tasmaniensis has prominent 

papillae and setae. The dorsal lobe of the bursa 

of P. tasmaniensis is shorter (about the same 

length as the lateral lobes), not longer than the 

lateral lobes as in P. wallabiae. Additional characters 

that distinguish P. tasmaniensis from P. 

irma are not having the base of the buccal capsule 

thickened by an outer sclerotized ring and 

having the nerve ring in a mid-esophageal, not 

posterior, position surrounding the isthmus. The 

shape of the posterior end of the female of P. 

irma, constricted between vulva and anus and 

markedly swollen in the vaginal region, is 

unique to P. irma. 

Popovastrongylus thylogale, also occurring in 

pademelons, can be further distinguished from 

P. tasmaniensis by an annular thickening around 

the middle of the buccal capsule, the posterior 

position of the nerve ring, and the dorsal lobe 

longer than the lateral lobes of the bursa. 

Popovastrongylus tasmaniensis differs further 

from P. macropodis in having a relatively thinner 

inflation of the lining of the buccal capsule, 

which is expanded anteriorly but does not almost 

occlude the lumen as in P. macropodis. 

Popovastrongylus pluteus sp. n. 

(Figs. 22-31) 

Description 

GENERAL DESCRIPTION: Small worms; body 

covered with numerous fine transverse striations; 

mouth opening circular, surrounded by elevated, 

finely striated collar indented on external margin; 

cephalic collar present, posterior to lateral 

collar bearing 2 amphids and 4 cephalic papillae 

each with 2 setae. Buccal capsule cylindrical, 

circular in cross-section, longer than wide; walls 

sclerotized, refractile, thickened in posterior 

part; inner lining thick, transparent, folded in 

mid-region to produce irregular shelf-like projection, 

almost occluding lumen. Esophageal 

corpus long, isthmus not distinct, bulb ovoid. 

MALES (measurements of 2 specimens): 


Length 5, 6 mm; width 240, 290; buccal capsule 

33, 46 long by 26, 26 wide; esophagus 0.985, 

1.01 mm long; nerve ring to anterior end 402, 

402; deirids to anterior end 135, excretory pore 

to anterior end 470, 455. Spicules 950. Dorsal 

and lateral lobes of bursa about equal in length, 

ventral lobes shorter. Ventral rays apposed, 

reaching margin of bursa; externolateral ray divergent, 

almost reaching margin of bursa; mediolateral 

and posterolateral rays apposed, reaching 

margin of bursa; externodorsal ray arising 

close to lateral trunk, almost reaching margin of 

bursa; dorsal ray dividing at midlength into 2 

arcuate branches that reach margin of bursa, lateral 

branchlets short, arising close to bifurcation; 

terminating in small elevations on internal surface 

of bursa. Anterior lip of genital cone large 

and conical, with single apical papilla; posterior 

lip smaller, with 2 bilobed appendages. Spicules 

elongate, alate, tips not seen. Gubernaculum absent. 

FEMALES (measurements of 10 specimens): 

Length 7-8 (7.4) mm; width 255-375 (305); 

buccal capsule 35-50 (40) long by 22-30 (26) 

wide; esophagus 1.02-1.14 (1.08) mm long; 

nerve ring 345-390 (370), deirids 105-140 

(125), excretory pore 400-475 (435) from anterior 

end; tail 470-585 (530) long, vulva to 

posterior end 705-885 (790); vagina 400-595 

(505); eggs 95-105 (100) by 42-52 (45). Tail 

long, slender with conical tip; vulva immediately 

anterior to anus; vagina short, broad at anterior 

end, ovejector with vestibule and sphincters 

about same length, infundibula shorter; eggs ellipsoidal. 

Taxonomic Summary 

TYPE SPECIMENS: Holotype male SAM A AHC 

31253, allotype female AHC 31324, paratypes 3 

female, 1 male AHC 14546. 

TYPE HOST: Macropus robustus Gould, 1841. 

TYPE LOCALITY: Rivertree, New South Wales. 


SPECIMENS STUDIED: Types from M. robustus, 

New South Wales; 17 female from Rivertree, 

28 August 1975, SAMA AHC 31252. 

ETYMOLOGY: The specific name refers to the 

shelf-like projection in the buccal capsule. 

Remarks 

Popovastrongylus pluteus sp. n. is 1 of 2 species 

with a shelf-like projection in the buccal 

capsule, the other being P. pearsoni. Popova- 




strongylus pluteus differs from P. pearsoni in 

the shape of the mouth opening, circular not 

quadrangular in apical view; the buccal capsule 

circular in cross section rather than slightly oval; 

and the amphids not on extremely prominent lateral 

projections. The nerve ring and excretory 

pore of P. pearsoni are more posterior (Mawson, 

1977, Fig. 31, p. 57), with the nerve ring surrounding 

the junction of the isthmus and corpus 

of the esophagus, than in P. pluteus, which has 

the nerve ring and excretory pore in the midesophageal 

region. The branchlets of the dorsal 

ray of P. pluteus arise closer to its bifurcation 

than do those of P. pearsoni. 

Popovastrongylus pluteus is similar in general 

features to P. wallabiae but differs in the features 

of the cephalic end, particularly in the form 

of the inner lining of the buccal capsule. Popovastrongylus 

wallabiae does not have an internal 

shelf, and the shape of the mouth opening is 

circular, not quadrangular. The deirids, nerve 

ring, and excretory pore of P. pluteus, although 

located in the mid-region of the esophagus, are 

each more anterior than their counterparts on P. 

wallabiae (135, 402, and 463 compared with 

270, 440, and 560, respectively, for males). The 

dorsal lobe of the bursa of P. pluteus is about 

the same length as the lateral lobes, but in P. 

wallabiae it is longer. The vagina of P. wallabiae 

(370-400) is shorter and its eggs (95-105 

by 42-52) are smaller (135 by 70) than in P. 

pluteus. 

Popovastrongylus pluteus can be distinguished 

from P. macropodis, which also occurs 

in M. robustus, by the presence of a shelf in the 

buccal capsule and in having a circular, not triangular 

mouth opening. The buccal capsule is 

more slender than that of P. macopodis (40 X 

26 compared with 37 X 30), and the inner lining 

is not as inflated as that of P. macropodis. The 

vagina is longer (400-595) in P. pluteus, compared 

with 360—400 in P. macropodis. 

SMALES—POPOVASTRONCYLUS FROM MARSUPIALS 57 

Discussion 

This study has increased the number of 

known hosts of Popovastrongylus to include T. 

billardierii and extended the known distribution 

of the genus to include New South Wales. Of 

the 2 new species, P. tasmaniensis has been 

found only in T. billardierii, the Tasmanian pademelon, 

from Tasmanian localities, and P. pluteus 

only in M. robustus, the common wallaroo 

from New South Wales. 

Of the previously known species, P. macropodis 

is found in wallaroos as well as the other 

large kangaroos, M. rufus and M. giganteus, the 

red and eastern grey kangaroos, but only in 

northern Queensland (Beveridge, 1986; Arundel 

et al., 1979, 1990). Popovastrongylus thylogale, 

also found in pademelons, has a distribution limited 

to T. stigmatica, the red-legged pademelon, 

and T. thetis, the red-necked pademelon in 

Queensland. There is a single report of an accidental 

infection of P. thylogale from a captive 

agile wallaby, Macropus agilis (Gould, 1842) 

(Spratt et al., 1991). Popovastrongylus thylogale 

does not, however, occur in free-ranging agile 

wallabies (Speare et al., 1983). Other northern 

hosts of this parasite are P. persephone, the 

Proserpine rock-wallaby, a host that harbors several 

nematode species that normally occur in pademelons 

and are not normally found in other 

species of rock-wallaby (Begg et al., 1995; Beveridge, 

1986), and T. brunii, the dusky pademelon, 

found only in Papua New Guinea. This 

latter occurrence emphasizes the northern distribution 

of P. thylogale as it has been found in 

neither the red-legged pademelon nor the rednecked 

pademelon in New South Wales (Beveridge, 

1986; Smales, 1997). 

Popovastrongylus wallabiae occurs only in 

the red-necked wallaby, M. rufogriseus, and is 

the most widely distributed species of the genus, 

being found in southern Queensland and Tasmania 

(Mawson, 1977). It has not been reported 

Figures 9-21. Popovastrongylus tasmaniensis sp. n. from Thylogale billardierii. 9. Anterior end (ventral 

view). 10. Cephalic end, optical section (lateral view). 11. Cephalic end, optical section (ventral view). 12. 

Buccal capsule, transverse optical section, at mid-level. 13. Spicule, anterior end (lateral view). 14. Spicule 

tip (lateral view). 15. Cephalic collar (lateral view). 16. Cephalic end (dorsal view). 17. Buccal capsule, 

transverse optical section at posterior level. 18. Genital cone (dorsal view). 19. Mouth opening (en face 

view). 20. Bursa (apical view). 21. Bursa (lateral view). Scale bars: Figure 9 = 200 u.m; Figures 10, 11, 

13-16, 18 = 25 jjim; Figures 12, 17, 19 = 10 |xm; Figures 20, 21 = 50 u.m. 



Figures 22—31. Popovastrongylus pluteus sp. n. from Macropus robustus. 22. Anterior end (lateral view). 

23. Cephalic end, optical section (lateral view). 24. Mouth opening (en face view). 25. Cephalic end, optical 

section (ventral view). 26. Cephalic collar (lateral view). 27. Buccal capsule, transverse optical section at 

level of shelf. 28. Bursa (ventral view). 29. Bursa (lateral view). 30. Ovejector (lateral view). 31. Female 

posterior end (lateral view). Scale bars: Figures 22, 31 = 200 urn; Figures 23, 25, 26 = 25 |xm; Figures 

24, 27 = 10 urn; Figures 28, 29 = 50 (mm; Figure 30 = 100 |xm. 

in red-necked wallabies from New South Wales, 

Victoria, or South Australia. This may be because 

of either a lack of sampling effort (the 

parasite being present but not detected) or a disjunct 

distribution of the parasite. Popovastrongylus 

pearsoni also occurs in red-necked wallabies 

from the same localities in Tasmania as 

P. wallabiae and has only been found on con- 


tinental Australia in a common wallaroo in the 

Tidbinbilla Nature Reserve in the Australian 

Capital Territory. Since the macropod population 

on the reserve includes red-necked wallabies, 

tammars, and species of rock-wallaby, it is 

reasonable to suppose that this record was an 

accidental infection. It does, however, occur in 

3 other hosts, the tammar and western grey kan-

garoo from Kangaroo Island (Smales and Mawson, 

1978; Beveridge, 1986) and Petrogale lateralis 

Gould, 1842, the black-footed wallaby 

from Pearson Island (Johnston and Mawson, 

1940; Mawson, 1971; Beveridge, 1986), both 

southern localities offshore from South Australia. 

Popovastrongylus irma is found only in the 

western brush wallaby in southwestern Australia 

(Mawson, 1977), but in contrast to P. pearsoni 

it has not been reported from sympatric hosts in 

the region. 

In general, species of Popovastrongylus infect 

mainly pademelons and the small wallabies, M. 

irma, M. eugenii, and M. rufogriseus. The genus 

is not common in the larger kangaroos from 

northern Queensland, with only 1 or 2 nematodes 

present in each individual host (Beveridge, 

1986) and does not normally occur in kangaroos 

in the southern states (Beveridge and Arundel, 

1979; Arundel et al., 1979, 1990). Neither is the 

genus found in Wallabia bicolor, the swamp 

wallaby (Beveridge et al., 1985), nor the macropodid 

genera Hypsiprymnodon, Aepyprymnus, 

Onychogalea, Lagorchestes, or Dendrolagus 

(Beveridge et al., 1992). 


My thanks go to Ms. J. Forrest from the South 

Australian Museum for making material available 

and to Dr. I. Beveridge for his unfailing 

help and generosity. 


Arundel, J. H., I. Beveridge, and P. J. Presidente. 

1979. Parasites and pathological findings in enclosed 

and free-ranging populations of Macropus 

rufiis (Desmarest) (Marsupialia) at Menindee, 

New South Wales. Australian Wildlife Research 

6:361-379. 

, K. J. Dempster, K. E. Harrigan, and R. 

Black. 1990. Epidemiological observations on the 

helminth parasites of Macropus giganteus Shaw 

in Victoria. Australian Wildlife Research 17:39- 

51. 

Begg, M., I. Beveridge, N. B. Chilton, P. M. Johnson, 

and M. G. O'Callaghan. 1995. Parasites of 

the Proserpine rock wallaby, Petrogale persepho- 


ne (Marsupialia: Macropodidae). Australian Mammalogy 

18:45-53. 

Beveridge, I. 1986. New species and new records of 

Popovastrongylus Mawson, 1977 (Nematoda: 

Cloacininae) from Australian marsupials. Bulletin 

du Museum National d'Histoire Naturelle, 4th Series 

8:257-265. 

. 1987. The systematic status of Australian 

Strongyloidea. Bulletin du Museum National 

d'Histoire Naturelle, 4th Series 9:107-126. 

, and J. H. Arundel. 1979. Helminth parasites 

of grey kangaroos, Macropus giganteus Shaw and 

M. fuliginosus (Desmarest) in Eastern Australia. 

Australian Wildlife Research 6:69-77. 

, P. J. A. Presidente, and R. Speare. 1985. 

Parasites and associated pathology of the swamp 

wallaby, Wallabia bicolor (Marsupialia). Journal 

of Wildlife Diseases 21:377-385. 

-, R. Speare, P. M. Johnson, and D. M. 

Spratt. 1992. Helminth parasite communities of 

macropodoid marsupials of the genera Hypsiprymnodon, 

Aepyprymnus, Thylogale, Onychogalea, 

Lagorchestes and Dendrolagus from Queensland. 

Wildlife Research 19:359-376. 

Johnston, T. H., and P. M. Mawson. 1939. Strongylate 

nematodes from marsupials in New South 

Wales. Proceedings of the Linnean Society of 

New South Wales 64:513-536. 

, and . 1940. Nematodes from South 

Australia marsupials. Transactions of the Royal 

Society of South Australia 64:95-100. 

Mawson, P. M. 1971. Pearson Island Expedition 

1969. 8. Helminths. Transactions of the Royal Society 

of South Australia 95:169-183. 

. 1977. Revision of the genus Macropostrongylus 

and descriptions of three new genera: Popovastrongylus, 

Dorcopsinema andArundelia (Nematoda: 

Trichonematidae). Transactions of the Royal 


Smales, L. R. 1997. The status of Cyclostrongylus medioannulatus 

Johnston and Mawson, 1940. Transactions 

of the Royal Society of South Australia 

121:165. 

, and P. M. Mawson. 1978. Nematode parasites 

of the Kangaroo Island Wallaby, Macropus 

eugenii (Desmarest). 1. Seasonal and geographic 

distribution. Transactions of the Royal Society of 

South Australia 102:9-16. 

Speare, R., I. Beveridge, P. M. Johnson, and L. A. 

Corner. 1983. Parasites of the agile wallaby Macropus 

agilis (Marsupialia). Australian Wildlife Research 

10:89-96. 

Spratt, D. M., I. Beveridge, and E. L. Walter. 1991. 

A catalogue of Australasian monotremes and marsupials 

and their recorded helminth parasites. Records 

of the South Australian Museum, Monograph 

Series 1:1-105. 




Angiostoma onychodactyla sp. n. (Nematoda: Angiostoniatidae) and 

Other Intestinal Helminths of the Japanese Clawed Salamander, 

Onychodactylus japonicus (Caudata: Hynobiidae), from Japan 

CHARLES R. BURSEY u AND STEPHEN R. GOLDBERG2 

1 Department of Biology, Pennsylvania State University, Shenango Campus, 147 Shenango Avenue, Sharon, 

Pennsylvania 16146, U.S.A. (e-mail: cxbl3@psu.edu) and 

2 Department of Biology, Whittier College, Whittier, California 90608, U.S.A. 

(e-mail: sgoldberg@mail.whittier.edu) 

ABSTRACT: Angiostoma onychodactyla sp. n. from the intestines of the Japanese clawed salamander, Onychodactylus 

japonicus, is described and illustrated. Angiostoma onychodactyla is most similar to Angiostoma plethodontis 

in that lateral alae are absent, and there is a bulb without valves. The major difference between these 2 

species is in the number and position of the caudal papillae. In addition, this sample of O. japonicus harbored 

3 species of trematodes, Cephalouterina leoi, Mesocoelium brevicaecum, and Pseudopolystoma dendriticiun, 1 

species of nematode, Parapharyngodon japonicus, and 1 acanthocephalan species (cystacanth stage). 

KEY WORDS: Angiostoma onychodactyla sp. n., Angiostoniatidae, Japanese clawed salamander, Onychodactylus 

japonicus, Hynobiidae, Japan. 

Onychodactylus japonicus (Houttuyn, 1782), 

the Japanese clawed salamander, is restricted to 

forested mountainous areas of Honshu and Shikoku 

Islands, Japan (Kuzmin, 1995). Previously 

reported helminths of Onychodactylus japonicus 

include the monogenetic trematode Pseudopolystoma 

dendriticum (Ozaki, 1948), the digenetic 

trematodes Cephalouterina leoi Uchida, Uchida, 

and Kamei, 1986, and Mesocoelium brevicaecum 

Ochi, 1930, the cestode Cylindrotaenia sp. 

(=Baerietta sp., larvae only), and the nematodes 

Amphibiocapillaria tritonispunctati (Diesing, 

1851) ( = Capillaria filiformis (Linstow, 1881)), 

Parapharyngodon japonicus Bursey and Goldberg, 

1999; Pseudoxyascaris japonicus Uchida 

and Itagaki, 1979, Pharyngodon sp., and Rhabditis 

sp. (Wilkie, 1930; Pearse, 1932; Ozaki, 

1948; Uchida and Itagaki, 1979; Uchida et al., 

1986; Bursey and Goldberg, 1999). 

Further study of the sample of Onychodactylus 

japonicus examined by Bursey and Goldberg 

(1999) revealed 43 females and 17 males of an 

undescribed species of Angiostoma. To our 

knowledge, there are no reports of species of 

Angiostoma from Japanese salamanders, although 

Wilkie (1930) reported unidentified rhabditids 

from Hynobius retardatus Dunn, 1923, the 

Hokkaido salamander, and O. japonicus collected 

in Yumoto, Fukushima Prefecture. The purpose 

of this paper is to describe a new species 

-1 Corresponding author. 


60 

of nematode, Angiostoma onychodactyla, from 

the salamander Onychodactylus japonicus from 

Japan and to provide a current parasite list for 

this host. 

Material and Methods 

Sixty-eight Onychodactylus japonicus were examined 

(collection data given in Bursey and Goldberg, 

1999). All had been captured by hand and fixed in 

neutral buffered 10% formalin, then preserved in 70% 

alcohol. The body cavity was opened by a longitudinal 

incision from vent to throat, and the gastrointestinal 

tract was removed and opened longitudinally. Nematodes 

were placed in undiluted glycerol, allowed to 

clear, and examined under a light microscope. Trematodes 

were stained in hematoxylin and mounted in 

balsam for study. Measurements are given in micrometers. 

Results 

In addition to the previously described Parapharyngodon 

japonicus and Angiostoma onychodactyla 

described below, 3 species of trematodes 

(Cephalouterina leoi, Mesocoelium brevicaecum, 

Pseudopolystoma dendriticum) and 1 

species of acanthocephalan (unidentified cystacanth) 

were also found. Forty (59%) of 68 salamanders 

were infected with helminths. Prevalence, 

mean intensity, and mean abundance for 

each helminth species are presented in Table 1. 

Angiostoma onychodactyla sp. n. 

(Figs. 1-9) 

Description 

GENERAL: Transparent nematodes lacking 

lateral alae. Cuticle thin, nonstriated. Sexual di-

BURSEY AND GOLDBERG~-/l/VG7aSTOAM ONYCHODACTYLA SP. N. 61 

Table 1. Prevalence, intensity, and abundance of helminths collected from 68 Onychodactylus japonicus. 

Helminth 

Trematoda 

Cephnlouterina leoi 

Mesocoelium brc vicaecum 

Pseudopolystoma dendriticum 

Nematoda 


Parapharyngodon japonicus 

Acanthocephala 

Unidentified cystacanlhs* 

* New host record. 

Prevalence Mean Mean 

(%) intensity ± SD abundance ± SD Site 

3 

5 

1 

24 

38 

morphism not prominent. Oral opening with 3 

lips. Esophagus with corpus, isthmus, and pseudobulb, 

nerve ring at level of anterior isthmus. 

Excretory pore anterior to the esophagointestinal 

junction. 

MALE (holotype and 9 paratypes; mean and 

range): Length 3.36 (2.60-3.90) mm. Maximum 

width 103 (89-128). Buccal cavity 9 (6- 

11) deep. Length of esophagus 297 (251-319), 

corpus 160 (145-175), isthmus 76 (66-88), bulb 

60 (55-68). Nerve ring 192 (188-285) and excretory 

pore 236 (188-285) from anterior end. 

Spicules equal, 128 (120-143), well chitinized, 

arcuate. Gubernaculum well chitinized, 44 (37— 

48). Testis single and reflexed. Caudal alae welldeveloped, 

supported by 8 pairs of postcloacal 

pedunculate papillae that do not reach the ala 

edge. Tail spike extends approximately 20 beyond 

bursa. Subventral cloacal sensilla absent. 

Phasmids lateral, immediately posterior to terminal 

pair of postcloacal papillae. 

FEMALE (allotype and 9 paratypes; mean and 

range): Length 4.21 (3.25-5.07) mm. Width at 

level of vulva 117 (89-153). Buccal cavity 9 (6- 

11) deep. Esophagus 301 (274-342), corpus 162 

(149-170), isthmus 78 (68-86), bulb 60 (57- 

63). Nerve ring 202 (171-274), excretory pore 

228 (200-268) from anterior end, respectively. 

Vulva 2.06 (1.53-2.40) mm from anterior end, 

slightly pre-equatorial. Tail elongated, 189 (171- 

239). Amphidelphic; uteri divergent; anterior 

uterus directed anteriorly, posterior uterus directed 

posteriorly; ovaries reflexed. Uteri containing 

numerous elliptical eggs, 56 (51—58) X 

48 (46-57), larvae absent. 


TYPE HOST: Onychodactylus japonicus 

(Houttuyn, 1782), Japanese clawed salamander. 

1 

1 0.03 ± 0.17 

5.0 ± 2.0 0.22 ± 1.09 

1 0.02 ±0.12 

3.8 ± 3.8 0.88 ± 2.41 

4.8 ± 5.6 1.82 ± 4.13 

1 0.02 ± 0.12 

Small intestine 


Bladder 


Large intestine 

Coelom 

TYPE LOCALITY: Hineomata, Fukushima Prefecture, 

Honshu, Japan, 37°01'N, 139°23'E. 

SITE OF INFECTION: Small intestine. 

TYPE SPECIMENS: Holotype: male, United 

States National Parasite Collection (USNPC), 

Beltsville, Maryland, USNPC 88645; allotype, 

female, USNPC 88646; paratypes (9 males, 9 

females) USNPC 88647. 

ETYMOLOGY: The new species is named in 

reference to the genus of the host. 

Remarks 

The genus Angiostoma now consists of 10 

species in the monogeneric family Angiostomatidae 

(order Rhabditida); 8 species infect terrestrial 

gastropods and 2 species are from salamanders. 

The type species, Angiostoma limacis 

Dujardin, 1845, has been collected from arionid 

gastropods in western Europe (Morand and Spiridonov, 

1989). Six additional species are known 

from terrestrial gastropods in the Palaearctic 

Realm: Angiostoma asamati Spiridonov, 1985, 

from a gigantolimacid (Spiridonov, 1985); Angiostoma 

aspersae Morand, 1986, from helicids 

(Morand, 1986); Angiostoma dentifera (Mengert, 

1953) from limacids (Morand and Spiridonov, 

1989); Angiostoma kimmeriensis Korol 

and Spiridonov, 1991, from a zonitid (Korol and 

Spiridonov, 1991); Angiostoma spiridonovi 

Morand, 1992, and Angiostoma stamrneri (Mengert, 

1953) from limacids (Mengert, 1953; Morand, 

1992). Angiostoma schizoglossae Morand 

and Barker, 1995, was described from a specimen 

taken from a rhytidid gastropod endemic to 

New Zealand, Australian Realm (Morand and 

Barker, 1995). Angiostoma plethodontis Chitwood, 

1933, was described from the northern 

redback salamander, Plethodon cine re us (Green, 



Figures 1-9. Angiostoma onychodactyla sp. n. 1. Female, entire, lateral view. 2. Male, entire, lateral 

view. 3. Female, anterior end. 4. Female, en face view of anterior end. 5. Male, esophageal region. 6. 

Spicule, gubernaculum. 7. Egg. 8. Male, posterior end, lateral view. 9. Male, posterior end, ventral view. 


Table 2. Parasite list for Onychodactylus japonicus. 

BURSEY AND GOLDBERG—ANGIOSTOMA ONYCHODACTYLA SP. N. 63 

Helminth Prevalence Reference 

Trematoda 

Pseiidopolystoma dendriticum 

Mesocoeliurn brevicaecum 

Cephalouterina leoi 

Cestoda 

Cylinclrotaenia sp. (immature) 

Nematoda 

Amphibiocapillaria tritonispunctati 


Parapharyngodon japonicus 

Pseudoxyascaris japonicus 

Rhabditis sp. 

Unidentified nematode 

Unidentified oxyurids 


Unidentified cystacanths 

Not given 

Not given 

1% (1/68) 

Not given 

4% (3/68) 

Not given 

3% (2/68) 

Not given 

5% (1/20) 

24% (16/68) 

38% (26/68) 

Not given 

Not given 

Not given 

Not given 

45% (9/20) 

1% (1/68) 

1818), a Nearctic salamander (Chitwood, 1933). 

Angiostoma onychodactyla is the second species 

to be described from salamanders, albeit a Palaearctic 

salamander. 

Discussion 

A key to the known species of Angiostoma 

was published by Morand and Barker (1995). Of 

these 8 species, Angiostoma onychodactyla is 

more similar to A. limacis and A. plethodontis 

in that lateral alae are absent, and there is a bulb 

without valves. In A. limacis, the tip of the tail 

has denticles, while in A. onychodactyla and A. 

plethodontis, the tail is elongated and without 

denticles. The major difference between A. onychodactyla 

and A. plethodontis is in the number 

and position of the caudal papillae, A. onychodactyla 

with 8 pairs (all postcloacal) compared 

with A. plethodontis with 9 pairs (2 precloacal 

pairs and 7 postcloacal). Other differences include 

length of spicules (128 in A. onychodactyla 

compared with 60) and length of gubernaculum 

(44 compared with 25). Adamson (1986) 

suggested that salamander hosts acquired infection 

by ingesting parasitized molluscs, but more 

work will be required to test this hypothesis. 

Onychodactylus japonicus also harbored 3 

species of trematodes: 2 individuals of Cephalouterina 

leoi, 12 of Mesocoeliwn brevicaecum, 

Ozaki, 1948 

Uchida and Itagaki, 

This study 

Uchida et al., 1986 

This study 


This study 


1979 

Pearse, 1932 

This study 

Bursey and Goldberg, 1999 

Uchida and Itagaki, 1979 

Wilkie, 1930 


Wilkie, 1930 

Pearse, 1932 

This study 

and 1 of Pseiidopolystoma dendriticum.', 1 species 

of nematode, 124 individuals of Parapharyngodon 

japonicus; and 1 cystacanth of an unidentified 

species of acanthocephalan. These 

species have been previously reported from O. 

japonicus. 

Cephalouterina leoi was described from 3 

specimens found by Uchida et al. (1986) during 

examination of the small intestines of 900 O. 

japonicus. This is the second report of C. leoi; 

the only known host is O. japonicus. Mesocoeliurn 

brevicaecum, originally described by Goto 

and Ozaki (1929a) from the intestine of the Japanese 

common toad, Bufo japonicus Schlegel, 

1838, is often found in the small intestine of 

other Japanese amphibians, namely, the Kajika 

frog, Buergeria buergeri (Temminck and Schlegel, 

1838), the wrinkled frog, Rana rugosa Temminck 

and Schlegel, 1838, the Mitsjama salamander, 

Hynobius nebulosus (Schlegel, 1838), 

the Stejneger's oriental salamander, H. stejnegeri 

Dunn, 1923, and the Japanese newt, Triturus 

pyrrhogaster (Boie, 1826) (Goto and Ozaki, 

1929a, b). Nasir and Diaz (1971) referred all 

Japanese species of Mesocoelium to M. brevicaecum. 

Pearse (1932) was the first to report M. 

brevicaecum from O. japonicus and this is the 

second report of M. brevicaecum in this host. 

Pseudopolystoma dendriticum was originally de- 



scribed as Polystoma dendriticum by Ozaki 

(1948) from individuals taken from the urinary 

bladder of O. japonicus. Yamaguti (1963) revised 

the taxonomy. Uchida and Itagaki (1979) 

reported it from the same host. This is the third 

report of P. dendriticum; the only known host is 

O. japonicus. 

In addition to these trematodes, 111 females 

and 13 males of Parapharyngodon japonicus 

were harbored by 26 (38%) O. japonicus, the 

only known host. To our knowledge, there are no 

other reports of Parapharyngodon from Japanese 

salamanders; however, Hasegawa (1988) reported 

an unidentified but different species of Parapharyngodon 

from a lizard, the Japanese ateuchosaurus, 

Ateuchosaurus pellopleurus (Hallowell, 

1860), from Okinawa, Japan. 

The single acanthocephalan was too immature 

to identify. Van Cleave (1925) described Acanthocephalus 

nanus from the intestine of Triturus 

(=Diemictylus) pyrrhogaster and Rana rugosa 

from Japan and Pearse (1932) reported A. nanus 

as well as unidentified encysted acanthocephalans 

from T. pyrrhogaster and the giant salamander, 

Megalobatrachus japonicus (Temminck, 

1837), collected near Tokyo. This is the 

first report of acanthocephalan cystacanths in O. 

japonicus. 

All helminths were deposited in the United 

States National Parasite Collection, Beltsville, 

Maryland: Cephalouterina leoi, USNPC 88648; 

Mesocoelium brevicaecum, USNPC 88649; 

Pseudopolystoma dendriticum, USNPC 88650; 

Parapharyngodon japonicus, USNPC 88651; 

acanthocephalan cystacanth, USNPC 88652. A 

list of the known parasites of O. japonicus is 

given in Table 2. More work will be required to 

determine the distribution patterns and the variety 

of hosts of the helminths found in this 

study. 


We thank Tatsuo Ishihara (Hakone Woodland 

Museum, Hakone, Japan) for the sample of Onychodactylus 

japonicus, Peggy Firth for the illustrations 

constituting Figures 1—9, and Hay 

Cheam for assistance with dissections. 


Adamson, M. L. 1986. Modes of transmission and 

evolution of life histories in zooparasitic nematodes. 

Canadian Journal of Zoology 64:1375- 

1384. 

Bursey, C. R., and S. R. Goldberg. 1999. Paraphar- 


yngodon japonicus sp. n. (Nematoda: Pharyngodonidae) 

from the Japanese clawed salamander, 

Onychodactylus japonicus (Caudata: Hynobiidae) 

from Japan. Journal of the Helminthological Society 

of Washington 66:180-186. 

Chitwood, B. G. 1933. On some nematodes of the 

superfamily Rhabditoidea and their status as parasites 

of reptiles and amphibians. Journal of the 

Washington Academy of Science 23:508-520. 

Goto, S., and Y. Ozaki. 1929a. Brief notes on new 

trematodes I. Japanese Journal of Zoology 2:213— 

217. 

, and . 1929b. Brief notes on new trematodes 

III. Japanese Journal of Zoology 3:73-82. 

Hasegawa, H. 1988. Parapharyngodon sp. (Nematoda: 

Pharyngodonidae) collected from the lizard, 

Ateuchosaurus pellopleurus (Sauria: Scincidae) 

on Okinawajima Island, Japan. Akamata 5:11-14. 

Korol, E. N., and S. E. Spiridonov. 1991. Angiostoma 

kimmeriensis sp. n. and Agfa tauricus sp. n.— 

parasitic Rhabditida (Nematoda) from Crimean 

terrestrial molluscs. Helminthologica 28:179-182. 

Kuzmin, S. L. 1995. The Clawed Salamanders of 

Asia. Genus Onychodactylus. Biology, Distribution, 

and Conservation. Westarp Wissenschaften, 

Magdeburg, Germany, 108 pp. 

Mengert, H. 1953. Nematoden und Schnecken. Zeitschrift 

fur Morphologic und Okologie der Tiere 

41:311-349. 

Morand, S. 1986. Angiostoma aspersae n. sp. (Nematoda, 

Angiostomatidae) parasite de Helix aspersa 

Miiller (Gastropoda, Helicidae). Bulletin du Museum 

National d'Histoire Naturelle, Paris 8:111- 

115. 

. 1992. Angiostoma spiridonovi sp. n. (Nematoda: 

Angiostomatidae) from Limax flavus (Gastropoda: 

Limacidae). Journal of the Helminthological 


, and G. M. Barker. 1995. Angiostoma scliizoglossae 

n. sp. (Nematoda: Angiostomatidae) 

from the New Zealand endemic slug Schizoglossa 

novoseelandica (Gastropoda: Rhytididae). Journal 


-, and S. Spiridonov. 1989. Redescription de 

trois especes d'Angiostomatidae (Nematoda, 

Rhabditida), parasites de gastropodes pulmones 

stylommatophores, et description du cycle evolutif 

de deux d'entre elles. Bulletin du Museum National 

d'Histoire Naturelle, Paris 11:367-385. 

Nasir, P., and M. T. Diaz. 1971. A redescription of 

Mesocoelium monas (Rudolphi, 1819) Freitas, 

1958, and specific determination in genus Mesocoelium 

Odhner, 1910 (Trematoda, Digenea). Rivista 

di Parassitologia 32:149-158. 

Ozaki, Y. 1948. A new trematode, Polystoma dendriticum 

from the urinary bladder of Onychodactylus 

japonicus in Shikoku. Biosphaera 2:33—37. 

Pearse, A. S. 1932. Parasites of Japanese salamanders. 

Ecology 13:135-152. 

Spiridonov, S. E. 1985. Angiostoma asamati sp. n. 

(Angiostomatidae: Rhabditida)—new species of 

nematodes from slugs (Mollusca). Helminthologia 

22:253-261. 

Uchida, A., and H. Itagaki. 1979. Studies on the am-

phibian helminths in Japan. VI. Pseudoxyascaris 

japonicus n. g. and n. sp. (Oxyascarididae; Nematoda) 

and Pseudopolystoma dendriticum (Monogenea; 

Trematoda) from a salamander. Japanese 


, K. Uchida, and A. Kamei. 1986. Studies on 

the amphibian helminth in Japan. IX. A new digenetic 

trematode, Cephalouterina leoi n. sp., 

from salamanders, Onychodactylus japonicus and 

the new host record of the digenetic trematode, 

January 19, 2000 

March 22, 2000 

May 6, 2000 

October, 2000 

November, 2000 

BURSEY AND GOLDBERG—ANGIOSTOMA ONYCHODACTYU*. SP. N. 65 

Mesocoelium brevicaecum. Bulletin of the Azabu 

University of Veterinary Medicine 7:97-101. 

Van Cleave, H. J. 1925. Acanthocephala from Japan. 


Wilkie, J. S. 1930. Some parasitic nematodes from 

Japanese Amphibia. Annals and Magazine of Natural 

History, Series 10, 6:606-614. 

Yamaguti, S. 1963. Systema Helminthum. Volume IV. 

Monogenea and Aspidocotylea. Interscience Publishers, 


2000 Meeting Schedule of the 

Helmiiithological Society of Washington 

Smithsonian Institution, National Museum of Natural History, Washington, 

DC, 7:30 pm (Contact person: Bill Moser, 202-357-2473). 

Johns Hopkins Montgomery County Center (Provisional), Rockville, MD, 

7:30 pm (Contact person: Tom Simpson (JHU), 410-366-8814, or Louis 

Miller (NIH), 301-496-2183). 

Joint Meeting with the New Jersey Society for Parasitology, at the New 

Bolton Center, University of Pennsylvania, Kennett Square, PA, 2:00 pm 

(Contact person: Jay Parrell, 215-898-8561). 

Date, time, and place to be announced. 

Anniversary Dinner Meeting. Date, time, and place to be announced 




Carolinensis tuffi sp. n. (Nematoda: Trichostrongylina: 

Heligmosomoidea) from the White-Ankled Mouse, Peromyscus 

pectoralis Osgood (Rodentia: Cricetidae) from Texas, U.S.A. 

M.-CL. DURETTE-DESSET1'3 AND A. SANTOS III2 

1 Museum National d'Histoire Naturelle, Laboratoire de Biologic Parasitaire Associe au Centre National de le 

Recherche Scientifique, 61 rue de Buffon, 75231 Paris Cedex 05, France (e-mail: mcdd@cimrsl.mnhn.fr), and 

2 Department of Biology, Southwest Texas State University, San Marcos, Texas 78666, U.S.A. 

(e-mail: alberto3@flash.net) 

ABSTRACT: Carolinensis tuffi sp. n. (Nematoda: Trichostrongylina: Heligmosomoidea) from the small intestine 

of the white-ankled mouse, Peromyscus pectoralis Osgood (Rodentia: Cricetidae), from Texas, U.S.A., is described 

and illustrated. The new species is closest to Carolinensis carolinensis in its synlophe and to Carolinensis 

dalrymplei and Carolinensis kinsellai in the pattern of the caudal bursa. Carolinensis romerolagi (Gibbons and 

Kumar, 1980) is transferred to the genus Paraheligmonella and becomes Paraheligmonella romerolagi (Gibbons 

and Kumar, 1980) comb. n. 

KEY WORDS: Nematoda, Trichostrongylina, Heligmosomoidea, Carolinensis tuffi sp. n., Peromyscus pectoralis, 

white-ankled mouse, Rodentia, Cricetidae, Texas, U.S.A. 

The Nippostrongylinae, parasites of rodents of 

the families Arvicolidae and Cricetidae, may 

have arisen in the Palearctic Region (with the 

genus Carolinensis (Travassos, 1937)) and may 

have evolved from North America (with the genus 

Hassalstrongylus Durette-Desset, 1971) to 

South America (with the genus Stilestrongylus 

Freitas, Lent, and Almeida, 1937) (Durette-Desset, 

1971, 1985). In the small intestine of a Nearctic 

cricetid, the white-ankled mouse Peromyscus 

pectoralis Osgood, 1904, we found a 

new species described below of particular interest, 

since it is a morphologic intermediary between 

the genera Carolinensis and Hassalstrongylus. 


Hosts were live-trapped in Sherman traps by one of 

us (A.S.) in 1995 and 1996 under Texas Parks and 

Wildlife Permit SPR-0890-234, killed, and the whole 

carcasses were frozen for later examination. Nematodes 

were fixed and stored in 70% ethanol with 5% 

glycerine, studied in temporary wet mounts in water, 

and, when necessary, cleared in lactophenol. En face 

views and sections were mounted and studied in lactophenol. 

Measurements are given in micrometers unless 

otherwise stated; those relating to the holotype and 

allotype are in parentheses. 

The nomenclature used for the family group is that 

of Durette-Desset and Chabaud (1993). The synlophe 

was studied following the method of Durette-Desset 

(1985), and the nomenclature used for the study of the 

caudal bursa is that of Durette-Desset and Chabaud 


(1981). Type specimens were deposited in the Helminthological 

Collections of the Museum National 

d'Histoire Naturelle, Paris, France (MNHN). Voucher 

specimens from the type locality were also deposited 

in the United States National Parasite Collection, 

Beltsville, Maryland, accession No. 88849. 

Results 

Carolinensis tuffi sp. n. 

(Figs. 1-8) 

Description 


66 

Small nematodes, coiled to varying degrees 

along ventral side. Position of excretory pore in 

relation to length of esophagus very variable, 

mainly within second third of esophagus between 

45% and 71% in male, 42% to 66% in 

female. Deirids, when visible, at same level but 

not visible in all specimens. 

HEAD (based on 2 specimens): Cephalic vesicle 

present; buccal aperture triangular; 4 externolabial 

papillae, 2 amphids and 4 cephalic papillae; 

dorsoesophageal gland visible (Fig. 2). 

SYNLOPHE (studied in transverse sections of 

body in 1 male and 1 female): In both sexes, 

cuticle surface bears continuous ridges with chitinous 

reinforcement, beginning at different levels 

between cephalic vesicle and nerve ring and 

ending immediately anterior to caudal bursa in 

male, at vulvar level in female (Fig. 3). Number 

of ridges 20 in male and 19 in female at mid 

body. Axis of orientation of ridges passing 

though ventral right and dorsal left quadrant, inclined 

about 60° on sagittal axis in ventral left

quadrant and 70° in male, 75° in female in dorsal 

left quadrant. Ridges of equivalent size, except 

ventral right ones and ventral ridge adjacent to 

left ridge, all of which are smaller (Figs. 5, 6). 

MALES (based on 5 specimens): Length 

3.75-6.3 mm (6.4 mm) and width 90-100 (100) 

at mid body. Cephalic vesicle 50X40-60X40 

(60X45). Nerve ring 120-170 (160), excretory 

pore 160—250 (230) from cephalic apex, respectively. 

Esophagus 350-380 (380) long (Fig. 1). 

Caudal bursa subsymmetric, very elongated laterally, 

of type 2-2-1 (Fig. 8). Rays 2 and 3 longer 

than ray 4; rays 4 and 5 divergent at their 

extremities; ray 8 arising perpendicularly at the 

root of the dorsal ray and not reaching edge of 

bursa; dorsal ray divided into 2 branches in distal 

third, each branch divided again into 2 unequal 

branches; externals (ray 9) being longer 

than the internal (ray 10), and almost reaching 

edge of caudal bursa. Spicules very thin, alate, 

380-500 (460) long, ending in a sharp tip (Fig. 

8). Gubernaculum absent. Genital cone triangular 

in ventral view, bearing a small papilla 0 on 

its ventral lip (Fig. 7). Papilla 7 not observed. 

Presence of membrane situated between genital 

cone and dorsal ray (Fig. 8). 

FEMALES (based on 10 specimens): Length 

7.3-8.8 mm (7.3 mm) and width 110-150 (150) 

at mid body. Cephalic vesicle 50X40-80X60 

(60X50). Nerve ring 130-220 (160), excretory 

pore 175—320 (210) from cephalic apex, respectively. 

Esophagus 420-480 (450) long. Monodelphic, 

vulva at 110-160 (100) from caudal extremity. 

Vagina vera 30—50 (40) long. Vestibule 

80—110 (70) long, with median constriction and 

posterior diverticulum, sphincter 40X30-50X40 

(50X40). Infundibulum with proximal section 

curving in and out (twisting) 90-130 (120) (Fig. 

4). Uterus 1.2—1.8 mm (1.7 mm) long, containing 

30-36 (25) eggs. Eggs 65X40-80X60 

(85X50) at morula stage. In 1 female, eggs in 

distal section of uterus embryonated. Tail conical, 

with round tip (Fig. 4). 


TYPE HOST: White-ankled mouse, Peromyscus 

pectoralis Osgood, 1904. 

TYPE LOCALITY: Colorado Bend State Park, 

San Saba County, Texas (31°05'N, 98°30'W), 

U.S.A. 

SITE: Small intestine. 

PREVALENCE AND INTENSITY: 57 of 189 hosts 

DURETTE-DESSET AND SANTOS—CAROL1NENSIS TUFFI SF'. N. 67 

(30%) infected with 11.2 ± 3.3 SD nematodes; 

range, 1—175. 

DEPOSITED SPECIMENS: Holotype male and 

allotype female MNHN 447 KXa; paratypes (4 

males, 9 females) MNHN 447 KXb. 

ETYMOLOGY: The species is named in honor 

of Dr. Donald W. Tuff of Southwest Texas State 

University. 

Discussion 

The specimens from P. pectoralis possess the 

main characters of the subgenus Carolinensis 

(Heligmonellidae: Nippostrongylinae), which 

was raised to the level of genus by Durette-Desset 

(1983): the caudal bursa is of type 2-2-1, 

the genital cone is poorly developed, and the left 

cuticular dilatation is absent. Species of this genus 

are mainly parasitic in Holarctic Arvicolidae 

and Cricetidae. Among the species described, 

the above specimens closely resemble Carolinensis 

carolinensis (Dikmans, 1935), a parasite 

of Peromyscus maniculatus (Wagner, 1845) and 

Microtus ochrogaster (Wagner, 1842) in the 

United States in the characters of the synlophe; 

the left lateral ridges are no more developed than 

the other ridges, the inclination of the axis of 

orientation is the same, and the number of cuticular 

ridges is relatively high. The new species 

differs by the pattern of the caudal bursa, the 

shape of the tips of the spicules, and 19-20 ridges 

versus 16 in C. carolinensis (Durette-Desset, 

1974). It closely resembles Carolinensis dalrymplei 

(Dikmans, 1935), a parasite of Ondatra zibethica 

(Linnaeus, 1766) and Microtus pennsylvanicus 

(Ord, 1815) in the United States and 

Carolinensis kinsellai (Durette-Desset, 1969), a 

parasite of Neofiber alleni True, 1884, in the 

United States, in the pattern of the caudal bursa 

and, as in C. kinsellai, by the presence of a small 

ventral ridge adjacent to the left ridge. It differs 

from these species by the arising of ray 8 at the 

root of the dorsal ray, by the presence of a membrane 

between the genital cone and the dorsal 

ray, by the proximal twisting of the infundibulum, 

and by the high number of cuticular ridges 

(13 in C. kinsellai, not known in C. dalrymplei) 

(Durette-Desset, 1969). 

According to Durette-Desset (1971), the genera 

Carolinensis, Hassalstrongylus, arid Stilestrongylus 

belong to the same evolutionary line. 

The line may have arisen in the Palearctic Region 

and may have evolved from North America to 

South America with the following elements: (1) 




increase in the number of cuticular ridges, (2) rotation 

of the axis of orientation, and (3) lengthening 

of the genital cone. This line was divided 

into 3 genera: Carolinensis in the Palearctic Region, 

Hassalstrongylus in the Nearctic Region, 

and Stilestrongylus in the Neotropical Region. 

But evolution being gradual, the generic separations 

are necessarily arbitrary, and the geographic 

localities overlap in the Americas. Carolinensis is 

also present in North America, and Hassalstrongylus 

is present in South America. 

The phyletic position of the new species is 

interesting since it possesses some characteristics 

of the genus Hassalstrongylus: a high number 

of cuticular ridges (13-16 in Carolinensis vs 

19-25 in Hassalstrongylus), disappearance of 

the gradient of size of the cuticular ridges, which 

tends to an equalization of their size and the appearance 

of a new symmetry in relation to the 

axis of orientation, and a relatively developed 

genital cone. According to Durette-Desset 

(1974), Hassalstrongylus musculi (Dikmans, 

1935) was an example of an intermediary species 

between the genera Hassalstrongylus and 

Stile strongylus. Carolinensis tuffi seems to be an 

intermediary between the genera Carolinensis 

and Hassalstrongylus. 

The species Boreostrongylus romerolagi Gibbons 

and Kumar (1980) was described from a 

Mexican lagomorph, Romerolagus diazi (Ferrari 

Arez, 1893), and was automatically transferred 

to the genus Carolinensis, since Boreostrongylus 

was considered a synonym of Carolinensis by 

Durette-Desset (1983). However, this species is 

very different from the other species of the genus 

and can be classified in the genus Paraheligmonella 

Durette-Desset, 1971, particularly 

because of its synlophe: the left and right ridges 

are hypertrophied; a lateromedial gradient in the 

size of the ridges is present; and the axis of orientation 

is inclined 45° to the sagittal axis (Gibbons 

and Kumar, 1980). We thus propose a new 

combination: Paraheligmonella romerolagi 

(Gibbons and Kumar, 1980) comb. n. (=Boreostrongylus 

romerolagi Gibbons and Kumar, 

DURETTE-DESSET AND SANTOS—CAROLINENSIS TUFF/ SP. N. 69 

1980; = Carolinensis romerolagi (Gibbons and 

Kumar, 1980), Durette-Desset, 1982). 


We wish to thank Drs. D.W. Tuff, J.T. Baccus, 

and J.M. Kinsella for their advice during the 

course of this study and comments on the manuscript. 

Additional thanks are due to Dr. Baccus 

for obtaining permission from the Texas Parks 

and Wildlife Department for use of the study 

site, obtaining the scientific collecting permit, 

and securing funding for the collection of the 

specimens. Thanks are due to Kevin Schwausch, 

T Wayne Schwertner, and Todd Pilcik for assistance 

in trapping and handling rodents and to 

the staff of Colorado Bend State Park, especially 

Robert Basse. 


Dikmans, G. 1935. New nematodes of the genus Longistriata 

in rodents. Journal of Parasilology 25: 

72-81. 

Durette-Desset, M. C. 1969. Etude du systeme des 

aretes cuticulaires de trois Nematodes Heligmosomes: 

Longistriata kinsellai n.sp., L. seurati Travassos 

et Darriba, 1929, L. hokkaidensis Chabaud, 

Rausch, et Desset, 1963, parasites de Rongeurs. 

Annales de Parasitologie Humaine et Comparee 

44:617-624. 

. 1971. Essai de classification des Nematodes 

Heligmosomes. Correlations avec la paleobiogeographie 

des holes. Memoires du Museum National 

d'Histoire Naturelle, Nouvelle serie, Serie A, 

Zoologie 69:1-126 

. 1974. Nippostrongylinae (Nematoda: Heligmosomidae) 

nearctiques. Annales de Parasitologie 

Humaine et Comparee 49:435-450. 

. 1983. Keys to Genera of the Super-Family 

Trichostrongyloidea. CIH Keys to the Nematode 

Parasites of Vertebrates, No. 10, R.C. Anderson, 

and A.G. Chabaud, eds. Commonwealth Agricultural 

Bureau, Farnham Royal, Buckinghamshire, 

England, 1-86. 

. 1985. Trichostrongyloid nematodes and their 

vertebrate hosts. Reconstruction of the phylogeny 

of a parasitic group. Advances in Parasitology 24: 

239-306. 

, and A. G. Chabaud. 1981. Nouvel essai de 

Figures 1-8. Carolinensis tuffi sp. n. in Peromyscus pectoralis from Texas, drawings based on paratypes. 

1. Male, anterior extremity, right lateral view. 2. Female, head, apical view. 3. Female tail, disappearance 

of cuticular ridges. 4. Female, posterior extremity, left lateral view. 5. Male synlophe at mid body. 6. 

Female synlophe at mid body. 7. Male, genital cone and membrane, ventral view. 8. Male, caudal bursa, 

ventral view. V = ventral side; R = right side. Scales in micrometers. 



classification des Nematodes Trichostrongyloidea. Gibbons, L., and V. Kumar. 1980. Boreostrongylus 

Annales de Parasitologie Humaine et Comparee romerolagi n.sp. (Nematoda: Heligmonellidae) 

56:297-312. from a Mexican volcano rabbit, Romerolagus dia- 

, and . 1993. Note sur la Nomenclature zi. Systematic Parasitology 1:117-122. 

des Strongylida au-dessus du groupe famille. An- Travassos, L. 1937. Revisao da famflia Trichostronnales 

de Parasitologie Humaine et Comparee 68: gylidae Leiper, 1912. Monographias do Institute 

111-112. Oswaldo Cruz 1:1-512. 




An Unusual Case of Anisakiasis in California, U.S.A. 

OMAR M. AMIN,M WILLIAM S. EiDELMAN,2 WILLIAM DoMKE,3 JONATHAN BAILEY,3 AND 

GEOFFREY PFEiFER2 

1 Institute of Parasitic Diseases, P. O. Box 28372, Tempe, Arizona 85285-8372, and Department of Zoology, 

Arizona State University, Tempe, Arizona 85287-1501, U.S.A. (e-mail: omaramin@aol.com), 

2 The Natural Medicine Center, 1434 East Ojai Avenue, Ojai, California 93023, U.S.A. and 

3 634V2 Rose Avenue, Venice, California 90291, U.S.A. (e-mail: colonichydrotherapy@USA.NET) 

ABSTRACT. In the first case of its kind, anisakiasis is documented in a 44-yr-old California male whose neck 

was penetrated transesophageally by 1 third-stage larva of Pseudoterranova decipiens. The larva subsequently 

emerged from the neck region through an ulcerating sore. The larva showed some evidence of development and 

is described. The clinical history of the patient is reviewed. The patient subsequently died of causes unrelated 

to the anisakiasis infection. 

KEY WORDS: anisakiasis, Pseudoterranova decipiens, third-stage larva, human infection, morphology, case 

history, California, U.S.A. 

Of the many genera of ascaroid (Anisakidae) 

nematodes causing anisakiasis in vertebrates 

(Myers, 1975), only 2 species cause human infections 

in North America (McKerrow and 

Deardorff, 1988; U.S. Food and Drug Administration/Center 

for Food Safety and Applied 

Nutrition [FDA/CFSAN], 1992). The cod worm, 

Pseudoterranova decipiens (Krabbe, 1878) Gibson 

and Colin, 1981, infects marine mammals, 

most importantly seals, in the North Atlantic and 

North and South Pacific; the herring worm, Anisakis 

simplex (Rudolphi, 1809) Baylis, 1920, 

infects marine mammals, particularly whales in 

the eastern Pacific and elsewhere in the world 

(see Myers [1959, 1975] and Gibson [1983] for 

synonymies). Despite the high incidence of 

worms of the genus Anisakis in fishes (Myers, 

1979) and whales in the western Pacific, human 

cases in North America involving larvae of Anisakis 

are rare. The higher incidence of human 

infection with larvae of the genus Pseudoterranova 

(Lichtenfels and Brancato, 1976; Kliks, 

1983), particularly in the northern Atlantic coast, 

appears to be related to the large seal populations 

there (Myers, 1976). 

Two patterns of disease describe the clinical 

symptomology of anisakiasis in North America. 

The asymptomatic luminal condition described 

for larvae of Pseudoterranova does not involve 

tissue penetration, and worms are expelled by 

coughing, vomiting, or defecating. In infections 

with larvae of Anisakis, however, penetration of 

Corresponding author. 

71 

the gut wall is reported by many observers 

(Kates et al., 1973; Lichtenfels and Brancato, 

1976; Myers, 1976; Margolis, 1977; Ishikura et 

al., 1993). These cases are easily misdiagnosed 

as appendicitis, Crohn's disease, gastric ulcer, or 

gastrointestinal cancer (McKerrow and Deardorff, 

1988; FDA/CFSAN, 1992; Alonso et al., 

1997). Documentation of our present case, however, 

demonstrates that larvae of Pseudoterranova 

can be as invasive as has traditionally been 

described in infections with Anisakis in Holland 

and Japan (Oshima, 1972, 1987; Yoshimura et 

al., 1979; Ishikura et al., 1993). 

In North America, the public health impact of 

anisakiasis is limited to consumers of such foods 

as sushi and sashimi. Approximately 50 cases 

were documented in the United States up to 

1988, and fewer than 10 cases have been documented 

annually (FDA/CFSAN, 1992) since 

the first North American cases in the United 

States were documented in the early 1970's (Little 

and Most, 1973; Pinkus et al., 1975). The 

first confirmed human case of anisakiasis was 

reported in Holland in 1960 (Van Theil et al., 

1960), and Holland remains the most important 

anisakiasis-endemic region of the world. By 

1990, 292 of the 559 European cases were reported 

in Holland, whereas 12,586 cases were 

reported in Japan. The Japanese cases included 

11,629 gastric, 567 intestinal, and 45 extragastrointestinal 

cases of infection by Anisakis and 

only 335 cases of gastric infection by Pseudoterranova 

(Ishikura et al., 1993). This report 

documents worm morphology and the clinical 



picture and compares our results with related 

findings in other cases. 


One 70% ethanol-preserved nematode extracted by 

J.B. and W.D. from the neck of a 44-yr-old Venice, 

California, Caucasian male patient on 12 April 1998 

was received by O.M.A. on 18 April 1998 for identification. 

The worm was first examined externally, then 

stained in Mayer's acid carmine overnight, destained 

in 4% HC1 in 70% ethanol, dehydrated in ascending 

concentrations of ethanol, cleared in graded terpineol- 

100% ethanol, and prepared as a whole mount in Canada 

balsam. Figures were made with the aid of photoprojection. 

All measurements are in millimeters unless 

otherwise indicated. Width measurements refer to 

maximum width. The specimen is deposited in the 

U.S. National Parasite Collection (USNPC), Beltsville, 

Maryland. 

Results 

The patient (T.S.) was a 44-yr-old Caucasian 

male with amyotrophic lateral sclerosis (ALS), 

a degenerative neuromuscular disorder. He was 

completely healthy until 1992, when he was diagnosed 

(spinal tap) with Lyme disease after 

suffering flu-like symptoms and joint pains. He 

received 2 courses of antibiotics, including ampicillin, 

bioxin, doxycycline, and vancomycin, 

before he felt cured. In 1994, he was further diagnosed 

with ALS at 2 major medical centers in 

South Carolina and New York and was told that 

he had 6 mo to live. Muscle biopsies showed 

cell death consistent with ALS. The patient 

sought help at The Natural Medicine Center in 

1996 as his condition continued to deteriorate. 

All his laboratory tests were normal (including 

explorations of possible neurotoxins) except for 

a spinal tap that showed Lyme disease in the 

central nervous system. He was treated with 

heavy doses of antibiotics but without favorable 

results. 

During April 1998, he received a series of co- 

Ionic irrigations, during which time "parasites" 

were claimed to have been observed. These presumed 

"parasites" were not collected by the junior 

authors nor observed by O.M.A. However, 

a worm was actually extracted from a neck sore 

and sent to O.M.A. for identification. Upon external 

examination, the worm was initially identified 

as an anisakid nematode. After processing 

(see above), the identity of the nematode was 

determined to be a third-stage larva of P. decipiens. 

At that time, T.S. indicated on the Requisition 

Form that he was experiencing "severe 


weakness, neuromuscular damage, severe 

weight loss, loss of balance, and speech impairment." 

He also indicated no travel history but a 

history of diet often including sushi and sashimi 

over the previous few years. After the worm diagnosis, 

T.S. was treated with pharmaceutical 

anti-parasitic medications (albendazole and 

praziquantel) in large doses. Subsequently, his 

symptoms of malaise disappeared and his red 

blood cell count dramatically increased to 4.30 

from a pretreatment low of 2.74 on 11 March 

1998. After repeat treatment with praziquantel, 

T.S. felt better though his muscular condition remained 

unchanged. For the past few years, T.S. 

had always felt ill and experienced loss of function. 

He recently weighed 105 Ib, down from a 

pre-illness weight of 160 Ib. Before his death in 

April 1999, T.S. was unable to use his hands and 

could barely ambulate, with help. He could talk 

only with difficulty and breathed adequately but 

not enough to blow his nose. 

Description of the third-stage larva of 

Pseudoterranova decipiens (Figs. 1-3) 

Body 42.12 long by 0.85 wide near middle. 

Cuticle wrinkled at regular intervals, about 

0.025 thick but thinner toward both ends. One 

dorsal, 2 subventral large fleshy lips each with 

2 rounded lobes, anterior dentigenous ridges, 

and large papilla (Fig. 1). Prominent boring 

tooth (spine) anteriorly. Excretory pore ventral 

at base of lips. Nerve ring prominent, 0.42 from 

anterior tip. Esophagus 2.03 long by 0.24 wide 

at base. Cecum extends anteriorly and about as 

long as ventriculus, 1.02 long by 0.18 wide (Fig. 

2). Ventricular appendage and alae absent. Reproductive 

structures not observed. Tail (anus to 

posterior end) 0.16 long. Anal glands prominent, 

each with a single darkly stained nucleus. Conically 

shaped fine-pointed mucron (caudal spine) 

0.025 long (Fig. 3). Evidence of development 

(molting) noted as the larva appeared trapped in 

the cuticle of the previous stage at various 

points. 


HOST: Homo sapiens Linnaeus, 1758. 

LOCALITY: California, U.S.A. 

SITE OF INFECTION: Neck. 

SPECIMEN DEPOSITED: USNPC No. 88504. 

Remarks 

The specimen was identified as P. decipens 

primarily because it possessed a cecum and no

Figures 1-3. Pseudoterranova decipiens third-stage 

larva extracted from a neck lesion of a patient in 

California. 1. Anterior tip of body showing details 

of lips and boring spine (BS). 2. Anterior portion 

of body showing anteriorly projecting intestinal cecum 

(C) overlapping the ventriculus (V), esophagus 

(E), intestine (I), and nerve ring (NR). 3. Posterior 

end of worm showing anal glands (AG), anus (A), 

tail (T), and tail spine (TS). Scale bar (200 u-m) 

applies to Figs. 1 and 3. 

ventricular appendage and its excretory pore 

opened at the base of the lips. The cecum was 

about as long as the ventriculus. Additional significant 

features include prominent boring and 

caudal spines and the structure of lips as well as 

measurements of the described organs and trunk 

(above). 

Discussion 

The morphological features of the described 

larva were similar to those reported for other 

larvae of P. decipiens (reported as Phocanemd) 

recovered from North American patients by 

AMIN ET AL.—PSEUDOTERRANOVA IN MAN 73 

Kates et al. (1973), Kliks (1983), Little and Most 

(1973), and Lichtenfels and Brancato (1976). 

There are minor differences in measurements, 

and none of the above authors reported anal 

glands; Kates et al. (1973) did not observe a 

boring tooth; Little and Most (1973) noted a female 

reproductive system but no caudal spine; 

Lichtenfels and Brancato (1976) noted cervical 

papillae and excretory gland about one-third the 

body length. Clearly, the morphological variations 

in human anisakids need to be documented 

to ascertain their identity and to determine the 

correct correlations with geographic distribution 

and histopathologic changes. 

In contrast with the considerably greater 

prevalence of human infections with the highly 

invasive A. simplex in Europe and Japan 

compared with the noninvasive P. decipiens, 

most anisakiasis cases in North America involve 

P. decipiens (Kates et al., 1973; Jackson, 

1975; Lichtenfels and Brancato, 1976; 

Myers, 1976; Margolis, 1977; Deardorff et al., 

1986; Oshima, 1987; Ishikura et al., 1993; 

Alonso et al., 1997). The pattern of differential 

pathogenicity has been documented in 

Holland (Yoshimura et al., 1979), the United 

States (Jackson, 1975; Lichtenfels and Brancato, 

1976; McKerrow and Deardorff, 1988), 

and Japan (Oshima, 1972, 1987; Ishikura et 

al., 1993) and was reviewed by Margolis 

(1977). Findings from our study, however, disagree 

with the above "pathogenic capacity" 

picture (Margolis, 1977) and document severe 

invasiveness of the larva of P. decipiens. Evidence 

of the invasiveness of the larvae of 

Pseudoterranova is extremely rare. When 

such cases occur (Little and MacPhail, 1972), 

as is usual in larvae of Anisakis (Hayasaka et 

al., 1971; Pinkus et al., 1975; Yoshimura et al., 

1979; Deardorff et al., 1986; Oshima, 1987; 

McKerrow and Deardorff, 1988; Ishikura et 

al., 1993), the larvae usually invade the gut 

wall lower at gastric or intestinal sites. In a 

very rare case of invasive Pseudoterranova, 

the larva was recovered from the abdominal 

cavity of a male from Massachusetts (Little 

and MacPhail, 1972). All other cases of human 

infection with Pseudoterranova in North 

America were detected when larvae were 

eliminated by the mouth (Lichtenfels and 

Brancato, 1976; McKerrow and Deardorff, 

1988). A larva was identified as "Anisakis" 

from histological sections in the tonsils of a 



6-yr-old Indian girl from Oman, Arabian Peninsula 

(Bhargava et al., 1996), and extragastrointestinal 

"anisakidosis" has been reported 

in the mucous membrane of pharynx and 

esophagus in Japan (Ishikura et al., 1993); the 

identity of these worms was not elaborated 

further. 

We attribute the upper gastrointestinal invasiveness 

of the larva of P. decipiens through the 

unusual esophageal site to the immune depression 

of the patient or weakness from ALS. The 

continued penetration of the worm through the 

neck tissue and the exiting through the neck sore 

represent an extreme case of invasiveness that, 

to the best of our knowledge, has not been previously 

reported in larvae of either Anisakis or 

Pseudoterranova. 

We believe that the state of the patient could 

have been related to 1 or more of the following 

3 factors: ALS, Lyme disease, or anisakid(s). 

Symptoms of anisakiasis may persist after worm 

death because some lesions have been found 

upon surgical removal that contain only nematode 

remnants. Stenosis of the pyloric sphincter 

was observed in a case where exploratory laparotomy 

had revealed a worm that was not removed 

(FDA/CSFAN, 1992). Simultaneous 

multiple infections with as many as 10 anisakid 

worms have been reported in Japan (Ishikura et 

al., 1993). Although acute necrotizing eosinophilic 

granulomatous inflammation involving the 

intestine has been documented in cases of invasive 

anisakiasis, hypersensitivity, sensitization, 

and a chronic form of the disease lasting 

about 2 yr have also been documented (Pinkus 

et al., 1975; Alonso et al., 1997). 


Alonso, A., A. Daschner, and A. Moreno-Ancillo. 

1997. Anaphylaxis with Anisakis simplex in the 

gastric mucosa. New England Journal of Medicine 

337:350-352. 

Bhargava, D., R. Raman, M. Z. El Azzouni, K. 

Bhargava, and B. Bhusnurmath. 1996. Anisakiasis 

of the tonsils. Journal of Laryngology and 

Otology 110:387-388. 

Deardorff, T. L., T. Fukumura, and R. B. Raybourne. 

1986. Invasive anisakiasis. A case report 

from Hawaii. Gastroenterology 90:1047— 

1050. 

Gibson, D. 1983. The systematics of ascaridoid nematodes: 

a current assessment. Pages 321-338 in A. 

F. Stone, H. M. Platt, and L. Khalil, eds. Nematode 

Systematics Association. Special Vol. 22. 

Academic Press, London. 

Hayasaka, H., H. Ishikura, and T. Takayama. 1971. 


Acute regional illeitis due to Anisakis larvae. International 

Surgery 55:8-14. 

Ishikura, H., K. Kikuchi, K. Nagasawa, T. Ooiwa, 

H. Takamiya, N. Sato, and K. Sugane. 1993. 

Anisakidae and anisakidosis. Progress in Clinical 


Jackson, G. J. 1975. The "new disease" status of human 

anisakiasis and North American cases: a review. 

Journal of Milk and Food Technology 38: 

769-773. 

Kates, S., K. A. Wright, and R. Wright. 1973. A 

case of human infection with the cod nematode 

Pseudoterranova sp. American Journal of Tropical 

Medicine and Hygiene 22:606-608. 

Kliks, M. M. 1983. Anisakiasis in the western United 

States. Four new case reports from California. 

American Journal of Tropical Medicine and Hygiene 

32:526-532. 

Lichtenfels, J. R., and F. P. Brancato. 1976. Anisakid 

larva from the throat of an Alaskan Eskimo. 

American Journal of Tropical Medicine and Hygiene 

25:691-693. 

Little, M. D., and J. C. MacPhail. 1972. Large nematode 

larva from the abdominal cavity of a man 

in Massachusetts. American Journal of Tropical 

Medicine and Hygiene 21:948-950. 

, and H. Most. 1973. Anisakid larva from the 

throat of a woman in New York. American Journal 

of Tropical Medicine and Hygiene 22:609— 

612. 

Margolis, L. 1977. Public health aspects of "codworm" 

infections: a review. Journal of Fisheries 

Research Board of Canada 34:887-898. 

McKerrow, J. H., and T. L. Deardorff. 1988. Anisakiasis: 

revenge of the sushi parasite (letter). 

New England Journal of Medicine 319:1228- 

1229. 

Myers, B. J. 1959. Phocanema, a new genus for the 

anisakid nematode of seals. Canadian Journal of 

Zoology 37:459-465. 

. 1975. The nematodes that cause anisakiasis. 

Journal of Milk and Food Technology 38:774- 

782. 

. 1976. Research then and now on the Anisakidae 

nematodes. Transactions of the American Microscopical 

Society 95:137—142. 

. 1979. Anisakine nematodes in fresh commercial 

fish from waters along the Washington, 

Oregon and California coasts. Journal of Food 

Protection 42:380-384. 

Oshinia T. 1972. Anisakis and anisakiasis in Japan and 

adjacent area(s). Pages 301-393 in K. Morishita, 

Y. Komiya, and H. Matsubayashi, eds. Progress of 

Medical Parasitology in Japan. Vol. 4. Meguro 

Parasitological Museum, Tokyo. 

. 1987. Anisakiasis—is the sushi bar guilty. 

Parasitology Today 3:44-48. 

Pinkus, G. S., C. Coolidge, and M. D. Little. 1975. 

Intestinal anisakiasis. First case report from North 

America. American Journal of Medicine 59:114— 

120. 

U.S. Food and Drug Administration/Center for 

Food Safety and Applied Nutrition. 1992. Bad 

bug book. Anisakis simplex and related worms.

AMIN ET M^.—PSEUDOTERRANOVA IN MAN 75 

Pages 1-3 in Foodborne Pathogenic Microorgan- Yoshimura, H., N. Akao, K. Kondo, and Y. Ohnishi. 

isms and Natural Toxins Handbook. World Wide 1979. Clinicopathological studies on larval ani- 

Web, http://vm.cfsan.fda.gov/~mow/chap25.html sakiasis, with special reference to the report of 

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1960. A nematode parasitic to herring causing ab- of Parasitology 28:347-354. 

dominal syndromes in man. Tropical and Geographical 

Medicine 12:97-115. 

Book Available 

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Neotropical Monogenoidea. 36. Dactylogyrids from the Gills of 

Rhamdia guatemalensis (Siluriformes: Pimelodidae) from Cenotes of 

the Yucatan Peninsula, Mexico, with Proposal of Ameloblastella 

gen. n. and Aphanoblastetta gen. n. (Dactylogyridae: 

Ancyrocephalinae) 

DELANE C. KRiTSKY,1-4 EDGAR F. MENDOZA-FRANCO,2 AND TOMAS ScHOLZ2'3 

1 Department of Health and Nutrition Sciences, Box 8090, Idaho State University, Pocatello, Idaho 83209, 

U.S.A. (e-mail: kritdela@isu.edu), 

2 Center for Investigation and Advanced Studies, National Polytechnic Institute (CINVESTAV-IPN), 

University of Merida, Carretera Antigua a Progreso Km 6, A.P. 73 "Cordemex," C. P. 97310 Merida, 

Yucatan, Mexico (e-mail: mfranco@kin.cieamer.conacyt.mx), and 

3 Institute of Parasitology, Academy of Sciences of the Czech Republic, Branisovska 31, 

370 05 80 Ceske Budejovice, Czech Republic (e-mail: tscholz@paru.cas.cz) 

ABSTRACT: Ameloblastella gen. n. and Aphanoblastella gen. n. are proposed for dactylogyrids from the gills of 

pimelodid catfishes (Siluriformes) in the Neotropical Biogeographical Region. Species of Ameloblastella and 

Aphanoblastella are characterized on the bases of gonadal position, hook shank morphology, presence/absence 

of eyes and eye granules, and morphology of the male reproductive system. Two species of Urocleidoides (sensu 

lato) and 1 of Vancleaveus are transferred to Ameloblastella as A. chavarriai (Price, 1938) comb. n. (type 

species), A. mamaevi (Kritsky and Thatcher, 1976) comb, n., and A. platensis (Suriano and Incorvaia, 1995) 

comb, n., respectively. Three species of Urocleidoides (sensu lato) from pimelodid catfishes are transferred to 

Aphanoblastella as A. travassosi (Price, 1938) comb. n. (type species), A. robiistus (Mizelle and Kritsky, 1969) 

comb, n., and A. mastigatus (Suriano, 1986) comb. n. 

KEY WORDS: Monogenoidea, Dactylogyridae, Ameloblastella, Aphanoblastella, Ameloblastella chavarriai 

comb, n., Ameloblastella mamaevi comb, n., Ameloblastella platensis comb, n., Aphanoblastella travassosi comb, 

n., Aphanoblastella mastigatus comb, n., Aphanoblastella robiistus comb, n., catfish, Siluriformes, Pimelodidae, 

Rhamdia guatemalensis, cenotes, Mexico. 

Price (1938) described the dactylogyrids, 

Cleidodiscus chavarriai and Clcidodiscus travassosi, 

from the gills of the pimelodid catfish, 

Rhamdia rogersi (Regan, 1907) (a junior synonym 

of Rhamdia laticauda (Kner, 1857) according 

to Silfvergrip, 1996) in Costa Rica. Molnar 

et al. (1974) transferred the 2 species to Urocleidoides 

Mizelle and Price, 1964, based on the 

emended diagnosis of the genus provided by 

Mizelle et al. (1968). The diagnosis in Mizelle 

et al. (1968) greatly expanded the generic 

bounds of Urocleidoides, and within 5 years, 

species of the genus had been described from 

fishes of 5 orders: Atheriniformes, Characiformes, 

Gymnotiformes, Perciformes, and Siluriformes. 

Kritsky et al. (1986) restricted Urocleidoides 

to species having a sinistral vaginal sclerite, 

transferred several species from the genus to 

Gussevia Kohn and Paperna, 1964, and consid- 



76 

ered 22 described species incertae sedis, the latter 

group including U. chavarriai and U. travassosi. 

The puipose of this investigation was to 

determine the generic placement of several previously 

described species of Urocleidoides sensu 

lato described from pimelodid catfishes in the 

Neotropical Biogeographical Region. The study 

is based on new collections of U. chavarriai and 

U. travassosi on Rhamdia guatemalensis (Giinther, 

1864) (a junior synonym of Rhamdia quelen 

(Quoy and Gaimard, 1824) according to 

Silfvergrip, 1996) from cenotes (sinkholes) in 

the Yucatan Peninsula, Mexico. 


Fish hosts, R. guatemalensis, were collected by hook 

and line or casting nets from cenotes on the Yucatan 

Peninsula, Mexico, during 1993-1998 (see Scholz et 

al., 1995). Gill baskets were removed from fish, placed 

in petri dishes with tap water, and examined with a 

dissection microscope. Methods of collection, preservation, 

mounting, and illustration of helminths were 

those described by Kritsky et al. (1986), except that

the gill baskets of some hosts were fixed in hot 

(~90°C) 4% formalin according to methods presented 

by Scholz and Hanzelova (1998); specimens fixed in 

hot formalin had extended or relaxed peduncles, while 

those fixed in ambient formalin (=30°C) had contracted 

peduncles. Measurements, all in micrometers, were 

made with a filar micrometer according to procedures 

of Mizelle and Klucka (1953), except that length of 

the inale copulatory organ is an approximation of total 

length obtained by using a calibrated Minerva curvimeter 

on camera lucida drawings; average measurements 

are followed by ranges and the number (n) of 

specimens measured in parentheses; unstained flattened 

specimens mounted in Hoyer's or Malmberg's 

media were used to obtain measurements of hooks, 

anchors, and the copulatory complex; all other measurements 

were obtained from unflattened specimens 

stained with Gomori's trichrome or Mayer's carmine 

and mounted in Canada balsam. Voucher specimens of 

helminths collected during this study were deposited 

in the United States National Parasite Collection 

(USNPC), Beltsville, Maryland, U.S.A., and the helminth 

collections of the University of Nebraska State 

Museum (HWML), Lincoln, Nebraska, U.S.A.; the Institute 

dc Biologfa, Universidad Nacional Autonoma 

de Mexico (UNAM), Mexico City, Mexico; the Parasitology 

Laboratory, Center for Investigation and Advanced 

Studies of the National Polytechnic Institute 

(CINVESTAV-IPN) (CHCM), Mcrida, Mexico, and 

the Institute of Parasitology, Academy of Sciences of 

the Czech Republic (IPCAS), Ceske Budejovice, 

Czech Republic, as indicated in the following redescriptions. 

For comparative purposes, the following 

specimens were examined: 2 voucher specimens of U. 

chavarriai (USNPC 73178) and 3 voucher specimens 

of U. travassosi (USNPC 73179), both lots deposited 

by Molnar et al. (1974); holotype and 9 paratypes of 

Urocleidoides robustus Mizelle and Kritsky, 1969 

(USNPC 71009, 73565, HWML 22941); and a voucher 

specimen of Philocorydoras sp. (probably =U. margolisi 

Molnar, Hanek, and Fernando, 1974) (USNPC 

88965). 

Results 

Class Monogenoidea Bychowsky, 1937 

Order Dactylogyridea Bychowsky, 1937 

Dactylogyridae Bychowsky, 1933 

Ameloblastella gen. n. 

DIAGNOSIS: Body fusiform, slightly flattened 

dorsoventrally, comprising cephalic region, 

trunk, peduncle, haptor. Tegument smooth. Two 

terminal, 2 bilateral cephalic lobes; 3 bilateral 

pairs of head organs; cephalic glands unicellular, 

lateral or posterolateral to pharynx. Eyes absent; 

accessory eye granules subspherical. Mouth subterminal, 

midventral, anterior to pharynx; pharynx 

muscular, glandular; esophagus present; 2 

intestinal ceca confluent posterior to gonads, 

lacking diverticula. Genital pore midventral near 

level of intestinal bifurcation. Gonads intercecal, 

KRITSKY BT AL.—DACTYLOGYRIDS FROM MEXICAN CENOTES 77 

overlapping; testis dorsal to germarium. Vas deferens 

looping left intestinal cecum; seminal vesicle 

a dilation of vas deferens. Copulatory complex 

comprising basally articulated male copulatory 

organ, accessory piece. Male copulatory 

organ tubular, coiled; coil with counterclockwise 

rings (see Kritsky et al., 1985). Accessory piece 

with complex distal region serving as guide for 

male copulatory organ, articulation piece extending 

within rings to base of male copulatory 

organ. Seminal receptacle pregermarial; vaginal 

aperture sinistral; vitellaria coextensive with intestine. 

Haptor globose to subhexagonal, armed 

with dorsal, ventral anchor/bar complexes, 7 

pairs of similar hooks; hook distribution ancyrocephaline 

(Mizelle, 1936; see Mizelle and 

Price, 1963). Ventral bar with posteromedial 

projection. Hook with shank comprising 2 subunits; 

proximal subunit expanded. Parasites of 

the gills of neotropical pimelodid catfishes (Siluriformes). 

TYPE SPECIES: Ameloblastella chavarriai 

(Price, 1938) comb. n. ( = Cleidodiscus chavarriai 

Price, 1938) from R. rogersi (Regan), R. 

guatemalensis (Giinther), Rhamdia sebae (Valenciennes, 

1840), and R. quelen (Quoy and Gaimard) 

in Costa Rica, Mexico, and Trinidad, respectively. 

OTHER SPECIES: Ameloblastella tnamaevi 

(Kritsky and Thatcher, 1976) comb. n. (= Urocleidoides 

mamaevi Kritsky and Thatcher, 

1976) from Cephalosilurus zungaro (Humboldt, 

1833) in Colombia, South America. 

Ameloblastella platensis (Suriano and Incorvaia, 

1995) comb. n. ( — Vancleaveus platensis 

Suriano and Incorvaia, 1995) from Pirnelodus 

clarias maculatus (Lacepede, 1803) in Argentina, 

South America. 

ETYMOLOGY: The generic name is from 

Greek (amel/o — neglected + blast/o = germ, 

branch) appended to the diminutive ending 

(-ella), and refers to the long period before recognition 

of generic placement of its members. 

REMARKS: Ameloblastella gen. n. is primarily 

characterized by dactylogyrids with 1) overlapping 

gonads (testis dorsal to germarium); 2) 

subspherical accessory eye granules; 3) a basally 

articulated male copulatory organ and accessory 

piece; 4) a coiled male copulatory organ with 

counterclockwise rings; 5) a ventral bar with a 

medial process; 6) a seminal vesicle formed by 

a simple dilation of the vas deferens; 7) inflated 

hook shanks, each composed of 2 subunits 



(proximal subunit expanded); 8) a sinistral vaginal 

aperture; and 9) absence of eyes. Of dactylogyrid 

genera with members infecting freshwater 

siluriforms in the Neotropics, characters 

defining Ameloblastella suggest a relationship 

with Vancleaveus Kritsky, Thatcher, and Boeger, 

1986, and Philocorydoras Suriano, 1986. Members 

of these 3 genera share the characteristics 

of possessing overlapping gonads (testis dorsal 

to germarium), a ventral bar with a medial process, 

hook shanks comprised of 2 subunits 

(proximal subunit expanded), subspherical eye 

granules, and a dilation of the vas deferens to 

form the seminal vesicle. Ameloblastella differs 

from both Vancleaveus and Philocotydoras by 

the position of the vaginal aperture (ventral in 

Vancleaveus and Philocorydoras). It further differs 

from Philocorydoras by lacking eyes and 

having a coiled male copulatory organ (male 

copulatory organ an arced tube in Philocorydoras)', 

and from Vancleaveus by the absence of a 

basal fold on the superficial root of the dorsal 

anchor and an expanded distal subunit of the 

hook shank (both present in Vancleaveus) (see 

Kritsky et al., 1986; Suriano, 1986b). 

Of the 22 species of Urocleidoides considered 

incertae sedis by Kritsky et al. (1986), 2 of them 

are transferred to Ameloblastella as A. chavarriai 

(Price, 1938) comb. n. and A. mamaevi 

(Kritsky and Thatcher, 1976) comb. n. While A. 

chavarriai is the type species of Ameloblastella 

and defines the genus, A. mamaevi possesses all 

diagnostic features of Ameloblastella (see Kritsky 

and Thatcher, 1976). 

Suriano and Incorvaia (1995) described Vancleaveus 

platensis from the gills of the pimelodid, 

P. c. maculatus. This helminth is not a member 

of Vancleaveus because of the absence of 

basal folds on the superficial root of the dorsal 

anchor and the presence of a sinistral vaginal 

aperture (vaginal pore ventral in Vancleaveus 

spp.). The original description of the species indicates 

that it possesses all of the diagnostic features 

of Ameloblastella, except for the presence 

of a nonarticulated male copulatory organ and 

accessory piece. However, specimens of this 

species in the senior author's collection and collected 

from Pimelodus clarias (Lacepede) from 

the Rio de la Plata, Argentina, show a delicate 

articulation process attaching the base of the 

male copulatory organ to the accessory piece. 

The latter finding supports the transfer of V. platensis 

to Ameloblastella. 


Ameloblastella chavarriai (Price, 1938) 

comb. n. 

(Figs. 1-9) 

REDESCRIPTION: Body 596 (408-742; n = 

30) long; greatest width 113 (92-134; n = 33) 

usually in posterior trunk. Cephalic lobes poorly 

to moderately developed. Accessory eye granules 

in cephalic, anterior trunk regions. Pharynx 

ovate, 27 (24-30; n = 33) in greatest width; 

esophagus short to moderately long. Peduncle 

contracted, broad (ambient temperature formalin 

fixation) or elongate, narrow (hot formalin fixation); 

haptor subhexagonal, 84 (69-108; n = 

28) wide, 72 (60-88; n = 29) long. Ventral anchor 

33 (30-36; n = 22) long, with elongate 

superficial root, short deep root, slightly curved 

shaft, straight point; base 19 (16-21; n = 16) 

wide. Dorsal anchor 27 (23—31; n = 16) long, 

with well-developed roots, slightly curved shaft, 

elongate straight point; deep root protruding 

posteriorly from anchor base; anchor base 18 

(17-20; n = 10) wide. Ventral bar 33 (29-37; 

n = 22) long, yoke-shaped, with posteromedial 

process usually bent anteriorly dorsal to bar. 

Dorsal bar 30 (26-34; n = 20) long, broadly Vshaped, 

with slightly enlarged ends. Hook with 

protruding truncate thumb, delicate point; hook 

24 (20-27; n = 36) long; filamentous booklet 

(FH) loop extending to level of union of shank 

subunits. Male copulatory organ 141 (128-158; 

n = 8) long, a coil of about 2.5 rings; diameter 

of proximal ring 17 (15-20; n = 20); base of 

male copulatory organ with small sclerotized 

plate. Accessory piece 32 (27—38; n = 26) long, 

25 (22—32; n — 22) wide, comprising 2 subunits; 

dextral subunit terminally acute, subtriangular, 

with expanded lateral margins; sinistral subunit 

L-shaped with flared termination, serving as 

guide for male copulatory organ. Testis elongate, 

fusiform (lateral margins indistinct); seminal 

vesicle large, fusiform, lying diagonally in median 

field of anterior trunk posterior to male copulatory 

organ; prostatic reservoir lying to right 

of seminal vesicle and body midline, posterior 

to male copulatory organ. Germarium an inverted 

elongate cone, 119 (84-166; n = 20) long, 

35 (27—53; n = 21) wide; oviduct, ootype not 

observed; uterus delicate, infrequently with single 

egg; vagina a sclerotized tube; vaginal aperture 

on sclerotized papilla lying in small indentation 

of body margin; seminal receptacle

KRITSKY ET AL.—DACTYLOGYRIDS FROM MEXICAN CENOTES 79 

Figures 1-9. Ameloblastella chavarriai (Price, 1938) comb. n. 1. Whole mount (composite, ventral). 2. 

Vagina. 3. Hook. 4. Copulatory complex (ventral). 5. Whole mount (fixed in hot formalin). 6. Ventral 

anchor. 7. Ventral bar. 8. Dorsal bar. 9. Dorsal anchor. All figures are to the 25-|j,m scale except Figures 

1 and 5 (200-n.m scales). 

large, subovate. Egg 63 (n — 1) long, 30 (n = 

1) wide, ovate, with short proximal filament. 

SYNONYMS: Cleidodiscm chavarriai Price, 

1938; Urocleidoides chavarriai (Price, 1938) 

Molnar, Hanek, and Fernando, 1974. 

HOST AND LOCALITY: Gills of Rhamdia guatemalensis 

(Giinther); Ixin-ha Cenote, Yucatan, 

Mexico (20°37'14"N; 89°06'40"W) (11 July 

1994; 11 May 1997; 26 October 1998). 

PREVIOUS RECORDS: Rhamdia rogersi (Regan) 

(type host), San Pedro Monies de Oca, Costa 

Rica (Price, 1938); R. quelen (Quoy and Gai- 

mard) and R. sebae (Valenciennes), Cumuto 

River near Coryal, Trinidad (Molnar et al., 

1974). 

SPECIMENS STUDIED: 57 vouchers, USNPC 

88963, HWML 15015, UNAM 3710, IPCAS M- 

354, CHCM 313; 2 vouchers deposited by Molnar 

et al. (1974), USNPC 73178. 

REMARKS: Ameloblastella chavarriai (Price, 

1938) comb. n. is the type species of the genus. 

Although the morphometrics of present specimens 

differ from those reported in the original 

description by Price (1938), our specimens pos- 



sess the diagnostic morphological features of the 

species. Measurements of the body (247 (Jim 

long, 80 (Jim wide), haptor (45 u-m long, 70 (xm 

wide), and pharynx (20 [Am wide) reported by 

Price (1938) are noticeably smaller than those 

presented herein, suggesting that the type specimens 

were strongly contracted as a result of fixation. 

We do not consider these differences sufficient 

to warrant description of a new species 

for the helminths in our collection, since the 

method of fixation greatly influences the morphometrics 

of soft body parts. Fixation of our 

material in hot formalin resulted in extended 

specimens (Fig. 5), while ambient temperature 

formalin fixation (the method most likely used 

by Price, 1938) resulted in contracted specimens 

with a body length of about half that of those 

fixed in hot formalin. Haptoral sclerites and the 

copulatory complex in our specimens correspond 

morphometrically to respective values 

provided by Price (1938). Measurements by 

Molnar et al. (1974) generally fall within the 

ranges of the combined measurements of Price 

(1938) and those presented herein, respectively. 

Although numerous collections of R. guatemalensis 

were made from cenotes throughout 

the Yucatan Peninsula (see Scholz et al., 1995), 

A. chavarriai was found only in Ixin-ha Cenote. 

This suggests an apparent limited distribution of 

the species in the Yucatan Peninsula. However, 

individual collections from Ixin-ha Cenote conducted 

at different periods of 1997-1998 

showed intensity levels of A. chavarriai relative 

to the other dactylogyrid species (Aphanoblastella 

travossosi) on this host to vary from being 

predominant (^95%) to nearly insignificant 

(

er, and Boeger, 1986, and Amphocleithrium 

Price and Gonzalez-Romero, 1969, by having 

tandem gonads, nondilated hook shanks each 

with 1 subunit, counterclockwise rings in the 

male copulatory organ, a seminal vesicle formed 

by a simple dilation of the vas deferens, a sinistral 

vaginal pore, and a nonsclerotized vagina. It 

differs from Cosmetocleithrum by lacking 2 submedial 

projections on the dorsal bar and by having 

well-developed eyes (Kritsky et al., 1986). 

Aphanoblastella differs from Amphocleithrium 

by possessing 2 pairs of eyes and a nonarticulated 

male copulatory organ and accessory piece 

(Suriano and Incorvaia, 1995). 

The internal anatomy of species of Aphanoblastella 

is also identical to that of Demidospermus 

Suriano, 1983, as emended by Kritsky 

and Gutierrez (1998). Aphanoblastella differs 

from Demidospermus spp. by possessing short 

ventral bars with a medial process (ventral bars 

elongate, V- or W-shaped, lacking a medial process 

in Demidospermus}. Thumbs of hook pairs 

5 and 6 are modified in species of Demidospermus 

(see Kritsky and Gutierrez, 1998), whereas 

all hooks are similar and unmodified in Aphanoblastella 

spp. 

Three previously described species of Urocleidoides 

(sensu lato) from Rhamdia spp., U. 

travassosi (Price, 1938), U. robustus Mizelle 

and Kritsky, 1969, and U. mastigatus Suriano, 

1986, are transferred to Aphanoblastella as A. 

travassosi (Price, 1938) comb, n., A. robustus 

(Mizelle and Kritsky, 1969) comb, n., and A. 

mastigatus (Suriano, 1986) comb, n., respectively. 

Aphanoblastella travassosi comb. n. is the 

type species and therefore defines the new genus. 

Aphanoblastella mastigatus comb. n. also 

is clearly a member of the genus based on the 

original description (compare figures and description 

in Suriano, 1986a). Aphanoblastella 

mastigatus appears to be the sister species of A. 

travassosi. 

The original description of U. robustus by 

Mizelle and Kritsky (1969) was based on unstained 

and cleared specimens mounted in Gray 

and Wess' medium. Mizelle and Kritsky (1969) 

described the gonads to be tandem or overlapping, 

suggesting that the germarium is anterior 

to the testis with which it may overlap; the type 

specimens of U. robustus available to us were 

not useful in confirming gonadal position. Thus, 

our transfer of this species to Aphanoblastella is 

based on the original statements by Mizelle and 

KRITSKY ET AL.—DACTYLOGYRIDS FROM MEXICAN CENOTES 81 

Kritsky (1969) concerning gonadal position and 

on the similar position and morphology of sclerotized 

haptoral and copulatory structures to 

those of A. travassosi. 

Aphanoblastella travassosi (Price, 1938) 

comb. n. 

(Figs. 10-18) 

REDESCRIPTION: Body 282 (204-364; n = 

34) long; greatest width 104 (77-127; n = 32) 

in posterior trunk. Cephalic lobes poorly to moderately 

developed. Eyes equidistant, posterior 

pair larger; accessory granules usually uncommon 

in cephalic region. Pharynx subspherical, 

28 (21-33; n = 23) in diameter; esophagus 

short. Peduncle broad; haptor 55 (45-63; n = 

31) wide, 40 (33-50; n = 32) long. Ventral anchor 

22 (21-24; n = 13) long, with elongate 

superficial root, short deep root, straight shaft, 

curved elongate point; base 16 (14-17; n = 11) 

wide, variable. Dorsal anchor 24 (21-27; n = 

11) long, with well-developed roots, straight 

shaft, elongate curved point; base 16 (14-18; 

n = 12) wide. Ventral bar 32 (29-37; n = 10) 

long, delicate, broadly V-shaped, with posteromedial 

process directed posteriorly; dorsal bar 

37 (31-44; n = 9) long, broadly V-shaped, with 

narrowed bulbous ends. Hook 13 (12—14; n = 

23) long, with protruding thumb, delicate point, 

fine shank; FH loop about two-thirds shank 

length. Male copulatory organ 41 (38-45; n = 

5) long, a coil of about 2 rings, base of male 

copulatory organ with small sclerotized plate; 

diameter of proximal ring 5 (4-6; n = 6). Accessory 

piece 31 (28-36; n = 4) long, rodshaped, 

with broad terminal acute tip. Testis 

ovate, 51 (40-59; n = 19) long, 35 (25-46; 

n = 18) wide; seminal vesicle indistinct, fusiform, 

lying to left of male copulatory organ; 

prostatic reservoir not observed. Germarium 28 

(20-44; n = 23) long, 22 (18-25; n = 23) wide, 

pyriform, comprising comparatively few cells; 

oviduct, ootype not observed; uterus delicate; 

vagina a diagonal tube extending to left body 

margin, vaginal aperture simple; seminal receptacle 

small. 

SYNONYMS: Cleidodiscus travassosi Price, 

1938; Urocleidoides travassosi (Price, 1938) 

Molnar, Hanek, and Fernando, 1974. 

HOST AND LOCALITY: Gills of Rhamdia guatemalensis 

(Giinther); Ixin-ha Cenote, Yucatan, 

Mexico (20°37'14"N; 89°06'40"W) (13 June 



Figures 10-18. Aphanoblastella travassosi (Price, 1938) comb. n. 10. Whole mount (composite, ventral). 

11. Ventral bar. 12. Dorsal bar. 13. Copulatory complex (ventral). 14. Hook. 15. Dorsal anchor. 16-18. 

Ventral anchors. All drawings are to the 25-fjum scale except Figure 10 (100-fjim scale). 

1994; 11 July 1994; 11 May 1997; 26 October 

1998). 

OTHER RECORDS (specimens not used in this 

study): R. guatemalensis: Hubiku Cenote 

(20°49'79"N; 88°01'21"W) (18 April 1994); cenote 

in village of Hunucma (21°00'03"N; 

89°52'06"W) (8 November 1993); Scan-Yui Cenote 

(20°40'20"N; 88°32'51"W) (25 January 

1994); Tixkanka Cenote (21°14'55"N; 

88°58'45"W) (23 May 1994); Xcanganchen Ce- 


note (20°36'43"N; 89°05'32"W) (16 November 

1993); Homun Cenote (20°44'19"N; 89°17'49"W) 

(3 November 1993); Xmucuy Cenote 

(20°33'63"N; 88°59'50"W) (16 November 1993) 

(Mendoza-Franco et al., 1999). 

PREVIOUS RECORDS: Rhamdia rogersi (Regan), 

type host, San Pedro Monies de Oca, Costa 

Rica (Price, 1938); R. quelen (Quoy and Gaimard) 

and R. sebae (Valenciennes), Cumuto 

River near Coryal, Trinidad (Molnar et al.,

1974); P. laticeps Eigenmann, Laguna de Chascomus, 

Buenos Aires, Argentina (Suriano, 

1986a). 

SPECIMENS STUDIED: 49 vouchers, USNPC 

88964, HWML 15016, UN AM 3711, IPCAS M- 

353, CHCM 314; 3 vouchers deposited by Molnar 

et al. (1974), USNPC 73179. 

REMARKS: Aphanoblastella travassosi is 

widely distributed in cenotes of the Yucatan 

Peninsula. All available specimens were slightly 

to strongly contracted as a result of fixation in 

ambient 4% formalin; however, our measurements 

correspond fairly closely to respective 

values reported by Price (1938), Molnar et al. 

(1974), and Suriano (1986a). Price (1938) did 

not describe or draw the accessory piece of the 

copulatory complex of this species but indicated 

that one was present; the drawing of the copulatory 

complex by Molnar et al. (1974) corresponds 

to our Figure 13, while that provided by 

Suriano (1986a) is apparently distorted. 

Discussion 

Of the 22 species of Urocleidoides from the 

Neotropical Region that were considered incertae 

sedis by Kritsky et al. (1986), 17 remain to 

be reassigned at the generic level: Urocleidoides 

affinis Mizelle, Kritsky, and Crane, 1968, from 

Characidae (Characiformes); Urocleidoides 

amazonensis Mizelle and Kritsky, 1969, from 

Pimelodidae (Siluriformes); Urocleidoides carapus 

Mizelle, Kritsky, and Crane, 1968, from 

Gymnotidae (Gymnotiformes); Urocleidoides 

catus Mizelle and Kritsky, 1969, from Pimelodidae 

(Siluriformes); Urocleidoides corydori 

Molnar, Hanek, and Fernando, 1974, from Callichthyidae 

(Siluriformes); Urocleidoides costaricensis 

(Price and Bussing, 1967) Kritsky and 

Leiby, 1972, from Characidae (Characiformes); 

Urocleidoides gymnotus Mizelle, Kritsky, and 

Crane, 1968, from Gymnotidae (Gymnotiformes); 

Urocleidoides heteroancistrium (Price and 

Bussing, 1968) Kritsky and Leiby, 1972, from 

Characidae (Characiformes); Urocleidoides kabatai 

Molnar, Hanek, and Fernando, 1974, from 

Characidae (Characiformes); Urocleidoides lebedevi 

Kritsky and Thatcher, 1976, from Pimelodidae 

(Siluriformes); Urocleidoides margolisi 

Molnar, Hanek, and Fernando, 1974, from Callichthyidae 

(Siluriformes); Urocleidoides megorchis 

Mizelle and Kritsky, 1969, from Pimelodidae 

(Siluriformes); Urocleidoides microstomus 


KRITSKY ET AL.—DACTYLOGYRIDS FROM MEXICAN CENOTES 

Characidae (Characiformes); Urocleidoides stictus 


Characidae (Characiformes); Urocleidoides 

strombicirrus (Price and Bussing, 1967) Kritsky 

and Thatcher, 1974, from Characidae (Characiformes); 

Urocleidoides trinidadensis Molnar, 

Hanek, and Fernando, 1974, from Characidae 

(Characiformes); and Urocleidoides virescens 

Mizelle, Kritsky, and Crane, 1968, from Gymnotidae 

(Gymnotiformes). Previously, Kritsky et 

al. (1989) transferred Urocleidoides variabilis 

Mizelle and Kritsky, 1969, a parasite of neotropical 

Cichlidae (Perciformes), to Sciadicleithrum 

Kritsky, Thatcher, and Boeger, 1989. In the 

present study, 5 species of Urocleidoides (sensu 

lato) from pimelodids (1 described subsequent 

to the emended diagnosis of Urocleidoides by 

Kritsky et al., 1986) are reassigned to Ameloblastella 

gen. n. or Aphanoblastella gen. n. 

Six of the Urocleidoides spp. remaining as incertae 

sedis occur on siluriform catfishes in the 

Neotropical Biogeographical Region. Based on 

the comparative morphology of the copulatory 

complexes of U. corydori, U. margolisi, and 

Philocorydoras platensis Suriano, 1986, the former 

2 species should probably be transferred to 

Philocorydoras (see Suriano, 1986b; Molnar et 

al., 1974). We have not formally made this transfer 

because details of the internal anatomy, particularly 

those of the reproductive systems, are 

lacking. 

A new genus for U. amazonensis, U. catus, 

U. megorchis, and perhaps U. lebedevi is probably 

justified based in part on presence of modified 

hook pairs 5 and 6 (slender hook shank, 

degenerate thumb, and straight point). While 

these species lack other generic characters of 

Demidospermus (as emended by Kritsky and 

Gutierrez, 1998) and therefore cannot be accommodated 

in it, species of Demidospermus also 

have modified hook pairs 5 and 6, suggesting a 

phylogenetic relationship between these species 

and Demidospermus spp. Mizelle and Kritsky's 

(1969) use of "gut normal" in their descriptions 

of U. amazonensis, U. catus, and U. megorchis 

is presumed to mean that the gut consists of a 

bifurcated esophagus and 2 ceca confluent posterior 

to the gonads. However, U. lebedevi was 

reported to have 2 blind ceca posterior to the 

gonads (Kritsky and Thatcher, 1976). Features 

of the digestive system in all of these species 

must be verified before formal proposals for generic 

placement can be made. 




The authors are indebted to Joaquin Vargas- 

Vasquez, Clara Vivas-Rodriguez, Raul Sima-Alvarez, 

Jorge Guemez-Ricalde, Gregory Arjona- 

TOITCS, Victor Ceja-Moreno, and Miguel Hen-era-Rodriguez, 

all of CINVESTAV-IPN, Merida, 

for field assistance. Dr. Victor Vidal-Martfnez, 

CINVESTAV-IPN, Merida, provided valuable 

advice on the species reported herein. Dr. J. 

Ralph Lichtenfels, USNPC, allowed us to examine 

type and voucher specimens in his care. 

Host identification was provided by Esperanza 

Perez-Diaz and Mirella Hernandez de Santillana, 

both of CINVESTAV-IPN, Merida. This study 

was supported by a grant (PO99) from the Comision 

Nacional para el Uso y Conocimiento de 

la Biodiversidad (CONABIO), Mexico. 


Kritsky, D. C., W. A. Boeger, and V. E. Thatcher. 

1985. Neotropical Monogenea. 7. Parasites of the 

pirarucu, Arapaima gigas (Cuvier), with descriptions 

of two new species and redescription of 

Dawestrema cycloancistrium Price and Nowlin. 

1967 (Dactylogyridae: Ancyrocephalinae). Proceedings 

of the Biological Society of Washington 

98:321-331. 

, and P. A. Gutierrez. 1998. Neotropical Monogenoidea. 

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Ancyrocephalinae) from the gills of 

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124.



Species of Sciadicleithrum (Dactylogyridae: Ancyrocephalinae) of 

Cichlid Fishes from Southeastern Mexico and Guatemala: New 

Morphological Data and Host and Geographical Records 

EDGAR MENDOZA-FRANCO, '-3 VICTOR VIDAL-MARTINEZ,' LEOPOLDINA AGUIRRE-MACEDO,' 

ROSSANNA RODRIGUEZ-CANUL,1 AND TOMAS SCHOLZ1'2 

1 Laboratory of Parasitology, Center for Research and Advanced Studies, National Polytechnic Institute 

(CINVESTAV-IPN), Carretera Antigua a Progreso Km. 6, A.P. 73 "Cordemex", C.P. 97310 Merida, Yucatan, 

Mexico (e-mail: mfranco@kin.cieamer.conacyt.mx), and 

2 Institute of Parasitology, Academy of Sciences of the Czech Republic, Branisovska 31, 

370 05 Ceske Budejovice, Czech Republic 

ABSTRACT: A survey of species of Sciadicleithrum (Monogenca: Dactylogyridae) from the gills of cichlid fishes 

from the Yucatan Peninsula of Mexico and neighboring regions is provided. Sciadicleithrum mexicanwn Kritsky, 

Vidal-Martfnez, and Rodrfguez-Canul is reported from Cichlasoma urophthalmus (type host), Cichlasoma aureum, 

and Petenia splendida (new host records) from Mexico, and Cichlasoma trimaculatum from Guatemala 

(new host and geographical record); Sciadicleithrum bravohollisae Kritsky, Vidal-Martfnez, and Rodrfguez-Canul 

from Cichlasoma geddesi, Cichlasoma lentiginosum, Cichlasoma managuense, Cichlasoma salvini, and Cichlasoma 

sp. (all new host records); Sciadicleithrum splendidae Kritsky, Vidal-Martfnez, and Rodrfguez-Canul 

from Cichlasoma friedrichstahli and C. managuense (new host records); and Sciadicleithrum rneekii Mendoza- 

Franco, Scholz, and Vidal-Martfnez from Cichlasoma callolepis, Cichlasoma helleri, and C. managuense (new 

host records) from Mexico. Data on morphological and biometrical variability of individual species from different 

hosts are provided. Species of Sciadicleithrum from Mexico and Guatemala exhibit wide host specificity. The 

present records expand distributional areas of all of the species of Sciadicleithrum studied. 

KKY WORDS: Sciadicleithrum, Monogenea, Dactylogyridae, Cichlidae, host specificity, zoogeography, Mexico, 

Guatemala. 

Sciadicleithrum was proposed by Kritsky et 

al. (1989) to accommodate 9 species of Ancyrocephalinae 

(Monogenea: Dactylogyridae) 

from cichlid fishes from South America. Since 

then, 4 other species have been described from 

cichlids of the Peninsula of Yucatan, Mexico, 

namely Sciadicleithrum mexicanwn Kritsky, Vidal-Martfnez, 

and Rodrfguez-Canul, 1994, from 

Cichlasoma urophthalmus (Gunther, 1862); 

Sciadicleithrum bravohollisae Kritsky. Vidal- 

Martfnez, and Rodrfguez-Canul, 1994, from 

Cichlasoma pearsei (Hubbs, 1936), Cichlasoma 

synspilum Hubbs, 1935, and Petenia splendida 

Gunther, 1862; Sciadicleithrum splendidae Kritsky, 

Vidal-Martfnez, and Rodrfguez-Canul, 

1994, from Petenia splendida; and Sciadicleithrum 

meekii Mendoza-Franco, Scholz, and Vidal- 

Martfnez, 1997, from Cichlasoma meeki (Brind, 

1918) (Kritsky et al., 1994; Mendoza-Franco et 

al., 1997). 

During a recent helminthological study on 

cichlid fishes from southeastern Mexico, monogeneans 

assigned to Sciadicleithrum were found 

-' Corresponding author. 

on the gills of several species of Cichlidae, including 

hosts not reported previously. This new 

material allowed us to supplement the original 

descriptions (sometimes based on a limited number 

of specimens) by morphological and biometrical 

data on intraspecific variability of individual 

species from different fish hosts. Numerous 

new host and geographical records also 

made it possible to evaluate the specificity of 

species of Sciadicleithrum from the Yucatan 

Peninsula. 

Material and Methods 

Cichlids were collected by line and hook, throw 

nets, or electrofishing from the following localities 

in southeastern Mexico and Guatemala: Mexico. 

State of Chiapas: Cedros River (16°45'21"N; 

91°09'30"W) and Lacanja River (16°46'21"N; 

91°04'21"W). State of Tabasco: Santa Anita Lagoon 

(18°22'15"N; 92°53'10"W); El Yucateco Lagoon 

(18°11'33"N 

(18°25'35"N 

(17°59'46"N 

(18°14'57"N 

(18°00'37"N 

94°00'35"W); Parafso River 

93°12'00"W); Ilusiones Lagoon 

92°56'17"W); Horizonte Lagoon 

92°49'59"W); Yumka Lake 

92°48'12"W); Puyacatengo River 

(17°34'58"N; 92°53'22"W). State of Campeche: Palizada 

River (18°17'16"N; 91°56'52"W); Silvituc La- 



goon (18°37'50"N; 90°16'50"W); La Pera Lagoon 

(18°16'57"N; 91°56'21"W); Terminos Lagoon, Santa 

Gertrudis station (18°26'51"N; 91°48'59"W); Rancho 

II station (18°20'30"N; 91°42'30"W); El Viento 

station (18°26'01"N; 91°49'48"W). State of Yucatan: 

Dzaptiin Cenote (20°51'19"N; 90°14'09"W); Chaamac 

Cenote (20°51'53"N; 90°09'18"W); Petentuche 

Cenote (21°33'90"N; 88°04'44"W); Dzonot Cervera 

Cenote (21°22'36"N; 88°49'59"W); Ojo de Agua ( = 

water spring), Celestun Lagoon (20°52'37"N; 

90°21'18"W). State of Quintana Roo: Mahahual 

(18°58'17"N; 87°57'30"W); Cenote Azul (Bacalar) 

(18°38'11"N; 88°24'46"W); Raudales Lagoon 

(18°42'27"N; 88°15'22"W); Hondo River (18°17'N; 

88°38'W); Valle Hermoso Lagoon (19°10'N; 

88°31'W); Rancho Don Milo (18°37'43"N; 

88°01'15"W). Guatemala: Champerico River, Department 

of Retalhuleu, near the border with El Salvador 

(14°20'N; 91°54'W). 

Sampling dates and parameters of infection are provided 

for each species in the results section. Fishes 

were transported alive to the laboratory and dissected 

using standard parasitological procedures. Monogeneans 

found on the gills were isolated and fixed with a 

glycerin-ammonium picrate mixture and then remounted 

in Canada balsam (Ergens, 1969). However, 

in most cases this technique was modified using Berland's 

solution before applying a glycerin—ammonium 

picrate mixture (Berland, 1961). A worm was placed 

in a small droplet of water on a slide, a small amount 

of Berland's solution was added using a fine brush, and 

the worm was covered with a coverslip. Excessive solution 

was removed with filter paper. Each corner of 

the coverslip was sealed with Du-Noyer sealant (Ergens 

and Gelnar, 1992) and glycerin-ammonium picrate 

solution was added to the edge of the coverslip. 

Processed worms were remounted in Canada balsam 

according to Ergens (1969). 

In addition, some worms, fixed in 4% formalin, 

were stained with Gomori's trichrome to study the 

morphology of internal organs; others were mounted 

unstained in glycerin jelly. All measurements are given 

in micrometers; the mean is followed by the range and 

number of specimens measured in parentheses. The 

number of fishes infected of the total examined is followed 

by the mean and the minimum and maximum 

in parentheses. Drawings were made with the aid of 

an Olympus drawing tube. 

Specimens were deposited in the National Helminthological 

Collection of Mexico, Institute of Biology, 

National Autonomous University of Mexico (UNAM), 

Mexico (CNHE); the United States National Parasite 

Collection, Beltsville, Maryland, U.S.A. (USNPC); the 

Institute of Parasitology, Academy of Sciences of the 

Czech Republic, Ceske Budejovice, Czech Republic 

(IPCAS); the Natural History Museum, London, United 

Kingdom (BMNH); and the Laboratory of Parasitology, 

Center for Research and Advanced Studies of 

the National Polytechnic Institute (CINVESTAV-IPN), 

Merida, Yucatan, Mexico (CHCM). 

Results 

Sciadicleithrum bravohollisae Kritsky, 

Vidal-Martinez, and Rodriguez-Canul, 1994 

MEASUREMENTS (based on 10 specimens from 

Cichlasoma salvini (Giinther 1862)): Haptor 


142 (120-190; n = 5) wide, 77 (62-105; n = 

6) long. Pharynx spherical, 47 (39=65; n = 4) 

in diameter. Ventral hamuli 29 (27-32; n = 18) 

long; base width 17 (16-18; n = 18). Dorsal 

hamuli 33 (31-34; n = 15) long; base width 15 

(13-16; n = 15). Ventral bar 35 (29-45; n = 7) 

long; dorsal bar 36 (31-44; n — 6) long. Hooks 

15 (13-15; n — 20) long. Male copulatory organ 

31 (25—36; n = 4) long. Accessory piece 20 

(18-22; n = 6) long. 

HOSTS, LOCALITIES, SAMPLING DATES, AND PA- 

RAMETERS OF INFECTION: Cichlasoma geddesi 

Regan, 1905, Horizonte Lagoon (17 November 

1998), 1 fish infected of 1 examined; mean intensity 

of infection 12 specimens; Cichlasoma 

lentiginosum (Steindachner, 1864), Lacanja River 

(21 May 1998), 2/3, 3 (minimum intensity 3, 

maximum intensity 4); Cichlasoma managuense 

(Gunther, 1869), Santa Gertrudis (17 March 

1998), 1/1, 2; C. pearsei, Santa Gertrudis (17 

March 1998), 1/7, 2; Lacanja River (21 May 

1998), 2/3, (3-6); Palizada River (15 June 

1998), 1/1, 4; C. salvini, Dzaptun Cenote (21 

August 1996; 1 October 1997), 3/4, 2 (3-5), 51 

5 (4-5); Lacanja River (21 May 1998), 1/1, 2; 

Ilusiones Lagoon (16 November 1998), 5/10, 2 

(1-3); Horizonte Lagoon (17 November 1998), 

1/1, 19; Yumka Lake (18 November 1998), 1/3, 

1; Puyacatengo River (19 November 1998), 21 

10, 3 (1—6); C. synspilum, Cenote Azul (2 March 

1998), 1/1, 6; Rancho II (17 March 1998), 1/6, 

1; Raudales Lagoon (8 May 1998), 2/16, 14 (8- 

21); Palizada River (15 June 1998), 1/6, 5; Cichlasoma 

sp., Paraiso River (20 March 1998), 1/1, 5. 

SPECIMENS DEPOSITED: Voucher specimens 

from C. pearsei and C. synspilum in CHCM 

(Nos. 215 and 214), from C. salvini in CNHE 

(Nos. 3132 and 3133), IPCAS (No. M-348), 

USNPC (Nos. 88946 and 88950), and CHCM 

(Nos. 229 and 231). 

REMARKS: Specimens found in C. salvini do 

not differ from those of S. bravohollisae, as described 

from C. pearsei, C. synspilum, and P. 

splendida by Kritsky et al. (1994). The present 

material enabled us to add some new data on the 

morphology of the copulatory complex and the 

vaginal aperture. Kritsky et al. (1994) reported 

the length of the accessory piece to be 31—45 

and 26-37 in specimens from C. pearsei and C. 

synspilum, respectively. The present specimens 

have the accessory piece considerably shorter, 

measuring only 18—22. 

The shape of the vaginal aperture is similar to

MENDOZA-FRANCO ET SCIADICLEITHRUM FROM MEXICO AND GUATEMALA 87 

Table 1. Measurements (in micrometers; mean with range in parentheses; n = number of measurements) 

of Sciadicleithrum mexicanum Kritsky, Vidal-Martinez, and Rodriguez-Canul, 1994, from 4 species of 

cichlid fishes from the Yucatan Peninsula of Mexico and Guatemala. 

Body length 

Pharynx width 

Ventral hamuli length 

Ventral hamuli width 

Dorsal hamuli length 

Dorsal hamuli width 

Ventral bar length 

Dorsal bar length 

Hooks 

MCO:j: length 

Accessory piece 

Cichlasoma 

urophthalmus* 

320 (245-398) 

18 (15-20) 

33 (29-35) 

16 (15-17) 

39 (35-41) 

14 (13-16) 

34 (30-37) 

31 (29-33) 

15 (14-17) 

62 (53-68) 

45 (37-52) 

n 

24 

20 

22 

17 

19 

16 

21 

21 

71 

17 

12 

Cichlasoma 

trimaculatum^ 

302 (249-319) 

22 (19-26) 

33 (32-35) 

15 (14-16) 

39 (35-41) 

16 (14-19) 

38 (31-44) 

34 (32-37) 

15 (15-16) 

42 (35-45) 

— 

* Original descriptions of S. mexicanum by Kritsky et al. (1994). 

t Champerico River, Guatemala. 

$ Male copulatory organ. 

the original description in the presence of 2 opposing 

funnel-shaped distal sclerites. Comparison 

of specimens from C. salvini and C. synspilum 

showed that this structure was smaller 

(length 10-11) and more delicate in the former 

fish host than in worms from C. synspilum 

(length 19-23). Measurements of the haptor of 

the currently studied specimens are also noticeably 

greater than those of this species reported 

from C. pearsei, C. synspilum, and P. splendida 

(Kritsky et al., 1994). It is possible that the specimens 

studied are more strongly extended, as a 

result of fixation with Berland's solution and a 

glycerin—ammonium picrate mixture, since the 

method of fixation greatly influences size in soft 

body parts. Specimens found on C. geddesi, C. 

lentiginosum, C. managuense, C. salvini, and 

Cichlasoma sp. represent new host records and 

expand the distributional area of S. bravohollisae 

to the Mexican states of Campeche, Chiapas, 

and Tabasco. 

Sciadicleithrum meekii Mendoza-Franco, 

Scholz, and Vidal-Martinez, 1997 

MEASUREMENTS (based on 8 specimens from 

C. meeki}: Haptor 74 (63-80; n = 3) wide. 

Pharynx spherical, 15 (13-15; n = 5) in diameter. 

Ventral hamuli 19 (16-23; n = 4) long; 

base width 12(ll-13;n = 4). Dorsal hamuli 33 

(32-34; n = 2) long; base width 11. Ventral bar 

19 (16-23; n = 4) long; dorsal bar 29 (27-30; 

n = 4) long. Hooks 13 (12-13; n = 14) long. 


n 

4 

3 

14 

14 

12 

11 

7 

7 

8 

4 

0 

Cichlasoma 

aureum 

— 

25 (16-32) 

30 (29-32) 

14 (13-15) 

36 (35-37) 

13 (13-15) 

38 (32-43) 

34 (29-39) 

15 (14-17) 

39 (32-44) 

48 (42-52) 

n 

0 

11 

22 

22 

18 

18 

11 

11 

31 

11 

11 

Petenia 

splendida 

— 28 

32 (31-33) 

15 (14-17) 

37 (34-39) 

12 (11-15) 

36 (35-40) 

34 (31-42) 

17 (15-18) 

45 (42-51) 

47 

n 

0 

1 

10 

10 

10 

10 

5 

5 

12 

5 

1 

RAMETERS OF INFECTION: Cichlasoma callolepis 

(Regan, 1904), Lacanja River (19 May 1998), I/ 

3, 9; Cichlasoma helleri (Steindachner, 1864), 

Ilusiones Lagoon (16 November), 2/10, 2 (1-3); 

Horizonte Lagoon (17 November 1998), 1/10, 1; 

Yumka Lake (18 November 1998), 1/10, 3; C. 

meeki, Mahahual (8 December 1997), 2/10 (2- 

12); Mahahual (2 March 1998), 2/2, 4 (3-5); 

Chaamac Cenote (16 April 1998), 2/6, 7 (2-12); 

C. managuense, El Viento (17 March 1998), II 

1, 2; Santa Anita Lagoon (24 April 1998), 1/1, 

3; Hondo River (11 May 1998), 1/4, 3. 


from C. helleri in CNHE (No. 3722), CHCM 

(No. 227) and USNPC (No. 88947). 

REMARKS: Findings of S. meekii, originally 

described from C. meeki, in 3 other cichlid species 

demonstrate that this parasite is not restricted 

to the type host, C. meeki. 

Sciadicleithrum mexicanum Kritsky, 

Vidal-Martinez, and Rodriguez-Canvil, 1994 

MEASUREMENTS: Measurements of 28 specimens 

studied from different hosts are given in 

Table 1. 


RAMETERS OF INFECTION: Cichlasoma aureum 

(Gunther, 1862), Petentuche Cenote (10 October 

1997), 2/2, 54 (32-76); Ojo de Agua in Celestun 

Lagoon (15 August 1997), 1/2, 13; Chaamac Cenote 

(16 April 1998), 1/1, 75; Dzonot Cervera 

Cenote (15 April 1998), 1/1, 5; Cichlasoma 

friedrichstahli (Heckel, 1840), Dzonot Cervera 



Cenote (15 April 1998), 1/1, 20; Cichlasoma octofasciatum 

(Regan, 1903), Cedros River (19 

May 1998), 4/4, 4 (1-7); Cichlasoma trimaculatum 

(Giinther, 1869), Champerico River (16 

December 1995), 3/3, 34 (14-37); C. urophthalmus, 

El Yucateco Lagoon (30 January 1998), 7/ 

8, 65 (2-284); Cenote Azul (2 March 1998), I/ 

3; 4, Mahahual (2 March 1998), 3/3, 16 (4-16); 

Dzonot Cervera Cenote (15 April 1998), 1/3, 1; 

Rancho Don Milo (8 May 1998), 1/3, 12; La 

Pera Lagoon (15 June 1998), 1/8, 50; Petentuche 

Cenote (10 October 1997), 1/1, 52; P. splendida, 

Dzaptun Cenote (21 August 1996), 1/1, 18; Silvituc 

Lagoon (15 July 1997), 1/1, 7; Valle Hermoso 

Lagoon (2 March 1998), 1/1, 15; Palizada 

River (15 June 1998), 1/2, 12; Santa Anita Lagoon 

(24 April 1998), 1/1. 


from C. aureum and C. friedrichstahli in 

USNPC (Nos. 88943 and 88945); from C. tri 

maculatum in CNHE (No. 3136), USNPC (No. 

88944), BMNH (No. 1999.7.13.25), and CHCM 

(Nos. 224 and 225); from P. splendida in CNHE 

(Nos. 3135 and 3136), IPCAS (No. M-343), 

USNPC (No. 87303), and CHCM (No. 220). 

REMARKS: The morphology and measurements 

of the specimens found in the different 

hosts correspond well to the description of S. 

mexicanum from C. urophthalmus by Kritsky et 

al. (1994). Cichlasoma aureum, C. trimaculatum, 

and P. splendida represent new host records. 

The finding of S. mexicanum in Guatemala 

is the first record of this parasite in Central 

America. The present data, together with those 

of Mendoza-Franco et al. (1999), who reported 

S. mexicanum from C. friedrichstahli, C. octofasciatum, 

and C. synspilum, demonstrate a wide 

host specificity of 5. mexicanum. 

Sciadicleithrum splendidae Kritsky, 

Vidal-Martmez, and Rodriguez-Canul, 1994 

(Figs. 1-11) 

MEASUREMENTS: Measurements of 41 specimens 

studied from different hosts and localities 

are given in Table 2. 


RAMETERS OF INFECTION: C. friedrichstahli, 

Dzaptun Cenote (1 August 1997), 1/1, 9; Mahahual 

(2 March 1998), 2/2, 9 (7-11); Cedros River 

(19 May 1998), 8/15, 10 (1-18); C. managuense, 

Santa Gertrudis (17 March 1998), 1/1, 4. 


from C. friedrichstahli in CNHE (Nos. 3720 and 


3721), CHCM (No. 218), USNPC (Nos. 88948 

and 88949), and BMNH (No. 1999.7.13.26). 

REMARKS: Both species of Cichlasoma studied 

are new hosts of S. splendidae. Specimens 

obtained from C. friedrichstahli closely resemble 

in their morphology those of S. splendidae 

from P. splendida previously described by Kritsky 

et al. (1994). All possess hamuli relatively 

similar in size and shape, the base of the copulatory 

organ with bilobed proximal branch, and 

a vagina comprising a sclerotized tube looping 

anteriorly on the dextromedial half of the trunk. 

However, there are slight differences between 

the present material and that of S. splendidae in 

the number of coils of the male copulatory organ 

(1.5 rings in the specimens studied versus more 

than 2 in S. splendidae) and the size of the accessory 

piece, 38 (30—45) in worms from C. 

friedrichstahli and 22 in specimens from the 

type host. Similarly to S. bravohollisae, the differences 

in the measurements of sclerotized and 

soft body parts of specimens from C. friedrichstahli 

might be related to the size of the worms 

and the method of fixation (see Fig. 6). A similar 

phenomenon has previously been observed 

among individual specimens of Sciadicleithrum 

umbilicum Kritsky, Thatcher, and Boeger, 1989, 

from South America (Kritsky et al., 1989). 

The original description of S. splendidae was 

based on only 2 specimens (Kritsky et al., 1994). 

The additional material from this study evidences 

that the shape and number of coils of the male 

copulatory organ vary among specimens from 

the same hosts (Figs. 2-4) and that this species 

possesses a seminal vesicle (see Fig. 1) that 

lacks a thickened wall, as is present in congeneric 

species of Sciadicleithrum from Yucatan 

(Kritsky et al., 1994; Mendoza-Franco et al., 

1997). As for S. bravohollisae, S. splendidae occurs 

in members of 2 genera of cichlid fishes, 

Cichlasoma and Petenia. 

Discussion 

Species of Sciadicleithrum were first reported 

from cichlids from South America (Kritsky et 

al., 1989) and subsequently from cichlid fishes 

from southeastern Mexico (Kritsky et al., 1994; 

Mendoza-Franco et al., 1997, 1999). The present 

study confirmed previous observations by the 

latter authors that the fauna of monogeneans assigned 

to Sciadicleithrum from the Yucatan Peninsula 

of Mexico and neighboring areas is depauperate 

in the number of species.

MENDOZA-FRANCO ET AL.—SCIADICLEITHRUM FROM MEXICO AND GUATEMALA 89 

Figures 1-11. Sciadicleithrum splendidae. 1. Total view (ventral). 2—4. Copulatory complexes (2, 3. 

ventral view; 4. dorsal view). 5. Vagina. 6. Whole mount (fixed with Berland's solution and a glycerinammonium 

picrate mixture). 7. Ventral bar. 8. Dorsal bar. 9. Ventral hamulus. 10. Hook. 11. Dorsal 

hamulus. Scale bars = 50 |xm (Fig. 1), 30 fxm (Figs. 2, 7-11), 40 urn (Figs. 3-5), and 200 (xm (Fig. 6). sv 

= seminal vesicle; f = filament. 



Table 2. Measurements (in micrometers; mean with range in parentheses; n = number of structures 

measured) of Sciadicleithrum splendidae Kritsky, Vidal-Martinez, and Rodriguez-Canul, 1994, from 3 

species of cichlid fishes from 4 localities (Chiapas, Tabasco, Yucatan, and Quintana Roo) from southeastern 

Mexico. 

Body length 

Pharynx width 

Ventral hamuli length 

Ventral hamuli width 

Dorsal hamuli length 

Dorsal hamuli width 

Ventral bar length 

Dorsal bar length 

Hooks 

MCOI length 

Accessory piece length 

Petenia 

splendida* 

250 

20 

32 

17 

40 

14 

39 

37 

(15-16) 

31 (27-35) 

22 

n 

1 

1 

1 

1 

1 

1 

2 

2 

6 

2 

1 

Cichlasoma 

friedrichstahlrf 

621 (406-690) 

35 (24-43) 

38 (36-38) 

16 (15-18) 

42 (39-44) 

12 (10-14) 

50 (42-53) 

41 (37-48) 

15 (15-16) 

44 (42-50) 

38 (30-45) 

n 

8 

8 

16 

16 

16 

15 

8 

8 

8 

9 

8 

* Original descriptions of S. splendidae by Kritsky et al. (1994). 

t Dzaptiin Cenote, Yucatan. 

t Cedros River, Chiapas. 

§ Mahahual, Quintana Roo. 

|| Santa Gertrudis, Tabasco. 

1 Male copulatory organ. 

In addition, this study expanded the spectrum 

of fish hosts of individual Sciadicleithrum taxa 

found in southeastern Mexico and Guatemala by 

13 new host records. Each of the 4 species of 

Sciadicleithrum found in this area exhibits relatively 

wide host specificity in the same family, 

since they occur in as many as 8 cichlid species 

(5. bravohollisae in C. geddesi, C. lentiginosum, 

C. managuense, C. pearsei, C. salvini, C. synspilum, 

P. splendida, and Cichlasoma sp.). 

Three species of Sciadicleithrum found in Yucatan 

occur even in members of 2 closely related 

genera, Cichlasoma and Petenia. It is also noteworthy 

that both P. splendida and C. managuense 

from southeastern Mexico harbor as 

many as 3 species of Sciadicleithrum, namely, 

S. bravohollisae, S. mexicanum, and S. splendi 

dae\d S. bravohollisae, S. splendidae, and S 

meekii, respectively. In the Terminos Lagoon 

(stations El Viento and Santa Gertrudis), 3 species 

of Sciadicleithrum (S. bravohollisae, S. 

meekii, and S. splendidae) occurred, and all 

these species are found on C. managuense. It 

can be assumed that horizontal transmission of 

these monogeneans to this cichlid occurred in 

this locality, with C. helleri probably serving as 

a source of S. meeki, and C. pearsei of S. bravohollisae. 

Sciadicleithrum splendidae was 

Cichlasoma 

friedrichstahlij. 

— 

19 (17-24) 

31 (29-34) 

14 (12-16) 

37 (33-39) 

12 (12-14) 

38 (36-43) 

30 (26-35) 

15 (15-16) 

40 (31-49) 

34 (29-36) 

Cichlasoma 

friedrichstahn 

//§ 

0 

2 

22 

20 

16 

10 

15 

14 

26 

20 

12 


19 (17-20) 

29 (22-31) 

12 (12-13) 

36 (36-37) 

13 

41 (40-41) 

32 (30-33) 

16 (15-17) 

36 (29-39) 

29 (20-39) 

n 

0 

8 

6 

4 

4 

2 

3 

3 

13 

7 

6 

Cichlasoma 

motaguense\\1 

(18-24) 

31 (30-32) 

16 

38 (33-41) 

14 (14-15) 

43 (40-46) 

32 (31-32) 

16 (15-17) 

38 (27-51) 

32 (24-47) 

found only on C. managuense at this locality 

and may represent the original host of S. splendidae. 

This study has also provided new data on intraspecific 

variability of Sciadicleithrum species 

from a wide spectrum of fish hosts and geographical 

regions. It is obvious that the knowledge 

of intraspecific morphological and biometrical 

variation is necessary to prevent descriptions 

of new taxa based only on slight morphological 

differences. This is important if the 

original descriptions were based on limited numbers 

of specimens, as in the case of S. splendidae 

(Kritsky et al., 1994). 

A species of Sciadicleithrum, S. mexicanum, 

is reported from Guatemala for the first time in 

this study. However, the occurrence of other 

Sciadicleithrum taxa in Guatemala is highly 

probable, and we suggest that more studies on 

the helminth parasites of freshwater in that 

country and Central America in general be carried 

out. Investigations into fish helminths, including 

gill monogeneans, are therefore needed 

for a better understanding of the evolution of 

these parasites and their hosts in the transient 

area between the Nearctic and Neotropical zoogeographical 

regions. 

n 

0 

4 

3 

1 

4 

2 

3 

2 

6 

4 

3

MENDOZA-FRANCO ET M^.—SCIADICLEITHRUM FROM MEXICO AND GUATEMALA 91 


The authors are indebted to Clara Vivas-Rodriguez, 

Ana Sanchez-Manzanilla, David Gonzalez-Solfs, 

and Isabel Jimenez-Garcfa for their excellent 

assistance in collecting and examining 

fishes, and to Dr. Frantisek Moravec, Institute of 

Parasitology, Academy of Sciences of the Czech 

Republic, Ceske Budejovice, for valuable suggestions 

on an early draft of the manuscript. 

This study was supported by grant No. M-135 

of the Comision Nacional para el Uso y Conocimiento 

de la Biodiversidad (CONABIO), 

Mexico. 


Berland, B. 1961. Use of glacial acetic acid for killing 

parasitic nematodes for collection purposes. Nature, 

London 191:1320-1321. 

Ergens, R. 1969. The suitability of ammonium picrate-glycerin 

in preparing slides of lower Monogenoidea. 

Folia Parasitologica 16:320. 

, and M. Gelnar. 1992. Monogenea and other 

ectoparasitic metazoans. Pages 4-32 /// Methods 

Meeting Announcement 

of Investigating Metazoan Parasites. Training 

course on fish parasites. Ceske Budejovice, March 

10-23. Institute of Parasitology, Czechoslovak 

Academy of Sciences. 

Kritsky, D. C., V. E. Thatcher, and W. A. Boeger. 

1989. Neotropical Monogenea. 15. Dactylogyrids 

from the gills of Brazilian Cichlidae with proposal 

of Sciadicleithrum gen. n. (Dactylogyridae). Proceedings 

of the Helminthological Society of 

Washington 56:128-140. 

, V. M. Vidal-Martfnez, and R. Rodriguez- 

Canul. 1994. Neotropical Monogenoidea. 19. 

Dactylogyridae of cichlids (Perciformes) from the 

Yucatan Peninsula, with descriptions of three new 

species of Sciadicleithrum Kritsky, Thatcher and 

Boeger, 1989. Journal of the Helminthological Society 


Mendoza-Franco, E. F., T. Scholz, and V. M. Vidal- 

Martinez. 1997. Sciadicleithrum meekii sp. n. 

(Monogenea: Ancyrocephalinae) from the gills of 

Cichlasoma mceki (Pisces: Cichlidae) from cenotes 

(=sinkholes) of the Yucatan Peninsula, Mexico. 

Folia Parasitologica 44:205-208. 

, , C. Vivas-Rodriguez, and J. Vargas- 

Vazquez. 1999. Monogeneans of freshwater fishes 

from cenotes ( = sinkholes) in the Yucatan Peninsula, 

Mexico. Folia Parasitologica 46:267-273. 

The Third Seminar on Food- and Water-Borne Parasitic Zoonoses in the 21st Century will 

be held December 6-8, 2000 at the Royal River Hotel in Bangkok, Thailand. The meeting is jointly 

organized by the Faculty of Tropical Medicine of Mahidol University, the Parasitology and Tropical 

Medicine Association of Thailand, the TROPMED Alumni Association, and the SEAMEO TROP- 

MED Network. For further information contact: Dr. Suvanee Supavej, Secretary of the 3rd FBPZ 

Organizing Committee, Faculty of Tropical Medicine, Mahidol University, 420/6 Rajvithi Road; 

Bangkok 10400, Thailand; phone (622) 2460321 or (662) 2469000-13, Fax (662) 2468340 or (662) 

2469006, e-mail: tmssp@mahidol.ac.th. 




Digenean Fauna of Amphibians from Central Mexico: Nearctic and 

Neotropical Influences 

G. PEREZ-PONCE DE LEON,' V. LEON-REGAGNON, L. GARCIA-PRIETO, U. RAZO-MENDIVIL, 

AND A. SANCHEZ-ALVAREZ 

Laboratorio de Helmintologia, Institute de Biologia, Universidad Nacional Autonoma de Mexico, A.P. 70-153, 

C.P. 04510, Mexico D.F., Mexico (e-mail: ppdleon@servidor.unam.mx: vleon@mail.ibiologia.unam.mx) 

ABSTRACT: Specimens from 20 amphibian species from central Mexico were examined for helminths. We found 

21 digenean species; 4 of them are recorded for the first time in Mexico. Twenty-two new host and 21 new 

locality reports are added. Previous reports of these helminth species are summarized, and biogeographical 

aspects of hosts and parasites are discussed. 

KEY WORDS: Digenea, taxonomy, amphibians, Mexico, biogeography. 

Mexico possesses one of the highest amphibian 

species richnesses in the world, with 285 

species recorded so far, and an unusual level of 

endemism (60.7%) (Flores-Villela, 1993, 1998). 

In spite of this richness and the importance of 

this group of vertebrates in ecosystems, only 

10% of the species in Mexico have been studied 

for helminth parasites. 

We recently conducted a study of helminth 

parasites of amphibians in selected aquatic ecosystems 

in Mexico. We surveyed helminths of 

frogs, toads, and salamanders from several lakes 

of the Mexican plateau (Mesa Central), a tropical 

rain forest (Los Tuxtlas, Veracruz State), and 

a tropical dry deciduous and semideciduous forest 

(Chamela, Jalisco State). In this paper, we 

present a list of the digenetic trematodes of 20 

species of amphibians that we analyzed during 

the last 3 yr. We also provide information about 

previous records of each helminth species in 

Mexico and discuss biogeographical aspects of 

parasites and hosts. 


Between July 1996 and May 1998, we examined 

647 specimens of amphibians belonging to 20 species 

and 8 genera (Table 1). We sampled in 12 localities: 8 

from the Mesa Central, 1 from the Pacific coast, and 

3 from the coast of the Gulf of Mexico (Map 1). However, 

digeneans were found only in frogs and salamanders 

of the following localities: Cienaga de Lerma, Estado 

de Mexico (19°17'N, 99°30'W); Lago de Chapala, 

Jalisco (20°17'N, 103°11'W); Lago de Cuitzeo, Michoacan 

(19°53'N, 100°50'W); Lago de Patzcuaro, Michoacan 

(19°30'N, 101°36'W); Lago de Zacapu, Michoacan 

(19°49'N, 101°47'W); Manantiales de Cointzio, 

Michoacan (19°35'N, 101°14'W); Los Tuxtlas, 



92 

Veracruz (Laguna El Zacatal, Laguna Escondida, and 

Los Tuxtlas Field Station; 20°37'N, 98°12'W); Estero 

Chamela, Jalisco (19°30'N, 105°6'W). 

Hosts were collected by hand or with seine nets and 

were kept alive before parasitological analysis, which 

was carried out within 24 hr after capture. Hosts were 

killed with an overdose of anesthetic (sodium pentobarbitol) 

and examined by standard procedures. 

Digeneans were relaxed with hot tap water, fixed in 

Bouin's fluid for 8 hr under coverglass pressure, and 

then placed in vials containing 70% alcohol; later, they 

were stained with Mayer's paracarmin, Delafield's hematoxylin, 

or Gomori's trichrome and mounted in permanent 

slides with Canada balsam. Drawings were 

made with the aid of a drawing tube. Voucher specimens 

of collected worms were deposited at the Coleccion 

Nacional de Helmintos (CNHE), Biology Institute, 

Mexico City. 

Hosts were fixed following standard procedures 

(Simmons, 1985) and deposited at the Coleccion Nacional 

de Anfibios y Reptiles (CNAR), Biology Institute, 

Universidad Nacional Autonoma de Mexico 

(UNAM), and in the Coleccion Herpetologica del Museo 

de Zoologfa (Faculty of Sciences, UNAM). 

Results 

We identified 21 digenean species (Figs. 1- 

20) of 11 genera and 10 families collected in 10 

of the 20 species of frogs and salamanders analyzed 

(Table 2). Four of these represent new 

records in Mexico, Catadiscus rodriguezi, Glypthelmins 

parva, Glypthelmins sp., and Fibricola 

sp. metacercariae. We also add 22 new host records 

and 21 new locality records. The frog 

Rana brownorurn, the salamanders Ambystoma 

dumerilii, Ambystoma mexicanum, and Ambystoma 

tigrinum, the toads Bufo marinus and Bufo 

valliceps, the hylids Hyla arenicolor, Hyla exirnia, 

and Pachymedusa dachnicolor, and the leptodactylid 

Eleutherodactylus rhodopis were free 

from digenean infections.

PEREZ-PONCE DE LEON ET AL.—DIGENEANS OF MEXICAN AMPHIBIANS 93 

Table 1. Hosts, localities, and numbers of hosts examined in Mexico. 

Anura 

Bufo marinux Linnaeus, 1758 

Host Locality 

Bufo valliceps Weigmann. 1833 

Eleutherodactylus rhodopis Cope, 1867 

Hyla arcnicolor Cope, 1886 

Hyla cximia Baird, 1854 

Leptodactylus melanonotus Hallowell, 1861 

Pachymedusa dachnicolor Cope, 1864 

Rana brownorum Sanders, 1973 

Rana dunni Zweifel, 1957 

Rana forreri Boulenger, 1883 

Rana megapoda Taylor, 1942 

Rana montezumae Baird, 1854 

Rana neovolcanica Hillis and Frost, 1985 

Rana vaillanti Brocchi. 1877 

Smilisca buudinii Dumeril and Bibron, 1841 

Urodela 

Ainb\stoma andersoni Krehs and Brandon, 1984 

Ambystoma dutnerilii Duges, 1870 

Anibvxtoma lermaensis (adults) Taylor, 1940 

Ambystoma lermaensis (larvae) 

Ambystoma mexicanum Shaw, 1789 

Ambvstoina tigrinum Green, 1825 

Discussion 

Three clearly distinguishable groups are in 

this list, not considering Fibricola sp. and Haematoloechus 

sp. (Map 1). The first group is composed 

of species with nearctic distribution, such 

as Cephalogonimus americanus, Glypthelmins 

californiensis, Glypthelmins quieta, Gorgoderina 

attenuata, Megalodiscus americanus, Halipegus 

occidualis, Haematoloechus complexus, 

Haematoloechits coloradensis, Haematoloechus 

longiplexus, and Haematoloechus medioplexus, 

which have been previously recorded in Mexico 

and other parts of North America (see Brooks 

[1984] and references therein). The second 

group of species, including C. rodriguezi, Glypthelmins 

facioi, G. parva, Loxogenes (Langeronia) 

macrocirra, and Mesocoelium monas, has 

been recorded in South and Central America 

(Prudhoe and Bray, 1982). Finally, the third 

group is composed of endemic species: Haematoloechus 

illimis, Haematoloechus pulcher, 

and Glypthelmins sp. 

Presa Miguel de la Madrid, Tuxtepec, Oaxaca 

Chamela, Jalisco 

Laguna Escondida, Los Tuxtlas, Veracruz 

Laguna El Zacatal, Los Tuxtlas, Veracruz 

Manantiales de Cointzio, Michoacan 



Chamela, Jalisco 

Laguna El Zacatal, Los Tuxtlas, Veracruz 

Lago de Patzcuaro, Michoacan 

Lago de Zacapu, Michoacan 

Estero Chamela, Chamela, Jalisco 


Lago de Chapala, Jalisco 

Cienaga de Lcrma, Estado de Mexico 

Lago de Cuitzeo, Michoacan 




Lago de Zacapu, Michoacan 

Lago de Patzcuaro, Michoacan 

Cienaga de Lerma, Estado de Mexico 

Cienaga de Lerma, Estado de Mexico 

Lago de Xochimilco, Mexico City 

Lago La Mina Preciosa, Puchla 

Total 

Total 

Sample 

si/.e 

18 

I 

4 

1 

11 

19 

4 

2 

14 

74 

18 

12 

27 

4 

46 

84 

41 

31 

5 

416 

48 

89 

16 

42 

34 

2 

231 

The digenean fauna of the endemic amphibians 

(A. andersoni, A. lermaense, A. dumerilii, R. 

montezumae, R. dunni, R. neovolcanica, and R. 

megapoda) in the Transverse Volcanic Axis 

clearly has a Nearctic origin because none of the 

neotropical species of digeneans was found in 

this region, and the trematode fauna is formed 

of nearctic and endemic species of digeneans. 

On the other hand, the digenean fauna of the 

nonendemic host species Leptodactylus melanonotus, 

Rana vaillanti, and Smilisca baudinii, all 

collected in the Los Tuxtlas region in the tropical 

lowlands of the Gulf of Mexico, has a strong 

neotropical influence. Five of the 9 species reported 

from that region show a neotropical distribution. 

In both cases, the parasite fauna reflects the 

biogeographic and phylogenetic links of the 

hosts. The endemic species of frogs in the Transverse 

Volcanic Axis, which represents the 

boundary between the nearctic and neotropical 

biogeographic zones, are members of the "Rana 


94 COMPARATIVE PARASITOLOGY, 67( 1), JANUARY 2000 

A = Nearctic helminth species 

• = Neotropical helminth species 

• = Endemic helminth species 

Map 1. Map of Mexico showing collecting sites; and limits of nearctic and neotropical regions (dotted 

line). 1 = Presa Miguel de la Madrid, Tuxtepec, Oaxaca; 2 = Laguna Escondida, Los Tuxtlas, Veracruz; 

3 = Laguna El Zacatal, Los Tuxtlas, Veracruz; 4 = Lago La Mina Preciosa, Puebla; 5 = Cienaga de 

Lerma, Estado de Mexico; 6 = Lago de Xochimilco, Mexico City; 7 = Manantiales de Cointzio, Michoacan; 

8 = Lago de Patzcuaro, Michoacan; 9 = Lago de Zacapu, Michoacan; 10 = Lago de Cuitzeo, 

Michoacan; 11 = Lago de Chapala, Jalisco; 12 = Chamela, Jalisco. 

pipiens complex," widely distributed from central 

Mexico to Canada (Hillis et al., 1983). Apparently, 

this group of frogs harbors a relatively 

homogeneous digenean fauna throughout its 

range to the volcanic axis. Little is known about 

the parasitic fauna of this group of frogs in the 

lowlands of Mexico. In some cases, as in the 

N 

A 

93°W 

21°N 

genus Haematoloechus, where an enormous diversity 

of species has been recorded, several 

speciation events have occurred in the endemic 

amphibians of this biogeographical area. This is 

the case for H. pulcher, probably derived from 

H. complexus, and Haematoloechus illimis, 

whose sister taxon is not clearly distinguished 

Figures 1-5. Ventral views. 1. Cephalogonimus americanus (Stafford, 1902) Stafford, 1905. 2. Gorgoderina 

attenuata (Stafford, 1902) Stafford, 1905. 3. Megalodiscus americanus Chandler, 1923. 4. Catadiscus 

rodriguezi Caballero, 1955. 5. Haematoloechus coloradensis (Cort, 1915) Ingles, 1932. Scales in millimeters. 

Figures 6-10. Ventral views. 6. Haematoloechus complexus (Seely, 1906) Krull, 1933. 7. Haematoloechus 

illimis Caballero, 1942. 8. Haematoloechus longiplexus Stafford, 1902. 9. Haematoloechus medioplexus 

Stafford, 1902. 10. Haematoloechus pulcher Bravo, 1943. Scales in millimeters. 

Figures 11-15. Ventral views. 11. Glypthelmins parva Travassos, 1934. 12. Glypthelmins sp. 13. Glypthelmins 

calif orniensis (Cort, 1919) Miller, 1930. 14. Glypthelmins quieta (Stafford, 1900) Stafford, 1905. 

15. Glypthelmins facioi Brenes, Arroyo, Jimenez, and Delgado, 1959. Scales in millimeters. 









(Leon-Regagnon et al., 1999). Species of Haematoloechus 

apparently have experienced a diversification 

in frogs and salamanders in central 

Mexico, representing the group with the highest 

species richness (6) in our samples. Glypthelmins, 

parasitic mainly in frogs of the new world, 

also shows high species richness. However, the 

presence at least of 4 species is mainly the result 

of independent host capture events, either from 

the neotropical or nearctic zones. 

The distribution of the nonendemic frogs from 

the lowlands ranges from Ecuador and Colombia 

to Veracruz, Mexico (R. vaillanti), to Sonora, 

northwestern Mexico (L. melanonotus), and Texas 

(S. baudinii). Their digenean fauna in Veracruz 

is composed of a combination of neotropical 

and nearctic species. Only 2 digenean species, 

Glypthelmins sp. and M. monas, were recovered 

from L. melanonotus and S. baudinii, 

respectively. The former probably represents an 

undescribed species, and M. monas has been reported 

in numerous host genera in South America 

and Africa (Prudhoe and Bray, 1982). Seven 

digenean species were collected from R. vaillanti, 

and 3 of them show a neotropical distribution: 

C. rodriguezi in Panama (Caballero, 1955) and 

G. parva in Brazil (Prudhoe and Bray, 1982), 

both described from Leptodactylus ocellatus, 

and G. facioi in Costa Rica (Brenes et al., 1959) 

and Veracruz, Mexico (Razo-Mendivil et al., 

1999), from Rana palmipes Spix, 1824, and R. 

vaillanti, respectively. The presence of these 

neotropical digeneans in Los Tuxtlas reflects the 

geographic distribution of the host genus Leptodactylus 

and the "Rana palmipes complex" 

(Frost, 1985; Hillis and De Sa, 1988). One species 

is endemic, L. (L.) macrocirra, and the 3 

remaining species parasitizing R. vaillanti have 

a nearctic distribution; 2 of these species (G. attenuata 

and C. americanus) are also present in 

the endemic frogs of the Transverse Volcanic 

Axis, and the third species (H. medioplexus) has 

been recorded in several species of frogs from 

the United States and Canada, most commonly 

in members of the "Rana pipiens complex." 

The 3 species have a low host specificity and 

have been able to colonize several host groups, 

thus expanding their distribution range. 

Apparently, a mixture of neotropical and 

nearctic species of parasites is taking effect in 

the lowlands of the Gulf of Mexico, with a series 

of very interesting phenomena of colonization of 

new hosts and habitats. Little is known about the 

amphibian parasite fauna of the tropical lowlands 

of the Pacific slope of Mexico or the 

southeastern part of the country. Those areas 

will undoubtedly be a source of extensive phylogenetic 

and biogeographic information on parasites 

and hosts in the future. 

Contemporary ecological conditions are also 

important determinants of the parasitic fauna of 

a host species. Several authors have demonstrated 

a marked correlation between the relative 

amount of time spent in association with aquatic 

habitats and the number of species of platyhelminths 

hosted by frogs (Brandt, 1936; Prokopic 

and Krivanec, 1975; Brooks, 1976, 1984; Guillen, 

1992). Our data clearly demonstrate that 

frogs and salamanders harbor the richer digenean 

fauna compared with the less water-dependent 

hylids or toads, where digeneans were almost 

or absolutely absent (the small sample size 

in leptodactylids precludes any discussion about 

their helminth fauna). Within frogs and salamanders, 

diet is the factor that most determines the 

richness of the digenean communities. Frogs become 

infected when they prey upon insects or 

copepods (which is the case in species of Haematoloechus 

and Halipegus, respectively), when 

they swallow their own skin bearing encysted 

metacercariae during ecdysis, or when they feed 

upon infected tadpoles (species of Catadiscus, 

Cephalogonimus, Glypthelmins, Gorgoderina, 

and Megalodiscus) (Yamaguti, 1975; Prudhoe 

and Bray, 1982). Salamanders of the genus Ambystoma 

Tschudi, 1838, hosted fewer digenean 

species than frogs. Garcia-Altamirano et al. 

(1993) reported that A. dumerilii in Lake Patzcuaro 

feeds mainly on crayfish and fish. As evidenced 

by the presence of C. americanus, G. 

attenuata, and Haematoloechus spp. in salamanders 

of our samples, it is possible that they oc- 

Figures 16-20. Ventral views. 16. Loxogenes (Iângeronia) macrocirra (Caballero y Bravo, 1949) Yamaguti, 

1971. 17. Mesocoelium monas (Rudolphi, 1819) Teixeira de Freitas, 1958. 18. Halipegus occidualis 

Stafford, 1905. 19. Fibricola sp. (inetacercaria). 20. Ochetosoma sp. (metacercaria). Scales in millimeters. 




20

Table 2. Digenetic trematodes of some amphibians in Mexico. 

Locali 

(CNHE acce 

Host 

Infection 

Helminth site 

LZAt (3409, 34 

LPA 

CLEt (3411) 

EZA 

LZA (3357, 335 

LPA (3408) 

LPA 

CLE (3359, 336 

LXO 

Ambystoma andersontf 

Ambystoma dumerlii 

Ambystoma lermaensis']' 

Rana berlandieri 

Rana dunni 

Family Cephalogonimidae (Looss, 1899) Nicoll, 1914 

Cephalogonimus americanus (Stafford, 1902) Intestine 

Stafford, 1905 (Fig. 1) 

Rana montezumae 

MCOt (3370) 

LXO 

Rana neovolcanica'f 

Rana pipiens'f 

LES (3425) 

LES 

SAL 

TUX, LES 

Rana vaillanti 

Rhyacosiredon altamirani 

Bufo marinus 

LZAt (3412, 34 

CLE (3414, 341 

LXO, CLE 

LZA (3402), LP 

LPA 

MCOt (3403, 3 

CLE (3401) 

CLE 

Unspecified loca 

Mexico 

LXO, LTE 

MCOt (3403, 3 

CLE 

LES (3428) 

LES 

Family Gorgoderidae Looss, 1901 

Gorgoderina attenuata (Stafford, 1902) (Fig. 2) Urinary bladder Ambystoma andersontf 

Ambystoma lermaensis^ 

Ambystoma tigrinum 

Rana dunni 

Rana megapodaj 


Rana neovolcanica'f 

Rana pipiens\ vaillanti 

Remarks: Pigulevsky (1953) stated that the material of Sokoloff and Caballero (1933) belonged to a new species, G. sk 

testes. We consider this difference to be a result of intraspecific variation. 


Table 2. Continued. 

Locality* 

(CNHE accessi 

Infection 

site Host 

Helminth 

Intestine Rana during 

Rana megapoda^ 

Family Paramphistomidae Fischoeder, 1901 

Megalodiscus americanus Chandler, 1923 (Fig. 3) 

LZAt (3353) 

LCUt (3351, 335 

MCOt (3356) 

CLE (3347-3350) 

LXO, CLE 

MCO (3354, 3355 

LMO 


Rana neovolcanica^ 

Rana pipiens^ 

Catadiscus rodriguezi Caballero, 1955 (Fig. 4) 

Intestine Rana vaillanti'r 

LESt (3308) 

Remarks: This species was originally described of Leptodactylus pentadactylus from Valle de Ant6n in Panama (Caballero 

LZAt (3395, 3396 

LPA 

Lungs Rana dunni 

Family Haematoloechidae Odening, 1964 

Haematoloechus coloradensis (Cort, 1915) 

Ingles, 1931 (Fig. 5) 

CLE (3397) 

CLE 


Leon-Regagnon et a 

Remarks: Kennedy (1981) considered H. coloradensis to be a junior synonym of H. complexus, but 

basis of molecular and morphological evidence. 

CLE (3417) 

CLE 

LXO, LTE 

MCOt (3380, 337 

CLE (3374-3378) 

CLE 

Lungs Ambystorna lermaensis 

Haematoloechus complexus (Seely, 1906) 

Krull, 1933 (Fig. 6) 

Rana megapodaj 


MCOt (3380, 337 

RPE, PLB 

Rana neovolcanica^ 

Rana pipiens± 

CLE (3381-3383) 

CLE 

Remarks: Originally recorded as Ostiolum complexum by Martinez (1969). 

Haematoloechus illimis Caballero, 1942 (Rg. 7) Eustachian tubes, Rana montezumae 

lungs 

CLE (3394) 

CLB 

CLE 

LTE 

Lungs Rana montezumae 

Haematoloechus longiplexus Stafford, 1902 

(Fig. 8) 

Rana pipiensi 

Remarks: Originally recorded as Haematoloechus macrorchis Caballero, 1941, this species was declared junior synonym o 



Locality * 

(CNHE accession 

Host 

Infection 

Helminth site 

EZA 

CLE, LXO 

CLE, LXO 

LES (3424) 

LES 

LES 

LES 

TUX 

CLE (3418) 

CLE 

CLE (3398-3400) 


Rana monteziimae 

Rana pipiensi 


Haematoloechus medioplexus Stafford, 1902 Lungs 

(Fig. 9) 

Bufo valliceps 

Bufo marinus 

Ambystoma lermaensis^ 

Arnbystoma tigrinum 

Rana montezumaef 

Haematoloechus pulcher Bravo-Hollis, 1943 Lungs 

(Fig. 10) 

Haematoloechus sp. Lungs Rana forreri'f 

ECHt 

Remarks: Specimens belong to a different species from those mentioned above, but their poor preservation condition preclu 

LPA (3280) 

LZAt (3281, 3283, 

LZA 

LPA 

MCO 

CLE (3282) 

CLE 

LXO 

Kana dunni 

Family Macroderoididae Goodman, 1 952 

Glypthelmins californiensis (Cort, 1919) Intestine 

Miller, 1930 (Fig. 13) 

Rana megapoda 


MCO 

Rana neovolcanica 

Remarks: Records of this species by Leon-Regagnon (1992) and Guillen (1992) belong to G. quieta and G. facial, respectiv 

LPA (3273), LZA ( 

LPA 

LZA 

LCUt (3346), MCO 

LCHt (3406) 

MCO 

CLE (3271, 3275-3 

CLE 

Intestine Rana dunni 

Glypthelmins quieta (Stafford, 1900) 

Stafford, 1905 (Fig. 14) 

Rana megapoda 


LXO, LTE 



Locality 

(CNHE accessi 

Host 

Infection 

site 

Helminth 

MCO (3272) 

MCO 


reported as G. californi 

of Pulido (1994) were orginally 

specimen 

Remarks: Specimens of Leon-Regagnon (1992) and 1 

(1999). 

EZA 

LES (3285) 

LES 



Intestine 

Glypthelmins facioi Brenes, Arroyo, Jimenez, and 

Delgado, 1959 (Fig. 15) 

Remarks: Specimens of Guillen (1992) were originally reported as G. californiensis and transferred to G. facioi by Razo-M 

Glypthelmis parva Travassos, 1934 (Fig. 11) 

Intestine Rana vaillanti'f 

LESt (3391) 

Remarks: This species was originally described in Leptodactylus ocellatus from Brazil (Travassos, 1924). This is the first 

Glypthelmins sp. (Fig. 12) Intestine Leptodactylus melanonotusj\t (3392) 

Remarks: These specimens represent a new species (Razo-Mend vil, unpubl. data) 

LCA, TUX 

Bufo marinus 

Intestine 

Family Lecithodendriidae Odhner, 1910 

Loxogenes (Langeronia) macrocirra (Caballero 

and Bravo-Hollis, 1949) Yamaguti, 1971 

(Fig. 16) 

EZA 


PLB 

Undetermined loc 

Mexico 

LES (3307) 

LES, TUX 

Rana pipiensi 


Remarks: Originally described as Langeronia macrocirra Caballero and Bravo-Hollis, 1949. 

LCA 

Intestine Bufo marinus 

Family Brachycoeliidae Johnston, 1912 

Mesocoelium monas (Rudolphi, 1819) 

Teixeira de Freitas, 1958 (Fig. 17) 

TI TV 

LESt (3309) 

EZA 

Smilisca baudini 



Locality* 

(CNHE accession 

Host 

Infection 

site 

Helminth 

MCO (3272) 



Eustachian tubes 

Family Hemiuridae Looss, 1907 

Halipegus occidualis Stafford, 1905 (Fig. 18) 

CLE (3361, 3362) 

LXO 

CLE 

LTE 

Rana pipiens± CLE 

Remarks: Caballero (1941) described H. lennensis, declared a junior synonym of//, occidualis by Rankin (1944). Caballero 

Rana montezumae from LXO, but after reexamination of specimens, McAlpine and Burt (1998) considered them to be H. o 

Family Diplostomidae Poirier, 1886 

Fibricola sp. (metacercariae) (Fig. 19) Urinary bladder Rana montezumae^ CLEf (3365, 3369) 

Remarks: Identification of this material is based on its comparison with the description of Fibricola texensis Chandler, 1942 

caballeroi Zerecero, 1943, in mammals from Mexico City (Zerecero, 1943). 

Family Plagiorchiidae (Liihe, 1901) Ward, 1917 

CLE (3363, 3371) 

LZAt (3364) 

MCOt (3372, 3373 

MCOt (3372, 3373 

LPA 

LPA 

LPA 

Rana montezumae^ 

Rana dunni 

Rana megapodaj\ neovolcanica']' 

Ochetosoma sp. (metacercariae) (Fig. 20) Intestine wall and 

liver 

Ambystoma dumerilii 

Goodea atripinnis 

Neoophorus diazi 

From fishes 

* CLE = Cienaga de Lerma; ECH = Estero Chamela; EZA = Laguna El Zacatal; LCA = Lago de Catemaco, Veracruz; LC 

Laguna Escondida; LMO = Laguna Montford, Nuevo Leon; LPA = Lago de Patzcuaro; LTE = Lago de Texcoco, Estado de M 

Cointzio; PLB = Presa La Boca, Nuevo Leon; RPE = Ri'o Pesquen'a, Nuevo Leon; SAL = Salazar, Estado de Mexico; TUX = 

t First host or locality record. 

4: Host record made before the species of the "Rana pipiens complex" were differentiated. The geographic range of R. pipiens 

1983; Frost, 1985; Flores-Villela, 1993). 


casionally prey on tadpoles and insect larvae 

also. 

Only 30 (10.5%) of the total number of species 

of amphibians reported in Mexico (285) 

(Flores-Villela, 1998) have been surveyed for 

helminth parasites so far. Seventy-three helminth 

species have been recorded. Interestingly 

enough, 25 of the 73 (34%) are endemic species 

found only in Mexico (see Baker [1987] and Lamothe 

et al. [1997]). However, our knowledge 

about helminth parasites of amphibians in Mexico 

is still far from complete. Parasitic organisms 

are becoming an important part of the body 

of knowledge about the natural history of their 

hosts, and this information can be easily used as 

a powerful and predictive tool to support biodiversity 

studies and conservation initiatives, as 

has been shown by Hoberg (1996, 1997). We 

plan to continue collecting data on the parasite 

fauna of amphibians in Mexico and, in this way, 

contribute to the understanding of their biology 

and their role in biodiversification and as monitors 

of climatic change. 


We gratefully acknowledge Agustin Jimenez, 

Berenit Mendoza, and Coral Rosas for their assistance 

in field trips and Dr. T. Scholz for his 

comments on an early version of the manuscript. 

Identification of hosts by Adrian Nieto and Edmundo 

Perez (Museo de Zoologia, Facultad de 

Ciencias) is greatly appreciated. This study was 

funded by Programa de Apoyo a Proyectos de 

Investigacion e Innovacion Tecnologica, Universidad 

Nacional Autonoma de Mexico (PA- 

PIIT-UNAM IN201396), and Consejo Nacional 

de Ciencia y Tecnologfa (CONACYT 2676PN) 

to G.P.P.L., PAPIIT-UNAM IN219198 to 

G.P.P.L. and V.L.R., and CONACYT J27985-N 

to V.L.R. 


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in amphibians and reptiles. Memorial University 

of Newfoundland Occasional Papers in Biology 

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Diesing, 1836 y Megalodiscus Chandler, 

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parasites de los "ajolotes" de Mexico I. Anales 


del Institute de Biologia, Universidad Nacional 

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Caballero, C. E. 1941. Trematodos de la Cienaga de 

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Chandler, A. C. 1942. The morphology and life cycle 

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Kennedy, M. J. 1981. A revision of species of Haematoloechus 

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contribucion al conocimiento de los parasites de 

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Autonoma de Mexico 14:507-526.



Research Note 

New Host and Distribution Record of Gordius difficilis 

(Nematomorpha: Gordioidea) from a Vivid Metallic Ground Beetle, 

Chlaenius prasinus (Coleoptera: Carabidae) from 

Western Nebraska, U.S.A. 

BEN HANELT' AND JOHN JANOVY, JR. 

School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska 68588-0118, U.S.A. 

(e-mail: bhanelt@unlserve.unl.edu; jjanovy@unlserve.unl.edu) 

ABSTRACT: Gordius difficilis (Montgomery, 1898) 

Smith, 1994 is recorded from a creek in a juniper forest 

in western Nebraska. Subsequent pitfall data shows 

Chlaenius prasinus Dejean, 1826 to be the definitive 

host. This represents the first report of G. difficilis from 

the American Midwest, of C. prasinus as a host of 

nematomorphs, and as a host for G. difficilis. 

KEY WORDS: Gordius difficilis, Chlaenius prasinus, 

vivid metallic ground beetles, Nematomorpha, Nebraska, 

U.S.A. 

Nematomorphs are a well-recognized, widely 

distributed but poorly studied phylum (Chandler, 

1985). Sometimes referred to as horsehair or 

gordian worms, freshwater nematomorphs are 

obligate parasites as larvae but free-living as 

adults. 

Gordius aquaticus difficilis Montgomery, 

1898 was originally described from a single 

male specimen. Although Montgomery (1898) 

recognized 5 structural differences between G. 

aquaticus difficilis and Gordius aquaticus robustus 

Montgomery, 1898, he assigned G. aquaticus 

difficilis as a subspecies rather than a distinct 

species. Based on this early description, 

Miralles (1975) synonymized G. aquaticus difficilis 

with G. robustus Leidy, 1851, but Chandler 

(1985) synonymized G. aquaticus difficilis 

with Gordius paraensis Camerano, 1892. 

More recently, Smith (1994) used scanning 

electron microscopy to show that G. aquaticus 

difficilis is distinct enough to warrant considering 

it as a separate species, G. difficilis. This 

determination was based on the presence of a 

parabolic line of hairlike structures anterior to 

the cloacal opening, as well as the presence of 

distinct areoles in the midbody of the female. 

In mid-June 1998, G. difficilis was found in 


107 

White Gate Creek, Keith County, Nebraska 

(41°12'20.5"N, 101°39'86.3"W). This site consists 

of a first-order, spring-fed creek suirounded 

by juniper trees (Juniperus scopulorum Sargent, 

1897) and various deciduous vegetation. The 

creek has a sandy bottom and often contains algal 

blooms because of the use of the creek by 

cattle. Nineteen free-living individuals were collected 

from the creek between late June and late 

July, 10 males ranging in size from 68-307 mm 

and 9 females ranging in size from 89-208 mm. 

Individuals were often found entangled in the 

algae or attached to sticks or rocks on the banks 

of the creek. 

In late June 1998, 4 lines of 10 pitfall traps 

were set adjacent to White Gate Creek. Of 6 

trapped Chlaenius prasinus Dejean, 1826, 2 

were infected with 3 worms each. None of the 

other invertebrates trapped contained nematomorphs. 

One host contained 2 female worms and 

1 male worm; the other host contained 3 female 

worms. The males ranged in size from 103-297 

mm, and the females ranged in size from 185- 

203 mm. The hosts were void of gonads, fatbodies, 

and intestines but appeared to behave 

normally. 

Worms were killed in 70% EtOH and brought 

up to 100% glycerine prior to examination. All 

specimens were temporarily mounted in glycerine 

for observation. Worms were as described 

by Montgomery (1898) and Smith (1994). Briefly, 

the male posterior is bifurcated with a subterminal 

ventral cloacal opening (Fig. 1). A line 

of hairlike structures curves around the anterior 

end of the cloacal opening. Posterior to the cloaca 

is a postcloacal crescent, extending about 

one-fourth the length of the lobed ends. Females 

have entire posteriors. Cuticular areoles are 

more prominent in females compared with males 

when viewed with light microscopy. 



Figure 1. Gordius difficilis, posterior end of a male. Scale bar = 35 fxm. Note cloacal opening (C), 

precloacal line of hairlike structure (H), and postcloacal ridge (R). 

Gordians have been recorded from one individual 

of Chlaenius sericeus Forster, 1771, but 

the worm could be identified only as Gordius 

sp. because of the immaturity of the specimen 

(Leffler, 1984). The only other record of the genus 

Chlaenius as a host for a "nematoid parasite" 

was from Chlaenius tomentosus Say, 1830 

In that report, insect parts and the worm were; 

located in the stomach of the beetle (Forbes, 

1880). However, nematomorphs are usually 

found outside the host's gut. Thus, it is likely 

that the worm was ingested while inside another 

insect and was not a parasite of the beetle. 

Gordius difficilis has only been reported from 

Roan Mountain, western North Carolina (Mont 

gomery, 1898) and from Franklin County, Massachusetts 

(Smith, 1994). This report extends the 

known range of G. difficilis and for the first time 

provides information of a host for this species. 

We would like to thank Myrna Gainsforth for 

providing access to White Gate Creek and the 

Cedar Point Biological Station for providing facilities. 

This project was partially funded by the 

Center for Great Plains Studies Research erants- 


in-aid for graduate students (University of Nebraska-Lincoln, 

fall 1998). 


Chandler, C. M. 1985. Horsehair worms (Nematomorpha, 

Gordioidea) from Tennessee, with a review 

of taxonomy and distribution in the United 

States. Journal of the Tennessee Academy of Sciences 

60:59-62. 

Forbes, S. A. 1880. Notes on insectivorous Coleoptera. 

Bulletin of the Illinois Laboratory of Natural 

History 1:167-176. 

Leffler, S. R. 1984. Record of a horsehair worm 

(Nematomorpha: Gordiidae) parasitizing Chlaenius 

sericeus Forster (Coleoptera: Carabidae) in 

Washington. Coleopterists Bulletin 38:130. 

Miralles, D. A. B. 1975. Nuevo aporte al conocimiento 

de la Gordiofauna Argentina. Neotropica 21: 

99-103. 

Montgomery, T. H. J. 1898. The Gordiacea of certain 

American collections with particular reference to 

the North American fauna. Bulletin of the Museum 

of Comparative Zoology, Harvard 32:23-59. 

Smith, D. G. 1994. A reevaluation of Gordius aquaticus 

difficilis Montgomery 1898 (Nematomorpha, 

Gordioidea, Gordiidae). Proceedings of the Academy 

of Natural Sciences of Philadelphia 145:29- 

34.



Research Note 

Intestinal Helminths of Seven Species of Agamid Lizards from 

Australia 

STEPHEN R. GOLDBERG,'-3 CHARLES R. BURSEY," AND CYNTHIA M. WALSER' 

1 Department of Biology, Whittier College, Whittier, California 90608, U.S.A. (e-mail: 

sgoldberg@whittier.edu) and 

2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, 

U.S.A. (e-mail: cxbl3@psu.edu) 

ABSTRACT: The intestinal tracts of 243 lizards representing 

7 species of Agamidae from Australia (Ctenophorus 

caudicinctus, Ctenophorus fordi, Ctenophorus 

isolepis, Ctenophorus reticulatus, Ctenophorus scutulatus, 

Lophognathus longirostris, and Pogona minor) 

were examined for helminths. One cestode species, 

Oochoristica piankai, and 8 nematode species, Abhreviata 

anomala, Kreisiella chrysocampa, Kreisiella 

lesueurii, Maxvachonia brygooi, Parapharyngodon 

fitzroyi, Skrjabinoptera gallardi, Skrjabinoptera goldmanae, 

and Wanaristrongylus ctenoti, were found. 

Larvae of Abbreviate* sp. were also present. Twelve 

new host records are reported. 

KEY WORDS: Sauria, lizards, Agamidae, survey, 

Cestoda, Oochoristica piankai, Nematoda, Abbreviata 

anomala, Kreisiella chrysocampa, Kreisiella lesueurii, 

Maxvachonia brygooi, Parapharyngodon fitzroyi, 

Skrjabinoptera gallardi, Skrjabinoptera goldmanae, 

Wanaristrongylus ctenoti, Abbreviata sp., Australia. 

The family Agamidae is well represented in 

Australia and about 60 species are known (Cogger, 

1992). Helminth records exist for 17 species 

(Baker, 1987; Jones, 1995a; Bursey et al., 1996). 

The puipose of this paper is to present the initial 

report of helminths harbored by Ctenophorus 

caudicinctus (Giinther, 1875) (the ring-tailed 

dragon), Ctenophorus fordi (Storr, 1965) (the 

mallee dragon), and Ctenophorus scutulatus 

(Stirling and Zietz, 1893) (the lozenge-marked 

dragon), and additional helminth data for 4 previously 

examined species: Ctenophorus isolepis 

(Fischer, 1881) (the military dragon), Ctenophorus 

reticulatus (Gray, 1845) (the western netted 

dragon), Lophognathus longirostris Boulenger, 

1883 (the Australian water dragon), and Pogona 

minor (Sternfeld, 1919) (the dwarf bearded 

dragon). In addition, patterns of infection for 

helminths of Australian agamids, were examined. 


109 

The 7 species examined in this study range 

through much of Australia but overlap in Western 

Australia (Table 1). Ctenophorus caudicinctus 

is known from western Queensland through 

the Northern Territory and northern South Australia 

to most of Western Australia; C. fordi is 

widely distributed through southeastern Western 

Australia and southern South Australia with outlying 

populations in western Victoria and western 

New South Wales; C. isolepis is found in 

Western Australia, Northern Territory, northern 

South Australia, and western Queensland; C. reticulatus 

occurs throughout most of the southern 

half of Western Australia and northern South 

Australia; C. scutulatus is known from southern 

Western Australia and northwestern South Australia; 

L. longirostris occurs from the coast of 

Western Australia through central Australia to 

western Queensland; P. minor ranges 1'rom the 

central coast of Western Australia through central 

Australia and South Australia (Cogger, 

1992). 

Two hundred forty-three lizards were borrowed 

from the herpetology collection of the 

Natural History Museum of Los Angeles. County 

(LACM), Los Angeles, California, U.S.A., and 

examined for intestinal helminths. These specimens 

had been collected in 1966-1968 for a series 

of ecological studies by Eric R. Piarika (The 

University of Texas at Austin, U.S.A.). The 

stomach of each lizard had been removed, examined 

for food contents, and deposited in the 

Western Australian Museum, Perth, Western 

Australia; the carcasses with livers and intact intestines 

were deposited in LACM. Numbers of 

individuals, mean snout-vent length (SVL), year 

of collection, and museum accession number of 

host species are as follows: Ctenophorus caudicinctus 

(N = 25, SVL = 63 mm ± 4 SD, range 

= 55-71 mm), Collected 1968, Western Austra- 



Table 1. Prevalence (%), mean intensity ± SD (x ± SD), and range (r) for intestinal helminths from 

Australian agamid lizards. 

Helminth 

Cestoda 

Oochoristica piankai 

Nematoda 

Abbreviata anomala 

Kreisiella chrysocampa 

Kreisiella lesueurii 

Maxvachonia brygooi 

Parapharyngodon fitzroyi 

Skrjabinoptera gallardi 

Skrjabinoptera goldmanae 

Wanaristrongylus ctenoti 

Abbreviata sp. (larvae) 

Ctenophorus caudicinctus 

% x ± SD r 

Host 

Ctenophorus fordi Ctenophorus isolepis 

% x ± SD % x ± SD 

— — — 23* 2.2 ± 1.2 1-4 

20* 1.0 — 

lia. LACM 55115, 55117-55119, 55123-55125, 

55127, 55128, 55130-55133, 55139, 55141- 

55143, 55145, 55152, 55154, 55156, 55163., 

55164, 55166, 55167; Ctenophorus fordi (N = 

26, SVL = 50 mm ± 3 SD, range = 46-58 mm). 

Collected 1967, Western Australia. LACM 

59240, 59245, 59246, 59251, 59259, 59262, 

59268, 59271, 59272, 59274, 59275, 59279, 

59290, 59296, 59299, 59300, 59304, 59306- 

59308, 59312, 59316, 59319, 59321-59322, 

59324; Ctenophorus isolepis (N = 127, SVL = 

55 mm ± 5 SD, range = 35-67 mm). Collected 

1967-1968, Western Australia. LACM 54575- 

54599, 54650-54676, 54678-54699, 54775- 

54799, 54825-54848, 54850-54853. Collected 

1966-1967, Northern Territory. LACM 54694- 

54699; Ctenophorus reticulatus (N = 5, SVL = 

76 mm ± 5 SD, range = 72-83 mm). Collected 

1967, Western Australia. LACM 55051, 55054, 

55055, 55062, 55063; Ctenophorus scutulatus 

(N = 25, SVL = 87 mm ± 11 SD, range = 71- 

107 mm). Collected 1966-1967, Western Australia. 

LACM 54933-54936, 54940, 54942, 

54946, 54949, 54952, 54956-54958, 54960, 

54962, 54963, 54970, 54975, 54982, 54993, 

54996, 54998, 54999, 55004, 55005, 55012; Lophognathus 

longirostris (N = 10, SVL = 74 mm 

± 19 SD, range = 48-98 mm). Collected 1966- 

1968, Western Australia. LACM 55334, 55335, 

55342, 55345, 55354, 55355, 55357, 55366, 

55373, 55377; Pogona minor (N = 25, SVL = 

111 mm ± 11 SD, range = 88-129 mm). Collected 

1967, Western Australia. LACM 54854- 

54857, 54859, 54862, 54864-54866, 54868, 


4* 1.0 — 18* 2.3 ± 1.6 1-8 

4 2.0 ± 1.4 1-4 

2* 1.0 — 

2.0 

1.0 

54869, 54872, 54873, 54875-54880, 54882, 

54884, 54890, 54892, 54896, 54899. 

The intestines, body cavity, and liver of each 

lizard were examined for adult helminths and 

helminth larvae (such as cystacanths, pleurocercoids, 

and tetrathyridia) using a dissecting 

microscope. Stomachs from these specimens 

were unavailable for our examination; however, 

Jones (1987) reported helminths from stomachs 

of C. isolepis, L. longirostris, and P. minor 

from the Pianka Collection in the Western Australian 

Museum, which are listed in Table 2. 

Helminths were placed on a glass slide in a 

drop of undiluted glycerol for study under a 

compound microscope. Nematodes were identified 

from these preparations; selected cestodes 

were stained with hematoxylin and mounted in 

balsam for identification. Nematodes in vials of 

70% ethanol, and permanent stained mounts of 

cestodes were deposited in the United States 

National Parasite Collection (USNPC), Beltsville, 

Maryland. 

One species of Cestoda, Oochoristica piankai 

Bursey, Goldberg, and Woolery, 1996 (USNPC 

88548, 88550, 88555) and 8 species of Nematoda, 

Abbreviata anomala Jones, 1986 (USNPC 

88559), Kreisiella chrysocampa Jones, 1985 

(USNPC 88551, 88560), Kreisiella lesueurii 

Jones, 1986 (USNPC 88549, 88561), Maxvachonia 

brygooi Mawson, 1972 (USNPC 88552, 

88556, 88562), Parapharyngodon fitzroyi Jones, 

1992 (USNPC 88563), Skrjabinoptera goldmanae 

Mawson, 1970 (USNPC 88557, 88564), 

Skrjabinoptera gallardi (Johnston and Mawson,

Table 1. Extended. 

Ctenophorus reticulatus 

% x ± SD r 

60* 7.0 ± 3.5 5-11 

* New host record. 

Ctenophorus 

scutulatus 

% x ± SD r 

4.1 ±4.1 1-13 

1.1 ± 0.4 1-2 

1.0 — 

1942) (USNPC 88547), and Wanaristrongylus 

ctenoti Jones, 1987 (USNPC 88553), were 

found. Larvae of Abbreviata sp. (USNPC 88554, 

88558, 88565) were also present. All of these 

helminths were found in the lumen of the intestines, 

with the exception of larval Abbreviata sp. 

which were found in cysts in the intestinal wall. 

No cystacanths, pleurocercoids, or tetrathyridia 

were found in the body cavity or attached to the 

viscera. 

Prevalences, mean intensity ± SD, and range 

are presented in Table 1. None of the helminths 

found in this study is host specific. Recorded 

helminths of agamid lizards from Australia are 

listed in Table 2. Of these, Pseudothamugadia 

physignathi Lopez-Neyra, 1956, Oswaldofilaria 

innisfailensis (Mackerras, 1962), Oswaldofilaria 

pflugfelderi (Frank, 1964) and Oswaldofilaria 

samfordensis Manzanell, 1982, all filarioids, 

have been found to infect a single host species 

and, surprisingly, the same host species, Physignathus 

lesueurii (Gray, 1831) (the eastern water 

dragon). Abbreviata anomala, Abbreviata pilbarensis 

Jones, 1986, Oswaldofilaria chlamydosauri 

(Breinl, 1913), 5. gallardi, Strongyluris 

paronai (Stossich, 1902), and Wanaristrongylus 

pogonae Jones, 1987 are known only from 

agamid hosts. The remaining helminths have 

been reported from agarnids as well as other lizard 

families: O. piankai from Gekkonidae; Abbreviata 

antarctica (Linstow, 1899), Scincidae, 

Varanidae; Abbreviata confusa (Johnston and 

Mawson, 1942), Varanidae, as well as several 

Host 

GOLDBERG ET AL.—RESEARCH NOTES 111 

Lophognathus 

longirostris 

% x ± SD r 

10* 1.0 

10 1.0 

Pogona minor 

% x ± SD r 

12 2.0 ± 1.0 

28 6.7 ± 5.6 

20* 1.2 ± 0.5 

1-3 

1-13 

1-2 

snake species; Abbreviata tumidocapitis Jones, 

1983, Gekkonidae, Varanidae; K. chrysocatnpa, 

Scincidae; K. lesueurii, Scincidae; M. brygooi, 

Scincidae, Varanidae; P. fitzroyi, Scincidae; Parapharyngodon 

kartana (Johnston and Mawson, 

1941), Gekkonidae, Scincidae; Physalopteroides 

filicauda Jones, 1985, Gekkonidae, Pygopodidae, 

Scincidae, Varanidae; Pseudorictularia dipsarilis 

(Irwin-Smith, 1922), Scincidae; S. goldmanae, 

Gekkonidae, Scincidae, Varanidae; W. 

ctenoti, Gekkonidae, Scincidae, Varanidae. 

Physalopterid larvae are widely distributed in 

Australia and have been reported from agamid, 

gekkonid, scincid, and varanid lizards as well as 

several species of snakes (Jones, 1995b). This is 

the first report of larvae of Abbreviata sp. from 

C. isolepis and C. scutulatus; however, Jones 

(1995b) reported physalopteran larvae from C. 

isolepis. Currently, species of Physaloptera are 

not known to occur in Australian reptiles. Physaloptera 

gallardi Johnston and Mawson, 1942, 

from Pogona barbata (Cuvier, 1829) (the bearded 

dragon) was reassigned to Skrjabinoptera by 

Chabaud (1956), and Physaloptera bancrofti Irwin-Smith, 

1922 from Phyllurus platurus 

(White, 1790) (the southern leaf-tailed gecko) 

was reassigned to Abbreviata by Schuh; (1927). 

Physalopterid larvae found in Australian lizards 

are most likely species of either Abbreviata or 

Skrjabinoptera. 

The data presented here suggest that Australian 

agamid lizards are infected by helminth 

generalists. Bush et al. (1997) presented a hier- 



Table 2. Helminths of agamid lizards from Australia. 

Helminth species 

•5 CJ C3 !3 3-2 

o "S ^ "3 ^ § ^ § ^ SJ 

Lizard species ^C^. ^!

Table 2. Extended. 

3 '£ 

Oswaldofilal 

chlamydosai 

xt 

xt 

a 

Oswaldofilal 

innisfailensi. 

— 

— xtt 

xt — 

a 

Oswaldofilal 

pflugfelderi 

a 

Oswaldofilal 

samfordensi. 

"a 

Parapharyn}. 

fitzroyi 

— 

1 

Parapharyn} 

kartana 

— 

— 


1 

Physalopten 

filicauda 

— 

xt 

.2 

Pseudorictlll 

dipsarilis 

GOLDBERG ET AL.—RESEARCH NOTES 

Pseudothamc 

-5 

2 

•£f 

P 

ft. 

a 

Skrjabinopte 

gallardi 

Xt 

•S 

•S 

•gl 

sgoldmanae Strongyluris 

paronai 

xt 

BO 

Wanaris stro 

ctenoti 

— 

="c 

Wanaris stro 

pogonae 

- - - xt xt - - 

— — — x§ 

— — X# X# — X§ 

— — — — X# — — — x# 

V" A-H. -I" •" A-1..J. V 4- -4- — — — — A "V -i- i 

— — x§§ x§§ — 

— x§ x§§ — 

— — — — x§§ — — 

archy of parasite community terms, including infracommunity 

(helminths in a single host), component 

community (helminths of a host species), 

and supracommunity (helminths in sympatric 

hosts). Table 2 represents the contribution of 

agamid lizards to the Australian helminth supracommunity. 

Mean number of helminth species 

harbored per host species was 3.50 ± 0.58 SE 

(range, 1-9). Aho (1990) compiled distributional 

x§ - — 

patterns for lizards in general and reported the 

mean total number of helminth species per host 

species to be 2.06 ± 0.13 SE (range, 1-4). 

Whether this greater number of helminth species 

per host species is a local Australian phenomenon 

or the result of insufficient data on the helminths 

of this diverse fauna must await further 

studies of Australian lizard helminths. 

We thank Robert L. Bezy, Natural History 


—


Museum of Los Angeles County, for the opportunity 

to examine the lizard specimens. 


Aho, J. M. 1990. Helminth communities of amphibians 

and reptiles: comparative approaches to understanding 

patterns and processes. Pages 157- 

195 in G. W. Esch, A. O. Bush, and J. M. Aho, 


Chapman and Hall, London. 

Baker, M. R. 1987. Synopsis of the Nematoda parasitic 

in amphibians and reptiles. Occasional Papers 

in Biology, Memorial University of Newfoundland 

11:1-325. 

Bursey, C. R., S. R. Goldberg, and D. N. Woolery. 

1996. Oochoristica piankai sp. n. (Cestoda: Linstowiidae) 

and other helminths of Moloch horridus 

(Sauria: Agamidae) from Australia. Journal of 

the Helminthological Society of Washington 63: 

215-221. 

Bush, A.O., K. D. Lafferty, J. M. Lotz, and A. W. 




Chabaud, A. G. 1956. Essai de revision des physalopteres 

parasites de reptiles. Annales de Parasitologie 


Cogger, H. G. 1992. Reptiles and Amphibians of Australia, 

5th ed., Reed Books, Chatswood, New 

South Wales, Australia. 775 pp. 

Johnston, T. H., and P. M. Mawson. 1942. The Gallard 

collection of parasitic nematodes in the Australian 

Museum. Records of the Australian Museum 

21:110-115. 

, and . 1943. Remarks on some nematodes 

from Australian reptiles. Transactions of the 

Royal Society of South Australia 67:183-186. 

Jones, H. I. 1986. Gastrointestinal nematodes in the 

lizard genus Pogona Storr (Agamidae) in Western 



Research Note 

Australia. Australian Journal of Zoology 34:689- 

705. 

. 1987. Wanaristrongylus gen. n. (Nematoda: 

Trichostrongyloidea) from Australian lizards, with 

descriptions of three new species. Proceedings of 


40-47. 

. 1994. Gastrointestinal nematodes of the frillneck 

lizard, Chlamydosaurus kingii (Agamidae), 

with particular reference to Skrjabinoptera goldmanae 

(Spirurida: Physalopteridae). Australian 


. 1995a. Gastric nematode communities in lizards 

from the Great Victoria Desert, and an hypothesis 

for their evolution. Australian Journal of 

Zoology 43:141-164. 

-. 1995b. Pathology associated with physalopterid 

larvae (Nematoda: Spirurida) in the gastric 

tissues of Australian reptiles. Journal of Wildlife 

Diseases 31:299-306. 

Mackerras, M. J. 1962. Filarial parasites (Nematoda: 

Filarioidea) of Australian animals. Australian 


Manzanell, R. 1982. Oswaldofilaria spp. (Filarioidea, 

Nematoda) in Australian agamid lizards with a description 

of a new species and a redescription of 

O. chlamydosauri (Breinl). Annales de Parasitologie 

Humaine et Comparee 57:127—143. 

Mawson, P. M. 1971. Pearson Island Expedition 

1969.—8. Helminths. Transactions of the Royal 


. 1972. The nematode genus Maxvachonia (Oxyurata: 

Cosmocercidae) in Australian reptiles and 

frogs. Transactions of the Royal Society of South 

Australia 96:101-108. 

Schulz, R. E. 1927. Die Familie Physalopteridae Leiper, 

1908 (Nematodes) und die Prinzipien ihrer 

Klassifikation. Pages 287-312 in Sammlung Helmintologischer 

Arbeiten Prof. K. I. Skrjabin Gewidmet. 

Moscow. 

Descriptions of Cystacanths of Mediorhynchus orientalis and 

Mediorhynchus wardi (Acanthocephala: Gigantorhynchidae) 

DAVID P. BOLETTE 

University of Pittsburgh, Division of Laboratory Animal Resources, S1040 Biomedical Science Tower, 

Pittsburgh, Pennsylvania 15261, U.S.A. (e-mail: dbolette@vms.cis.pitt.edu) 

ABSTRACT: Cystacanths of Mediorhynchus orientalis 

Belopol'skaya and 1 cystacanth of Mediorhynchus 

wardi Schmidt and Canaris were collected from opportunistically 

infected Surinam cockroaches, Pycnoscelis 

surinamensis (Linnaeus), at the National Aviary 

in Pittsburgh, Pennsylvania, U.S.A. Morphological 


measurements and descriptions of Cystacanths of M. 

orientalis and M. wardi are provided for the first time. 

KEY WORDS: Mediorhynchus orientalis, Mediorhynchus 

wardi, Acanthocephala, Gigantorhynchidae, 

Cystacanths, Surinam cockroach, aviary, description, 

Pennsylvania, U.S.A.

Mediorhynchus orientalis Belopol'skaya, 

1953 was originally described from juvenile 

specimens collected from a little ringed plover, 

Charadrius duhius curonicm Gmelin, 1789, in 

Russia. Schmidt and Kuntz (1977) subsequently 

redescribed the species from numerous adults 

and juveniles collected from 10 species of passeriform 

birds and a Pacific golden plover, Pluvialis 

fulva (Gmelin, 1789); (as Charadrius 

dominions fulvus), from Taiwan, Borneo, and 

Hawaii. Mediorhynchus wardi Schmidt and 

Canaris, 1967 was described from numerous 

adult specimens collected from 4 species of passeriform 

birds in Njoro, Kenya. 

Forty-five species of Mediorhynchus were recorded 

as valid in Amin's (1985) list of Acanthocephala. 

Two additional species not included 

in Amin's list were apparently described during 

its preparation (George and Nadakal, 1984). 

Five of these have the cystacanths described. 

Cystacanths of Mediorhynchus petrochenkoi 

Gvosdev and Soboleva, 1966, were described by 

Lisitsina and Tkach (1994); of Mediorhynchus 

centurorum Nickol, 1969 by Nickol (1977); and 

of Mediorhynchus grandis Van Cleave, 1916 by 

Moore (1962). Brief descriptions of the cystacanth 

stage of Mediorhynchus papillosus Van 

Cleave, 1916, were provided by Ivashkin and 

Shmitova (1969) and Gafurov (1975), and of 

Mediorhynchus micracanthus (Rudolphi, 1819) 

Meyer, 1933 by Rizhikov and Dizer (1954). 

Cystacanths of Mediorhynchus orientalis 

were reported from opportunistically infected 

Surinam cockroaches, Pycnoscelis surinamensis 

(Linnaeus, 1758) (Blaberidae) at the National 

Aviary in Pittsburgh, Pennsylvania, U.S.A. 

(Bolette, 1990). These cockroaches occurred 

within a free-flight exhibit that housed a variety 

of birds originating from various geographical 

localities. This method of housing most likely 

contributed to the accidental introduction of M. 

orientalis into the enclosure. The following description 

of M. orientalis cystacanths is based on 

9 everted specimens, 1 male and 8 females, collected 

from the coelomic cavities of infected P. 

surinamensis from the previous report (Bolette, 

1990). Additionally, while reexamining the cystacanths 

previously recovered from Surinam 

cockroaches (Bolette, 1990), 1 specimen was determined 

to be M. wardi. The following description 

of M. wardi is based on this single everted 

female cystacanth. This report represents the 

BOLETTE—RESEARCH NOTES 115 

first description of M. orientalis and M. wardi 

cystacanths. 

The cockroaches were killed with ethyl acetate. 

Cystacanths were mechanically excysted, 

placed in refrigerated tap water to elicit proboscis 

evagination, killed and preserved in AFA fixative, 

and later transferred to 70% ethyl alcohol. 

Selected specimens were stained in borax-carmine, 

dehydrated in ascending concentrations of 

ethyl alcohol, cleared in ascending concentrations 

of xylene, and mounted in Permount® 

(Fisher Scientific, Fairlawn, New Jersey, 

U.S.A.). Voucher specimens were deposited in 

the United States National Parasite Collection, 

Beltsville, Maryland (USNPC No. 88032). Measurements 

are in jxm unless stated otherwise, 

with means in parentheses. Trunk measurements 

do not include the neck. Hook and spine measurements 

were determined in complete profile. 

Mediorhynchus orientalis Belopol'skaya, 

1953 

GENERAL (CYSTACANTH): Trunk short, oblong, 

slightly tapered at distal end. Proboscis 

truncate, conical (Fig. 1). Proboscis armature 

similar in both sexes. 19-24 (usually 20-21) 

nearly longitudinal rows of 4-6 (usually 5) 

hooks each. Anterior 2—3 hooks 37.5—50.0 

(47.3); middle 2-3 hooks 37.5-45.0 (40.7); posterior 

1-2 hooks 20.0-40.0 (29.2). Rootless 

spines arranged in 34—38 rows of 3-6 (usually 

4-5) spines each; 27.5-45.0 (36.75) long. Lemnisci 

long, slender, usually folded, and partly retained 

in neck region and anterior part of trunk. 

FEMALE CYSTACANTHS (based on 8 specimens): 

Trunk 1.49-1.89 (1.66) mm long, 0.48-0.73 

(0.58) mm wide at widest point. Proboscis 637— 

726 (695) long. Anterior proboscis 398-458 

(428) long, 308-338 (318) wide at base. Posterior 

proboscis 199-348 (272) long, 289-398 

(350) wide at base. Neck 131-192 (158) long, 

364-455 (391) wide at base. Sensory pit 27.5- 

30.0 (24.0) long, 27.5-45.0 (35.0) wide, located 

22.5-140 (87.0) distal to posteriormost spine. 

MALE CYSTACANTH (1 specimen): Trunk 1.59 

mm long, 0.62 mm wide at widest point. Proboscis 

662 long. Anterior proboscis 384 long, 

283 wide at base. Posterior proboscis 278 long, 

318 wide at base. Neck 167 long, 333 wide at 

base. Sensory pit 22.5 long, 30.0 wide, located 

17.5 distal to posteriormost spine. 



Figures 1, 2. Everted cystacanths of Mediorhynchus recovered from Surinam cockroaches, Pycnoscelis 

surinamensis. 1. Proboscis of M. orientalis', bar == 200 jmm. AP, anterior proboscis; BPPN, borderline 

between posterior proboscis and neck; N, neck; PP, posterior proboscis; RAPP, ridge between anterior 

and posterior proboscis. 2. Female M. wardi; bar = 250 jjim. GP, gonopore; L, lemniscus; LS, ligament 

strand; SP, sensory pit, U, uterus; V, vagina. 

Mediorhynchus wardi Schmidt and Canaris, 

1967 

FEMALE CYSTACANTH (1 specimen): Trunk 

short, subglobose, rounded at distal end (Fig. 2), 

1.89 mm long, 0.63 mm wide at widest point. 

proboscis 468 long, 402 wide at base. Posterior 

proboscis 250 long, 409 wide at base. 25 nearly 

longitudinal rows of 7-8 hooks each. Anterior 

2-3 hooks 32.5-37.5 (36.3); middle 2-3 hooks 

27.5-30.0 (29.6); posterior 2 hooks 22.5-30.0 

Proboscis truncate, conical, 718 long. Anterior (25.6). Rootless spines arranged in 40 rows of 


4-5 spines each: 25.0-35.0 (31.4). Neck 202 

long, 343 wide at base. Sensory pit 25.0 long, 

32.5 wide, located 125 distal to most posterior 

spine. Lemnisci long, slender, partly folded, extended 

far into trunk. 

The proboscis armature arrangement of M. orientalis 

cystacanths is identical to that of adults 

of this species as redescribed by Schmidt and 

Kuntz (1977). However, the proboscis armature 

and neck measurements of the cystacanths examined 

differed from those of adults in the following 

respects. The lengths of the middle 2-3 

and posterior 1-2 hooks of cystacanths were 

37.5-45.0 and 20.0-40.0, respectively, while 

those listed for adults were 34-42 and 30-44 

(Schmidt and Kuntz, 1977). The neck length and 

width of female cystacanths and the neck width 

of the male measured 131—192 by 364-455 and 

333, respectively; the measurements of adult females 

and males were reported as 216—240 by 

530-600 and 500-535, respectively. The proboscis 

of the male cystacanth was slightly longer 

at 662, while the proboscides of adult males 

were 500-600 long. 

The proboscis hook and spine length measurements 

of the cystacanth of M. wardi differed 

slightly from those given for adults of this species 

by Schmidt and Canaris (1967). Cystacanth 

hook and spine length measurements ranged 

from 22.5-37.5 and 25.0-35.0, respectively, 

while those listed for adult M. wardi were 31.0— 

36.0 and 21.0-28.0. The proboscis width of the 

cystacanth was slightly narrower than in adults; 

anterior and posterior proboscis width for the 

cystacanth measured 402 and 409, respectively, 

while the corresponding measurements reported 

for adults were 425 and 515-545. Neck length 

of the cystacanth was slightly longer than adults, 

measuring 202, while the reported adult neck 

length was 165. Additionally, the cystacanth did 

not show any evidence of an anterior trunk 

BOLETTE—RESEARCH NOTES 117 

swelling, as described for adults. However, because 

the armature arrangement and all other 

proboscis measurements are consistent with 

those described by Schmidt and Canaris (1967) 

for adult M. wardi, the single female specimen 

was assigned to this species. 


Amin, O. M. 1985. Classification. Pages 27-72 in D. 

W. T. Crompton and B. B. Nickol, eds. Biology 

of the Acanthocephala. Cambridge University 

Press, Cambridge, United Kingdom. 

Bolette, D. P. 1990. Intermediate host of Mediorhynchus 

orientalis (Acanthocephala: Gigantorhynchidae). 


Gafurov, A. K. 1975. New intermediate hosts of the 

acanthocephalan Mediorhynchus papillosus Van 

Cleave, 1916. Zoologicheskii Sbornik 2:103-104. 

(In Russian). 

George, P. V., and A. M. Nadakal. 1984. Three new 

species of Acanthocephala (Gigantorhynchidea) 

from birds of Kerala. Acta Parasitologica Polonica 

29:97-106. 

Ivashkin, V. M., and G. Y. Shmitova. 1969. The life 

cycle of Mediorhynchus papillosus. Trudy 

Gel'mintologicheskoi Laboratorii 20:62-63. 

Lisitsina, O. I., and V. V. Tkach. 1994. Morphology 

of cystacanths of some acanthocephalans from 

aquatic and terrestrial intermediate hosts in the 

Ukraine. Helminthologia 31:83-90. 

Moore, D. V. 1962. Morphology, life history, and development 

of the acanthocephalan Mediorhynchus 

grandis Van Cleave, 1916. Journal of Parasitology 

48:76-86. 

Nickol, B. B. 1977. Life history and host specificity 

of Mediorhynchus centurorum Nickol 1969 

(Acanthocephala: Gigantorhynchidae). Journal of 


Rizhikov, K. M., and Y. B. Dizer. 1954. Biology of 

Macracanthorhynchus catulinus and Mediorhynchus 

micracanthus. Doklady Akademii Nauk 

SSSR 95:1367-1369. 

Schmidt, G. D., and A. G. Canaris. 1967. Acanthocephala 

from Kenya with descriptions of two new 

species. Journal of Parasitology 53:634-637. 

, and R. E. Kuntz. 1977. Revision of Mediorhynchus 

Van Cleave 1916 (Acanthocephala) with 

a key to species. Journal of Parasitology 63:500- 

507. 




Research Note 

Gastrointestinal Helminths of Four Lizard Species from 

Moorea, French Polynesia 

STEPHEN R. GOLDBERG, u CHARLES R. BuRSEY,2 AND HAY CHEAM' 


(e-mail: sgoldberg@whitticr.edu) and 

2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, 

U.S.A. (e-mail: cxbl3@psu.edu) 

ABSTRACT: The gastrointestinal tracts of 82 lizards 

comprising 2 gekkonids, Gehyra oceanica (N = 20) 

and Lepidodactylus lugubris (N =31), and 2 scincids, 

Cryptoblepharus poecilopleurus (N = 4) and Emoia 

cyanura (N = 27), from Moorea, French Polynesia, 

were examined for helminths. One species of cestode, 

Cylindrotaenia decidua, 5 species of nematodes, Maxvachonia 

chabaudi, Pharyngodon oceanicus, Spauligodon 

gehyrae, Skrjabinoptera sp. (larvae), and an unidentified 

oxyurid were found. Eleven new host records 

and 11 new locality records are reported. 

KEY WORDS: lizard, Cryptoblepharus poecilopleurus, 

Emoia cyanura, Gehyra oceanica, Lepidodactylus 

lugubris, Cestoda, Nematoda, Moorea, French Poly- 

Eight species of lizards—the snake-eyed 

skink, Cryptoblepharus poecilopleurus (Wiegmann, 

1834); the moth skink, Lipinia noctua 

(Lesson, 1830); the copper-tailed skink, Emoia 

cyanura (Lesson, 1830); the stump-toed gecko, 

Gehyra mutilata (Wiegmann, 1834); the oceanic 

gecko, Gehyra oceanica (Lesson, 1830); the 

Indo-Pacific gecko, Hemidactylus garnotii Dumeril 

and Bibron, 1836; the Indo-Pacific tree 

gecko, Hemiphyllodactylus typus Bleeker, 1860; 

and the mourning gecko, Lepidodactylus lugubris 

(Dumeril and Bibron, 1836)—occur on Moorea, 

French Polynesia (Ineich and Blanc, 1988). 

These species are widely distributed in the Pacific 

Islands (Burt and Burt, 1932). Helminths 

have been reported from G. oceanica, H. garnotii, 

and L. lugubris (Table 1), but to our 

knowledge, there are no published reports of 

helminths from the other 5 lizard species. The 

purpose of this note is to report helminths for C. 

poecilopleurus, E. cyanura, G. oceanica, and L. 

lugubris from Moorea, French Polynesia, and to 

list 11 new host and 11 new locality records for 

these helminths. 


118 


Of the 8 species of lizards on Moorea, 82 individuals 

representing 4 species were collected by 

hand by one of us (S.R.G.) in April 1992: 4 C. 

poecilopleurus, 7 E. cyanura, 3 G. oceanica at 

Marae Titiroa, 2 km below Belvedere Viewpoint, 

ca. 457 m elevation, Opunohu Valley (17°33'S, 

149°50'W); 20 E. cyanura, 12 G. oceanica, 11 L. 

lugubris at the Richard B. Gump South Pacific 

Biological Research Station, ca. 60 m elevation, 

ca. 3 km west of Paopao (17°31'S, 149°49'W); 5 

G. oceanica, 20 L. lugubris at Paopao, ca. 20 m 

elevation (17°31'S, 149°51'W). These were the 

only lizard species observed at the time of collection. 

Lizards were fixed in 10% formalin for 24 

hours and preserved in 70% ethanol. The abdominal 

cavity was opened, and the esophagus, 

stomach, and small and large intestines were removed, 

slit longitudinally, and examined under 

a dissecting microscope. All lizards were deposited 

in the herpetology collection of the Natural 

History Museum of Los Angeles County 

(LACM), Los Angeles, California, U.S.A.: C. 

poecilopleurus: LACM 141065-141068; E. cyanura: 

LACM 141038-141064; G. oceanica: 

LACM 141009-141028; L. lugubris: LACM 

140976-141006. 

Each nematode was cleared on a glass slide 

in undiluted glycerol. Cestodes were stained 

with hematoxylin and mounted in balsam. Identifications 

were made from these preparations 

with use of a compound microscope. Number of 

helminths, prevalence, mean intensity, and range 

of infection are given in Table 2. Terminology 

is in accordance with Bush et al. (1997). 

One species of cestode, Cylindrotaenia decidua 

(Ainsworth, 1985), and 5 species of nematodes, 

Maxvachonia chabaudi Mawson, 1972; 

Pharyngodon oceanicus Bursey and Goldberg, 

1999; Spauligodon gehyrae Bursey and Gold-

Table 1. Previous helminth records for Gehyra oceanica, Hemidactylus garnotii, and Lepidodactylus lug 

Host 

Helminth Locality 

Guam 

Moorea, Rarotonga, Tahiti 

Federated States of Micronesia, Fiji, 

Marquesas, Moorea, Rota, Tuamotu 

Guam, Rota 

Gehyra oceanica (Lesson, Lesson, 1830) 

Oochoristica javaensis zensis Kennedy Kennedy, Killick, and Beverley-Burton, 1982 

Pharyngodon oceanicus Bursey and Goldberg, 1999 

Spauligodon gehyrae Bursey and Goldberg, 1996 

Hemidactylus garnotii Dumeril and Bibron, 1836 

Platynosomum fastosum Kossack, 1910 

Island of Oahu, Hawaii 


Leyte, Luzon 


Skrjabinodon dossae (Caballero, 1968) 


Guam 

Rota 

Lepidodactylus lugubris (Dumeril and Bibron, 1836) 

Allopharynx macallisten Dailey, Goldberg, and Bursey, 1998 

Islands of Hawaii, Oahu 

Rota 



Guam, Rota 





Cyiindrotaenia allisonae (Schmidt, 1980) 

Pharyngodon lepidodactylus Bursey and Goldberg, 1996 

Skrjabinelazia machidai Hasegawa, 1984 


Raillietiella frenatus AH, Riley, and Self, 1981 



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hyrae from a collection of lizards. Gehyra 

oceanica is the only known host. 

Cryptoblepharus poecilopleurus, E. cyanura, 

and L. lugubris are new host records for larvae 

of Skrjabinoptera sp.; Moorea is a new locality 

record. Oxyurids have not been previously reported 

in C. poecilopleurus; however, once identified, 

this species would be a new host and locality 

record. Identification of oxyurids requires 

male specimens, thus, a description cannot be 

done at this time. 

Further examinations of lizards from additional 

localities will be needed before the helminth 

fauna of Pacific Island lizards can be known. 

Lizards were collected under permit 4186/ 

BCO issued to S.R.G. by the Haut-Commissariat 

de la Republique en Polynesie Francaise. 


Ainsworth, R. 1985. Baerietta decidua n. sp. (Cestoda: 

Nematotaeniidae) from the New Zealand skink 

Leiolopisina nigriplantare maccani Hardy, 1977. 

New Zealand Journal of Zoology 12:131-135. 

Brown, S. G., S. Kwan, and S. Shero. 1995. The 

parasitic theory of sexual reproduction: parasitism 

in unisexual and bisexual geckos. Proceedings of 

the Royal Society of London B 260:317-320. 

Bursey, C. R., and S. R. Goldberg. 1996a. Spauligodon 

gehyrae n. sp. (Nematoda: Pharyngodonidae) 

from Gehyra oceanica (Sauria: Gekkonidae) 

from Guam, Mariana Islands, Micronesia. Journal 


, and . 19965. Pharyngodon lepidodactylus 

sp. n. (Nematoda: Pharyngodonidae) from 

the mourning gecko, Lepidodactylus lugubris 

(Lacertilia: Gekkonidae), from Hawaii. Journal of 


51-55. 

-, and . 1999. Pharyngodon oceanicus 

sp. n. (Nematoda: Pharyngodonidae) from the 

oceanic gecko, Gehyra oceanica (Sauria: Gekkonidae) 

of the Pacific Islands. Journal of the Helminthological 


Burt, C. E., and M. D. Burt. 1932. Herpetological 

results of the Whitney South Sea Expedition. VI. 

Pacific Island amphibians and reptiles in the collection 

of the American Museum of Natural History. 

Bulletin of the American Museum of Natural 

History 63:461-597. 

GOLDBERG ET AL.—RESEARCH NOTES 121 





Dailey, M. D., S. R. Goldberg, and C. R. Bursey. 

1998. Allopharynx macallisteri sp. n. (Trematoda: 

Plagiorchiidae) from the mourning gecko, Lepidodactylus 

lugubris, from Guam, Mariana Islands, 

Micronesia, with a key to the species of the genus 

Allopharynx. Journal of the Helminthological Society 


Goldberg, S. R., and C. R. Bursey. 1995. Gastrointestinal 

nematodes of two Australian skinks, Ctenotus 

regius and Ctenotus schomburgkii. Journal of 


237-238. 

, and . 1997. New helminth records for 

the mourning gecko, Lepidodactylus lugubris 

(Gekkonidae) from Hawaii. Bishop Museum Occasional 

Papers. Records of the Hawaii Biological 

Survey for 1996. Part 2: Notes, 49:54-56. 

, , and H. Cheam. 1998. Gastrointestinal 

helminths of four gekkonid lizards, Gehyra 

mutilata, Gehyra oceanica, Hemidactylus frenatus 

and Lepidodactylus lugubris from the Mariana Islands, 

Micronesia. Journal of Parasitology 84: 

1295-1298. 

, , and S. Hernandez. 1999. Nematodes 

of two skinks, Ctenotus leonhardii and Ctenotus 

quattuordecimlineatus (Sauria: Scincidae), from 

Western Australia. Journal of the Helminthological 


Ineich, I., and C. P. Blanc. 1988. Distribution des 

reptiles terrestres en Polynesie oriental. Atoll Research 

Bulletin 318:1-75. 

Jones, H. I. 1988. Nematodes from nine species of 

Varamts (Reptilia) from tropical northern Australia, 

with particular reference to the genus Abbreviata 

(Physalopteridae). Australian Journal of Zoology 

36:691-708. 

Jones, M. K. 1987. A taxonomic revision of the Nematotaeniidae 

Liihe, 1910 (Cestoda: Cyclophyllidea). 

Systematic Parasitology 10:165-245. 

Loo, B. 1971. The gecko as a new intermediate host 

for the cat liver fluke, Platynosomum fastosum, in 

Hawaii. Honors thesis, University of Hawaii, 34 

pp. 

Mawson, P. M. 1972. The nematode genus Maxvachonia 

(Oxyurata: Cosmocercidae) in Australian 

reptiles and frogs. Transactions of the Royal Society 

of South Australia 96:101-108. 

Schmidt, G. D., and R. E. Kuntz. 1972. Nematode 

parasites of Oceanica. XIX. Report on a collection 

from Philippine reptiles. Transactions of the 

American Microscopical Society 91:63—66. 




Research Note 

New Records of Endohelminths of the Alligator Snapping Turtle 

(Macroclemys temminckii} from Arkansas and Louisiana, U.S.A. 

MICHELLE WEST,' TIMOTHY P. SCOTT,'-3 STEVE R. SIMCIK,' AND RUTH M. ELSEY2 

1 Department of Biology, Texas A&M University, College Station, Texas 77843-3258, U.S.A. 

(e-mail: tims@mail.bio.tamu.edu) and 

2 Louisiana Department of Wildlife and Fisheries, Rockefeller Wildlife Refuge, Grand Chenier, 

Louisiana 70643, U.S.A. (e-mail: Elsey_RM@wlf.state.la.us) 

ABSTRACT: Viscera were collected from alligator 

snapping turtles, Macroclemys temminckii (Harlan), 

caught by commercial trappers in Arkansas and Louisiana. 

A total of 1,708 parasites were recovered from 

44 turtles. Endohelminths identified were 4 species of 

nematodes {Brevimulticaecum tenuicolle Rudolphi, 

Falcaustra chelydrae Harwood, Falcaustra wardi 

Mackin, and Serpinema trispinosus Leidy) and 3 species 

of acanthocephalans (Neoechinorhynchus chrysemydis 

Cable and Hopp, Neoechinorhynchus emydis 

Leidy, and Neoechinorhynchus pseudemydis Cable and 

Hopp). All but F. chelydrae are new records for Macroclemys 

temminckii. 

KEY WORDS: acanthocephalan, alligator snapping 

turtle, endohelminth, Macroclemys temminckii, nematode, 

parasite, Arkansas, Louisiana, U.S.A. 

The alligator snapping turtle, Macroclemys 

temminckii Harlan, 1835, is a large freshwater 

chelydrid found along the Gulf Coastal Plains 

and the Mississippi River Valley, U.S.A. (Lovich, 

1993). Although some endohelminths are 

known to be harbored by this turtle, this study 

documents several endohelminths not previously 

reported. The most recent parasite work of M. 

temminckii was conducted by McAllister et al. 

(1995). In their report, 2 alligator snapping turtles 

were found to harbor 3 different forms of 

hemogregarines and the nematode Falcaustra 

chelydrae Harwood, 1932. Additional parasites 

recovered from M. temminckii include the trematode 

Lophotaspis interiora Ward and Hopkins, 

1931, and a new species of Eimeria Upton et al., 

1992. Here, we provide further details on the 

variation of the endohelminth fauna of M. temminckii. 

Alligator snapping turtles were caught by 

commercial trappers in southeastern Arkansas 

and Louisiana, U.S.A., in the spring and summer 

of 1993 and 1994. Turtles were generally caught 


122 


in hoop nets or on baited hooks. Often a number 

of turtles were delivered to a processor in Louisiana 

and held in a storage tank for several days 

until there was a sufficient quantity to process. 

Viscera were collected and frozen for later analysis. 

Samples were collected as part of another 

study on the food habits of M. temminckii (Elsey, 

unpubl.). Viscera were thawed, and stomachs 

and intestinal tracts were examined for endohelminths. 

If present, grossly visible parasites 

were counted and preserved in 70% ethanol for 

later identification. When required, nematodes 

were cleared using lactophenol. Temporary 

mounts of the specimens were made using glycerin 

jelly. Once identified, the nematodes were 

returned to 70% ethanol. The acanthocephalans 

were stained with Semichon's acetocarmine for 

24 hours and destained with acid alcohol. Destaining 

was arrested using 0.1% sodium bicarbonate. 

Specimens were dehydrated in ethanol, 

cleared using methyl salicylate, and mounted in 

Kleermount®. Identifications of nematodes were 

made using descriptions provided by Baker 

(1979, 1986) and Sprent (1979). Use of ecological 

terms follow suggestions of Margolis et al. 

(1982). 

Seven species of helminths were recovered 

from 44 alligator snapping turtles (Table 1). The 

parasites include 4 species of nematodes and 3 

species of 1 genus of acanthocephalan. In this 

study, F. chelydrae was the only endohelminth 

found that has been previously documented as a 

parasite of this turtle. To our knowledge, this is 

the first record of the nematodes Brevimulticaecum 

tenuicolle Rudolphi, 1819, Falcaustra wardi 

Mackin, 1936, Serpinema trispinosus Leidy, 

1852, and the acanthocephalans Neoechinorhynchus 

chrysemydis Cable and Hopp, 1954, 

Neoechinorhynchus emydis Leidy, 1851, and 

Neoechinorhynchus pseudemydis Cable and

WEST ET AL.—RESEARCH NOTES 123 

Table 1. Parasites recovered from Macroclemys temminckii in southeastern Arkansas and Louisiana. 

Parasite Prevalence* Mean intensity ± SDf Range Abundance ± SDi 


Neoechinarhynchus chrysemydis 

(USNPC 88658) 

Neoechinorhynchus emydis 

(USNPC 88659) 

Neoechinarhynchus pseudemydis 

(USNPC 88660) 

Nematoda 

Brevimultlcaecum tenuicolle 

(USNPC 88661) 

Falcaustra die/yd rat- 

(USNPC 88663) 

Falcaustra wardi 

(USNPC 88662) 

Serpinema trispinosus 

(USNPC 88664) 

9% 

2% 

2% 

9% 

98% 

14% 

84% 

2% 

16% 

26.0 ± 44.1 

21.0 

51.0 

8.0 ± 8.3 

37.3 ± 56.4 

5.2 ± 9.7 

41.4 ± 59.5 

1.0 

5.9 ± 5.8 

1-51 

— 

— 

1-20 

1-319 

1-25 

1-319 

— 

1-14 

2.4 ± 13.9 

0.5 ± 3.2 

1.2 ± 7.7 

0.7 ± 3.2 

36.5 ± 56.0 

1.0 ± 4.1 

34.8 ± 56.6 

0.0 ± 0.2 

0.9 ± 3.1 

* Prevalence = number of individuals of a host species infected with a particular parasite species -=- number of hosts examined. 

t Abundance = total number of individuals of a particular parasite species in a sample of hosts -^ total number of individuals 

of the host species in the sample. 

$ Mean intensity = total number of individuals of a particular parasite species in a sample of a host species •*• number of 

infected individuals of the host species in the sample. 

Hopp, 1954, from the alligator snapping turtle. 

Individual turtles harbored up to 4 species of 

parasites. Thirty-five turtles (79.5%) contained 1 

species, 7 turtles (15.9%) had 2 species, and 2 

(4.6%) had 4 species. A total of 1,708 parasite 

specimens were identified. Infected hosts held 

from 1 to 319 parasites. 

Species of Falcaustra are commonly reported 

parasites of aquatic turtles (Conboy et al., 1993). 

In this study, F. chelydrae accounted for 89.6% 

(1,531) of the total parasites identified and was 

harbored by 84.1% (37) of the turtles studied. 

Falcaustra wardi accounted for less than 1.0% 

(1) of the total number of parasites and was detected 

in only 1 turtle (2.3%). 

Serpinema trispinosus is another nematode 

common in aquatic turtles (Conboy et al., 1993). 

However, this is the first account of M. temminckii 

harboring this parasite. Serpinema trispinosus 

accounted for 2.4% (41) of the total 

number of parasites recovered and was found in 

15.9% (7) of the turtles. 

Brevimulticaecum tenuicolle has been found 

only in the American alligator, Alligator mississippiensis 

Daudin, 1803 (Sprent, 1979). This 

nematode can be differentiated from other species 

based on lobulated, teat-shaped ventricular 

appendices (Sprent, 1979). In this study 1.8% 

(31) of the total parasites were B. tenuicolle. Of 

the turtles studied, 13.6% (6) harbored this par- 

asite. This is the first record of this species of 

helminth in the alligator snapping turtle. 

Acanthocephalans of the genus Neoechinorhynchus 

are common endohelminths of aquatic 

turtles (Petrochenko, 1971). Prior to this report, 

none has been observed in M. temminckii. Species 

of Neoechinorhynchus represented 6.1% 

(104) of the parasites in this study (1.2% TV. 

chrysemydis, 3.0% N. emydis, and 1.9% N. pseudemydis), 

and parasitized 9.1% (4) of the turtles. 

In summary, this research added 6 new species 

to the helminth fauna of the alligator snapping 

turtle. Future natural history and endohelminth 

surveys of M. temminckii could contribute 

to a better overall understanding of the parasitic 

life cycle, parasite diversity, and host-parasite 

relationship. 

Thanks are extended to Ms. Came Kilgore for 

assistance in laboratory identification of endohelminths, 

to Mr. Lee Caubarreaux and Mr. 

James Manning of the Louisiana Department of 

Wildlife and Fisheries (L.D.W.F.) for administrative 

support, and to several L.D.W.F. specialists 

and in-service students for assistance with field 

collections and necropsies. Much appreciation 

also goes to the Department of Biology at Texas 

A&M University for the use of its facilities. 

Thanks are extended to Dr. J. R. Lichtenfels, 

United States National Parasite Collection, Ag- 



ricultural Research Service, Beltsville, Maryland 

for lending specimens for comparative purposes. 


Baker, M. R. 1979. Serpinema species (Nematoda: 

Camallanidae) from turtles of North America and 

Europe. Canadian Journal of Zoology 57:934- 

939. 

. 1986. Falcaustra species (Nematoda: Kathlaniidae) 

parasitic in turtles and frogs in Ontario. 


Conboy, G. A., J. R. Laursen, G. A. Averbeck, and 

B. E. Stromberg. 1993. Diagnostic guide to some 

of the helminth parasites of aquatic turtles. The 

Compendium 15:1217-1224. 

Lovich, J. E. 1993. Macroclemys, M. te/nminckii. Pages 

562.1-562.4 in C. H. Ernst, ed. Catalogue of 



Research Note 

American Amphibians and Reptiles. Society for 

the Study of Amphibians and Reptiles, New York. 

Margolis, L., G. W. Esch, J. C. Holmes, A. M. 

Kuaris, and G. A Schad. 1982. The use of ecological 

terms in parasitology (report of an ad hoc 

committee of the American Society of Parasitologists). 


McAllister, C. T., S. J. Upton, and S. E. Trauth. 

1995. Hemogregarines (Apicomplexa) and Falcaustra 

chelydrae (Nematoda) in an alligator 

snapping turtle, Macroclemys temminckii (Reptilia: 

Testudines), from Arkansas. Journal of the 

Helminthological Society of Washington 62:74- 

77. 

Petrochenko, V. I. 1971. Acanthocephala of Domestic 

and Wild Animals. Keter Press Binding: Winer 

Bindery Ltd., Jerusalem, Israel. 465 pp. 

Sprent, J. F. A. 1979. Ascaridoid nematodes of amphibians 

and reptiles: Multicaecum and Brevimulticaecum. 

Journal of Helminthology 53:91-116. 

Parasites of Eastern Indigo Snakes (Drymarchon corais couperi} from 

Florida, U.S.A. 

GARRY W. FOSTER,' PAUL E. MoLER,2 JOHN M. KINSELLA,' SCOTT P. TERRELL,' AND 

DONALD J. FORRESTER'-3 

1 Department of Pathobiology, College of Veterinary Medicine, University of Florida, Gainesville, 

Florida 32611, U.S.A. (e-mail: FosterG@mail.vetmed.ufl.edu; wormdwb@aol.com; 

TerrellS@mail.vetmed.ufl.edu; ForresterD@mail.vetmed.ufl.edu); and 

2 Florida Fish and Wildlife Conservation Commission, Gainesville, Florida 32601, U.S.A. 

(e-mail: molerp@gfc.state.fl.us) 

ABSTRACT: Nineteen species of parasites (2 trematodes, 

3 cestodes, 10 nematodes, 2 acanthocephalans. 

1 pentastomid, and 1 tick) were identified from 21 

eastern indigo snakes (Drymarchon corais couperi 

Holbrook, 1842) collected in Florida, U.S.A., between 

1967 and 1999. For the 12 indigo snakes from which 

quantitative data were obtained, the most prevalent 

parasites were the nematodes Kalicephalus inermis corone 

llae Ortlepp, 1923, and Kalicephalus appendiculatus 

Molin, 1861, each occurring in 10 snakes, and 

cystacanths of Macracanthorhynchus ingens (Listow, 

1C79), which were present in all 12 snakes. The tick 

Arnblyomma dissimile Koch, 1844, infested indigo 

snakes from Brevard County. Twelve new host records; 

are presented. 

KEY WORDS: eastern indigo snake, Drymarchon 

corais couperi, parasites, trematodes, cestodes, nematodes, 

acanthocephalans, pentastomids, cystacanths, 

Florida, U.S.A. 

The eastern indigo snake (Drymarchon corais 

couperi Holbrook, 1842) occurs throughout 

Florida and much of southern Georgia, U.S.A., 

although the populations located in Georgia and 

the Florida panhandle may be very localized 

(Moler, 1992). It was first protected by the state 

of Florida in 1972 (Florida Game and Fresh Water 

Fish Commission, 1972) and was federally 

listed as threatened in 1978 (U.S. Fish and Wildlife 

Service, 1978). This project was undertaken 

to identify the possible impact parasites have on 

the threatened indigo snake in Florida. 

Nine road-killed indigo snakes were necropsied 

at the Archbold Biological Station (ABS), 

Highlands County, Florida, between 1967 and 

-1 Corresponding author. 


1987, and from these only a sample of parasites 

that were seen grossly was collected. Twelve additional 

eastern indigo snakes were quantitatively 

examined for parasites between 1992 and 

1999. Snakes were collected as roadkills in the 

following counties in Florida: Alachua (n =1), 

Brevard (n = 4), Charlotte (n = 1), Indian River 

(n = 1), Levy (n = 1), Monroe (n = 2), Okaloosa 

(n = 1), and Osceola (n — 1). Most snakes 

were frozen until necropsy, when they were examined 

following the methods of Kinsella and 

Forrester (1972). Because of small sample size 

and the lack of comparable sampling techniques, 

no statistical analysis was attempted. All indigo 

snake specimens were deposited in the Florida 

Museum of Natural History, Gainesville, Florida. 

Snakes were collected under state and federal 

collection and salvage permits. Cestodes 

and trematodes were preserved in Roudabush's 

AFA and nematodes in 70% ethanol with glycerin. 

Cestodes and trematodes were stained with 

either Hams' hematoxylin or Semichon's acetocarmine 

and mounted in neutral Canada balsam. 

Nematodes were cleared and mounted in 

lactophenol. Tissues for histological examination 

were fixed in 10% neutral buffered formalin, 

routinely processed, paraffin-embedded, sectioned 

at 5 (Am, and stained with hematoxylin 

and eosin. Terminology used follows Bush et al. 

(1997). Voucher specimens of helminths were 

deposited in the United States National Parasite 

Collection, Beltsville, Maryland (accession 

numbers 88619-88632, 88642-88643), and 

ticks were deposited in the National Tick Collection, 

Statesboro, Georgia, U.S.A. (accession 

numbers RML122786, RML122787). 

A total of 17 species of helminths (2 trematodes, 

3 cestodes, 10 nematodes, 2 acanthocephalans), 

1 pentastomid, and 1 tick was collected 

from the 21 indigo snakes (Table 1). All helminths, 

except for the 3 species of Kalicephalus, 

are new host records. 

From the 9 ABS snakes, the following were 

identified: Kalicephalus rectiphilus, Kiricephalus 

coarctatus, and cystacanths of Macracanthorhynchus 

ingens. These samples were not included 

in Table 1 and will not be discussed further, 

but are presented here as Highlands County 

records only. 

Prevalences and intensities of parasites for the 

12 quantitatively examined snakes are listed in 

Table 1. Three species of Kalicephalus (K. inermis 

coronellae, K. appendiculatus, and K. rec- 

FOSTER ET AL.—RESEARCH NOTES 125 

tiphilus) were collected; 6 indigo snakes had all 

3 species present, and the other 6 indigo snakes 

had 2 species. Schad (1962) reported that, as 

adults, Kalicephalus localize themselves in the 

gut without overlapping in their distribution in 

the host. This seems to be true for the 3 species 

of Kalicephalus in the indigo snakes we examined. 

There was some overlapping in distribution 

of the 3 species (Table 1), but this might 

have been because of postmortem migration or 

passive displacement of gut contents when the 

snakes were killed. 

Cystacanths of M. ingens were encysted in the 

mesenteries, mainly on the serosal surface of the 

small intestine. In histological sections, the cystacanths 

were located predominantly within the 

expanded intestinal serosa, with fewer present in 

the muscular tunics, and were rarely found within 

the mucosal lamina propria. The intact cystacanths 

were surrounded by 1—3 layers of fibrous 

connective tissue with no discernible inflammatory 

response. Many of the cystacanths 

were degenerated as characterized by the loss of 

histological anatomic detail. In these cases, the 

celomic cavities of the cystacanths were replaced 

by necrotic cellular debris and fragments 

of mineralized debris. This accumulation of debris 

was surrounded by a rim of degenerated heterophils 

and macrophages, which in turn was 

surrounded by 1-3 layers of fibrous connective 

tissue. Cystacanths present within the mucosal 

lamina propria had been replaced entirely by 

dense infiltrates of degenerated leucocytes surrounded 

by multiple layers of fibrous connective 

tissue. Inflammatory cells were not present outside 

the fibrous capsule surrounding the degenerated 

cystacanths. The presence of an inflammatory 

reaction and degenerated cys.tacanths 

was not reported by Goldberg et al. (1998) with 

the oligacanthorhynchid cystacanths in the longnose 

snakes (Rhinocheilus lecontei Baird & Girard, 

1853) that they surveyed. 

Elkins and Nickol (1983) reported 7 species 

of Louisiana snakes that were infected with cystacanths 

of M. ingens. They indicated also that 

snakes may be a significant epizootiological factor 

in the life cycle of M. ingens. The indigo 

snake should be considered a paratenic host for 

these acanthocephalans. They probably become 

infected with cystacanths by several routes. Being 

vertebrate generalists in their food habits, 

indigo snakes in Florida prey on several species 

of snakes, fishes, frogs, toads, lizards, small tur- 



Table 1. Parasites from 12 eastern indigo snakes collected in Florida, U.S.A. 

Species of parasite Location in host* 

Trematoda 

Ochetosoma kansense± 

(Crow, 1913) 

Ochetosoma elongation^ 

(Pratt, 1903) 

Cestoda 

Proteocephalus sp.t 

Larval cestode (tetrathyridium):]: 

Larval cestode (sparganum):t 

Nematoda 

Kalicephalus inennis coronellae 

Ortlepp, 1923 

Kalicephalus appendiculatus 

Molin, 1861 

Kalicephalus rectiphilus 

Harwood, 1932 

Physaloptera obtussima^- 

Molin, 1860 

Terranova caballerotf. 

Barus and Coy Otero, 1966 

Strongyloides sp. 

Eustrongylides larvae:]: 

Gnathostoma larvaet 

Physaloptera larvae^: 

Larval nematodes 

Acanthocephalan (cystacanths) 

Centrorhynchus spinosusi 

(Kaiser, 1893) 

Macracanthorhynchus ingens% 

(Listow, 1879) 

Pentastoma 

Kiricephalus coarctatus 

(Diesing, 1850) 

Acari 

Amblyomma dissimile 

Koch, 1844 

ES, OC, ST 

BC, ES, SI, LI, LN 

SI 

ME 

ME 

ES, ST 

ST, SI 

SI, LI 

ES 

ST 

SI, LI 

ST 

ME 

ST 

SI 

ME 

ME 

BC, LN 

SK 

Number of 

snakes 

infected 

7 

3 

1 

2 

2 

10 

10 

9 

1 

1 

3 

1 

1 

6 

5 

3 

12 

Intensity 

Mean Range Counties! 

15 

337 

2 

7 

3 

37 

27 

17 

1 

1 

3 

2 

2 

16 

5 

18 

151 

3-34 B, C, I, L, O 

35-541 B 

3-10 

2-3 

2-128 

5-50 

1-77 

1-5 

1-80 

1-9 

3-30 

1-515 

1-7 

2-10 

B 

O 

I, K 

A, B, C, K, L, M, O 

B, C, I, L, M, O, 

A, B, C, K, L, M, O 

K 

K 

B, C, I 

B 

M 

A, B, I, M, O 

B, I, O 

B, K 

A, B, C, I, K, L, M, O 

B, C, I, K, L, M, O 

* BC = body cavity; ES = esophagus; LI = large intestine; LN = lungs; ME = mesenteries; OC = oral cavity; SI = small 

intestine; SK = skin; ST = stomach. 

t County where parasite was found: A = Alachua; B = Brevard; C = Charlotte; I = Indian River; K = Okaloosa; L = Levy; 

M = Monroe; O = Osceola. 

£ New host records. 

ties, birds, and small mammals (Moler, 1992)., 

which may also be paratenic hosts for M. ingens. 

Larval stages have been identified from Florida 

mice (Podomys floridanus (Chapman, 1889)) 

and cotton mice (Peromyscus gossypinus (Le 

Conte, 1853)) in Florida (Forrester, 1992). In 

Florida, adults of M. ingens have been reported 

mainly from raccoons (Procyon lotor (Linnaeus, 

1758)) (Forrester, 1992) and black bears (Ursus 

americanus floridanus (Merriam, 1896)) (Conti 

et al., 1983). Cystacanths of Centrorhynchus 

spinosus also were encysted in the mesenteries. 


They encysted mainly on the serosal surface of 

the small intestine, intermixed with the cystacanths 

of M. ingens, but in much lower intensities 

(Table 1). The definitive hosts for C. spinosus 

are several species of birds, primarily 

owls (Nickol, 1983). In Florida we have unpublished 

records of them in barred owls, Strix varia 

Barton, 1799, eastern screech-owls, Otus asio 

Linnaeus, 1758, and great horned owls, Bubo 

virginianus (Gmelin, 1788). Raccoons and raptors 

in Florida could acquire these acanthocephalan 

infections from indigo snakes if these

snakes are part of their diet. The indigo snake 

has not been reported as a food item of black 

bears in Florida (Maehr and DeFazio, 1985). 

The encysted cystacanths did not seem to have 

any obvious detrimental effect on any of the indigo 

snakes necropsied. One road-killed female 

indigo snake with 515 M. ingens encysted in 

mesenteries around the small intestines had a 

large amount of visceral fat present and 11 eggs 

in utero. 

Only 1 indigo snake (Okaloosa County) was 

infected with a single Terranova caballeroi. 

This ascarid is a common parasite of water 

snakes (Nerodia spp.) and cottonmouths (Agkistrodon 

piscivorus Lacepede, 1789) in the southeastern 

United States (Fontenot and Font, 1996). 

Fourth-stage larvae of a species of Eustrongylides 

were found in the stomach wall of 1 

snake from Brevard County. These were most 

likely the larvae of Eustrongylides ignotus, 

adults of which are parasitic in birds, most commonly 

Ciconiiformes (Spalding et al., 1993). 

The most important intermediate host for E. ignotis 

in Florida is the small mosquitofish (Gambusia 

holbrooki Girard, 1859), with some amphibians 

and reptiles serving as paratenic hosts 

(Coyner, 1998). This would be considered an accidental 

infection of a snake with a bird parasite. 

In this study, Amblyomma dissimile infested 

indigo snakes only from Merritt Island in Brevard 

County. The ticks seemed to aggregate to 

a small localized area of about 5 cm in diameter. 

The skin in the areas of tick attachment was 

swollen, with some of the scales malformed. 

Histologically, the areas of tick attachment were 

marked by a pustular dermatitis that was acute, 

multifocal, and severe, with intralesional bacterial 

and fungal colonization. At the junctions between 

numerous scales were multifocal, locally 

extensive subcorneal pustules that contained degenerate 

heterophils intermixed with numerous 

gram-positive bacterial cocci. At several of the 

scale junctions the subcorneal aggregate of degenerate 

heterophils extended through the epidermis 

into the dermis. Durden et al. (1993) reported 

A. dissimile from an eastern indigo snake 

and a cotton mouse (P. gossypinus) from Merritt 

Island in 1990. Most indigo snakes seen on Merritt 

Island by one of us (P.E.M.) have been infested 

with A. dissimile, and Durden et al. (1993) 

suggested that a viable population of this tick 

species occurs there. Amblyomma dissimile has 

been reported infesting these additional hosts in 

FOSTER ET AL.—RESEARCH NOTES 127 

Florida: pygmy rattlesnake (Sistrurus miliarius 

Linnaeus, 1766), yellow rat snake (E lap he obsoleta 

quadrivittata Holbrook, 1836), Florida 

kingsnake (Lampropeltis getula floridana Blanchard, 

1919), common kingsnake (Lampropeltis 

getula Linnaeus, 1766), eastern diamond rattlesnake 

(Crotalus adamanteus Palisot de Beauvois, 

1799), pine snake (Pituophis melanoleucus 

Daudin, 1803), cottonmouth (A. piscivorus), gopher 

tortoise (Gopherus polyphemus Daudin, 

1802), and giant toad (Bufo marinus Linnaeus, 

1855), and reported in the following counties: 

Broward, Collier, Dade, Indian River, Lee, Martin, 

Palm Beach, and St. Lucie (Bequaert, 1932; 

Bequaert, 1945; Wilson and Kale, 1972; unpublished 

computer and manual searches of the data 

records of the Florida State Collection of Arthropods, 

Gainesville, Florida, U.S.A., and the 

National Tick Collection, Statesboro, Georgia, 

U.S.A., 1999). From these records A. dissimile 

seems to be well established in southern peninsular 

Florida. 

Because most of the indigo snakes we examined 

were in good flesh and had deposits of 

visceral fat and several of the females had a normal 

number of eggs in utero, it is our assessment 

that the general health of the snakes, did not 

seem to be compromised by the parasite intensities 

we report here. The attachment sites of A. 

dissimile may allow a pathway for secondary 

bacterial infections to infiltrate to deeper tissues. 

However, in the indigo snakes we examined, the 

bacterial infections were very localized. 

We thank Stephen S. Curran and Robin M. 

Overstreet for their help with identifying the 

pentastomids. We also thank Omar M. Amin for 

his opinion on the acanthocephalan identifications, 

and Sandra A. Allan for our tick identifications. 

Ellis C. Greiner and Donald F. Coyner 

reviewed an early draft of the manuscript and 

gave helpful suggestions for improvement. Marie-Joelle 

Thatcher was kind enough to translate 

the French literature. Rebecca Smith helped in 

procuring road-killed specimens from the Kennedy 

Space Center, Merritt Island, and the following 

people also collected specimens for us: 

K. Dryden, J. Duquesnal, M. Folk, B. Hagedorn, 

S. Klett, M. Legare, R. Lowes, T. Miller, C. Petrick, 

and S. Quintana. James N. Layne of the 

Archbold Biological Station provided us with 

samples from his parasite collection. We also appreciated 

the comments of the 2 anonymous reviewers. 

This research was supported in part by 



contracts from the Florida Game and Fresh Water 

Fish Commission and is a contribution of 

Federal Aid to Wildlife Restoration, Florida Pittman-Robertson 

Project W-41. This is Florida 

Agricultural Experiment Station Journal Series 

No. R-06872. 


Bequaert, J. 1932. Amblyomma dissimile Koch, a tick 

indigenous to the United States (Acarina: Ixodidae). 

Psyche 39:45-47. 

. 1945. Further records of the snake tick, Amblyomma 

dissimile Koch, in Florida. Bulletin of 

the Brooklyn Entomological Society 40:129. 





Conti, J. A., D. J. Forrester, and J. R. Brady. 1983. 

Helminths of black bears in Florida. Proceedings 


50:252-256. 

Coyner, D. F. 1998. The epizootiology and transmission 

of Eustrongylides ignotus (Dioctophymatoidea) 

in intermediate hosts in Florida. Ph.D. Dissertation, 

University of Florida, Gainesville. 245 

pp. 

Durden, L. A., J. S. H. Klompen, and J. E. Keirans. 

1993. Parasitic arthropods of sympatric opossums, 

cotton rats, and cotton mice from Merritt Island, 

Florida. Journal of Parasitology 79:283—286. 

Elkins, C. A., and B. B. Nickol. 1983. The epizootiology 

of Macracanthorhynchus ingens in Louisiana. 


Fontenot, L. W., and W. F. Font. 1996. Helminth 

parasites of four species of aquatic snakes from 

two habitats in southeastern Louisiana. Journal of 


66-75. 

Forrester, D. J. 1992. Parasites and Diseases of Wild 

Mammals in Florida. University Press of Florida, 

Gainesville. 459 pp. 


Florida Game and Fresh Water Fish Commission. 

1972. Wildlife Code of the State of Florida. Chapter 

16-E, Rules 16-E-3.00 and 16-E-4.02, pages 

86-92. Effective date July 1972. Florida Game 

and Fresh Water Fish Commission, Tallahassee, 

Florida. 

Goldberg, S. R., C. H. Bursey, and H. J. Holshuh. 

1998. Prevalence and distribution of cystacanths 

of an oligacanthorhynchid acanthocephalan from 

the longnose snake, Rhinocheilus lecontei (Colubridae), 

in southwestern North America. Journal 


65:262-265. 

Kinsella, J. M., and D. J. Forrester. 1972. Helminths 

of the Florida duck, Anas platyrhynchos fulvigula. 

Proceedings of the Helminthological Society of 


Maehr, D. S., and J. T. DeFazio, Jr. 1985. Foods of 

black bears in Florida. Florida Field Naturalist 13: 

8-12. 

Moler, P. E. 1992. Eastern indigo snake. Pages 181- 

186 in P. E. Moler, ed. Rare and Endangered Biota 

of Florida. Volume III: Amphibians and Reptiles. 

University Press of Florida, Gainesville. 

Nickol, B. B. 1983. Centrorhynchm kuntzi from the 

USA with description of the male and redescription 

of C. spinosus (Acanthocephala: Centrorhynchidae). 


Schad, G. A. 1962. Studies on the genus Kalicephalus 

(Nematoda: Diaphanocephalidae). II. A taxonomic 

revision of the genus Kalicephalus Molin, 1861. 


Spalding, M. G., G. T. Bancroft, and D. J. Forrester. 

1993. The epizootiology of eustrongylidosis 

in wading birds. Journal of Wildlife Diseases 29: 

237-249. 

U.S. Fish and Wildlife Service. 1978. Part 17. En 

dangered and threatened wildlife and plants. Listing 

of the eastern indigo snake as a threatened 

species. Federal Register 43:4026-4028. 

Wilson, N., and H. W. Kale III. 1972. Ticks collected 

from Indian River County, Florida (Acari: Metastigmata: 

Ixodidae). Florida Entomologist 55:53- 

57.



Research Note 

Helminths of Two Sympatric Toad Species, Bufo marinus (Linnaeus) 

and Bufo marmoreus Wiegmann, 1833 (Anura: Bufonidae) from 

Chamela, Jalisco, Mexico 

SOL GALICIA-GUERRERO,1 CHARLES R. BURSEY,2 STEPHEN R. GOLDBERG,3 AND 

GUILLERMO SALGADO-MALDONADO1'4 

1 Institute de Biologfa, Universidad Nacional Autonoma de Mexico, Apartado Postal 70-153, 

Mexico 04510 D.F., 

2 Department of Biology, Pennsylvania State University, Shenango Campus, 147 Shenango Avenue, Sharon, 

Pennsylvania 16146, U.S.A. (e-mail: cxbl3@psu.edu), and 


(e-mail: sgoldberg@whittier.edu) 

ABSTRACT: Helminths of sympatric Bufo marinus 

(Linnaeus) (N = 49) and Bufo marmoreus Wiegmann 

(TV = 19) from the Pacific coast of Jalisco, Mexico, 

are reported. Bufo marinus harbored Ochoterenella 

digiticauda Caballero y Caballero, Rhabdias fuelleborni 

Travassos, Physaloptera sp. (larvae), an unidentified 

species of nematode, and cystacanths of Centrorhynchus 

sp. Bufo marinus is a new host and Jalisco 

a new locality record for R. fuelleborni and Physaloptera 

sp. Bufo marmoreus harbored Aplectana incerta 

Caballero y Caballero, R. fuelleborni, Physocephalus 

sp. (larvae), and cystacanths of Centrorhynchus sp. 

Bufo marmoreus is a new host record for each of these 

helminths. 

KEY WORDS: Bufo marinus, Bufo marmoreus, nematodes, 

Aplectana incerta, Ochoterenella digiticauda, 

Rhabdias fuelleborni, Physaloptera sp., Physocephalus 

sp., Centrorhynchus sp., cystacanth, Jalisco, Mexico. 

Twenty-five species of Bufo have been reported 

from various regions of Mexico; 8 species 

are endemic (Flores-Villela, 1993). During 

September 1995, individuals of 2 species, Bufo 

marinus (Linnaeus, 1758) and Bufo marmoreus 

Wiegmann, 1833, from the Pacific coast of Jalisco 

State, Mexico, became available for examination 

for parasites. The cane toad, B. marinus, 

originally ranged from southern Texas to central 

Brazil but now has worldwide distribution (Zug 

and Zug, 1979). The marbled toad, B. marmoreus, 

is endemic to Mexico, occurring from the 

Transverse Volcanic Axis, Sierra Madre del Sur, 

and highlands of northern Oaxaca State eastward 

to the Gulf of Mexico coastal plain and Yucatan 

Peninsula, westward to the Pacific coast, and 

4 Corresponding author (e-mail: 

ibiologia.unam.mx). 

gsalgado@mail. 

129 

south to the Rio Balsas basin and the; central 

depression of Chiapas State (Flores-Villela, 

1993). There are several reports of helminths 

from B. marinus (Caballero y Caballero, 1949, 

1954; Kloss, 1971; Goldberg and Bursey, 1992; 

Goldberg et al., 1995; Barton, 1997; Linzey et 

al., 1998), but to our knowlege there are no reports 

of helminths from B. marmoreus. The purpose 

of this note is to report helminths of B. 

marinus and B. marmoreus from Jalisco, Mexico. 

Forty-nine Bufo marinus (mean snout-vent 

length, SVL = 129 mm ± 30 mm SD; range, 

75-190 mm) and 19 B. marmoreus (SVL = 76 

mm ± 5 mm SD; range, 65-83 mm) were examined. 

The toads had been collected by hand 

from Emiliano Zapata Village (19°24'N, 

104°59'W) about 30 km south of the Chamela 

Biological Station, Institute de Biologfa, Universidad 

Nacional Autonoma de Mexico (IB UN- 

AM), Jalisco, Mexico, and were deposited in the 

Coleccion Nacional de Anfibios y Reptiles, 

IBUNAM. The toads were killed by freezing, 

the body cavity was opened by a longitudinal 

incision from vent to throat, and the gastrointestinal 

tract was excised by cutting across the 

esophagus and the rectum. Stomachs and intestines 

were opened longitudinally and examined 

under a stereomicroscope. Helminths were removed 

and counted. Acanthocephalans and 

nematodes were fixed using 4% saline-formalin. 

Acanthocephalans were stained with Meyer's 

paracarmine, dehydrated in a graded ethanol series, 

cleared in methyl salicylate, and mounted 

in Canada balsam. Nematodes were dehydrated 

to 70% ethanol, cleared in glycerol, and exam- 



Table 1. Number, prevalence, mean intensity, range, and abundance for helminths collected from Bufo 

marinus and Bufo marmoreus from Chamela, Jalisco, Mexico. 

Toad species 


Bufo marinus (N = 49) 

Ochoterenella digiticauda 

Rhabdias fuelleborni* 

Physaloptera sp. (larvae)* 

Unidentified nematode 

Centrorhynchus sp. cystacanths 

Bufo marmoreus (N = 19) 

Aplectana incerta* 

Rhabdias fuelleborni* 

Physocephalus sp. (encysted larvae)* 

Centrorhynchus sp. cystacanths* 

New host record. 

Number 

of 

helminths 

24 

145 

184 

6 

12 

848 

17 

7 

1 

Site 

Codom 

Lungs 

Stomach 

Intestine 

Coelom 

Intestine 

Lung 

Coelom 

Coelom 

ined as temporary wet mounts. Voucher specimens 

were deposited in the Coleccion Nacional 

de Helmintos (CNHE), IBUNAM, B. marinus: 

Ochoterenella digiticauda Caballero y Caballero, 

1944 (3775); Rhabdias fuelleborni Travassos, 

1926 (3776); Physaloptera sp. (3774), Centrorhynchus 

sp. (3777); B. marmoreus: Aplectana 

incerta Caballero y Caballero, 1949 (3772), R. 

fuelleborni (3771), Physocephalus sp. (3773), 

Centrorhynchus sp. (3778). Terminology is in 

accordance with Bush et al. (1997). 

Four species of nematodes and 1 species of 

acanthocephalan were found in B. marinus; 3 

species of nematodes and 1 species of acanthocephalan 

were found in B. marmoreus. Numbers 

of parasites, prevalence, abundance, and sites of 

infection are given in Table 1. Bufo marinus harbored 

371 helminths. Rhabdias fuelleborni had 

the highest prevalence (37%); Physaloptera sp. 

(larvae) had the greatest mean intensity (12.3). 

Mean number of helminth species per host was 

1.0 ± 0.8 SD, mean intensity per host was 8.1 

± 15.3 SD. Twelve toads had no parasites, 23 

were parasitized by 1 species, 13 had 2 or more 

helminth species. Bufo marmoreus harbored 873 

helminths. The helminth species with highest 

prevalence (63%) and greatest mean intensity 

(45) was A. incerta. Mean number of helminth 

species per host was 0.9 ± 0.7 SD; mean intensity 

per host was 46.0 ± 67.0 SD. Six toads had 

no helminths, 9 were parasitized by 1 species, 

and 4 had 2 or more species. In B. marinus, 

species richness and mean abundance for the 

helminth fauna fell within the ranges reported 

by Aho (1990) for amphibians in general, i.e., a 

Prevalence Mean intensity ± SD 

(%) (range) 

8 

37 

31 

6 

22 

63 

16 

5 

5 

6.0 ± 6.0 

5.4 ± 1.2 

12.3 

2.0 ± 7.4 

1.1 ± 0.3 

70.7 

5.7 


(3-16) 

d-38) 

± 18.0 (1-59) 

± 42 

± 6.4 

7 

1 

(1-4) 

(1-2) 

(1-250) 

(2-13) 

Mean 

abundance ± SD 

0.5 ± 2.4 

3.0 ± 6.0 

3.8 ± 11.3 

0.1 ± 0.6 

0.2 ± 0.5 

4.47 ± 66.4 

0.9 ± 13.0 

0.36 

0.05 

mean species richness per host individual of 

0.98 ± 0.07 SE, and a mean abundance of 11.55 

± 1.86 SE. However, for B. marmoreus, mean 

abundance was much greater, in part because of 

the large number of individuals of A. incerta 

harbored by a few hosts. 

The known helminth fauna for B. marinus in 

Mexico is presented in Table 2. This list includes 

5 species of trematodes, 1 species of cestode, at 

least 13 species of nematodes, and 1 species of 

acanthocephalan. Bufo marinus is a new host 

and locality record for Rhabdias fuelleborni and 

Physaloptera sp. Bufo marmoreus is a new host 

and locality record for A. incerta, R. fuelleborni, 

Physocephalus sp., and cystacanths of Centrorhynchus 

sp. 

None of the parasites found in this study was 

unique to B. marinus or B. marmoreus; all are 

shared with other amphibian or reptile species 

(Baker, 1987). However, 3 of these species, A. 

incerta, O. digiticauda, and R. fuelleborni, are 

typically found in toads. Aplectana incerta was 

originally described by Caballero y Caballero 

(1949) from B. marinus collected in Chiapas 

State, Mexico, and was subsequently reported 

from Bufo debilis Girard, 1854, Bufo retifonnis 

Sanders and Smith, 1951, Scaphiopus couchii 

Baird, 1854, and Spea multiplicata Cope, 1863, 

from Arizona and New Mexico, U.S.A. (Goldberg 

and Bursey, 1991; Goldberg et al., 1995; 

Goldberg et al., 1996). Ochoterenella digiticauda 

is a common parasite of B. marinus in Costa 

Rica, Guatemala, Mexico, and Jamaica (Brenes 

and Bravo-Hollis, 1959; Wong and Bundy, 

1985). Rhabdias fuelleborni is a neotropical spe-

Table 2. Published records of helminths from Bufo marinus from Mexico. 

Species 

Digenea 

Clinostomum atlenuatum 

Clypthelmiiis intermedia 

Gorgoderina megalorchis 

Langeronia macrocirra 

Mesocoelium monas 

Cestoda 

Distoichometra huftmix 

Nematoda 

Aplectana hoffmani* 

Aplcctana incerta 

Aplectana itzoccinensix 

Aplectana sp. 

Cruzia morleyi 

Cosmocerca sp. 

Ochoterenella cabal leroi 

Ochoterenella chiapensis 

Ochoterenella digiticauda 

Ochoterenella figueroai 

Ochoterenella lamothei 

Ochoterenella nanolarvate 

Ochoterenella sp. 

Oswaldocruzia subauricularix 

Oswaldocruzia pipiens 

Oswaldocruzia sp. 

Rhabdias fuelleborni 

Rhabdias sphaerocephala^ 

Physaloptera sp. (larvae) 

Acanthoccphala 

Centrorhynchus sp. 

Centrorhynchus sp. 

Locality 

Not given 

Chiapas 

Oaxaca 

Oaxaca 

Veracruz 

Veracruz 

Nuevo Leon 

Puebla 

Chiapas 

Veracruz 

Veracruz 

Veracruz 

Veracruz 

Chiapas 

Chiapas 

Chiapas 

Jalisco 

Chiapas 

Chiapas 

Chiapas 

Veracruz 

Chiapas 

Nuevo Leon 

Veracruz 

Jalisco 

Chiapas 

Veracruz 

Veracruz 

Nuevo Leon 

Veracruz 

Jalisco 

Veracruz 

Jalisco 

* Junior homonym of Aplectana incerta per Baker (1985). 

t Considered a Palaearactic species only by Baker (1987). 

cies previously reported from B. marinus from 

Brazil, Costa Rica, Guatemala, and Bermuda 

(Brenes and Bravo-Hollis, 1959; Caballero y 

Caballero, 1954; Kloss, 1971; Goldberg et al., 

1995; Linzey et al., 1998) as well as Bufo arenarum 

Hansel, 1867, Bufo ictericus Spix, 1824, 

Bufo paracnemis Lutz, 1925, and Thoropa miliaris 

(Spix, 1824), from Brazil, Uruguay, and 

Paraguay (Kloss, 1974; Masi-Pallares and Maciel, 

1974). 

The remaining helminths found in this study 

were juveniles of species requiring intermediate 

hosts to complete their life cycles. Larvae of 

Physaloptera sp. and Physocephalus sp. and 

cystacanths of Centrorhynchus sp. have fre- 

GALICIA-GUERRERO ET AL.—RESEARCH NOTES 131 

Reference 

Etges, 1991 

Caballero y Caballero ct al., 1944 

Bravo-Hollis, 1948 


Guillen-Hernandez, 1992 


Martinez, 1969 


Caballero y Caballero, 1949, 1954 

Caballero-Deloya, 1974 




Esslinger, 1987b 


Esslinger, 1987a 

This study 







Guillen-Hernandez, 1 992 

This study 



Bravo-Hollis and Caballero y Caballero, 1940 



This study 


This study 

quently been reported from amphibians as well 

as from mammals, birds, and reptiles that habitually 

feed on insects (Goldberg et al., 1993). 

Larvae of Physaloptera sp. were found in the 

lumen of the stomach; larvae of Physocephalus 

sp. and the cystacanths were encysted in the 

peritoneum. The presence of larvae of Physaloptera 

sp. may reflect host diet preferences 

rather than host-parasite interactions, because 

encystment would be expected in paratenism. 

However, the number of cysts containing Physocephalus 

sp. and the cystacanths was too low 

to conclude that B. marinus is a paratenic host 

for these helminth species; rather, incidental infection 

is more likely. 



Too few studies have been undertaken to draw 

conclusions about helminth communities in species 

of toads from Mexico. The data in Table 2 

suggest that helminth species composition in 

Bufo marinus is variable from population to 

population. However, 3 features characterize 

these faunas: nematode species predominate; 

they are depauperate; and they are dominated by 

a single species. 

We thank Guillermina Cabanas-Carranza, 

Elizabeth Mayen-Pena, Nancy Lopez, Cristina 

Caneda, and Rafael Baez-Vale for assistance in 

collecting toads. Thanks are also due to anonymous 

referees who made valuable comments on 

the manuscript. This work was supported by 

grant SI37 from the Comision Nacional para el 

Conocimiento y Uso de la Biodiversidad (CON- 

ABIO), Mexico. 


Aho, J. M. 1990. Helminth communities of amphibians 

and reptiles: comparative approaches to understanding 

patterns and processes. Pages 157— 

195 in G. W. Esch, A. O. Bush, and J. M. Aho, 


Chapman and Hall, New York. 

Baker, M. R. 1985. Redescription of Aplcctana itzocanensis 

and A. incerta (Nematoda: Cosmocercidae) 

from amphibians. Transactions of the American 

Microscopical Society 104:272—277. 

. 1987. Synopsis of the Nematoda parasitic in 

amphibians and reptiles. Memorial University of 

Newfoundland, Occasional Papers in Biology 1 1: 

1-325. 

Barton, D. P. 1997. Introduced animals and their parasites: 

the cane toad, Bufo marinus, in Australia. 

Australian Journal of Ecology 22:316-324. 

Bravo-Hollis, M. 1943. Dos nuevos nematodos parasitos 

de anuros del sur de Puebla. Anales del Institute 

de Biologfa, Universidad Nacional Autonoma 

de Mexico 14:69-78. 

. 1948. Descripcion de dos especies de trematodos 

parasitos de Bufo marinus L. procedentes de 

Tuxtepec, Oaxaca. Anales del Institute de Biologia, 


19:153-161. 

-, and E. Caballero y Caballero. 1940. Nematodos 

parasitos de los batracios de Mexico. IV. 

Anales del Institute de Biologfa, Universidad Nacional 


Brenes, R. R., and M. Bravo-Hollis. 1959. Helmintos 

de la Repiiblica de Costa Rica VIII. Nematoda. 2. 

Algunos nematodos de Bufo marinus (L) y algunas 

consideraciones sobre los generos Oxysomatium 

y Aplectana. Revista de Biologfa Tropical 7: 

35-55. 






Caballero y Caballero, E. 1949. Estudios helmintologicos 

de la region oncocercosa de Mexico y de 

la Repiiblica de Guatemala. Nematoda. Parte 5. 

Anales del Institute de Biologfa, Universidad Nacional 


. 1954. Estudios helmintologicos de la region 

oncocercosa de Mexico y de la Repiiblica de Guatemala. 

Nematoda. Parte 8. Anales del Institute de 


Mexico 25:259-274. 

, M. Bravo-Hollis, and M. C. Cerecero. 1944. 

Estudios helmintologicos de la region oncocercosa 

de Mexico y de la Repiiblica de Guatemala. Trematoda. 

1. Anales del Institute de Biologfa, Universidad 

Nacional Autonoma de Mexico 15:59-72. 

Caballero-Deloya, J. 1974. Estudios helmintologicos 

de los animales silvestres de la Estacion de Biologfa 

Tropical "Los Tuxtlas," Veracruz. Nematoda. 

1. Algunos nematodos parasitos de Bufo horribilis 

Weigmann, 1833. Anales del Institute dc 


Mexico 45:45-50. 

Esslinger, J. H. 1987a. Redescription of Ochoterenella 

digiticauda Caballero, 1944 (Nematoda: Filarioidea) 

from the toad Bufo marinus, with a redefinition 

of the genus Ochoterenella Caballero, 

1944. Proceedings of the Helminthological Society 


. 1987b. Ochoterenella caballeroi sp. n. and O. 

nanolarvata sp. n. (Nematoda: Filarioidea) from 

the toad Bufo marinus. Proceedings of the Helminthological 


. 1988a. Ochoterenella figueroai sp. n. and O. 

lamothei sp. n. (Nematoda: Filarioidea) from the 

toad Bufo marinus. Proceedings of the Helminthological 


. 1988b. Ochoterenella chiapanaensis sp. n. 

(Nematoda: Filarioidea) from the toad Bufo marinns 

in Mexico and Guatemala. Transactions of 

the American Microscopical Society 107:203- 

208. 

Etges, J. F. 1991. Clinostomum attenuatum (Digenea) 

from the eye of Bufo marinus. Journal of Parasitology 

77:634-635. 

Flores-Villela, O. 1993. Herpetofauna Mexicana. Annotated 

list of the species of amphibians and reptiles 

of Mexico, recent taxonomic changes, and 

new species. Carnegie Museum of Natural History, 

Special Publication 17:1—73. 

Goldberg, S. R., and C. R. Bursey. 1991. Helminths 

of three toads, Bufo alvarius, Bufo cognatus (Bufonidae) 

and Scaphiopus couchi (Pelobatidae) 

from southern Arizona. Journal of the Helminthological 


, and . 1992. Helminths of the marine 

toad, Bufo marinus (Anura: Bufonidae) from 

American Samoa. Journal of the Helminthological 


, , and I. Ramos. 1995. The component 

helminth community of three sympatric toad species, 

Bufo cognatus, Bufo dehilis (Bufonidae), and 

Spea multiplicata (Pelobatidae) from New Mexico. 

Journal of the Helminthological Society of 

Washington 62:57-61.

, , B. K. Sullivan, and Q. A. Truong. 

1996. Helminths of the Sonoran green toad, Bufo 

retiformis (Bufonidae), from southern Arizona. 


63:120-122. 

-, and R. Tawil. 1993. Gastrointestinal 

helminths of the western bush lizard, Urosaurus 

graciosus graciosus (Phrynosomatidae). Bulletin 

of the Southern California Academy of Science 

92:43-51. 

, , and . 1995. Helminths of an 

introduced population of the giant toad, Bufo marinus 

(Anura: Bufonidae), from Bermuda. Journal 


62:64-67. 

Guillen-Hernandez, S. 1992. Comunidades de helmintos 

de algunos anuros de "Los Tuxtlas," Veracruz. 

Tesis de Maestiia. Facultad de Ciencias, 

Universidad Nacional Autonoma de Mexico. 

90pp. 

Kloss, G. R. 1971. Alguns Rhahdias (Nematoda) de 

Bufo no Brasil. Papeis Avulsos de Zoologia 24:1- 

52. 

. 1974. Rhabdias (Nematoda: Rhabditoidea) 

from the marinus group of Bufo. A study of sibling 

species. Arquivos de Zoologia 25:61—120. 



Research Note 

EMERY AND JOY—RESEARCH NOTES 133 

Linzey, D. W., C. R. Bursey, and J. B. Linzey. 1998. 

Seasonal occurrence of helminths of the giant 

toad, Bufo marinus (Amphibia, Bufonidae), in 

Bermuda. Journal of the Helminthological Society 

of Washington 65:25 1-258. 

Martinez, V. J. M. 1969. Parasitos de algunos anfibios 

colectados en diferentes areas de los Municipios 

de Escobedo, Pesqueria y Santiago, Nuevo 

Leon, Mexico. Tesis Licenciatura. Facultad de 

Ciencias Biologicas, Universidad Autonoma de 

Nuevo Leon, Monterrey. 51 pp. 

Masi-Pallares, R., and S. Maciel. 1974. Helminthes 

en batracios del Paraguay (Parte 1), con descripcion 

de una nueva especie, Aplectana pudenda 

(Oxyuridae: Cosmocercinae). Revista Paraguaya 

de Microbiologfa 9:55—60. 

Wong, M. S., and D. A. P. Bundy. 1985. Population 

distribution of Ochoterenella digiticauda (Nematoda: 

Onchocercidae) and Mesocoelium monas 

(Digenea: Brachycoeliidae) in naturally infected 

Bufo marinus (Amphibia: Bufonidae) from Jamaica. 


Zug, G. R., and P. B. Zug. 1979. The marine toad, 

Bufo marinus: a natural history resume of native 

populations. Smithsonian Contributions to Zoology 

284:1-58. 

Endohelminths of the Ravine Salamander, Plethodon richmondi, from 

Southwestern West Virginia, U.S.A. 

MATTHEW B. EMERY AND JAMES E. JOY' 

Department of Biological Sciences, Marshall University, Huntington, West Virginia 25755, U.S.A. 

(e-mail: joy@marshall.edu) 

ABSTRACT: Four species of endohelminths were found 

in 51 ravine salamanders, Plethodon richmondi, from 

southwestern West Virginia in February, March, April, 

October, and November 1996, and February 1997. The 

nematode Angiostoma plethodontis had the highest 

prevalence (29.4%), and the trematode Brachycoelium 

storeriae had the highest mean intensity (2.3). Larvae 

of Batracholandros salamandrac were present in both 

the small and large intestines of 5 hosts. An unidentified 

acanthocephalan cystacanth was found encapsulated 

in the mesentery of a single host. Plethodon richmondi 

represents new host records for Angiostoma 

plethodontis and Brachycoelium storeriae, and West 

Virginia is a new locality record for all of the helminth 

species identified. 

KEY WORDS: Angiostoma plethodontis, Batracholandros 

salamandrae, Brachycoelium storeriae, Pleth- 


odon richmondi, ravine salamander, West Virginia, 

U.S.A. 

The ravine salamander, Plethodon richmondi 

Netting and Mittleman, 1938, is a small, slender 

terrestrial plethodontid species inhabiting the 

wooded slopes of valleys and ravines from western 

Pennsylvania south to northeastern Tennessee 

and northwestern North Carolina and west 

to southeastern Indiana (Green and Pauley, 

1987). In a parasite survey of plethodontid salamanders 

in Tennessee, Dunbar and Moore 

(1979) reported 2 species of helminths from P. 

richmondi\e tapeworm Cylindrotaenia americana 

Trowbridge and Hefley, 1934, and the 

nematode Batracholandros salamandrae (Schad, 

1960) Fetter and Quentin, 1976. Fifteen P. rich- 



Table 1. Prevalence and mean intensity of helminth parasites found in 51 Plethodon richmondi from 

southwestern West Virginia. 

Parasite species 

Brachycoelium storeriae 

Angiostoma plethodontis 

Batracholandros salamandrae 

Acanthocephalan cystacanth (unidentified) 

* Number (%) infected. 

Prevalence* Mean intensity ± 1 SD (range) 

10 (19.6) 

15 (29.4) 

5 (9.8) 

1 (2.0) 

mondi individuals were included in that survey, 

and prevalences were 6.7% and 20.0% for C. 

americana and B. salamandrae, respectively. 

These are the only reported helminths from this 

salamander host to date. Accordingly, this report 

presents new information on helminths of this 

plethodontid species, including prevalences and 

intensities of infection. 

A total of 51 ravine salamanders (28 females 

and 23 males) was collected in Cabell and 

Wayne counties of West Virginia in February- 

April, October, and November 1996 and in February 

1997. Salamanders were captured by hand 

in mature forests of beech, maple, and oak trees 

on cool rainy evenings. Hosts were placed in 

plastic bags with damp leaf litter and returned 

to the laboratory where they were maintained in 

a refrigerator at approximately 4°C. All salamanders 

were necropsied within 18 hr of capture. 

Immediately prior to necropsy, each salamander 

was measured for snout-vent length 

(SVL) to the nearest mm with vernier calipers, 

and weighed to the nearest 0.1 g on a Mettler 

Model BB300® electronic balance. Mean SVL 

of 50 mm (±SE =1.5 mm) for females did not 

differ significantly from the mean SVL of 47 

mm (±SE = 1.3 mm) for males (f0.o5,49 = 1-471; 

P > 0.05). Mean weight of 1.53 g (±SE = 0.11 

g) for females did not differ significantly from 

the mean of 1.28 g (±SE = 0.77) for males 

(*o.o5,49 = 1-852; P > 0.05). Since neither mean 

snout-vent lengths nor total body weights for female 

versus male P. richmondi were statistically 

significant, data were pooled for both host sexes 

to determine the prevalences and mean intensities 

of infection for the various helminth species. 

Salamanders were killed by decapitation. The 

sex of each individual was determined. At time 

of necropsy, the gastrointestinal tract was removed, 

and the small and large intestines were 

examined with a dissecting microscope for helminths. 

Nematodes were initially studied in tem- 

2.3 ± 1.70 (1-7) 

1.5 ± 0.64 (1-3) 

1.2 ± 0.45 (1-2) 

1.0 — (1) 


Site of infection 



Small, large intestine 

Mesentery 

porary lactophenol mounts and then stored in 

70% ethanol. Voucher specimens representing 

each helminth species were stained in Semichon's 

acetic carmine, dehydrated in an ethanol 

series, cleared in xylene, and mounted in Permount®. 

The terms prevalence and mean intensity 

follow the definitions of Bush et al. (1997). 

In the study, 4 helminth species were found 

in P. richmondi individuals (Table 1). The trematode 

appears to be Brachycoelium storeriae 

Harwood, 1932, a diagnosis based, in part, on 

the morphological similarity of specimens in this 

study with the description provided by Cheng 

(1958), who argued convincingly for the separation 

of this trematode species from Brachycoelium 

salamandrae (Frolich, 1789). The diagnosis 

of B. storeriae from the terrestrial P. 

richmondi in West Virginia can be supported on 

an ecological basis as well. For example, Parker 

(1941) identified trematodes of this species from 

Opheodrys aestivus (Linnaeus, 1766) and Ambystoma 

opacum (Gravenhorst, 1807), both terrestrial 

hosts. Cheng (1958) also collected B. storeriae 

individuals from Plethodon cinereus 

(Green, 1818), another terrestrial host species. 

Brachycoelium storeriae has also been reported 

from Pseudotriton ruber (Sonnini, 1802) (Parker, 

1941; Dunbar and Moore, 1979), a salamander 

species considered semiaquatic to semiterrestrial 

by the latter authors. 

The nematode Angiostoma plethodontis Chitwood, 

1933 found in the present study clearly 

conforms to its original description (Chitwood, 

1933). A total of 22 A. plethodontis (13 females 

and 9 males) was collected from 15 P. richmondi 

(Table 1). This female:male ratio of 1.44:1.00 

did not deviate significantly from the expected 

1.00:1.00 ratio (x2 = 0.752; df = 1; 0.5 > P > 

0.1). 

The identification of B. salamandrae from P. 

richmondi may not be definitive, because all 6 

individuals of this nematode species collected

were larvae. Still, we have concluded that the 

oxyuroid species found in this study is most 

likely B. salamandrae (Schad, 1960) Fetter and 

Quentin, 1976 rather than B. magnavulvaris 

(Rankin, 1937) Fetter and Quentin, 1976, because 

Dunbar and Moore (1979) argued that the 

latter species is not found in terrestrial hosts, 

such as P. richmondi. 

Since only 1 acanthocephalan was found and 

it was in an encapsulated cystacanth stage, we 

offer no species or generic diagnoses. 

This is the first report of B. storeriae and A. 

plethodontis from P. richmondi, and West Virginia 

is a new locality record for all helminth 

species collected. Voucher material is deposited 

in the United States National Parasite Collection, 

Beltsville, Maryland 20705, under accession 

numbers USNPC 88638 (Angiostoma plethodontis 

female and male); USNPC 88639 (Batracholandros 

salamandrae); USNPC 88640 (Brachycoelium 

storeriae); and USNPC 88641 

(acanthocephalan cystacanth). 

This work was done to partially fulfill a Marshall 

University Yeager Thesis requirement by 

the senior author. Thanks are extended to Yeager 

Thesis Committee member Martha Woodard for 

review of the manuscript. Our appreciation is 

also extended to Robert Tucker for his help with 



Research Note 

RESEARCH NOTES 135 

host collections and to Charles Bursey for the 

identification of A. plethodontis. Specimens of 

P. richmondi were collected under a permit issued 

by the West Virginia Division of Natural 

Resources. 






Cheng, T. C. 1958. Studies on the trematode family 

Dicrocoeliidae. I. The genus Brachycoeiium (Dujardin, 

1845) and Leptophallus Liihe, 1909 (Brachycoeliinae). 

American Midland Naturalist 59: 

67-81. 

Chitwood, B. G. 1933. On some nematodes of the 

superfamily Rhabditoidea and their status as parasites 

of reptiles and amphibians. Journal of the 

Washington Academy of Sciences 23:508-520. 

Dunbar, J. R., and J. D. Moore. 1979. Correlations 

of host specificity with host habitat in helminths 

parasitizing the plethodontids of Washington 

County, Tennessee. Journal of the Tennessee 

Academy of Science 54:106-109. 

Green, N. B., and T. K. Pauley. 1987. Amphibians 

and Reptiles in West Virginia. University of Pittsburgh 

Press, Pittsburgh, Pennsylvania, 241 pp. 

Parker, M. V. 1941. The trematode parasites from a 

collection of amphibians and reptiles. Report of 

the Reelfoot Lake Biological Station, 5. Journal 

of the Tennessee Academy of Science 16:27-44. 

Abomasal Parasites in Southern Mule Deer (Odocoileus hemionus 

fuliginatus} from Coastal San Diego County, California, U.S.A. 

STEPHEN LADD-WILSON,' SLADER BucK,2 AND RICHARD G. BoTZLER1-3 

1 Department of Wildlife, Humboldt State University, Arcata, California 95521, U.S.A. (S.L.W. e-mail: 

ladwil@teleport.com; R.G.B. e-mail: rgb2@humboldt.edu), and 

2 Camp Pendleton Marine Corps Base, Camp Pendleton, California 92055, U.S.A. (e-mail: 

bucksl@pendleton.usmc.mil) 

ABSTRACT: Trichostrongylid nematodes were collected 

from the abomasa of 15 (6.6%) of 227 southern mule 

deer (Odocoileus hemionus fuliginatus) from Camp Pendleton 

Marine Corps Base, San Diego County, California 

(U.S.A.). Three species of nematodes were found: Haemonchus 

contoitus, Teladorsagia circumcincta, and Nem- 


atodirus odocoilei. Mean (±1 SD) intensity was 11.5 ± 

24.6 nematodes per infected deer. All 15 infected deer 

were among the 184 animals shot during 2 controlled 

hunts in November 1990 and November 1991; no parasites 

were found in an additional 43 abomasa collected 

during 2 additional hunts in March 1991 arid March 

1992. This is the first known published report of abomasal 

nematodes from southern mule deer. 



Table 1. Abomasal parasites collected from 227 southern mule deer (Odocoileus hemionus fulginatus) at 

Camp Pendleton, San Diego County, California. All deer were collected in the November 1990 and 1991 

hunts. No abomasal parasites were observed among the 43 deer sampled in the March 1991 and 1992 

hunts. 

Parasite species 

Haemonchus contortus 

Teladorsagia circumcincta 

Nematodirus odocoilei 

Unknown* 

Totals 

infected 

5 

2 

5 

4 

15t 

(%) 

2.2 

0.9 

2.2 

1.8 

6.6 

* Unidentifiable worm fragments were found in 4 additional deer. 

t One deer was infected with both H. contortus and T. circumcincta. 

KEY WORDS: southern mule deer, Odocoileus hemionus 

fuliginatus, abomasal nematodes, Haemonchus 

contortus, Teladorsagia circumcincta, Nematodirus 

odocoilei, California, U.S.A. 

A number of studies have been published of 

abomasal parasites among mule deer (Odocoileus 

hemionus Rafinesque, 1817) of North 

America, and some controversy exists on the 

management value of using abomasal parasites 

as indicators of the physical condition and habitat 

relationships of these deer (Moore and Garner, 

1980; Waid et al., 1985; Stubblefield et al., 

1987). Among southern mule deer (Odocoileus 

hemionus fuliginatus Cowan, 1933) no published 

reports are known of abomasal parasites; 

on the basis of a single unpublished anonymous 

1955 report of the California Department of Fish 

and Game, Nematodirus filicollis (Rudolphi, 

1802) Ransom, 1907, was purportedly observed 

in 1 of 17 southern mule deer from Camp Pendleton 

Marine Corps Base, San Diego County, 

California (33°20'N, 117°20"W). Our objective 

was to identify the prevalence and intensity of 

abomasal parasites infecting the southern mule 

deer subspecies on Camp Pendleton. 

Camp Pendleton comprises a 50,588-ha area, 

with riparian and oak woodlands, coastal sage 

scrub, grassland, and chaparral, in the northwestern 

corner of San Diego County. We collected 

184 abomasa from 225 southern mule 

deer shot during 2 either-sex hunts in November 

1990 and November 1991. An additional 43 abomasa 

were collected from 45 animals killed 

during 2 antlerless hunts in March 1991 and 

March 1992. At hunter-check stations, each abomasum 

was removed after ligation and frozen 

Mean 

20.8 

12.0 

5.6 

4.0 

11.5 

No. parasites/deer 

SD 

37.6 

0.0 

3.6 

0.0 

24.6 


Range 

4-88 

12 

4-12 

4 

4-100 

Total no. 

parasites 

collected 

104 

24 

28 

16 

172 

at — 10°C prior to transportation to the laboratory. 

Abomasa were thawed at 18-20°C. Abomasal 

contents first were rinsed through a 1.9-mm 

mesh to remove coarse material and then rinsed 

through a 150-u.m mesh. Parasites and other material 

remaining on the 150-u,m mesh were diluted 

with tap water and examined in 10-ml aliquots 

until 25% of the total volume for each 

abomasum was evaluated. From this 25% sample, 

the total number of each abomasal parasite 

species was estimated for each deer. Helminths 

collected were stored in 70% ethanol, mounted 

on slides in glycerin, and identified to species 

according to Skrjabin (1952), Durette-Desset 

(1974), and Levine (1980). Representative samples 

of all helminths were deposited into the 

U.S. National Parasite Collection, Beltsville, 

Maryland (Accession Numbers 84382-84387). 

Of the 227 abomasa examined, 212 (93%) had 

no detectable helminths, 12 (5.2%) had an estimated 

total of 4 helminths, 2 (0.9%) had an estimated 

12 helminths, and 1 (

and their habitats. These low parasite levels may 

have been influenced by several factors. A semiarid 

climate has been associated with low helminth 

prevalences (Waid et al., 1985; Stubblefield 

et al., 1987); at 3 weather stations on Camp 

Pendleton, annual rainfall ranged from 225 to 

483 mm over the 2 yr of the study. Also, in an 

earlier study, Pious (1989) found that grasses 

comprised only 9% of the diet for deer at Camp 

Pendleton; low level of grass intake may reduce 

the likelihood of deer ingesting infective nematode 

larvae. Another factor is that during the unavoidable 

time lapse between killing the deer 

and collecting the abomasa, some abomasal parasites 

may have migrated out of the abomasum 

or some parasites (e.g., Nematodirus odocoilei} 

may have migrated into the abomasum. In addition, 

basing prevalence on the number of parasites 

found in only 25% of each abomasum 

could have resulted in overlooking very low intensities. 

Further, use of the 150-u,m mesh for 

collecting parasites may have resulted in loss of 

small parasites, especially larvae. Finally, the 

frequent fires from incendiary devices on Camp 

Pendleton could serve to reduce the abundance 

of infective larvae on vegetation. Thus, the parasite 

prevalences and intensities we observed 

probably should be considered minimum values 

for this southern mule deer population. 

The apparent absence of abomasal parasites 

from the 43 deer killed in the 2 March hunts is 

interesting. This phenomenon may be related to 

the development of a seasonal host immunity 

against intestinal parasites (Soulsby, 1966). 

Haemonchus conforms and T. circumcincta 

both are common parasites of sheep. Camp Pendleton 

has had a history of grazing by sheep, 

cattle, and bison. 

Although all of these parasites have been reported 

from other subspecies of mule deer, this 

is the first published report for the southern rnule 

deer subspecies. The unpublished anonymous 

1955 California Department of Fish and Game 

report of N. filicollis in 1 (6%) of 17 abomasa 

evaluated at Camp Pendleton reported a prevalence 

of abomasal parasites comparable with 

that found in our study (Table 1). Walker and 

Becklund (1970) noted that they examined many 

specimens of N. filicollis collected from deer and 

in every case reidentified them as N. odocoilei; 

thus, the original unpublished report probably 

also was of N. odocoilei. Finding parasite spe- 

RESEARCH NOTES 137 

cies characteristic of other mule deer subspecies 

(Walker and Becklund, 1970) among O. hemionus 

fuliginatus supports the notion that these abomasal 

parasites exercise little selectivity among 

mule deer subspecies. No clinical pathological 

lesions were associated with any of the infected 

deer in this study. 

We greatly appreciate the assistance of Dr. Archie 

Mossman and Ms. Denise Bradley for help 

in several phases of this study and of Dr. John 

DeMartini and Dr. J. Ralph Lichtenfels for assistance 

in identifying the parasites. 


E>urette-Desset, M. 1974. Keys to the genera of the 

superfamily Trichostrongyloidea. In R. C. Anderson 

and A. G. Chabaud, eds. Commonwealth Institute 

of Helminthology Number 10. Commonwealth 

Institute of Helminthology, The White 

House, St. Albans, England. 86 pp. 

Levine, N. D. 1980. Nematode Parasites of Domestic 

Animals and of Man, 2nd ed. Burgess Publishing 

Company, Minneapolis, Minnesota. 477 pp. 

Moore, G. M., and G. N. Garner. 1980. The relationship 

of abomasal parasite counts to physical 

condition of mule deer in southwestern Texas. 

Western Association of Fish and Wildlife Agencies 

60:593-600. 

Pious, M. 1989. Forage composition and physical condition 

of southern mule deer in San Diego County, 

California. M.S. Thesis, Humboldt State University, 

Arcata, California. 61 pp. 

Skrjabin, K. I. 1952. Key to the Parasitic Nematodes. 

Volume III: Strongylata. Academy of the Sciences 

of the U.S.S.R. Translated from Russian for the 

National Science Foundation, Washington, D.C., 

and the U.S. Department of Agriculture by the 

Israel Program for Scientific Translations, The Office 

of Technical Services. 1961. U.S. Department 

of Commerce, Washington, D.C. 434 pp. 

Soulsby, E. J. L. 1966. The mechanisms of immunity 

to gastro-intestinal nematodes. Pages 255-276 in 

E. J. L. Soulsby, ed. Biology of Parasites. Academic 

Press, New York. 354 pp. 

Stubblefield, S. S., D. B. Pence, and R. J. Warren. 

1987. Visceral helminth communities of s.ympatric 

mule deer and white-tailed deer from the Davis 

Mountains of Texas. Journal of Wildlife Diseases 

23:113-120. 

Waid, D. D., D. B. Pence, and R. J. Warren. 1985. 

Effects of season and physical condition on the 

gastrointestinal helminth community of whitetailed 

deer from the Texas Edwards Plateau. Journal 

of Wildlife Diseases 21:264-273. 

Walker, M. L., and W. W. Becklund. 1970. Checklist 

of the internal and external parasites of deer, 

Odocoileus hemionus and O. virginianus in the 

United States and Canada. Index-Catalogue of 

Medical and Veterinary Zoology, Special Publication 

No. 1. U.S. Department of Agriculture, 

Washington, D.C. 45 pp. 




THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON 

CONSTITUTION AND BY-LAWS 

The name of the Society shall be the Helminthological 

Society of Washington. 

The object of the Society shall be to provide 

for the association of persons interested in parasitology 

and related sciences for the presentation 

and discussion of items of interest pertaining to 

those sciences. 

BY-LAWS 

ARTICLE 1 

Membership 

Section 1. There shall be four classes of members, 

namely regular, life, honorary, and emeritus. 

Section 2. Any person interested in parasitology 

or related sciences may be elected to regular 

membership in the Society. The privileges 

and responsibilities of regular members include 

eligibility to hold office, to vote, and to receive 

Society publications. Spouses of regular members 

may apply for election to regular membership 

with all the privileges and responsibilities 

except that they will not receive the Society publications 

and will pay annual dues at a reduced 

rate. 

Section 3. Any person who has rendered conspicuous 

and continuous service as a member of 

the Society for a period of not less than 15 years, 

and has reached the age of retirement, may be 

elected to life membership. Life members shall 

have all of the privileges of regular members but 

shall be exempted from payment of dues. The 

number of life members shall not exceed five 

percent of the membership at the time of election. 

Section 4. Any person who has attained eminent 

distinction in parasitology or related sciences 

may be elected to honorary membership. 

An honorary member shall have all the privileges 

of membership except voting, holding office, 

or having any interest in the real or personal 

property of the Society, and shall be exempted 

from the payment of dues. The number of honorary 

members shall not exceed 10 at any one 

time, and not more than one honorary member 

shall be elected in any one year. 

Section 5. Any person who has been a member 

in good standing for not less than 10 years, 


and who has retired from active professional 

life, may upon application in writing to the Corresponding 

Secretary-Treasurer have the membership 

status changed to emeritus. An emeritus 

member shall be exempt from payment of dues 

and, with exception of receiving the Society's 

publications shall enjoy all privileges of membership. 

An emeritus member, upon payment of 

75 percent of the current dues, may elect to receive 

the Society's publications. 

Section 6. Candidates for election to regular 

membership may be sponsored and proposed 

only by members in good standing. The candidate 

shall submit a duly executed and signed application 

to the Recording Secretary, who in turn 

shall submit the application to the Executive 

Committee. The Executive Committee shall review 

the application, vote upon its acceptance, 

and report its actions at the next scheduled business 

meeting. Voting may be by voice or by ballot. 

In the event that there is no scheduled Executive 

Committee meeting within 60 days of 

receipt of the application, voting may be conducted 

by mail or by other expeditious means of 

communication. The Corresponding Secretary- 

Treasurer shall inform the applicant of the action 

of the Committee. 

Section 7. Payment of dues shall be considered 

as evidence of acceptance of membership 

in the Society. Election to membership shall be 

void if the person elected does not pay dues 

within 3 months after the date of notification of 

election. 

Section 8. Nominations for honorary and life 

membership, approved by the Executive Committee, 

shall be submitted to the membership for 

election at a regular meeting. 

ARTICLE 2 

Officers 

Section 1. The officers of the Society shall be 

a President, a Vice-President, a Recording Secretary, 

u Corresponding Secretary-Treasurer, and 

such other officers as the Society may deem necessary. 

The four named officers shall also be the 

Directors of the Society. Only members in good 

standing and whose dues are not in arrears shall

e eligible for election to office. Terms of office 

shall be for 1 year. 

Section 2. The President shall preside over all 

meetings, appoint all committees except the Executive 

Committee, and perform such other duties 

as may properly devolve upon a presiding 

officer. The President may appoint an Archivist, 

a Librarian, a Custodian of Back Issues, and an 

Assistant Corresponding Secretary-Treasurer, as 

needed. 

Section 3. The Vice-President shall preside in 

the absence of the President and, when so acting, 

shall perform such duties as would otherwise 

devolve upon the President. The Vice-President 

shall serve as Program Officer. 

Section 4. In the absence of both President 

and Vice-President, the member, among those 

present, who last held the office of President 

shall be the presiding officer. Under other circumstances, 

members may elect a presiding officer 

but business action taken shall be reviewed 

by the Executive Committee. 

Section 5. The Recording Secretary shall record 

the proceedings of all meetings and shall 

present at each meeting a written report of the 

transactions of the preceding meeting, shall keep 

an accurate and complete record of the business 

transacted by the Society in its meetings, and 

shall notify the Corresponding Secretary-Treasurer 

of the election of new members. The Recording 

Secretary shall prepare for publication 

in the Society's publications an annual digest of 

scientific meetings and business transacted, including 

elections of officers and new members. 

Section 6. The Corresponding Secretary-Treasurer 

shall be responsible for all funds, collections, 

payment of bills, and maintenance of financial 

records. At the beginning of each year, 

the Corresponding Secretary-Treasurer shall present 

to the Society an itemized statement of receipts 

and expenditures of the previous year; this 

statement shall be audited by at least two members 

of the Society. 

ARTICLE 3 

Executive Committee 

Section 1. There shall be an Executive Committee 

that shall be the administrative body of 

the Society. 

Section 2. The Executive Committee shall 

consist of 10 members in good standing as follows: 

the President, Vice-President, Recording 

Secretary, Corresponding Secretary-Treasurer, 

CONSTITUTION AND BY-LAWS 139 

Editor, Immediate Past President, and four Members-at-Large. 

The Committee shall represent to 

the fullest practicable degree the varied scientific 

interests of the Society's membership and the 

local distribution of its members. 

Section 3. The President shall serve as chairperson 

of the Executive Committee. 

Section 4. Members-at-Large shall serve for a 

term of 2 years. Two Members-at Large shall be 

appointed each year in November by the President-elect 

for the prescribed term of 2 years. 

Section 5. Vacancies occurring on the Executive 

Committee for any reason shall be filled 

by appointment by the President, and except as 

otherwise provided, the appointee shall serve for 

the remainder of the unexpired term. 


carry out the provisions of the Constitution and 

By-Laws and shall make decisions on all matters 

of general and financial policy not otherwise set 

forth in the Constitution and By-Law:; and shall 

report its action to the Society annually at the 

last regular meeting. 

Section 7. The Executive Committee shall approve 

the selection of a depository for the current 

funds, direct the investment of the permanent 

funds, and act as the administrative body 

of the Society on all matters involving finance. 

It shall prepare and present to the Society at the 

beginning of each calendar year a budget based 

on the estimated receipts and expenditures of the 

coming year with such recommendations as may 

be desirable. 

Section 8. With the presentation of the annual 

budget, the Executive Committee shall present 

to the Society, if feasible, the estimated cost for 

publication to be charged to contributors to the 

Society's publications for that year. 

Section 9. Costs of publication, in excess of 

amounts borne by the Society, shall be borne by 

the authors in accordance with guidelines established 



pass on all applications for membership and on 

the reinstatement of delinquent members, except 

as otherwise provided, and shall report its actions 

to the Society. 

ARTICLE 4 

Nomination and Election of Officers 

Section 1. The Executive Committee, acting 

as the Nominating Committee of the Society, 

shall prepare a slate of officers and present this 



to the Society at the Anniversary meeting of 

each year. Independent nominations may be 

made in writing by any five members. In order 

to receive consideration, such nominations must 

be in the hands of the Recording Secretary at 

the time of the Anniversary meeting. The election 

will be held at the next regular meeting of 

the Society. 

Section 2. The election of officers shall be 

held prior to the presentation of notes and papers 

at the last regular meeting of the calendar year. 

Voting may be either by voice or by ballot. 

Section 3. The last order of business at the 

last meeting of the calendar year shall be the 

installation of officers, the naming of officers, 

and the naming of necessary appointees. 

ARTICLE 5 

Awards Committee 

Section 1. There shall be an Awards Committee 

to select individuals for special commendation. 

The Committee shall consist of three 

members. 

Section 2. Members shall serve for a term of 

3 years with appointments staggered so that one 

new member is added each year. The senior 

member of the Committee shall serve as chairperson. 

Section 3. The Awards Committee shall be 

charged with the duty of recommending candidates 

for the Anniversary Award, which may be 

given annually or less frequently at the discretion 

of the Committee. 

Section 4. The recipient of the Anniversary 

Award shall be, or have been, a Society member 

who is honored for one or more achievements 

of the following nature: (a) outstanding contributions 

to parasitology or related sciences that 

bring honor and credit to the Society, (b) an exceptional 

paper read at a meeting of the Society 

or published in Comparative Parasitology, (c) 

outstanding service to the Society, and (d) other 

achievement or contribution of distinction that 

warrants highest and special recognition by the 

Society. 

Section 5. The individual recommended for 

the Anniversary Award shall be subject to approval 


ARTICLE 6 

Editorial Board 

Section 1. There shall be an Editorial Board 

for the Society's publications, which shall include 

Comparative Parasitology. 


Section 2. The Editorial Board shall consist of 

an Editor and other members in good standing, 

representing to the fullest practicable degree the 

varied scientific interests and the employmentgroup 

affiliations of the Society's membership. 

Section 3. The Editor shall be elected by the 

Society, on the nomination by the Executive 

Committee, for a term of 3 to 5 years. 

Section 4. Other members of the Editorial 

Board shall be appointed for terms of 3 years. 

Section 5. The Editor, after consulting with 

the Editorial Board, shall appoint new members, 

formulate publication policies, and make all decisions 

with respect to format and content of the 

Society's publications. The Editor shall operate 

within financial limitations determined by the 

Executive Committee. 

ARTICLE 7 

Publications 

The publications of the Society shall be issued 

at such times and in such form as the Society, 

through its Editorial Board, may determine. 

ARTICLE 8 

Meetings 

Section 1. Meetings of the Society shall be 

held as often as deemed desirable by the Executive 

Committee. 

Section 2. The November meeting of the Society 

shall be known as the Anniversary meeting, 

and the Anniversary Award, when made, 

ordinarily shall be presented at this meeting. 

Section 3. Notice of the time and place of 

meetings shall be given by the Recording Secretary 

at least 10 days before the date of the 

meeting. 

ARTICLE 9 

Procedure 

The rules contained in Robert's Rules of Order, 

Revised, shall govern the Society in all cases 

to which they are applicable and in which 

they are not inconsistent with the By-Laws or 

the special rules of order of the Society. 

ARTICLE 10 

Order of Business 

Call to order. 

Reading of minutes of the previous meeting. 

Announcement of new members. 

Reports of committees. 

Unfinished business.

New business. 

Presentation of notes and papers. 

Installation of new officers. 

Adjournment. 

ARTICLE 11 

Quorum 

The members in attendance at any regular 

meeting shall constitute a quorum. 

ARTICLE 12 

Dues and Debts Owed to the Society 

Section 1. Annual dues for regular and spouse 

members shall be fixed by the Executive Committee, 

subject to ratification by the Society. 

Spouse members shall pay dues at a reduced 

rate. 

Section 2. The fiscal year for payment of dues 

and for all other business purposes shall be the 

same as the calendar year, that is, from 1 January 

to 31 December, and dues shall be payable 

on or before 1 January. The dues of a newly 

elected member paid prior to 1 July of the year 

of the new member's election shall be credited 

to that year; if paid after 1 July, they shall be 

credited either to the current fiscal year or to the 

following one, at the option of the new member. 

The dues shall include subscription to the Society's 

publications; only those members whose 

dues are paid shall receive the publication(s). 

Section 3. All other obligations owed to the 

CONSTITUTION AND BY-LAWS 141 

Society by members or nonmembers shall be 

due and payable 30 days after bills an; rendered; 

the further extension of credit to those whose 

obligations are in arrears shall be a matter for 

decision by the Executive Committee. 

ARTICLE 13 

Suspension and Reinstatement 

Any member whose dues are in arrears for 2 

years shall be dropped from membership. Members 

who have been dropped for nonpayment of 

dues may be reinstated automatically upon payment 

of the dues in arrears and dues for the current 

year or may be otherwise reinstated by action 

of the Executive Committee. 

ARTICLE 14 

Provision for Dissolution of Funds 

In the event the Society is disbanded, all monies 

shall be presented to the Trustees of the 

Brayton Howard Ransom Memorial Trust Fund 

to be used for such purposes as that continuing 

body may deem advisable. 

ARTICLE 15 

Amendments to the By-Laws 

Any amendment to these By-Laws shall be 

presented in writing at a regular meeting. It shall 

not be acted upon until the following meeting. 

A two-thirds vote of the members in attendance 

shall be required for adoption. 

ARTICLES OF INCORPORATION 

OF 

THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, INC. 

(A Non-stock Corporation) 

FIRST: I the undersigned, Charles A. Dukes, 

Jr., whose post office address in 300 Landover 

Mall West, Landover, Maryland 20785, being at 

least twenty-one years of age, do hereby form a 

corporation under and by virtue of the General 

Laws of the State of Maryland. 

SECOND: The name of the corporation 

(which is hereinafter called the Corporation) is 

The Helminthological Society of Washington, 

Inc. 

THIRD: The puiposes for which the Corporation 

is formed are as follows: 

(a) To provide for the association of persons 

interested in parasitology and related sciences 

for the presentation and discussion of items of 

interest pertaining to these sciences; 

(b) To advance the science of parasitology, in 

both its fundamental and its economise aspects; 

to act as an agency for the exchange of information; 

to hold regular meetings and to promote 

and extend knowledge in all phases of parasitology; 

(c) And to generally carry out any other business 

in connection therewith not contrary to the 

laws of the State of Maryland, and with all the 

powers conferred upon non-profit corporations 

which are contained in the General Laws of the 

State of Maryland. 



FOURTH: The post office address of the principal 

office of the Corporation in this state is 

9110 Drake Place, College Park, Maryland 

20740. The name and post office address of the 

resident agent of the Corporation in this state is 

A. Morgan Golden, 9110 Drake Place, College 

Park, Maryland 20740. Said resident agent is a 

citizen of the State of Maryland and actually resides 

therein. 

FIFTH: The Corporation is not authorized to 

issue capital stock. 

SIXTH: The number of directors of the Corporation 

shall be four, which number may be 

increased or decreased pursuant to the By-Laws 

of the Corporation, but shall never be less than 

three; and the names of the directors who shall 

act until their successors are duly chosen and 

qualified are Nancy D. Pacheco, Louis S. Diamond, 

Sherman S. Hendrix, and Milford N. 

Lunde. 

SEVENTH: The duration of the Coiporation 

shall be perpetual. 

IN WITNESS WHEREOF, I have signed 

these Articles of Incorporation on the 3rd day 

November, 1981. I acknowledge these Articles 

and this signature to by my act. 

WITNESS: 

[signed] 

Gary Greenwald 


[signed] 

Charles A. Dukes, Jr.

Name: 

MEMBERSHIP APPLICATION 143 

APPLICATION FOR MEMBERSHIP 

in the 

HELMINTHOLOGICAL SOCIETY OF WASHINGTON 

Mailing Address: 

Present Position and Name of Institution: 

(Please Type or Print Legibly) 

Phone: FAX: 

E-Mail: 

Highest Degree Earned and the Year Received: 

Are You a Student? If so, for what degree and where? 

Fields of Interest: 

If you are experienced in your field, would you consent to be a reviewer for manuscripts 

submitted for publication in the Society's journal, Comparative Parasitologyl If so, what 

specific subject area(s) do you feel most qualified to review? 

Signature of Applicant Date 

Signature of Sponsor (a member) Date 

Mail the completed application along with a check (on a U.S. bank) or money order (in 

U.S. currency) for the first year's dues (US$25 for domestic active members ami US$28 

for foreign active members) to the Corresponding Secretary-Treasurer, Nancy D. Pacheco, 

9708 DePaul Drive, Bethesda, MD, U.S.A. 20817 

Helminthological Society of Washington Home Page: http://www.gettysburg.edU/~shendrix/helms:oc.html 



THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON 

MISSION AND VISION STATEMENTS 

May 7, 1999 

THE MISSION 

The Helminthological Society of Washington, the prototype scientific organization for parasitological 

research in North America, was founded in 1910 by a devoted group of parasitologists in 

Washington, D.C. Forging a niche in national and international parasitology over the past century, 

the Society focuses on comparative research, emphasizing taxonomy, systematics, ecology, biogeography, 

and faunal survey and inventory within a morphological and molecular foundation. Interdisciplinary 

and crosscutting, comparative parasitology links contemporary biodiversity studies with 

historical approaches to biogeography, ecology, and coevolution within a cohesive framework. 

Through its 5 meetings in the Washington area annually, and via the peer reviewed Comparative 

Parasitology (continuing the Journal of the Helminthological Society of Washington in its 67th 

Volume), the Society actively supports and builds recognition for modern parasitological research. 

Taxonomic diversity represented in the pages of the Society's journal treats the rich helminth faunas 

in terrestrial and aquatic plants, invertebrates, arid vertebrates, as well as parasitic protozoans and 

arthropods. Parasitology, among the most integrative of the biological sciences, provides data critical 

to elucidation of general patterns of global biodiversity. 

THE VISION 

The Helminthological Society of Washington celebrates a century of tradition and excellence 

in global parasitology, solving challenges and responding to opportunities for the future of society 

and the environment. 

Members of the Helminthological Society of Washington contribute to understanding and protecting 

human health, agriculture, and the biosphere through comparative research emphasizing 

taxonomy, systematics, ecology, biogeography, and biodiversity assessment of all parasites. The 

Society projects the exceptional relevance of its programs to broader research and education in 

global biodiversity and conservation biology through the activities of its members and its journal, 

Comparative Parasitology. 


*Edna M. Buhrer 

*Mildred A. Doss 

*Allen Mclntosh 

•Jesse R. Christie 

^Gilbert F. Otto 

*George R. LaRue 

•William W. Cort 

•Gerard Dikmans 

•Benjamin Schwartz 

*Willard H. Wright 

*Aurel O. Foster 

*Carlton M. Herman 

*May Belle Chitwood 

•ElvioH. Sadun 

E. J. Lawson Soulsby 

David R. Lincicome 

Margaret A. Stirewalt 

*Leo A- Jachowski, Jr. 

•Horace W. Stunkard 

•Kenneth C. Kates 

•Everett E. Wehr 

•George R. LaRue 

•Vladimir S. Ershov 

•Norman R. Stoll 

•Horace W. Stunkard 

•Justus F. 'Mueller 

John F. A. Sprent 

Bernard Bezubik 

Hugh M. Gordon 

•W. E. Chambers 

•Nathan A. Cobb 

•Howard Crawley , 

* Winthrop D. Foster 

•"Maurice C. Hall , 

•Albert Hassall 

•Charles W. Stiles , 

•PaulJBartsch 

* Henry =E. Ewing 

•William W. Cort ' 

•Gerard Dikmans 

•Jesse R/Christie 

'•Gotthold Steiner 

•EmmettW. Price 

•Eloise B. Cram 

•Gerald Thorne 

•Allen Mclntosh 

,*Edna M::Buhrer 

•Benjamin G. Chitwood 

•Aurel O. Foster - 

•Gilbert F. Otto 

•Theodor von Brand 

•May Belle Chitwood 

•Carlton M. Herman 

Lloyd E/Rozeboom 

•Albert L. Taylor 

David R. Lincicome 

Margaret A. Stirewalt 

•Willard H: Wright 

•Benjamin Schwartz ' 

•Mildred A. Doss. 

•Deceased. 

1960 

1961 

1962 

1964 

1965 

1966 

1966 

1967 

1969 

1969 

1970 

1971 

1972 

1973 

1974 

1975 

1975 

1976 

1977 

1978 

1979 

*O. Wilford Olsen 

•Frank D. Enzie 

Lloyd E. Rozeboom 

•Leon Jacobs 

Harley G. Sheffield 

A. Morgan Golden 

Louis S. Diamond 

•Everett L. Schiller 

MilfordN. Lunde 

J. Ralph Lichtenfels 

A. James Haley 

•Francis G. Tromba 

Thomas K. Sawyer 

Ralph P. Eckerlin 

Willis A. Reid, Jr. 

Gerhard A. Schad 

Franklin A. Neva 

Burton Y. Endo 

Sherman S. Hendrix 

Frank W. Douvres - 

E. J. Lawson Soulsby 

/ Roy C. Anderson 

Louis Euze^ 

John C. Holmes 

Purnomo 

NaftaleKatz 

^Robert Traub _ 

* Alan F. Bird 

CHARTER MEMBERS 1910 

•*. Philip E. Garrison 

•Joseph Goldberger 

•Henry W. Graybill 

LIFE MEMBERS 

1931 

1931 

1931 

1937 

1945 

1952^ 

1953 

1956 

1956 

1956 

1956 

1961 

1963 

1963 

1968 

.1972 

1972 

1975 

1975 

1975 

1975 

1975 

1976 

1976 

1976 

1976 

1977 

•Maurice C. Hall 

•Albert Hassall , 

•George F. Leonard 

;:*Evereft E. Wehr 

.Marion M. Farr 

•JohnTXucker, Jr. 

cGebrge W. Luttermoser 

•John's. Andrews 

•Leo A. Jachowski, Jrc 

•Kenneth C. Kates 

•Francis G. Tromba 

A; James Haley 

•Leon Jacobs 

•Paul C. Beaver 

"•Raymond M. Cable 

Harry Herlieh 

Glenn L. Hoffman 

Robert E. Kuntz ; : 

Raymond V Rebois 

Frank W. Douvres 

A. Morgan Golden 

Thomas'K. Sawyer 

•J. Allen Scott 

Judith H.Shaw 

Milford N, Lunde 

•Everett L. Schiller 

Harley G. Sheffield 

Louis S. Diamond 

Mary Hanson Pritchard 


1980 

1981 

1982 

1983 

1984 

1985 

1986 

1987 

1988 

1989 

1990 

1991 

1992 

1993 

1994 

1995 

1996 

1997 

1998 

1999 

'1990 

1991 

1992 

1993 

1994 

1995 

1996 

1997 

•Charles A. Pfender 

•Brayton H. Ransom 

•Charles W. Stiles 

1977 

1979 

1979 

1979 

1980 

1981 

1981 

1983 

1984 

1985 

1986 

1986 

1987 

_ 1988 

1988 

1988 

1989 

1989 

1989 

1990 

1990 

1991 

1991 

1991 

1994 

1994

JANUARY 2000 

CONTENTS 

(Continuedfrom Front Cover) 

NUMBER 1 

PEREZ-PONCE DE LEON, G., V. LEON-REGAGNON, L. GARGIA-PRIETO, U. RAZO-MENDIVEL, AND A. SANCHEZ- ; 

ALVAREZ. Digenean Fauna of Amphibians from Central Mexico: Nearctic and Neotropical 

y Influences ; . . — : '. •. i 92 

; , 'RESEARCH NOTES 

'••HANELT, B., AND J. JANOVY, JR. New Host and Distribution Record ofGordius difficilis (Nematomorpha: 

Gordioidea) fromua Vivid Metallic Ground Beetle, Chlaenius prasinus (Coleoptera: Carabidae) from 

Western Nebraska, U.S.A „_____ * - : ,___ =. 107 

GOLDBERG, S. R., C. R. BURSEY, AND C. M. WALSER. Intestinal Helminths of Seven Species of Agamid 

Lizards from Australia ___ 1 

'. 

BOLETTE, D. P. Descriptions of Cystacanths of Mediorhynchus orienialis and Mediorhynchus wardi 

(Acanthocephala: Gigantorhynchidae) ...... . : _ :—.— _ _ 114 

GOLDBERG, S. R., C. R, BURSEY, AND H. CHEAM. Gastrointestinal Helminths of Four Lizard Species from 

•Moorea; French Polynesia _, —„_! '.—. .-—-~ _ 118 

WEST, M.,T.'P. SCOTT, S. R. SIMCQC, AND R. M. ELSEY. New Records of Endohelminths of the Alligator 

Snapping Turtle (Mdcroclemys temmincTdi) from Arkansas and Louisiana, U.S.A. ;__ . 

122 

FOSTER, G. W., P. E. MOLER,7. M. KINSELLA, S. P. TERRELL, AND D. J. FORRESTER. Parasites of Eastern 

Indigo Snakes (Drymarchon corais couperi) from Florida, U.S.A. , '. ~ 

124 

' G ALICIA-GUERRERO, S., C. R.~BURSEY, S. R. GOLDBERG, G. SALGADO-MALDONABO. Helminths of Two 

Sympatric Toad Species^ JBufo marinus (Linnaeus) and Bufo marmoreus Wiegmann, 1833 (Anura: 

Bufonidae) from Chamela, Jalisco, Mexico ._ . . .. .". —: . 129 

EMERY, M. B., AND J. E. ,JOY. Endohehninths of the Ravine Salamander, Plethodon richmondi, from 

Southwestern West Virginia,JLJ.S.A. ._.__>. i._ .—. ,— =—. 133 

LADD-WILSON, S., Si BUCK, AND R. G. BOTZLER. Abomasal Parasites m Southern Mule Deer (Odocoileus 

hemionus fitliginatus) from Coastal San Diego County, California, U.S.A. ..__ 135 

ANNOUNCEMENTS 

OBITUARY NOTICE __„_ '. __u___: L_ 

DIAGNOSTIC PARASITOLOGY COURSE , . ^ — 

-MEETING SCHEDULE OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON __.. __ 

INTERNATIONAL CODE OF ZOOLOGICAL NOMENCLATURE (FOURTH EDITION) :„_;_., 

MEETING ANNOUNCEMENT ._„/: , ,—.—.

Comparative Parasitology 67(1) 2000 - Peru State College

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