The Helminthological Society of Washington - Peru State College

Volume 66 

JOURNAL 

of 

The Helminthological Society 

of Washington 

A semiannual journal of^research devoted to 

Helminthology and all branches of Parasitology 

Supported in part by the 

Braytbn H. Ransom Memorial Trust Fund 

.-- '< K - r ^ CONTENTS } 

-FiORlLLO, -R. /A;, AND W. F. FONT. - Seasonal Dynamics >and Community Structure of 

Helminths of Spotted Surifish, JLepomis miriiatus (Osteichthys: Centrarchidae) 

from an Oligohaline Estuary in Southeastern Louisiana, U;S. A ....... ------ __.~.H_ 101 

YABSLEY, M. J., AND G. P. NOBLET. Nematodes and Acanthocephalans of Raccoons 

(Procyon lotor), with a New Geographical .Record for Centrorhynchus conspectus 

(Acanthoeephala) in South Carolina, U.S.A. —,---------*.---------—.— ~- — ~ —.i- 111~ 

JVluzZALL, P. M.^Nematode Parasites of Yellow Perch, Perca flavescens, from the , 

âurentian Great Lakes ___ .____________________. ----------- •-— ~ —-,-/..... — 115 • 

AMIN, O. M., A. G. CANARIS, AND J. M. KINSELLA. A Taxoriomic Reconsideration (of 

the Genus Plagiorhynchus s. lat. (Acanthoeephala: Plagiorhynchidae), with De- _ 

- scriptions of South African Plagiorhynchus (Prosthorhynchus) cylindraceus from 

Shore Birds and P. (P.) malayensis, and a -Key to the Species of the Subgenus 

"- ProsthorhyncHus _____ .__ ~ _______________ ^ -------- —— ~^-------- ~— . ~, ------ 123 

REGO, A.yA., P. M. MACHADO, AND'G. C. PAVANELLI. Sciadocephalus megalodiscus 

Diesing, 1 850 (Cestoda: ;Corall6bothriinae), a Parasite of Cichla monoculiis Spix, 

1831 -(Cichlidae), in the Parana River, State of Parana, Brazil ______________s^_L£ 133 

KRITSKY, D. VC., AND S.-D. KULO. Revisions of Protoancylodiscoides and Bagrobdella, 

with Redescriptions of P. chrysichthes and B. auchenoglanii ^

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; MARK C. JENKINS, 1999 :>.' 

- .. WILLIAM E. MOSER, 2000, N "V 

•u DENNIS J. RICHARpSONr2000 

Immediate Past President: ELLEN ANDERSEN c , _x - ;; - , 

THE JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON 

The Journal -is published semiannually at Lawrence, Kansas -by the HelmiiKhologidal Society of 

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the EDITORS. ' ' • • • _ ' ' , 

. JOHN S. MACKIEWICZ 

/ BRENT B.NICKOL , 

•-v •:"" 2000 

, _ROY C. ANDERSON v < 

^ RALPH ;P ECKERLIN v " 

RONALD PAYER 

•A: MORGAN GOLDEN - > ". 

^' ROBIN N: HUETTEL 

- - FUAD M. NAHHAS \Y B. PENCE 

VASSILIOS THEODORIDES , i 

JOSEPH F. URBAN .--- 

' •" ". - / ' 

The Helfmnthological Society of Washington 1999 ' 

ISSN 1049-233X 

This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper). 

Copyright © 2011, The Helminthological Society of Washington

J. Helminthol. Soc. Wash. 

66(2), 1999 pp. 101-110 

Seasonal Dynamics and Community Structure of Helminths of 

Spotted Sunfish, Lepomis miniatus (Osteichthyes: Centrarchidae) 

from an Oligohaline Estuary in Southeastern Louisiana, U.S.A. 

RlCCARDO A. FlORILLO1 AND WILLIAM F. FONT 

Department of Biological Sciences, Southeastern Louisiana University, Hammond, Louisiana 70402 U.S.A. (email: 

raf3@ra.msstate.edu and wffont@selu.edu). 

ABSTRACT: The seasonal dynamics of the helminth community of the spotted sunfish Lepomis miniatus Warren, 

1992, from an oligohaline estuary were investigated over a 1-yr period. From 26 May 1991 to 25 May 1992, 7 

helminth species (3 Trematoda, 2 Nematoda, 2 Acanthocephala) were recovered from the gastrointestinal tracts 

of 200 specimens of L. miniatus. The parasite community of this host was dominated by the trematodes Barbulostomum 

cupuloris and Genarchella sp. Both helminths were recruited and matured in this host throughout 

the year, but their times of peak abundance differed. Barbulostomum cupuloris was most abundant in February- 

May, whereas Genarchella sp. abundance peaked in November-February. Camallanus oxycephalus and Leptorhynchoides 

thecatus showed a similar pattern of seasonal abundance, which was highest in May-August for 

both species. The remaining 3 helminths, Crepidostomutn cornutum, Neoechinorhyncus cylindratus, and Spinitectus 

carolini, were too rare to detect annual patterns of abundance. Infra- and component community diversity 

and richness did not vary seasonally, but infracommunity predictability was greatest in February-May. 

KEY WORDS: parasite, helminth, seasonal dynamics, Centrarchidae, Lepomis miniatus, estuary, infracommunity, 

component community, community, Louisiana, USA. 

Seasonal fluctuations in prevalence and abundance 

are common in many helminths of freshwater 

fishes (Eure, 1976; Chubb, 1979), but the 

mechanisms influencing seasonality are sometimes 

difficult to identify. Chubb (1979) concluded 

that, in general, seasonal patterns of occurrence 

of helminths are often species-specific 

and dependent upon: 1) how the helminth invades 

its host, 2) helminth growth and maturation, 

3) accumulation of eggs, and 4) loss of 

gravid worms. Abiotic factors such as temperature 

may also affect the seasonal cycles of many 

helminths (Chappell, 1969; Anderson, 1974, 

1976; Eure, 1976; Granath and Esch, 1983a-c). 

Seasonal patterns of abundance of the helminths 

of centrarchid fishes in freshwater environments 

have been previously examined 

(McDaniel and Bailey, 1974; Cloutman, 1975; 

Eure, 1976), but studies addressing temporal 

variability of helminths in nongame centrarchids 

are lacking. More importantly, the helminth fauna 

of centrarchid fishes inhabiting estuarine environments 

has received little attention. Fiorillo 

and Font (1996) characterized the helminth communities 

of 4 species of Lepomis from a lowsalinity 

estuary and showed that the compound 

1 Present address of corresponding author: Department 

of Biological Sciences, Drawer GY, Mississippi 

State University, Mississippi State, Mississippi 39762. 

community of centrarchid fishes in brackish water 

habitats differed from that of centrarchids in 

freshwater environments. 

In this study, we examined the seasonal pattern 

of abundance of all helminths that utilize 

Lepomis miniatus Warren, 1992, as a definitive 

host in an oligohaline estuary. In addition, we 

used community measures to investigate seasonal 

fluctuations in the infracommunity and component 

community structure of L. miniatus. 

Materials and Methods 

From 26 May 1991 to 25 May 1992, 200 specimens 

of L. miniatus were collected from a 1.1-km section of 

a canal along Interstate Highway 55 located between 

the south bank of Pass Manchac and Ruddock, Louisiana, 

in St. John the Baptist Parish. This man-made 

canal is part of the oligohaline Lake Pontchartrain- 

Lake Maurepas estuary located in southeastern Louisiana. 

The salinity of this large estuary ranges from 0 

ppt at the western shore of Lake Maurepas to 15 ppt 

at the eastern shore of Lake Pontchartrain, but at our 

study site, salinity never exceeded 3 ppt. Temporal variation 

in water temperature was determined using a 

Datasonde 3® water quality data logger (Hydrolab Corporation, 

Austin, Texas) located near our study site at 

the Turtle Cove Research Station on Pass Manchac, 

Louisiana. 

Our 1-yr collection period was divided into 4 periods 

of equal duration. Forty-five specimens were collected 

during the May-August period (May 26-August 

26), 53 during August-November (August 27-November 

26), and 51 each during the November—February 

101 


102 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 66(2), JULY 1999 

(November 27-February 26) and February-May (February 

27-May 25) periods. There was a minimum interval 

of 1 mo between collections made in different 

time periods. All hosts were captured by angling or 

with hoop nets and crab traps baited with cat food and 

checked at 1-2-day intervals. The sex and standard 

length of each fish were recorded, and the stomach, 

pyloric ceca, and intestinal tract were examined for 

adult helminths. Trematodes were fixed in Berland's 

solution (9 parts acetic acid, 1 part 37% formaldehyde) 

and stored in AFA (alcohol-formalin-acetic acid). 

Nematodes were fixed in Berland's solution and placed 

in glycerine alcohol. After acanthocephalans were refrigerated 

in distilled water overnight to extrude the 

proboscis, several small holes were made in the body 

wall with fine dissecting pins prior to fixation in AFA. 

Trematodes and acanthocephalans were stained with 

Semichon's carmine, dehydrated in a graded alcohol 

series, cleared in xylene, and mounted in Permount®. 

Nematodes were cleared and mounted in glycerine jeliy- 

The influence of host body size (standard length, 

mm) on helminth abundance and community attributes 

was examined with Pearson's correlations. The prevalence 

and abundance (Bush et al., 1997) of all helminths 

were calculated overall and for each time period. 

Helminth abundance data were square root transformed 

prior to statistical analyses. Seasonal patterns 

of helminth prevalence and abundance were analyzed 

with chi-square tests and ANOVA or ANCOVA, respectively. 

Because Barbidostomum cupuloris and Genarchella 

sp. were the most abundant helminths in the component 

community of this host, a contingency table analysis 

was used to examine for concurrent patterns of 

infection. Based on gonadal development, these 2 

trematodes were assigned to 1 of 3 developmental 

stages. Specimens of B. cupuloris were scored as immature, 

mature, or gravid, and specimens of Genarchella 

sp. were categorized as nongravid, gravid, or 

heavily gravid. Immature specimens of B. cupuloris 

were defined as individuals having incomplete gonadal 

development and lacking vitellaria. Mature worms 

were characterized by complete gonadal development, 

but egg production had not yet begun. Individuals with 

eggs and highly packed vitellaria were classified as 

gravid. Specimens of Genarchella sp. that possessed 

incompletely developed gonads and lacked eggs were 

classified as nongravid. Gravid worms were characterized 

by completely formed testes and ovary, but the 

lobes of the vitellaria of these specimens were not 

clearly distinct. The uteri of these gravid specimens 

contained eggs, but they were only slightly convoluted 

and well confined within the intercecal space. Heavily 

gravid worms were characterized by vitellaria possessing 

distinct lobes. The uteri of heavily gravid specimens 

were distended with eggs, highly convoluted, 

and typically extended laterally beyond the ceca. The 

seasonal patterns of abundance of these developmental 

stages were examined with ANOVA or ANCOVA. 

Voucher specimens of all species and developmental 

stages have been deposited in the U.S. National Parasite 

Collection (USNPC), Beltsville, Maryland, under 

USNPC accession numbers 84483-84485, 84489, 

84490, 88573 and 88574. 

Overall and within each time period, Brillouins's diversity 

index, which is appropriate for fully censused 

communities (Pielou, 1977), was used to estimate infracommunity 

and component community diversity. 

Seasonal mean infracommunity diversity was compared 

using ANOVA. As a measure of infracommunity 

predictability, Renkonen's coefficient of similarity was 

used to determine overall and within-season infracommunity 

similarity. Seasonal mean infracommunity similarity 

was compared using ANOVA, and in addition, 

Renkonen's coefficient of similarity was used to compare 

the component community of this host among 

time periods. 

Results 

Seven helminth species (3 Trematoda, 2 Nematoda, 

2 Acanthocephala), Barbidostomum cupuloris, 

Genarchella sp., Crepidostomum cornutum, 

Camallanus oxycephalus, Spinitectus 

carolini, Leptorhynchoides thecatus, and Neoechinorhyncus 

cylindratus, were recovered from 

the alimentary tracts of 200 L, miniatus (standard 

length in mm: x ± SE, range; 96.9 ± 0.91, 

68-126) collected from the Lake Pontchartrain- 

Lake Maurepas estuary. Host body size differed 

significantly among seasons (ANOVA, P < 

0.05). The largest hosts were collected in the 

May-August time period (104 ± 1.51, 84.5- 

126). Host body size decreased through August- 

November (101 ± 1.3, 83.1-121) and November-February 

(99.1 ± 1.42, 78.1-118) and was 

lowest in February-May (84.0 ± 1.6, 68.0-109). 

Water temperature in this oligohaline estuary 

was highest in July and gradually decreased to 

its lowest value in January (Fig. 1). 

With the exception of C. cornutum, whose 

abundance was greater in female hosts (x ± SE, 

range; 0.12 ± 0.04, 0-3) (male hosts, 0.02 ± 

0.02, 0-2) (r-test, P < 0.05), there were no sexrelated 

differences in helminth abundance. In 

addition, only C. cornutum (x2 = 5.137, P < 

0.05) and L. thecatus (x2 = 10.442, P < 0.05) 

showed host sex-related differences in prevalence, 

and as a result, both sexes were pooled 

for subsequent statistical analyses. 

Only the abundance of B. cupuloris displayed 

a statistically significant relationship with host 

body size (overall, r = -0.254, P < 0.01). In 

addition, no statistically significant correlations 

between host size and helminth species abundance 

were found within each collecting period 

(P > 0.05). 


FIORILLO AND FONT—SEASONAL DYNAMICS OF HELMINTH INFECTIONS 103 

35 

30 

^•1 All stages 

I I IMM 

f~1 MAT 

1777, GRV 

25 

E 20 

15 

10 

Ifeii 

May-Aug Aug-Nov Nov-Feb Feb-May 

May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr 

Figure 1. Mean monthly water temperature 

(°C) in Lake Pontchartrain-Lake Maurepas estuary 

(1992-1995). Vertical hars represent ±1 standard 

error of the mean. 

All stages 

NGR 

GRV 

HGR 

Helminth seasonal dynamics 

Prevalence of B. cupuloris differed significantly 

among time periods (x2 = 28.98, P < 

0.05). Thirty-six percent of hosts examined in 

May-August harbored at least 1 specimen. Prevalence 

increased to 40% in August-November 

and 41% in November-February before reaching 

82% in February-May. Irrespective of developmental 

stage, B. cupuloris was most abundant 

in February-May (8.8 ± 1.28, 0-37), displaying 

an 82% increase in abundance from the 

previous November-February time period (1.6 

± 0.47, 0-20) and a considerable decrease in the 

subsequent May-August period (1.1 ± 0.4, 0- 

15) (2-way ANCOVA, P < 0.05) (Fig. 2a). 

Abundance also differed with respect to developmental 

stage (2-way ANCOVA, P < 0.05), 

but no interaction effect was found (2-way AN- 

COVA, P > 0.05). Mature specimens were most 

abundant (1.5 ± 0.24, 0-21), followed by gravid 

specimens (1.4 ± 0.22, 0-18) and immature 

worms (0.6 ± 0.13, 0-14). In addition, each developmental 

stage of B. cupuloris showed a statistically 

significant seasonal cycle of abundance 

(ANCOVA, P < 0.05 for each stage). The abundance 

of each stage was lowest in May-August, 

remained low in the following August-November 

and November-February periods, and 

reached maximum abundance in February-May 

(Fig. 2a). 

Thirteen percent of hosts in May-August 


Figure 2. Seasonal abundances of (a) Barbulostomum 

cupuloris (all stages) and each developmental 

stage (IMM, immature; MAT, mature; GRV, 

gravid); (b) Genarchella sp. (all stages) and each 

developmental stage (NGR, nongravid; GRV, gravid; 

HGR, heavily gravid). Vertical bars represent 

± 1 standard error of the mean. 

were infected with Genarchella sp. Prevalence 

increased through August-November (34%) to 

reach a peak in November-February (49%) before 

decreasing in February-May (39%) (x2 = 

13.69, P < 0.05). Genarchella sp. was most 

abundant in November—February (6.9 ± 1.62, 

0-41), a 44% increase from the previous August—November 

time period (3.9 ± 1.39, 0—43) 

and showed its lowest abundance in May—August 

(1.4 ± 0.74, 0-23) (2-way ANOVA, P < 

0.05) (Fig. 2b). Overall, there was no difference 

in abundance among developmental stages and 

no interaction effect (2-way ANOVA, P > 

0.05). Both nongravid and gravid worms showed 

statistically significant seasonal cycles of abundance 

(ANOVA, P < 0.05 for each stage). Nongravid 

and gravid worms were most abundant in 

November-February (2.5 ± 0.89, 0-27) and Au- 



gust-November (2.2 ± 0.94, 0-41), respectively, 

and least abundant in May-August (nongravid: 

0.09 ± 0.09, 0-4; gravid: 0.1 ± 0.08, 0-3) 

(Fig. 2b). 

Camallanus oxycephalus was most prevalent 

and abundant in May-August (36%) (0.7 ± 

0.26, 0-11). Prevalence and abundance declined 

throughout the year and were lowest in February-May 

(10%) (0.1 ± 0.05, 0-2), (x2 = 12.888, 

P < 0.05) (ANOVA, P < 0.01), respectively 

(Table 1, Fig. 3). Prevalence of L. thecatus did 

not change seasonally (x2 = 5.278, P > 0.05) 

(Table 1), but its abundance did vary among 

time periods and peaked in May-August (0.6 ± 

0.19, 0-5) (ANOVA, P < 0.05) (Fig. 3). Crepidostomum 

cornutum, S. carolini, and N. cylindratus 

were uncommon (prevalence of each, 

< 7%), and too few individuals (abundance of 

each, < 0.1) were recovered to determine seasonal 

patterns of prevalence and abundance (Table 

1). 

Parasite abundance (overall: 8.2 ± 0.8, 0—56) 

differed significantly among time periods (AN- 

COVA, P < 0.05). Abundance was lowest in 

May-August (4.0 ± 0.87, 0-26), increased during 

August-November (7.3 ± 1.66, 0-53) and 

November-February (8.5 ± 1.54, 0-45), and 

reached its highest value during February-May 

(12.8 ± 1.81, 0-56). 

Infracommunity analysis 

Overall, host body size was correlated with 

infracommunity diversity (r = 0.18, P < 0.05), 

but this relationship was not significant within 

time periods. The most diverse infracommunity 

was found in November-February (1.294 ± 

0.197, 0.0-4.14), whereas in February-May, infracommunity 

diversity was lowest (0.689 ± 

0.136, 0.0—3.35). The remaining 2 time periods, 

May—August and August-November, showed intermediate 

levels of infracommunity diversity 

(0.889 ± 0.151, 0.0-3.40 and 0.959 ± 0.185, 

0.0-4.01, respectively). However, infracommunity 

diversity did not differ significantly among 

time periods (ANCOVA, P > 0.05). Overall infracommunity 

diversity was 0.963 ± 0.087 (0.0- 

4.14). 

Both overall and within time periods, host 

body size did not influence infracommunity species 

richness. Helminth richness was lowest in 

May-August (1.244 ± 0.143, 0-4) and increased 

in August—November (1.302 ± 0.139, 

0-3) and November-February (1.353 ± 0.096, 

0-3). Infracommunity richness was greatest in 

February-May (1.549 ± 0.113, 0-3). However, 

infracommunity species richness did not differ 

significantly among time periods (ANOVA, P > 

0.05). Overall infracommunity species richness 

was 1.365 ± 0.062 (0-4). Infracommunity predictability 

differed significantly among time periods 

(ANOVA, P < 0.001). Infracommunity 

similarity was greatest in February-May (0.56 

± 0.01, 0-1) and lowest in May-August (0.22 

± 0.01, 0-1). In August-November and November-February, 

infracommunity similarity values 

were intermediate (0.31 ± 0.01, 0-1 and 0.34 ± 

0.01, 0-1, respectively). Overall infracommunity 

similarity was low (0.31 ± 0.003, 0-1). 

Component community analysis 

The trematodes B. cupuloris and Genarchella 

sp. were the most prevalent and abundant helminths 

and dominated the component community 

of Lepomis miniatus (Table 1). Barbulostomum 

cupuloris was most prevalent (50%), and 

although Genarchella sp. was recovered from 

fewer hosts (35%), its overall abundance (3.9 ± 

0.64, 0-43) did not differ significantly from that 

of B. cupuloris (3.5 ± 0.46, 0-37) (Mest, P > 

0.05). Although together these 2 trematodes accounted 

for 1,485 of the total 1,662 worms recovered 

during this study (89%), no significant 

association was found between them with respect 

to concurrent patterns of infection (x2 = 

0.032, P > 0.05). The nematode C. oxycephalus 

was recovered from 24% of hosts examined, but 

its abundance was low (0.4 ± 0.08, 0-11). The 

remaining 4 helminth species showed low prevalence 

and abundance and, together with C. oxycephalus, 

represented only 11 % of the total helminth 

specimens recovered (Table 1). 

Component community diversity was low 

(0.47). It was greatest in February-May (1.16), 

progressively declined through May-August 

(0.63) and August-November (0.45), and was 

lowest in November-February (0.34). Component 

community species richness changed slightly 

over the year. Six helminth species were recovered 

during May—August, August—November, 

and November-February, whereas 7 helminth 

species were found in February-May 

(Table 1). The trematode C. cornutum and the 

acanthocephalan TV. cylindratus were the only 

helminths not found in all 4 time periods (Table 

1). Component community comparisons among 

time periods were made using Renkonen's co- 





Table 2. Renkonen's coefficients of component 

community similarity of helminths of Lepomis miniatus 

between paired time periods. 

Caox 

Leth 

May-Aug. 

Aug.—Nov. 

Nov.-Feb. 

Aug.-Nov. Nov.—Feb. Feb.—May 

0.46 0.41 

0.77 

0.46 

0.62 

0.45 

suit, the nature of the observed seasonal patterns 

of this and all other helminth species is biological 

and not a result of changes in host demographics. 


Figure 3. Seasonal abundance of Camallanus 

oxycephalus (Caox) and Leptorhynchoides thecatus 

(Leth). Vertical bars represent ±1 standard error 

of the mean. 

efficient of similarity. Mean seasonal component 

community similarity was 0.53 ± 0.058, 0.41- 

0.77. The helminth community of L. miniatus in 

August-November and November-February 

showed the greatest similarity (0.77), whereas 

the May-August and November-February communities 

were least similar (0.45). The remaining 

comparisons are shown in Table 2. 

Discussion 

The species composition, richness, and diversity 

of the helminth community of L. miniatus 

were similar throughout the year. Species-specific 

and overall abundance of these helminths, 

infracommunity similarity, and host body size 

did vary somewhat with season. The trematodes 

B. cupuloris, described from L. miniatus (as Lepomis 

punctatus (Valenciennes, 1831)) collected 

within our study site (Ramsey, 1965), and Genarchella 

sp. were the most prevalent and abundant 

helminths recovered in this study. These 

parasites have been reported only in estuarine 

centrarchid fishes (Fiorillo and Font, 1996), in 

which they showed distinct seasonal cycles of 

prevalence and abundance. 

Barbulostomum cupuloris was the only helminth 

to show, possibly as a result of an ontogenetic 

shift in diet, a significant relationship 

with host body size. However, the influence of 

host size was removed statistically from the subsequent 

seasonal abundance analysis. As a re- 

Seasonal dynamics of helminth infections 

Conditions were optimal for the recruitment 

and maturation of B. cupuloris in February- 

May, when prevalence was greatest, and each 

developmental stage of this worm displayed 

maximum abundance. Following that period, the 

abundance of each developmental stage and the 

overall prevalence declined to their lowest values 

(Fig. 2a). Overall, most B. cupuloris specimens 

recovered were mature or gravid. These 

data suggest that B. cupuloris matures quickly 

after recruitment. Immature, mature, and gravid 

specimens were recovered in all 4 collecting periods, 

indicating that recruitment and egg production 

occurred throughout the year, irrespective 

of water temperature. Because of south Louisiana's 

near-subtropical climate, seasonal 

changes in water temperature are not extreme 

(Fig. 1). Although water temperature does not 

affect egg production in B. cupuloris, temperature 

can influence timing and rate of cercarial 

production and dispersal (Chappell, 1969; review 

in Chubb, 1979) and the seasonal abundance 

of first or second intermediate hosts (Fernandez 

and Esch, 199la, b). It is likely that both 

factors interact to affect the seasonal abundance 

of B. cupuloris in its definitive host. 

Similarly, water temperature did not affect recruitment 

and maturation of Genarchella sp. in 

L. miniatus. As with B. cupuloris, all 3 developmental 

stages of Genarchella sp. were found 

throughout the year, but this helminth showed a 

more gradual increase in recruitment, which 

peaked in November-February (Fig. 2b). At that 

time of year, many gravid worms were also recovered. 

The seasonal cycles of Genarchella sp. 

and B. cupuloris were asynchronous. Unlike B. 

cupuloris, which showed maximum prevalence 



and abundance in February-May, Genarchella 

sp. was more common and numerous in November—February 

(Fig. 2a, b). However, as in B. cupuloris, 

the seasonal cycle of Genarchella sp. in 

L. rniniatus may be linked to the seasonal dynamics 

of cercarial production and dispersal and 

to the abundance of the intermediate host. 

The life cycles of B. cupuloris and Genarchella 

sp. are not known but are probably dependent 

on brackish water food webs for successful 

transmission (Ramsey, 1965; Fiorillo and 

Font, 1996). The lack of a concurrent pattern of 

infection, as well as the apparent asynchrony in 

the seasonal cycles of these trematodes, suggest 

that they do not share the same intermediate 

hosts. 

A qualitative analysis of the gut contents of 

L. miniatus in May-August showed that this 

centrarchid preyed primarily on amphipods 

(Fiorillo and Font, 1996). Similarly, Levine 

(1980) reported that amphipods made up 75% of 

all prey items of L. miniatus in the Lake Pontchartrain-Lake 

Maurepas estuary. However, 

Fiorillo and Font (1996) showed that in May- 

August, both helminths were much more prevalent 

and abundant in redear sunfish Lepomis 

microlophus (Giinther, 1859), a host well known 

for its specialized diet of bivalves and other mollusks 

(Wilburn, 1969; Lauder, 1983). In this estuary, 

Levine (1980) reported that the diet of L. 

microlophus consisted primarily of molluscs, but 

some amphipods were also taken. A qualitative 

gut analysis in May-August showed that L. microlophus 

preyed on amphipods, isopods, and 

bivalves (Fiorillo and Font, 1996). These data 

suggest that amphipods and bivalves may represent 

potential second intermediate hosts for 

these 2 trematodes. 

The nematode C. oxycephalus was most prevalent 

and abundant in May-August. Prevalence 

and abundance declined through the subsequent 

time periods and were lowest in February-May. 

It is likely that the seasonal dynamics of C. oxycephalus 

in this estuary are dependent on the 

seasonal abundance of its copepod intermediate 

host as shown by Stromberg and Crites (1975) 

in Lake Erie. Unfortunately, we have no data on 

the seasonal dynamics of copepod populations 

in the Lake Ponchartrain-Lake Maurepas estuary 

to support this assumption, but, generally, zooplankton 

populations in temperate climates increase 

in the summer months (Pennak, 1989). 

Although in our study C. oxycephalus abundance 

was low, we did recover gravid specimens, 

suggesting that L. miniatus is a suitable 

host for this nematode. 

As in C. oxycephalus, abundance of L. thecatus 

was low, but this acanthocephalan did 

show a seasonal cycle of abundance that peaked 

in May-August. Fiorillo and Font (1996) 

showed that, in this estuary, L. thecatus was 

much more prevalent and abundant in redear 

sunfish, L. microlophus, and C. oxycephalus occurred 

more frequently in bluegill, L. macrochirus 

Rafinesque, 1819, suggesting that L. miniatus 

is a suitable rather then a required host for 

these helminths. Leong and Holmes (1981) suggested 

that, within its environment, the seasonal 

cycle of a helminth is mostly determined by its 

seasonal dynamics within its most common host 

in which the parasite can become reproductive 

(required host). Therefore, the seasonal cycles of 

L. thecatus and C. oxycephalus in L. miniatus 

may not be indicative of the seasonal pattern 

found in L. microlophus and L. macrochirus, respectively. 

Too few specimens of the remaining 

3 helminth species were found to determine seasonal 

cycles of prevalence and abundance, but 

all are common parasites of centrarchids and 

other fishes from freshwater environments (see 

Hoffman, 1967) (Table 1). 

Mostly because of increases in abundance of 

B. cupuloris and Genarchella sp. (Fig. 2a, b), 

the overall parasite abundance was greatest in 

February-May. That time of year is generally 

associated with an increase in the feeding activity 

of fishes in Louisiana as water temperature 

begins to rise (Fig. 1) and many centrarchid species 

approach the reproductive season (Carlander, 

1977). Many invertebrate potential intermediate 

hosts also show seasonal changes in 

density, with abundance peaks in early spring 

(Heard, 1982). Seasonal dynamics of invertebrate 

intermediate hosts, coupled with seasonal 

variation in feeding rates and diet of L. miniatus, 

may play an important role in determining the 

seasonal cycles of abundance of these helminths. 

Infracommunity structure 

Kennedy (1990) characterized the helminth 

community of freshwater fishes as depauperate 

and isolationist. The infracommunity of L. miniatus 

displayed both characteristics. Infracommunities 

were characterized by a lack of helminth 

interactions, were species-poor, and included 

a small number of worms. Consequently, 



overall mean infracommunity diversity and species 

richness of L. miniatus were low, similar to 

other freshwater fishes (Kennedy et al., 1986). 

Most fish display indeterminate growth (Wooten, 

1990), so that body size is often highly correlated 

with age (Ricker, 1979; Swales, 1986). 

In the present study, larger hosts harbored a 

more diverse infracommunity. This was probably 

because of greater exposure time, which may 

increase the probability of these hosts being colonized 

by the less common helminth species. 

Cloutman (1975) noted a similar relationship between 

age and helminth diversity in largemouth 

bass, Micropterus salmoides (Lacepede, 1802). 

Seasonality did not affect infracommunity diversity 

and species richness. With the exception 

of C. cornutum and TV. cylindratus, all remaining 

helminths were recovered in all time periods, 

suggesting that the larval forms of the majority 

of these helminths are capable of colonizing L. 

miniatus year-round. However, the proportion of 

infected intermediate hosts, as shown by Fernandez 

and Esch (199la, b), may have changed 

seasonally, resulting in the discrete cycles of 

abundance shown by some of these helminths. 

Overall, the infracommunity structure of L. 

miniatus was not highly predictable, suggesting 

that each infracommunity represented a random 

subset of the parasites found in the component 

community of this host. Poulin (1997) noted that 

low infracommunity predictability is also a characteristic 

of isolationist communities, because 

helminth interactions, which often result in more 

predictably structured assemblages, are lacking. 

Infracommunity predictability did differ 

among time periods. Infracommunity structure 

was most and least predictable in February—May 

and May—August, respectively. In February- 

May, increases in prevalence and abundance of 

B. cupuloris were largely responsible for the 

greatest degree of infracommunity similarity, 

whereas reductions in prevalence and abundance 

of this trematode, along with Genarchella sp., 

may have contributed to low infracommunity 

predictability in the following season. The greater 

predictability in February-May suggests that 

larval helminths are more prevalent in their intermediate 

hosts during that time of year so that 

the probability of individual hosts acquiring a 

similar suite of parasites is greater. 

Component community structure 

The trematodes B. cupuloris and Genarchella 

sp. were the dominant species in the component 

community of L. punctatus and accounted for 

the majority of all worms recovered during this 

year-long study. These helminths are not found 

in freshwater centrarchids but have been reported 

from other Lepomis spp. in the Lake Pontchartrain-Lake 

Maurepas estuary (Fiorillo and 

Font, 1996). Ramsey (1965) noted that B. cupuloris 

was replaced by the closely related Homalometron 

armatum (MacCallum, 1895) in centrarchid 

hosts collected in freshwater ponds located 

near this estuary. In this estuary, B. cupuloris 

and Genarchella sp. are more prevalent 

and abundant in L. microlophus (Fiorillo and 

Font, 1996), suggesting that L. miniatus is a suitable 

but not a required host for these trematodes 

(Leong and Holmes, 1981). However, the specificity 

of B. cupuloris and Genarchella sp. for 

estuarine hosts reaffirms the importance of ecological 

associations to the component community 

structure of L. miniatus. 

The remaining 5 helminths recovered from L. 

miniatus are common parasites of freshwater 

centrarchid fishes (see Hoffman, 1967). Although 

mature forms were found in L. miniatus, 

these helminths showed low prevalence and 

abundance (Table 1). However, all 5 species 

were more prevalent and abundant in other Lepomis 

spp. from this estuary (Fiorillo and Font, 

1996). These patterns suggest that L. miniatus is 

a suitable host for these helminths (Leong and 

Holmes, 1981) but that their occurrence in L. 

miniatus may represent accidental infections. 

Component community diversity was low and 

similar to that of other freshwater fishes (Kennedy 

et al., 1986). Qualitatively, component diversity 

varied seasonally and was greatest in 

February—May when B. cupuloris and Genarchella 

sp. occurred frequently and abundances 

were high. The component community of this 

host in August-November and November-February 

was most similar. In those time periods, 

most of the helminths recovered displayed similar 

measures of prevalence and abundance (Table 

1), resulting in a greater degree of similarity. 

Overall, the helminth species composition of 

L. miniatus was similar to that of other centrarchid 

hosts in this estuary (see Fiorillo and Font, 

1996). All helminths found in the present study 

were also recovered in L. macrochirus and, with 

the exception of C. cornutum, in L. megalotis. 

However, compared to L. miniatus, species richness 

was much lower in L. microlophus. Dietary 

differences between and among hosts may ac- 



count for this result (Bell and Burt, 1991), but 

unequal sampling effort may have biased this 

pattern (see Levine, 1980; Fiorillo and Font, 

1996, for diet analyses). 

Further studies are necessary to determine the 

life cycles of B. cupuloris and Genarchella sp. 

Knowledge of the intermediate hosts of these 

trematodes and their seasonal patterns of abundance, 

as well as of temporal changes in the trophic 

interactions of intermediate hosts and fish, 

is essential to our understanding of the mechanisms 

that determine the seasonal dynamics of 

these helminths and the parasite community 

structure of this centrarchid host. In addition, a 

better understanding of these life cycles and seasonal 

patterns of incidence and abundance 

would further elucidate the importance of L. 

miniatus to the circulation of these helminths in 

this estuarine ecosystem. 

Acknowledgments 

We thank G. W. Childers, R. A. Seigel, R. W. 

Hastings, and G. P. Shaffer for their counsel and 

support. We thank Bill Lutterschmidt, Becky 

Fiorillo, John Chelchowski, Scott Thompson, 

and Kelley Smith for their help in the field. We 

are especially grateful to Tom Blanchard for his 

relentless help in the field and support throughout 

the duration of this study and to an anonymous 

reviewer for a critical and perceptive review 

of the manuscript and recommendations 

for its improvement. 

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Editors' Acknowledgments 

In addition to the members of the Editorial Board, we would like to acknowledge, with thanks, 

the following persons for providing their valuable help and insights in reviewing manuscripts for 

the Journal: Jasem Abdul-Salam, Martin Adamson, Omar Amin, James Baldwin, Diane Barton, 

George Benz, Ian Beveridge, Walter Boeger, Burton Bogitsh, Daniel Brooks, Charles Bursey, Albert 

Bush, Gilbert Castro, Hilda Ching, Rebecca Cole, Bruce Conn, John Crites, John Cross, Murray 

Dailey, Tommy Dunagan, Donald Forrester, Stephen Goldberg, David Hall, Hideo Hasegawa, Richard 

Heard, Gary Hendrickson, Sherman Hendrix, Russell Hobbs, Jane Huffman, Hugh Jones, 

James Joy, Michael Kinsella, Thomas Klei, Delane Kritsky, Ralph Lichtenfels, Donald Linzey, 

Jeffrey Lotz, Eugene Lyons, David Marcogliese, Gary MacCallister, Donald McAlpine, Lena Measures, 

Frantisek Moravec, Darwin Murrell, Patrick Muzzall, Brent Nickol, Thomas Nolan, Paul 

Nollen, David Oetinger, Robin Overstreet, Raphael Payne, Danny Pence, Thomas Platt, Mark Pokras, 

Dennis Richardson, Guillermo Salgado-Maldonado, Gerhard Schad, Mark Siddall, Donald 

Smith, Marilyn Spalding, George Stewart, Michael Sukhdeo, Dennis Thoney, John Ubelaker. 



66(2), 1999 pp. 11 1-114 

Nematodes and Acanthocephalans of Raccoons (Procyon lotor}, with 

a New Geographical Record for Centrorhynchus conspectus 

(Acanthocephala) in South Carolina, U.S.A. 

MICHAEL J. YABSLEY AND GAYLE PITTMAN NoBLET1 

Department of Biological Sciences, Clemson University, Clemson, South Carolina 29634-1903, U.S.A. (e-- 

mail: myabsle@clemson.cdu; gnoblet@clemson.edu) 

ABSTRACT: From April 1997 through April 1998, 128 raccoons (Procyon lotor (Linnaeus)) collected from 7 

sites representing 4 physiographic areas in South Carolina were examined for gastrointestinal helminth parasites. 

Four species of nematodes (Gnathostoma procyonis (Chandler), Physaloptera rara Hall and Wigdor, Arthrocephahis 

lotoris (Schwartz), and Molineus barhatus Chandler) and 2 species of acanthocephalans (Macracanthorhynchus 

ingens (von Linstow) and Centrorhynchus conspectus Van Cleave and Pratt) were collected. The 

finding of 11 immature C. conspectus in 3 South Carolina raccoons represents a new geographical record for 

this species. 

KEY WORDS: Centrorhynchus conspectus, raccoon, Procyon lotor, Nematoda, Acanthocephala, helminths, 

Gnathostoma procyonis, Physaloptera rara, Arthrocephalus lotoris, Molineus barbatus, Macracanthorhynchus 

ingens, South Carolina, U.S.A. 

The raccoon (Procyon lotor (Linnaeus, 1758)) 

is an omnivore that ranges over most of North 

America and occurs in both rural and urban settings. 

Consequently, the range of zoonoses for 

raccoons is important in assessing risk to humans 

and domestic animals. In South Carolina, 

only limited studies on helminth parasites of raccoons 

have been reported previously (Harkema 

and Miller, 1964; Stansell, 1974). More recent 

reports of serious human illnesses from the 

northern and midwestern United States, such as 

cerebrospinal nematodiasis because of infection 

with the gastrointestinal nematode Baylisascaris 

procyonis (Stefanski and Zarnowski, 1951), led 

to the current study, which includes raccoons 

collected statewide from a wide variety of habitats 

(e.g., mountains, farms, urban areas, beaches, 

swamps, and barrier islands), allowing for a 

comparison of parasite burdens and consideration 

of human health risks associated with these 

parasites (Williams et al., 1997; Boschetti and 

Kasznica, 1995). 

Materials and Materials 

Raccoons (n = 128) were collected between April 

1997 and April 1998 with foot-hold traps or wire livetraps. 

Traps were set at 7 sites that included 4 of the 

5 physiographic areas of South Carolina. Site 1 included 

both urban and waterfowl management areas 

(WMA) in Pickens County (Foothills); Site 2 was a 

WMA in Union County (Piedmont); Site 3 was inland 

1 Corresponding author. 

111 

farm areas of Horry County (Lower Coastal Plains 

North, LCPN); Site 4 included both beach and wooded 

habitats in the tourist area of Myrtle Beach, Horry 

County (LCPN); Site 5 was a swamp located on the 

Savannah River in Hampton County (Lower Coastal 

Plains South, LCPS); and Sites 6 and 7 were both on 

barrier islands located in Charleston County (LCPS). 

John's Island (Site 6), next to and continuous with the 

mainland at times of low tide, is primarily forest and 

farmland with many freshwater ponds, whereas Seabrook 

Island (Site 7) is a small residential island about 

1.5 km offshore, which lacks freshwater habitats. Each 

raccoon was subjected to multiple evaluations, which 

included not only our study of gastrointestinal helminth 

parasites, but also seroprevalence, culture and 

DNA studies for Trypanosoma cruzi, and museum 

study specimens. In addition, most animals were included 

in a trap-type capture effectiveness study conducted 

by the South Carolina Department of Natural 

Resources (SCDNR). 

Raccoons were either euthanized by intramuscular 

injection of 0.2 ml/kg ketamine/xylazine followed by 

intraperitoneal injection of 1 ml/kg sodium pentobarbital, 

or were hunter-shot. Stomach and intestines from each 

animal were examined as soon as possible after death 

(within 1-2 hr). However, animals from 2 of the physiographic 

regions (Sites 3-7) were frozen at — 4°C for 

1-3 mo prior to examination for helminths because of 

the use of the animals for a trap-type study conducted 

by the International Association of Fish and Wildlife 

Agencies. Therefore, trematodes and cestodes were excluded 

from the overall analyses because freezing of a 

large number of hosts resulted in difficult collection 

and unreliable identification of flatworms. 

All nematodes collected from the stomachs and 

small intestines of raccoons were preserved and stored 

in a 70% ethanol-5% glycerine solution. Representative 

specimens of each nematode were mounted in glycerine 

jelly. Acanthocephalans collected from the small 


M 

* 


intestine were placed in water until the proboscis everted, 

preserved in acetic acid-formalin-alcohol (AFA), 

and stored in 70% ethanol. Temporary wet mounts and 

permanent Mayer's acid carmine-stained mounts in 

Canada balsam were made for identification. Voucher 

specimens deposited at the U.S. National Parasite Collection 

in Beltsville, Maryland, have been assigned 

USNPC accession numbers 87838-87843. Fisher's exact 

test was used to detect significant differences (P < 

0.05) in helminth prevalence (%) between study sites. 

Two-thirds of the animals caught were male, and 85% 

of all animals were mature. Because of the large bias 

toward males and adults, no statistical analyses were 

performed. 

Results and Discussion 

Of the 128 raccoons examined, 103 (80%) 

were infected with 1 or more of the 4 nematodes 

and 2 acanthocephalans listed in Table 1. Gnathostoma 

procyonis Chandler, 1942, and Physaloptera 

rara Hall and Wigdor, 1918, were recovered 

primarily from the stomach. Arthrocephalus 

(=Placoconus) lotoris (Schwartz, 1925) 

and Molineus barbatus Chandler, 1942, were 

collected from the posterior and anterior ends of 

the small intestine, respectively. Both Macracanthorhynchus 

ingens (von Linstow, 1879) and 

Centrorhynchus conspectus Van Cleave and 

Pratt, 1940, were recovered exclusively from the 

small intestine. Interestingly, 96.1% of raccoons 

examined from Sites 1-6 were infected with at 

least 1 helminth species, whereas only 5 of 26 

(19.2%) raccoons examined from Seabrook Island 

(Site 7) were infected. 

Gnathostoma procyonis, a stomach nematode 

that forms large nodules in the mucosa, was 

found at Sites 3 and 5 in significantly larger 

numbers than at other sites (Table 1). Extensive 

freshwater habitats were present at both sites, 

providing a favorable environment for the required 

first intermediate host, which is 1 of several 

species of cyclopoid copepods (Miyazaki, 

1960). In contrast, no infections of G. procyonis 

were observed at 2 coastal locations (Sites 4 and 

7), which lacked permanent freshwater habitats. 

Physaloptera rara, a spirurid nematode recovered 

from both the stomach and small intestine 

of hosts, does not require the presence of freshwater 

habitats, because raccoons become infected 

by ingestion of various terrestrial arthropods 

(e.g., Gryllus pennsylvanicus Burmeister, 1838, 

Pennsylvania field cricket; Blattella germanica 

(Linnaeus, 1767), German cockroach; and Centophiles 

spp., camel crickets) (Lincoln and Anderson, 

1973). Compared to all other sites, a sig- 

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YABSLEY AND NOBLET—HELMINTHS OF RACCOONS 13 

nificantly higher prevalence of P. ram was observed 

in raccoons trapped at Site 1, with urbancaptured 

animals dominating the number of 

infected animals. Because broad host specificity 

has been documented for physalopteroids, domesticated 

animals could accumulate large numbers 

of these worms by ingesting an infected intermediate 

host that commonly occurs in urban 

settings (Morgan, 1941). 

High prevalences of both the raccoon hookworm, 

A. lotoris, and the trichostrongylid, M. 

barbatus, frequently have been reported in previous 

surveys (Harkema and Miller, 1964; Cole 

and Shoop, 1987). In the present study, however, 

overall prevalence of A. lotoris and M. barbatus 

was 28.1 and 12.5%, respectively (Table 1). 

Data from Seabrook Island are consistent with 

those of Harkema and Miller (1962), who previously 

reported an almost complete absence of 

A. lotoris and M. barbatus from Cape Island, 

South Carolina. These investigators suggested 

that the low prevalence of these 2 nematodes on 

coastal islands was due possibly to the detrimental 

effect of high tides, salinity of soil, and 

dry habitats on the free-living larval stages of 

these helminths. Additionally, seasonal variations 

have been documented, with lower prevalence 

during winter months (Smith et al., 1985), 

which could have contributed to the lower numbers 

observed in the current survey. 

Although B. procyonis was not collected from 

any raccoon examined in this study, surveillance 

for this parasite should be continued because of 

its medical and veterinary significance and its 

reported widespread distribution in the United 

States (Kazacos and Boyce, 1989). Based on reports 

from southeastern states, Jones and Mc- 

Ginnes (1983) suggested that B. procyonis was 

found primarily in the more mountainous regions. 

The northwestern range of our study site, 

although classified as "Foothills," is not truly 

mountainous, which might account for the lack 

of B. procyonis. In contrast, however, B. procyonis 

recently was found in 70% of 33 raccoons 

examined in southern coastal Texas (Kerr 

et al., 1997). These investigators suggested that 

the nematode could have been acquired by ingestion 

of larvae in migratory wild birds, introduced 

from infected translocated raccoons, or 

the result of a northern expansion from Latin 

America. This recent finding of B. procyonis in 

southern Texas and limited reports from the adjacent 

state of Georgia (only 2 reports, each of 

a single infected raccoon [Babero and Shepperson, 

1958; Kazacos and Boyce, 1989]) suggests 

the possibility of introduction of this nematode 

into South Carolina. 

The most prevalent parasite collected was the 

acanthocephalan M. ingens. Infections occurred 

in raccoons from all study sites, with an overall 

prevalence of 53%. Although not considered a 

threat to public health, M. ingens infection in 

humans has been reported (Dingley and Beaver, 

1985). 

Six species of the acanthocephalan genus 

Centrorhynchus have been reported from North 

American birds of prey; however, little is known 

about the life cycle, geographical distribution, or 

prevalence of these acanthocephalan species. 

Read (1950) demonstrated experimentally that 

Centrorhynchus spinosus (Kaiser, 1893) was capable 

of developing to adults in laboratory rats, 

suggesting that members of this genus have the 

ability to complete development not only in bird 

definitive hosts, but also in mammalian hosts. 

One raccoon from John's Island (Site 6) and 2 

raccoons from the Horry County inland site (Site 

3) were infected with immature C. conspectus. 

Prior to the current study, immature forms of C. 

conspectus had been reported from 26 mammals 

representing 6 host species (3 Didelphis virginiana 

Kerr, 1792, Virginia opossum; 3 P. lotor, 

raccoon; 17 Mustela vison Schreber, 1775, mink; 

1 Spilogale putorius (Linnaeus, 1758), spotted 

skunk; 1 Blarina brevicauda Gray, 1838, shorttailed 

shrew; and 1 Urocyon cinereoargenteus 

Schreber, 1775, gray fox) from 5 states (Virginia, 

Arkansas, North Carolina, Ohio, and Florida) 

(Nickol, 1969; see Richardson and Nickol, 

1995). The largest number of worms previously 

reported from any individual mammalian host 

was 2 worms, whereas 1 raccoon in the current 

survey from the inland Horry County site (Site 

3) was infected with 9 C. conspectus (see Richardson 

and Nickol, 1995). Several owl species, 

including Bubo virginianus (Gmelin, 1788), the 

great horned owl; Otus asio (Linnaeus, 1758), 

the eastern screech owl; and Strix varia Barton, 

1799, the barred owl, have been reported as definitive 

hosts for C. conspectus (Richardson and 

Nickol, 1995). No intermediate host has been 

identified, although cystacanths of C. conspectus 

have been found in paratenic hosts (Nerodia sipedon 

(Linnaeus, 1758), the water snake, from 

North Carolina; Rana clamitans Latreille, 1801, 

the aquatic green frog, from Virginia; and Des- 



inognathus fuscus (Green, 1818), the northern 

dusky salamander and Plethodon glutinosus 

(Green, 1818), the slimy salamander from Louisiana) 

(Nickol, 1969; see Richardson and Nickol, 

1995). The finding of 11 immature C. conspectus 

in 3 South Carolina raccoons represents 

a new geographical record for this species. The 

collection only of immature C. conspectus from 

raccoons in this study supports earlier reports 

that suggested that wild mammals are aberrant 

hosts for this parasite (Richardson, 1993). 


The authors thank Osborne E. (Buddy) Baker 

III, SCDNR, for aid in procuring coastal raccoon 

specimens, and Dr. William C. Bridges, Jr., Department 

of Experimental Statistics, Clemson 

University, for assistance with statistical methods. 


Babero, B. B., and J. R. Shepperson. 1958. Some 

helminths of raccoons in Georgia. Journal of Parasitology 

44:519. 

Boschetti, A., and J. Kasznica. 1995. Visceral larva 

migrans induced eosinophilic cardiac pseudotumor: 

a cause of sudden death in a child. Journal 

of Forensic Sciences 40:1097-1099. 

Cole, R. A., and W. L. Shoop. 1987. Helminths of 

the raccoon (Procyon lotor) in western Kentucky. 


Dingley, D., and P. C. Beaver. 1985. Macracanthorhynchus 

ingens from a child in Texas. American 

Journal of Tropical Medicine and Hygiene 34: 

918-920. 

Harkema, R., and G. C. Miller. 1962. Helminths of 

Procyon lotor solutus from Cape Island, South 

Carolina. Journal of Parasitology 48:333-335. 

, and . 1964. Helminth parasites of the 

raccoon, Procyon lotor, in the southeastern United 

States. Journal of Parasitology 50:60-66. 

Jones, E. J., and B. S. McGinnes. 1983. Distribution 

of adult Baylisascaris procyonis in raccoons from 

Virginia. Journal of Parasitology 69:653. 

Kazacos, K. R., and W. M. Boyce. 1989. Baylisascaris 

larva migrans. Journal of the American Veterinary 

Medical Association 195:894-903. 

Kerr, C. L., S. C. Henke, and D. B. Pence. 1997 

Baylisascariasis in raccoons from southern coastal 

Texas. Journal of Wildlife Diseases 33:653-655. 

Lincoln, R. C., and R. C. Anderson. 1973. The relationship 

of Physaloptera maxillaris (Nematoda: 

Physalopteroidea) to skunk (Mephitis mephitis). 

Canadian Journal of Zoology 51:437-441. 

Miyazaki, I. 1960. On the genus Gnathostoma and 

human gnathostomiasis, with special reference to 

Japan. Experimental Parasitology 9:338-370. 

Morgan, B. B. 1941. A summary of Physalopterinae 

(Nematoda) of North America. Proceedings of the 

Helminthological Society of Washington 8:28-30. 

Nickol, B. B. 1969. Acanthocephala of Louisiana Caudata 

with notes on the life history of Centrorhynchus 

conspectus. American Midland Naturalist 81: 

262-265. 

Read, C. P. 1950. The rat as an experimental host of 

Centrorhynchus spinosus (Kaiser, 1893), with remarks 

on host specificity of the Acanthocephala. 

Transactions of the American Microscopical Society 

69:179-182. 

Richardson, D. J. 1993. Acanthocephala of the Virginia 

opossum (Didelphis virginiand) in Arkansas, 

with a note on the life history of Centrorhynchus 

wardae (Centrorhynchidae). Journal of the Helminthological 


, and B. B. Nickol. 1995. The genus Centrorhynchus 

(Acanthocephala) in North America 

with description of Centrorhynchus robustus n. 

sp., redescription of Centrorhynchus conspectus, 

and a key to species. Journal of Parasitology 81: 

737-772. 

Smith, R. A., M. L. Kennedy, and W. E. Wilhelm. 

1985. Helminth parasites of the raccoon (Procyon 

lotor) from Tennessee and Kentucky. Journal of 


Stansell, K. B. 1974. Internal parasites of coastal raccoons 

with notes on changes in parasite burdens 

after transportation and release in the upper Piedmont 

section of South Carolina. Statewide Wildlife 

Research Project, South Carolina Wildlife and 

Marine Resources Department, 112 pp. 

Williams, C. K., R. D. McKown, J. K. Veatch, and 

R. D. Applegate. 1997. Baylisascaris sp. found 

in a wild northern bobwhite (Colinus virginianus). 

Journal of Wildlife Diseases 33:158-160. 



66(2), 1999 pp. 115-122 

Nematode Parasites of Yellow Perch, Perca flavescens, from the 

Laurentian Great Lakes 

PATRICK M. MUZZALL 

Department of Zoology, Natural Science Building, Michigan State University, East Lansing, Michigan 48824 

U.S.A. (e-mail: muzzall@pilot.msu.edu) 

ABSTRACT: Yellow perch, Perca flavescens (Mitchill), from 4 localities in the Laurentian (North American) 

Great Lakes were examined for nematodes: from eastern Lake Michigan in 1990; from southern Lake Michigan 

in 1991; from The Black Hole, Saginaw Bay, Lake Huron in 1991; and from Oak Point, Saginaw Bay, Lake 

Huron in 1996. Dichelyne cotylophora (Ward and Magath) infected perch from each location and had the highest 

prevalence, mean intensity, and mean abundance at Oak Point. Eustrongylides tubifex (Nitzsch) Jagerskiold was 

a common parasite of perch from Saginaw Bay, but it infrequently infected Lake Michigan perch. Philometra 

cylindracea (Ward and Magath) Van Cleave and Mueller was found in perch only from Saginaw Bay. Contracaecum 

sp. infrequently infected perch from Lake Michigan and The Black Hole. A comparative summary of 

the literature on nematodes infecting yellow perch from the Great Lakes is presented, listing 27 studies published 

since 1917. Four nematode genera utilize perch as intermediate hosts, and 5 genera utilize them as definitive 

hosts. Information on the life cycles and pathology caused by nematodes infecting yellow perch is presented. 

KEY WORDS: Yellow perch, Perca flavescens, Percidae, Pisces, parasites, nematodes, Laurentian Great Lakes, 

Lake Michigan, Lake Huron, Saginaw Bay. 

Several nematodes have been reported from 

yellow perch, Perca flavescens (Mitchill, 1814) 

(Percidae), in the Laurentian (North American) 

Great Lakes. In recent years, federal and state 

fisheries personnel, aquaculturists, and anglers 

have asked me to identify nematodes infecting 

yellow perch from the Great Lakes and to answer 

questions about them. Declines in the catch 

rates of perch have been reported in southern 

Lake Michigan; Saginaw Bay, Lake Huron; and 

western Lake Erie (Francis et al., 1996). The 

present study reports on the occurrence of Dichelyne 

cotylophora (Ward and Magath, 1917); 

Eustrongylides tubifex (Nitzsch, 1819) Jagerskiold, 

1909; Philometra cylindracea (Ward and 

Magath, 1917) Van Cleave and Mueller, 1934; 

and Contracaecum sp. in yellow perch from 

Lake Michigan and Saginaw Bay, Lake Huron. 

A summary of the nematodes infecting yellow 

perch from the Great Lakes is presented, with 

accompanying information on their life cycles 

and pathology. The possible relationship between 

the decline of yellow perch populations 

in some areas of the Great Lakes and the occurrence 

of parasitic nematodes is also discussed. 


A total of 364 yellow perch was collected by beach 

seine and trawl from southern Lake Michigan (Michigan 

City, Indiana) in 1991; eastern Lake Michigan 

(Ludington, Michigan) in 1990; Saginaw Bay, Lake 

Huron (The Black Hole) in 1991; and Saginaw Bay, 

Lake Huron (Oak Point) in 1996. Ludington is approximately 

247 km north of Michigan City. Fish were 

sampled from the open water in Lake Michigan and 

also along the shore at Ludington. Saginaw Bay, a 

large shallow eutrophic bay divided into inner and outer 

areas, is the southwestern extension of Lake Huron 

located in east central Michigan. The inner area is shallower 

and warmer than the outer area, and is enriched 

with domestic, agricultural, and industrial inputs from 

the Saginaw River. The Black Hole in the Inner Saginaw 

Area and Oak Point in the Outer Saginaw Area 

are approximately 50 km apart. 

Perch were put on ice in the field, frozen at the 

laboratory, and measured and sexed at necropsy when 

the abdominal cavity, viscera, muscle, gastrointestinal 

tract, and head were examined. Dichelyne cotylophora, 

Eustrongylides tubifex, and Contracaecum sp. were 

preserved in 70% alcohol and later cleared in glycerin 

for identification. Philometra cylindracea were broken 

during necropsy and pieces were placed in glycerin on 

a glass slide, allowed to clear, and examined with a 

light microscope; specimens were not kept. Prevalence 

is the percentage of fish infected in each sample, mean 

intensity is the mean number of nematodes of a species 

per infected fish, and mean abundance is the mean 

number of worms per examined fish. Voucher specimens 

have been deposited in the United States National 

Parasite Collection (USNPC), Beltsville, Maryland 

20705: Dichelyne cotylophora (USNPC 88506) 

and Eustrongylides tubifex (USNPC 88507). 

Results 

Yellow perch from 2 locations in Lake Michigan 

and 2 locations in Saginaw Bay, Lake Huron, 

were examined for nematodes (Table 1). 

115 



Table 1. Number, collection time, and mean total length (mm) of Perca flavescens examined from Lake 

Michigan and Saginaw Bay, Lake Huron. 

Location 

Month(s), year 

Mean total length 

± SD (range, 95% 

confidence interval) 

Michigan City, Indiana, southern Lake Michigan (100)* August 1991 

Ludington, Michigan, eastern Lake Michigan (64)* May-September 1990 

The Black Hole, inner Saginaw Bay, Lake Huron, Michigan September 1991 

(100)* 

Oak Point, outer Saginaw Bay, Lake Huron, Michigan (100)* August 1996 

154 ± 67(50-280, 141-168) 

136 ± 23(105-177, 131-142) 

172 ± 36(110-278, 164-178) 

202 ± 23(170-287,197-206) 

* (Number of yellow perch examined.) 

There was a significant difference in the lengths 

of perch between locations (analysis of variance, 

F = 35.9, P < 0.0001) with those from Oak 

Point being larger. Forty-eight percent (48) of 

yellow perch from Michigan City in 1991, 26% 

(17) from Ludington in 1990, 96% (96) from 

The Black Hole in 1991, and 98% (98) from 

Oak Point in 1996 were infected with 1 or more 

nematodes. 

Gravid Dichelyne cotylophora infected the intestines 

of yellow perch from each location (Table 

2). It was significantly more prevalent in 

perch from Michigan City than from Ludington, 

Michigan (chi-square, x2 = 26.6, P < 0.005); 

intensities were not significantly different, but 

abundances were (Mann-Whitney test, U = 

9,187, P < 0.0001). In Saginaw Bay, prevalence 

(chi-square, x2 = 128.6, P < 0.005) and abundance 

(Mann-Whitney test, U = 6,064, P < 

0.0001) of D. cotylophora were significantly 

higher in perch from Oak Point than from The 

Black Hole. Contracaecum sp. infrequently occurred 

encysted on the surface of the heart, in 

the liver, and associated with the mesentery of 

perch from Lake Michigan and The Black Hole. 

Eustrongylides tubifex was most common in 

perch from Saginaw Bay. The intensity (Mann- 

Whitney test, U = 9,773, P < 0.0001) and abundance 

(Mann-Whitney test, U = 12,798, P < 

0.0001) of E. tubifex were significantly higher 

in perch from The Black Hole than from Oak 

Point. Larvae occurred in capsules associated 

with the mesentery on the surface of the ovaries, 

testes, liver, spleen, and gastrointestinal tract and 

free in the body cavity, viscera, and muscle. Of 

the 303 E. tubifex found in perch from Oak Point 

in 1996, 92% of the worms or capsules with 

worms were seen with the unaided eye, whereas 

8% were detected only with a dissecting microscope. 

Small and large E. tubifex were found in 

perch from both Saginaw Bay locations. 

Philometra cylindracea, some of which were 

larvigerous, occurred free in the body cavity of 

perch only from Saginaw Bay, and was most 

common at Oak Point. Remains of crenulated 

and hardened masses of nematodes, probably 

dead P. cylindracea from past infections, were 

found in the body cavities and viscera of yellow 

perch from The Black Hole and Oak Point. All 

perch from Saginaw Bay in 1991 and 69% of 

them in 1996 that were infected with P. cylindracea 

were concurrently infected with E. tubifex. 

Ninety-six percent of Oak Point perch harbored 

at least 1 E. tubifex or P. cylindracea or 

remains of dead P. cylindracea. 

There were no significant differences in the 

prevalence (chi-square analysis, P > 0.05) and 

intensity or abundance (Mann-Whitney test, P 

> 0.05) of D. cotylophora, E. tubifex, P. cylindracea, 

and Contracaecum sp. between female 

and male perch at any location. There were no 

significant correlations between the intensities of 

each nematode species and host length. 

Discussion 

At least 27 studies mentioning the nematode 

parasites of yellow perch from the Great Lakes 

have been published since 1917. The number of 

studies (in parentheses) performed in each Great 

Lake and associated connecting waters are: Lake 

Michigan (5), Lake Superior (1), St. Marys River 

(1), Lake Huron (7), Lake St. Clair (1), Lake 

Erie (12), and Lake Ontario (3) (Table 3). Many 

of these investigations did not report the number, 

length, and age of perch. Rosinski et al. (1997) 

reported that the nematode fauna of yellow 

perch in Saginaw Bay, Lake Huron, and Lake 

Huron proper are similar. 


MUZZALL—NEMATODES OF YELLOW PERCH 17 

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A total of 15 nematode taxa has been reported 

from yellow perch in the Great Lakes (Table 3). 

Of these, Agamonema sp., Contracaecum sp., E. 

tubifex, Eustrongylides sp., Hysterothylacium 

brachyurum (Ward and Magath, 1917) Van 

Cleave and Mueller, 1934, Raphidascaris acus 

(Bloch, 1779) Railliet and Henry, 1915, and Raphidascaris 

sp. are represented by larval or immature 

stages. Of the 10 nematodes identified to 

species, 6 mature in the intestine of perch. Prevalence 

data from the literature indicate that D. 

cotylophora is the most common nematode infecting 

perch from Lake Michigan, R. acus is 

most common in Lake Superior perch, and D. 

cotylophora and E. tubifex are most common in 

perch from Lakes Huron and Erie. The nematodes 

of perch from Lake Ontario have prevalences 

of 8% or less. The report of Bangham and 

Hunter (1939) of Agamonema sp. from perch in 

Lake Erie refers to an unidentified larval form, 

an immature nematode (J. Crites, pers. comm.), 

and will not be considered further. 

In the present study, Contracaecum sp. is reported 

for the first time from perch in Lakes 

Michigan and Huron; all other nematodes found 

have been reported infecting perch from these 

lakes. Four nematode taxa were found in perch 

in the present study compared to the 15 nematode 

taxa reported in the literature. There are 

several possible reasons for this, including 1) I 

only examined perch from 2 Lake Michigan locations 

and Saginaw Bay, 2) more parasitological 

studies have been done on perch in Lakes 

Erie and Huron, and 3) it is difficult to determine 

if fish were collected from different habitats. It 

is pointless to discuss whether some nematodes 

of yellow perch have disappeared in the Great 

Lakes, because so few studies have been done 

in the past to which I can compare this study. 

Dichelyne cotylophora infects yellow perch 

from all the Great Lakes and is commonly found 

in the anterior intestine. Visible lesions were not 

observed at the sites of adult attachment. I have 

found worms up to 8 mm in length. Based on 

experimental evidence, Baker (1984b) suggested 

that prey fish (cyprinid minnows) are intermediate 

hosts for D. cotylophora. This parasite is 

not host-specific to perch, since it has been reported 

from several fish species in Lake Michigan, 

St. Marys River, Lake Huron, Lake St. 

Clair, Lake Erie, and Lake Ontario (Ward and 

Magath, 1917; Pearse, 1924; Bangham, 1933, 

1955; Bangham and Hunter, 1939; Muzzall, 



Table 3. Reported nematodes of Perca flavescens from the Laurentian Great Lakes. 

Species 

Lake* 

Prevalencet 

Locality 

Reference 

Agamonema sp.± 

E 

2(2/128) 

OH 

Bangham and Hunter, 1939 

Contracaecum sp.i 

M 

H 

3 (3/100) 

8 (5/640) 

4 (4/100) 

IN 

MI 

MI 

Michigan City, this study 

Ludington, this study 

The Black Hole, this study 

Camallanus oxycephalus 

H 

E 

— § 

2(1/45) 

5 (5/93) 

— S 

6 (45/735) 

7 (27/408) 

MI 

OH, ONT 

OH 

OH 

OH 

ONT 

Rosinski et al., 1997 


Bangham, 1972 

Stromberg and Crites, 1972 

Cooper et al., 1977 

Dechtiar and Nepszy, 1988 

Dichelync cotylophora 

Eustrongylid.es tubifex'j. 

Eustrongylides sp . ± 

Hysterothylacium brachyiintm^ 

Philometra cylindracea 

M 

S 

SMR 

H 

LSC 

E 

0 

M 

H 

E 

E 

0 

E 

S 

E 

O 

H 

—8 

9(1/11) 

47 (47/100) 

19(12/64) 

42(10/24) 

33 (24/73) 

— § 

55(110/201) 

2(3/134) 

— § 

4(4/100) 

68 (68/100) 

— § 

— S 

65 (45/69) 

10 (76/735) 

— § 

50(6/12)|| 

6 (25/408) 

— § 

— S 

5 (7/150) 

2 (4/374) 

3 (3/100) 

35(293/831) 

2(3/134) 

80(193/240) 

95 (95/100) 

74 (74/100) 

38 (19/50) 

41 (304/735) 

—5 

— § 

50 (204/408) 

8(5/150) 

8 (8/98) 

33 (8/24) 

4(16/408) 

8(5/150) 

1 (2/201) 

4(5/134) 

— § 

24 (57/240) 

10(10/100) 

16(16/100) 

WI 

WI, IL 

IN 

MI 

ONT 

MI 

ONT 

ONT 

ONT 

MI 

MI 

MI 

— 

ONT 

OH, ONT, 

NY, PA 

OH 

ONT 

ONT 

ONT 

ONT 

ONT 

ONT 

MI 

IN 

MI 

ONT 

MI 

MI 

MI 

OH 

OH 

OH 

OH 

ONT 

ONT 

OH 

ONT 

ONT 

ONT 

ONT 

ONT 

MI 

MI 

MI 

MI 

Pearse, 1924 

Amin, 1977 


Ludington, this study 

Dechtiar and Lawrie, 1988 

Muz/.all, 1984 

Smedley, 1934 

Bangham, 1955 

Dechtiar et al., 1988 



Oak Point, this study 

Ward and Magath, 1917 

Smedley, 1934 



Baker, 1984a 

Baker, 1984b 


Tedla and Fernando, 1 969 

Tedla and Fernando, 1970 

Dechtiar and Christie, 1988 

Allison, 1966 


Allison, 1966 





Measures, 1988b 



Crites, 1982 



Bangham, 1972 




Bangham, 1955 


Salz, 1989 






Table 3. Continued. 

Species 

Lake* 

Prevalencet 

Locality 

Reference 

Raphidascaris acus$ 

Raphidascaris sp.t 

Rhabdochona canadensis 

Moravec and Aral, 1971 

Rhabdochona ovtfikanenta 

Weller, 1938 

Spinitectux carolini Roll, 

1928 

E 

0 

S 

11 

E 

M 

S 

E 

S 

1 (1/128) 

8 (62/735) 

— § 

10(40/408) 

5(8/150) 

63(15/24) 

2(3/134) 

— § 

8 (32/408) 

1 (1/136) 

8 (2/24) 

9 (6/69) 

8 (2/24) 

OH, ONT 

OH 

OH 

ONT 

ONT 

ONT 

ONT 

Spinitectus gracilis Ward 0 

1 (2/150) ONT 


and Magath, 1917 

Spinitectus sp. 5 (5/98) OH Bangham, 1972 

* E, Lake Erie; M, Lake Michigan; H, Lake Huron; S, Lake Superior; 

Ontario. 

t Percent infected (number of fish infected/number of fish examined). 

± Larval stage. 

S Parasite present but prevalence not given. 

|| Prevalence calculated from winter 1984 sample. 

MI 

ONT 

MI 

ONT 

OH 

ONT 



Crites, 1982 







Weller, 1938 


Jilek and Crites, 1981 


SMR, St. Marys River; LSC, Lake St. Clair; O, Lake 

1984; Dechtiar and Christie, 1988). Cooper et 

al. (1977) demonstrated that the prevalence of 

D. cotylophora in perch in the western basin of 

Lake Erie decreased from 1927-1929, to 1957, 

to 1974. 

Rhabdochona spp. and Spinitectus spp. infrequently 

occur in yellow perch from Lakes Michigan, 

Superior, and Erie, and Lakes Superior, 

Erie, and Ontario, respectively. Both genera are 

found in the intestine of several fish species and 

do little or no damage to their hosts. They utilize 

mayfly larvae and other arthropods as intermediate 

hosts. 

Species not found as adults in the intestine of 

yellow perch are: H. brachyurum, R. acus, Raphidascaris 

sp., Contracaecum sp., P. cylindracea, 

E. tubifex, and Eustrongylides sp. Larval H. 

brachyurum have been reported in perch from 3 

of the Great Lakes. Dechtiar and Lawrie (1988) 

found H. brachyurum and R. acus larvae in the 

liver of perch from Lake Superior and suggested 

that moderate to heavy liver damage occurred 

with iibrosis. Similarly, encysted H. brachyurum 

caused liver damage to perch in Lake Ontario 

(Dechtiar and Christie, 1988). Piscivorous fishes 

serve as definitive hosts for H. brachyurum and 

Raphidascaris spp. Contracaecum spp. mature 

in piscivorous birds and mammals. 

The redworm nematode complex of yellow 

perch in the Great Lakes is composed of Camallanus 

oxycephalus, P. cylindracea, and E. tubifex. 

The term "redworm" was coined by anglers 

asking the question, "What are these red 

worms in my fish?" (J. Crites, pers. comm.). Camallanus 

oxycephalus has been reported from 

yellow perch in 2 of the Great Lakes. Stromberg 

and Crites (1974) found that during July and August 

in Lake Erie, female C. oxycephalus protrude 

from the anus of white bass, Morone chrysops, 

and rupture, releasing infective larvae that 

are ingested by copepods. The life cycle is completed 

when infected copepods or small paratenic 

forage fish hosts are eaten by larger fish. Cooper 

et al. (1977) found that the prevalence of C. 

oxycephalus in yellow perch in western Lake 

Erie increased from 1927-1929, to 1957, to 

1974. 

In the present study, P. cylindracea only occurred 

in yellow perch from Saginaw Bay. Copepods 

are intermediate hosts for P. cylindracea 

(see Molnar and Fernando, 1975; Crites, 1982). 

It is not known if P. cylindracea utilizes a trans- 



port host in its life cycle. Philometra cylindracea 

has been found in perch from 3 of the Great 

Lakes, occurring unencysted in the body cavity. 

This nematode matures in, and is host-specific 

to, yellow perch, since it has been reported from 

no other fish species. Mature females are about 

the same length as males (4 mm) or longer. Larvigerous 

females, which are delicate and have a 

thin transparent cuticle, may exceed 100 mm in 

length and are easily broken during host necropsy. 

Eustrongylides tubifex had significantly higher 

prevalences, mean intensities, and mean abundances 

in yellow perch from Saginaw Bay than 

in those from Lake Michigan. Karmanova 

(1968) and Measures (1988a, b) reported that 

tubificid oligochaetes serve as intermediate hosts 

for E. tubifex. Although Brinkhurst (1967) and 

Schneider et al. (1969) found large numbers of 

tubificids in Saginaw Bay, Haas and Schaeffer 

(1992) did not find tubificids in perch stomachs 

in Saginaw Bay, and Rosinski et al. (1997) 

found them to be infrequent. The lack of tubificids 

in stomachs is surprising, since perch from 

Saginaw Bay and other areas of Lake Huron are 

heavily infected. Tubificids have been found in 

the stomachs of yellow perch from Lake Erie (J. 

Crites, pers. comm.), another lake where E. tubifex 

commonly occurs. The difference in infection 

values of E. tubifex between Saginaw Bay 

and Lake Michigan may be explained by the 

large number of tubificids in the bay and by the 

small numbers of them in Lake Michigan. Piscivorous 

birds (e.g., mergansers, Mergus merganser 

Linnaeus, 1758; see Measures, 1988c) 

serve as definitive hosts for E. tubifex, and differences 

in their numbers between these locations 

may also play a role in this difference. 

Eustrongylides tubifex has been reported from 

yellow perch in 4 of the Great Lakes. It is infrequent 

in Lake Michigan, and the small number 

of perch examined from Lake Superior may 

not reflect its absence. Allison (1966) reported 

perch from the Detroit River infected with E. 

tubifex. Dechtiar and Christie (1988) found E. 

tubifex in several fish species from Lake Ontario 

and suggested that it caused damage to perch. 

This nematode is very common in yellow perch 

from Lake Erie. Interestingly, Bangham and 

Hunter (1939) did not report E. tubifex in an 

extensive survey of parasites of Lake Erie fishes, 

including 128 yellow perch. Bangham (1972) 

was the first to report the occurrence of E. tubifex 

in yellow perch collected in 1957 from 

Lake Erie. 

Eustrongylides tubifex is pink to red in color 

and thicker than P. cylindracea. Larval E. tubifex 

in fish intermediate hosts can reach 10 cm in 

length. Cooper et al. (1978) and Crites (1982) 

demonstrated experimentally that E. tubifex can 

be transferred when a small infected fish is eaten 

by a larger one. Crites (1982) reported that E. 

tubifex can live in capsules of host origin for at 

least 1.5 yr and demonstrated that the walls of 

the capsule have several different tissues and are 

furnished with capillaries. The larvae are nourished 

during their development and growth in 

these capsules. Measures (1988b) reported on 

the pathology of E. tubifex in fishes, including 

the yellow perch. It appears that E. tubifex infections 

in perch do not give rise to immunity, 

since larvae of different lengths were found in 

the same perch in the present study. 

Crites (1982) showed that E. tubifex and P. 

cylindracea were associated with weight loss in 

yellow perch. It is not known if this weight loss 

affected fecundity. In addition, P. cylindracea 

sometimes infected the ovaries of perch, but 

whether this impairs reproductive capacity was 

not determined. Allison (1966) and Salz (1989) 

suggested these E. tubifex and P. cylindracea 

play a role in reduced perch growth and high 

mortality. 

Excluding the Salmoniformes, percids are 

probably the most important group of fishes in 

the Great Lakes. Based on a review of the literature 

and the present study, it appears that 

nematodes do not greatly harm yellow perch, except 

for E. tubifex and P. cylindracea, which 

commonly infect perch in Saginaw Bay, other 

areas of Lake Huron, and Lake Erie (Allison, 

1966; Crites, 1982; Salz, 1989; Rosinski et al., 

1997). These are Great Lakes areas where the 

catch rates of perch have declined (Francis et al., 

1996), but the direct effects of E. tubifex and P. 

cylindracea on reducing the numbers of perch 

in these areas are not known. 


I thank Dan Brazo, Indiana Department of 

Natural Resources, Michigan City, Indiana; Tom 

McComish, Ball State University, Muncie, Indiana; 

Rob Elliott and Doug Peterson, Michigan 

State University, East Lansing, Michigan; and 

Bob Haas, Jack Hodge, Dave Fielder, and Larry 

Shubel, Michigan Department of Natural Re- 



sources, Mt. Clemens and Alpena, Michigan, for 

providing the yellow perch; Bernadette Hermann 

for technical assistance in 1996; and John 

Crites for reviewing an early draft of the manuscript 

and sharing information on the nematodes 

of yellow perch in the Great Lakes. 


Allison, L. N. 1966. The redworm (Philometra cylindraced) 

of yellow perch (ferca flavescens) in 

Michigan waters of the Great Lakes. Michigan 

Department of Conservation Research and Development 

Report 53, Institute for Fisheries Report 

1712. 8 pp. 

Amin, O. M. 1977. Helminth parasites of some southwestern 

Lake Michigan fishes. Proceedings of the 

Helminthological Society of Washington 44:210— 

217. 

Baker, M. R. 1984a. Redescription of Dichelyne (Cucullanellus) 

cotylophora (Ward and Magath, 

1917) (Nematoda: Cucullanidae) parasitic in 

freshwater fishes of eastern North America. Canadian 

Journal of Zoology 62:2053—2061. 

. 1984b. On the biology of Dichelyne (Cucullanellus) 

cotylophora (Ward and Magath, 1917) 

(Nematoda: Cucullanidae) in perch (Perca flavescens) 

from Lake Erie, Ontario. Canadian Journal 

of Zoology 62:2062-2073. 

Bangham, R. V. 1933. Parasites of the spotted bass, 

Micropterus pseudoalplites Hubbs, and summary 

of parasites of smallmouth and largemouth bass 

from Ohio streams. Transactions of the American 

Fisheries Society 63:220-227. 

. 1955. Studies on fish parasites of Lake Huron 

and Manitoulin Island. American Midland Naturalist 

53:184-194. 

. 1972. A resurvey of the fish parasites of western 

Lake Erie. Bulletin of the Ohio Biological 

Survey 4:1-23. 

-, and G. W. Hunter III. 1939. Studies on fish 

parasites of Lake Erie. Distribution studies. Zoologica 

24:385-448. 

Brinkhurst, R. O. 1967. The distribution of aquatic 

oligochaetes in Saginaw Bay, Lake Huron. Limnology 

and Oceanography 12:137-143. 

Cooper, C. L., R. R. Ashmead, and J. L. Crites. 

1977. Prevalence of certain endoparasitic helminths 

of the yellow perch from western Lake 

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, J. L. Crites, and D. J. Sprinkle-Fastkie. 

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64:102-107. 

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Eiistrongylides tubifex on yellow perch in Lake 

Erie. U.S. Department of Commerce Commercial 

Fisheries Research and Developmental Project. 3- 

298-D. Clear Technical Report 258. 84 pp. 

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the parasite fauna of Lake Ontario fishes, 1961- 

1971. Great Lakes Fisheries Commission, Technical 

Report 51:66-106. 

, J. J. Collins, and J. A. Reckahn. 1988. Survey 

of the parasite fauna of Lake Huron fishes, 

1961-1971. Great Lakes Fisheries Commission, 

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fauna of Lake Superior fishes, 1969-1975. 

Great Lakes Fisheries Commission, Technical Report 

51:1-18. 

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fauna of selected fish species from Lake Erie, 

1970-1975. Great Lakes Fisheries Commission, 

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a multi-jurisdictional challenge. Fisheries 21: 

18-20. 

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and competitive interactions among walleye, yellow 

perch, and other forage fishes in Saginaw 

Bay, Lake Huron. Michigan Department of Natural 

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carolini Holl, 1928, and Spinitectus gracilis 

Ward and Magath, 1916 (Spirurida: Nematoda) 

in fishes from Lake Erie. Canadian Journal of 

Zoology 59:141-142. 

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and Man and Diseases Caused by Them. Fundamentals 

of Nematology. Vol. 20. Academy of Science 

of the USSR. Translated and published for 

U.S. Department of Agriculture. Amerind Publishing, 

New Delhi, 1985. 383 pp. 

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tubifex (Nematoda: Dioctophymatoidea) in 

oligochaetes. Journal of Parasitology 74:296-304. 

. 1988b. Epizootiology, pathology, and description 

of Eustrongylides tubifex (Nematoda: Dioctophymatoidea) 

in fish. Canadian Journal of Zoology 

68:2212-2222. 

. 1988c. The development and pathogenesis of 

Eustrongylides tubifex (Nematoda: Dioctophymatoidea) 

in piscivorous birds. Canadian Journal of 

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cylindracea (Philometridae). Journal of the Helminthological 


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of yellow perch from Saginaw Bay, Lake 


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fauna in Saginaw Bay, Lake Huron. Proceedings Quinte, Lake Ontario. Journal of the Fisheries Reof 

the 12th Conference of Great Lakes Research search Board of Canada 26:833-843. 

1969:80-90. , and . 1970. On the characterization of 

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nematode Dichelyne bullocki sp. n. (Cucullanidae) Notes on some nematodes from freshwater fishes, 

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66(2), 1999 pp. 123-132 

A Taxonomic Reconsideration of the Genus Plagiorhynchus s. lat. 

(Acanthocephala: Plagiorhynchidae), with Descriptions of South 

African Plagiorhynchus (Prosthorhynchus) cylindraceus from Shore 

Birds and P. (P.) malayensis, and a Key to the Species of the 

Subgenus Prosthorhynchus 

OMAR M. AMIN,M ALBERT G. CANARis,2 AND J. MICHAEL KINSELLAS 

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

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

2 P.O. Box 1479, Hamilton, Montana 59840-1479 U.S.A. (e-mail: acanaris@bitterroot.net), and 

3 2108 Hilda Avenue, Missoula, Montana 59801 U.S.A. (e-mail: wormdwb@aol.com) 

ABSTRACT: A population of Plagiorhynchus (Prosthorhynchus) cylindraceus (Goeze) Schmidt and Kuntz is 

described from 4 species of shore birds in South Africa. Specimens of 3 supposed synonyms of P. (P.) cylindraceus, 

namely P. (P.) formosus Van Cleave, P. (P.) taiwanensis Schmidt and Kuntz, and P. (P.) transversus 

(Rudolphi) Travassos, were studied and this synonymy was verified. The taxonomic status of Plagiorhynchus s. 

str. and of Prosthorhynchus was reconsidered, and both were retained as subgenera. Females of Plagiorhynchus 

(Prosthorhynchus) malayensis (Tubangui) Schmidt and Kuntz (nee malayense) are described for the first time; 

males are redescribed. A key to species of the subgenus Prosthorhynchus is provided. 

KEY WORDS: Acanthocephala, Plagiorhynchus (Prosthorhynchus) cylindraceus, description, South Africa, 

shore birds, Aves, subgenera Plagiorhynchus s. str. and Prosthorhynchus, Plagiorhynchus (Prosthorhynchus) 

malayensis, taxonomic key. 

A collection of acanthocephalans was made 

by one of us (A.G.C.) from 7 species of shore 

birds in South Africa in 1981. All 7 species 

yielded a new centrorhynchid acanthocephalan, 

Neolacunisoma geraldschmidti Amin and Canaris, 

1997. Additionally, 5 of these 7 host species 

harbored 2 species of plagiorhynchid acanthocephalans. 

One unidentified species of Plagiorhynchus 

infected 1 host species, and the other 4 host species 

were infected with Plagiorhynchus (Prosthorhynchus) 

cylindraceus (Goeze, 1782) 

Schmidt and Kuntz, 1966. The study of the latter 

species, a number of its synonyms, and various 

plagiorhynchid species prompted reconsideration 

of the generic-subgeneric status of Plagiorhynchus 

and Prosthorhynchus and the construction 

of a key to species of the latter subgenus. 

Among the acanthocephalans borrowed for this 

study were a few specimens of Plagiorhynchus 

(Prosthorhynchus) malayensis (Tubangui, 1935) 

Schmidt and Kuntz, 1966 (nee malayense), that 

were sufficiently informative to describe females 

for the first time and redescribe males. This paper 

reports on these findings. 



Twenty-eight individuals (12 males and 16 females) 

of P. (P.) cylindraceus were recovered from 4 species 

of shore birds (Charadriiformes) collected by one of 

us (A.G.C.) from the Berg River, Cape Province, South 

Africa, between 24 May and 31 July 1981. The host 

species were the curlew sandpiper (Calidris ferruginea 

(Pontoppidan, 1763), 1 individual infected with 25 

acanthocephalans); Kittlitz' plover (Charadrius pecuarius 

(Temminck, 1823), 1 of 4 individuals infected 

with 1 acanthocephalan); triple-banded plover (Charadrius 

tricollaris (Vieillot, 1818), 1 of 5 individuals 

infected with 1 acanthocephalan); and blacksmith plover 

(Holopterus armatus (Burchell, 1822), 1 of 7 individuals 

infected with 1 acanthocephalan). In addition, 

26 unidentifiable plagiorhynchid acanthocephalans 

were collected by A.G.C. from 2 white-fronted 

sand plovers (Charadrius marginatus Vieillot, 1818) 

and 10 uninformative plagiorhynchid acanthocephalans 

from the stilt (Himantopus hirnantopus (Linnaeus, 

1758)), H. armatus, Charadrius pallidus Strickland, 

1852, and C. pecuarius. These unidentified specimens 

are in the collection of M. Kinsella, Missoula, Montana. 

Specimens were processed by the late Gerald D. 

Schmidt. We do not know the processing method used. 

Measurements, made using an ocular micrometer and 

conversion table, are in micrometers unless otherwise 

stated. Width measurements refer to maximum width. 

Most specimens were deposited in the United States 

National Parasite Collection (USNPC), Beltsville, 

Maryland, and a few were retained in the collection of 

the first author (O.M.A.). A few study specimens were 

123 



loaned from USNPC, but most were from the Harold 

W. Manter Laboratory Collection (HWMLC), University 

of Nebraska State Museum, Lincoln, Nebraska. 

We report the results of examination of the specimens 

collected from the South African shore birds. 

Results and Discussion 

Plagiorhynchus (Plagiorhynchus} sp. 

The 26 specimens of Plagiorhynchus (Plagiorhynchus) 

sp. collected from C. marginatus 

were slender, with the proboscis wider near its 

middle, long lemnisci and uterus, a near-terminal 

female gonopore, elliptical eggs with polar prolongation 

of the fertilization membrane, and cement 

glands of unequal length and altogether 

about as long as the 2 testes. The specimens 

were not sufficiently informative to make a specific 

designation. 

Plagiorhynchus (Prosthorhynchus) 

cylindraceus (Goeze, 1782) Schmidt and 

Kuntz, 1966 

Except for 1 female in the ovarian ball stage, 

all 13 other female and 11 male P. (P.) cylindraceus 

collected from the single curlew sandpiper 

examined were sexually mature adults 

with ripe eggs and sperm, respectively. Of the 

other 3 host species examined, 1 individual of 

each was infected with 1 immature female. The 

curlew sandpiper appears to be the natural host 

of P. (P.) cylindraceus in South Africa. 

Our South African specimens were diagnosed 

as P. (P.) cylindraceus based on their close similarities 

with that species and taxa now synonymized 

with it, as listed in Amin (1985) and 

compared herein (Table 1). Measurements of the 

1 available female Plagiorynchus (Prosthorhynchus) 

transversus (Rudolphi, 1819) Travassos, 

1926, the other supposed synonym (USNPC 

#65269) agreed with those listed in the table. 

Some of the specimens examined, and particularly 

European P. (P.) cylindraceus, however, 

appeared less robust and more slender, and females 

as long as 40 mm were reported (Golvan, 

1956, Fig. 1). Another difference was related to 

the roots of the middle proboscis hooks, which 

were longer than the blades in European P. (P.) 

cylindraceus (see Golvan, 1956, pi. 1A). This 

was also observed in some but not all P. (P.) 

cylindraceus from Long Island, New York, and 

New Hampshire, U.S.A. (HWMLC 33444- 

33452), but not in specimens from Israel 

(HWMLC 34871). Golvan's specimens reached 

lengths of 15 mm in males and 40 mm in females 

and had as many as 24 longitudinal rows 

of proboscis hooks. In all other respects, the synonymy 

of P. (P.) cylindraceus, P. (P.) transversus, 

Plagiorhynchus (Prosthorhynchus) formosus 

Van Cleave, 1918, and Plagiorhynchus 

(Prosthorhynchus) taiwanensis Schmidt and 

Kuntz, 1966, was upheld. 

Description of South African Plagiorhynchus 

(Prosthorhynchus) cylindraceus 

GENERAL: Specimens robust and bluntly 

pointed, females not much longer but more 

plump than males. Subdermal nuclei discoidal, 

in shallow ameboid branched interconnected 

vesicles, appearing rod-shaped in profile, with 

vertical orientation at almost regular intervals 

from anterior end of trunk to short distance from 

posterior end. Secondary lacunar vessels transverse 

throughout trunk. Proboscis hooks in 

straight longitudinal rows, without dorsoventral 

or any other differentiation. Blades generally 

similar in length, but becoming slightly shorter 

abruptly anteriorly and more gradually posteriorly 

(Table 1). Hook roots simple, posteriorly 

directed, and usually about as long as or slightly 

shorter than blades. Posterior 2 hooks of each 

row spiniform, second to last hook with short 

root which may be further reduced to large 

knob; last hook rootless and invariably with 

small knob instead. Lemnisci long and slender, 

much longer than proboscis receptacle, nucleated, 

subequal, sometimes branched or multiple, 

may extend past posterior end of posterior testis. 

Testes ovoid, contiguous, usually in anterior half 

of trunk. Four cement glands in 2 sets of 2 each, 

originating at various levels beginning anteriorly 

near posterior end of posterior testis. Four separate 

cement gland ducts originating anteriorly 

at level of anterior end of Saefttigen's pouch and 

joining pouch at its posterior end. Gonopore 

near-terminal in adult males but distinctly subterminal 

in adult females, vagina usually curved 

anteriad in a 90 degree angle. Ripe eggs mostly 

elliptical with concentric shell and no polar prolongation 

of fertilization membrane. Fertilization 

membrane of a few eggs in gravid females (5— 

15%) may exhibit unipolar or, less frequently, 

bipolar prolongation. 

SPECIMENS DEPOSITED: USNPC 88031 (10 

males and 10 females on 10 slides from Calidris 

ferruginea in the Berg River, Cape Province, 

South Africa). 


Table 1. Comparison between the South African Plagiorhynchus (Prosthorhynchus) cylindraceus and 

paper) in selected diagnostic characteristics. 

South Africa, 

this paper 

(n = 23) 

P. cylindraceus 

Golvan, 

1956 

(n = ?) 

This paper 

(n = 20) 

P. formosus 

Van Cleave, 1918, 1942; 

Schmidt and Olsen, 

1964 (n = ?) 

This pape 

(n = 20) 

Trunk (mm) 

Males 

Females 

7.79-0.15 

8.97-11.06 

X 1.67-1.88 

X 2.06-2.55 

Proboscis (mm) 

Males 1.15-1.21 X 0.21-0.24 

Females 1.24-1.39 X 0.24-0.27 

Proboscis hooks 

Rows (no.) 14-17 

10-15 X 

20-40 X 

14-20, up 

to 24 

Hooks/row 15-18 10-18 

Proboscis hooks (mean length from anterior) 

M(ll)* 59 62 64 68 68 71 70 71 69 72 71 69 68 62 59 56 53 Eggs 64-78 F(12)* 56 66 69 69 69 73 75 76 76 73 73 73 69 66 62 60 60 X 25-28 M 

NGt 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

80 X 

F 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

NG 

30 

4.545-10.45 

5.15-12.12 

X 0.61-1.82 

X 0.45-2.818 

0.88-1.03 X 0.24-0.33 

0.97-1.15 x 0.27-0.33 

M(8) 

53 

66 

67 

66 

70 

70 

69 

74 

71 

67 

71 

71 

66 

66 

56 

— 

— 

42-70 X 

16-17 

13-15 

F(12) 

55 

67 

66 

72 

73 

79 

79 

78 

82 

80 

75 

72 

64 

63 

61 

— 

— 

12-34 

8-13 X 1.5-2.5 

9-15 X 2-3 

0.80-1.10 X 0.25-0.33 

0.80-1.10 X 0.25-0.33 

V.C. 

71 

77 

83 

83 

83 

83 

83 

83 

83 

77 

77 

77 

65 

— 

— 

— 

— 

40-75+ 

15-18 

11-15 

S.&O. 

60 

79 

79 

79 

79 

79 

79 

79 

79 

79 

79 

79 

79 

60 

60 

— 

— 

X 18-30+ 

5.61-12.42 

8.03-13.32 

X 1.2 

X 1.3 

0.94-1.12 X 0.2 

1.00-1.21 X 0. 

M(10) 

56 

56 

62 

70 

72 

73 

77 

77 

75 

73 

75 

69 

66 

63 

60 

— 

— 

56-73 

13-17 

13-15 

F 

X 25- 

* Numbers in parentheses indicate the numbers of specimens used for determination. 

t ?, Number of specimens examined not given. 

± NG, not given. 



Figures 1-8. Species of Plagiorhynchus (Prosthorhynchus) and /*. (Plagiorhynchus). 1-5. Plagiorhynchus 

(Prosthorhynchus) inalayensis, female. 1. Lateral view of whole specimen. 2. Posterior end and reproductive 

system. 3. Egg from the body cavity. 4. Proboscis. 5. Proboscis hook numbers 1, 4, 8, 13, 18, 20 of 1 row. 

6. Plagiorhynchus (Prosthorhynchus) bullocki, egg from the body cavity of a gravid female. 7, 8. Plagiorhynchus 

(Plagiorhynchus) paulus. 7. Egg from the body cavity of a gravid female. 8. Posterior end and 

reproductive system of a female, showing the subterminal position of the gonopore. 

SPECIMENS EXAMINED: P. (P.) cylindraceus 

adults: HWMLC 33443-33449, 33451, 35658, 

36785 (Nebraska, New Hampshire, New York, 

U.S.A.); 34871, 34882 (Israel). P. (P.)formosus 

adults: USNPC 4598 (syntypes), 60023; 

HWMLC 30539, 30978, 30983, 30987, 31037, 

33877, 33938-33941, 34480, 34652, 35005 

(Colorado, Oregon, and Kansas, U.S.A.), many 

slides of larvae from various intermediate hosts. 

HWMLC 30975, 30978, 30983, 30987, 31037, 

31037, 31061 labeled "Plagiorhynchus formosus 

ex. Sturnus vulgaris, intestine; Kansas" 


AMIN ET AL.—PLAGIORHYNCHUS IN SOUTH AFRICA AND REVIEW 127 

were clearly misidentified and placed in the 

wrong genus as judged by their thin body form 

and small size, proboscis size and armature, and 

eggs; some had spiny trunks. P. (P.) taiwanensis 

adults: USNPC 60718 (paratypes). HWMLC 

34124-34126 (paratypes). P. (P.) transversus 

adult: USNPC 65269. 

The examined specimens provided additional 

data that are not included in Table 1: 1 P. (P.) 

transversus female (USNPC 65269) had hook 

roots that were considerably longer than the 

blades and eggs with concentric membranes, 

with no more than 5% having polar prolongation 

of the fertilization membrane. The position of 

the gonopore was obscured. The P. (P.) formosus 

specimens had proboscides with only up to 

15 hooks per row. The roots of the middle proboscis 

hooks were longer than the blades in 

some specimens. Gravid females had up to 10% 

of their ripe eggs showing some polar prolongation 

of the fertilization membrane. The female 

gonopore was invariably and definitively subterminal. 

The P. (P.) taiwanensis specimens were 

robust and almost identical to P. (P.) formosus. 

Distinct differences in lemniscal length, which 

were used to justify the designation of P. (P.) 

taiwanensis as a separate species (Schmidt and 

Kuntz, 1966), were not observed in this study, 

in agreement with later observations by Schmidt 

(1981). The proboscis had only up to 15 hooks 

per row. The roots of the middle proboscis 

hooks were invariably slightly shorter than the 

blades. Up to 15% of the ripe eggs had some 

polar prolongation of the fertilization membrane. 

The female gonopore was definitively subterminal. 

Plagiorhynchus (Prosthorhynchus) malayensis 

(Tubangui, 1935) Schmidt and Kuntz, 1966 

(Figs. 1-5) 

GENERAL: Tubangui (1935) originally described 

this species from 1 male specimen obtained 

from the gruiform bird, the banded landrail 

Gallirallus (=Hypotaenidia) philippensis 

Linnaeus, 1766, in Luzon, Philippines, as Oligoterorhynchus 

malayensis. It was later transferred 

to the genus Prosthorhynchus by Yamaguti 

(1963) because of its cylindrical proboscis. 

Schmidt and Kuntz (1966) redescribed the males 

based on 2 new specimens (USNPC 60730) collected 

from 2 other species of gruiform birds 

from Taiwan (the white-breasted water hen, 

Amauromis phoenicurus chinensis (Boddaert, 

1783) and the banded crake, Rallina eurozonoides 

formosana Seebohm, 1894) and on the original 

description. The female remained unknown. 

Eleven specimens (6 males and 5 females on 8 

slides) of the same species, all from the G. D. 

Schmidt collection, became available for this 

study (10 specimens from HWMLC, 1 from 

USNPC). Seven of the 8 slides were dated 1965; 

the remaining slide (1 male specimen) was dated 

1972. One of the 2 males described by Schmidt 

and Kuntz (1966) (USNPC 60730) was also dated 

1965. The 5 female specimens in this collection 

were adequate for description. The 6 male 

specimens in the same collection also provided 

additional new information. 

FEMALE: Trunk elongate, slender, cylindrical 

(Fig. 1), 11.5-18.2 (Jc = 15.1) mm long by 1.12- 

1.37 (1.23) mm wide. Proboscis cylindrical, 

rounded anteriorly 1.06-1.30 (1.18) mm long by 

0.26-0.30 (0.28) mm wide (Fig. 4), with 19 

hook rows, each with 20-21 hooks. All hooks 

similar in shape, except basal hooks spiniform. 

Hooks increasing in size posteriorly to hooks 4- 

8, then gradually decreasing to hooks 20, 21, 

reaching size of anterior hooks. Lengths of 1 

row of hooks of 1 female (Figs. 1, 4, 5) from 

anterior 48, 53, 56, 56, 62, 62, 62, 64, 62, 62, 

62, 59, 56, 56, 56, 56, 56, 53, 53, 50, 50. Roots 

of posterior 4 hooks in each row greatly and 

more progressively reduced posteriorly, well developed 

in all other hooks, and with anterior manubria 

in anterior 4-6 hooks; manubria most developed 

anteriorly (Fig. 5). Neck of same female 

303 long by 333 wide. Proboscis receptacle 

1.97-2.03 (2.00) mm long by 0.27-0.48 (0.37) 

mm wide. Lemnisci narrow and much longer 

than proboscis receptacle, 4.30-5.45 (4.74) mm 

long by 0.12 mm wide. Reproductive system 

short, robust with well-developed vagina, very 

short uterus, and comparatively large uterine 

bell, 757 long (5% of trunk length). Gonopore 

decidedly subterminal (Fig. 2). Eggs elongate 

ovoid, 53-84 (64) long by 22-31 (28) wide; external 

shell sculptured with elevated ridges and 

grooves particularly at poles, all shells concentric 

(Fig. 3) with less than 5% of ripe eggs showing 

mild to moderate polar prolongation of fertilization 

membrane. 

FEMALE (Fig. 1): HWMLC 36329. 

OTHER FEMALES: HWMLC 33878, 36327, 

36328. 

HOST: Amauromis phoenicurus (Boddaert, 

1783). 


JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 66(2), JULY 1999 

SITE OF INFECTION: Intestine. 

17, 16) and most ripe eggs (at least 80%) 

LOCALITY: Borneo, Indonesia; Taiwan. showed mild to strong polar prolongation of the 

MALE: Trunk slender, cylindrical, 10.0-13.0 fertilization membrane (Fig. 6). Schmidt and 

(11.5) mm long by 0.82-1.42 (1.09) mm wide. 

Proboscis cylindrical with rounded anterior end, 

1.00-1.21 (1.11) mm long by 0.20-0.24 (0.23) 

mm wide. Proboscis with 16-21 longitudinal 

rows of 20-22 hooks each. Differences between 

anterior, middle, and posterior hook sizes and 

shape and size of roots comparable to females. 

Lengths of hooks from anterior 42 (42), 48-56 

(52), 53-56 (54), 53-59 (56), 50-59 (54), 50- 

62 (57), 50-56 (54), 48-59 (54), 48-64 (57), 

Kuntz (1966) did not refer to a polar prolongation 

of the fertilization membrane, and their figure 

11 shows none. The gonopore of both sexes 

is decidedly subterminal. The above 2 traits are 

in conflict with the traditional criteria for the 

subgenus Prosthorhynchus (females with subterminal 

gonopore and eggs with concentric shells) 

or the subgenus Plagiorhynchus (females with 

terminal gonopore and eggs with polar prolongation 

of fertilization membrane). See Remarks 

48-56 (53), 45-56 (52), 45-59 (53), 48-56 (53), following. 

48-56 (53), 48-56 (53), 45-56 (51), 45-56 (50), SPECIMENS EXAMINED: HWMLC 34074, 

45-56 (51), 45-53 (49), 45-50 (47), 42-48 (45). 34133. 

Neck 151-242 (181) long by 212-333 (273) 

wide. Proboscis receptacle 1.88-2.12 (1.98) mm 

long by 0.30-0.42 (0.34) mm wide. Lemnisci 

narrow and markedly longer than proboscis receptacle, 

2.36-3.33 (2.82) mm long. Testes 

ovoid, contiguous, at middle of trunk. Anterior 

testis 0.94-1.15 (1.05) mm long by 0.45-0.70 

(0.52) mm wide. Posterior testis 0.91-1.88 

(1.14) mm long by 0.45-0.73 (0.55) mm wide. 

Four tubular cement glands, 2.12-4.24 (3.14) 

mm long by 0.09-0.30 (0.18) mm wide; cement 

glands begin at posterior end of posterior testis 

and join into 2 cement ducts posteriorly at level 

of anterior end of Saefftigen's pouch, which they 

join at its posterior end. Saefftigen's pouch 

1.21-1.36 (1.29) mm long by 0.45-0.48 (0.47) 

mm wide. Bursa 0.94—1.36 (1.15) mm long by 

0.97-1.21 (1.09) mm wide. 

SPECIMENS EXAMINED: USNPC 60730; 

HWMLC 33878, 36327, 36328, 36329. 

Other species of the 2 Plagiorhynchus subgenera 

were studied to help with the construction 

of the following key. This study produced 

the following unexpected information, which 

demonstrated the wide variability within the genus 

Plagiorhynchus and provided a context 

against which its taxonomic complexity could be 

evaluated. 

Plagiorhynchus (Prosthorhynchus) bullocki 

Schmidt and Kuntz, 1966 

The specimens (5 males and 4 females from 

the Formosan hill partridge, Arborophilia crudigularis 

(Swinhoe, 1864) from Taiwan) were in 

general agreement with the original description, 

except that proboscis hooks numbered 17—18 in 

each of 14-16 longitudinal rows (instead of 16- 

Plagiorhynchus (Prosthorhynchus) gracilis 

(Petrochenko, 1958) Schmidt and Kuntz, 1966 

One male from the intestine of the masked 

lapwing, Vanellus miles (Boddaert, 1783), in 

Tasmania was slender and somewhat robust anteriorly, 

with lemnisci about as long as the proboscis 

receptacle. The proboscis had 21 rows of 

more than 15 hooks each and 6 tubular cement 

glands. All of Petrochenko's (1958) male specimens 

were "wrinkled," and the resulting "corrugation" 

affected the "subsequent distribution 

of internal organs." His males had 20 proboscis 

hook rows, each with 16 hooks and only 3 tubular 

cement glands (Petrochenko, 1958, p. 

182). 

SPECIMEN EXAMINED: HWMLC 39385. 

Plagiorhynchus (Prosthorhynchus) golvani 


Observations on 1 male from the intestine of 

a collared bush-robin, Tarsiger (=Erithacus) 

johnstoniae (Ogilvie-Grant, 1906) (Turdidae), in 

Taiwan were in agreement with the original description. 


Plagiorhynchus (Plagiorhynchus) charadrii 

(Yamaguti, 1939) Van Cleave, 1951 

The specimens (9 males and 12 females on 10 

slides), dated 1965 to 1978 and collected from 

shore birds in Taiwan, Hawaii, and Tasmania, 

generally agreed with the descriptions of Yamaguti 

(1939) and Schmidt and Kuntz (1966). 

The proboscides had 17-18 rows of 14-15 

hooks each. The gonopore was terminal in both 

sexes, but eggs varied considerably in size and 


AMIN ET M_.—PLAGIORHYNCHUS IN SOUTH AFRICA AND REVIEW 129 

degree of polar prolongation of the middle membrane, 

if any. For example, females collected 

from the Kentish plover, Charadrius alexandrinus 

Deignan, 1941, and the golden plover Pluvialis 

dominica Gmelin, 1789, in Taiwan and 

Hawaii had eggs up to 85 X 28 and 132 X 50, 

respectively. These eggs mostly had a polar prolongation 

of the middle membrane as described 

by Yamaguti (1939) and Schmidt and Kuntz 

(1966), whose specimens' eggs measured 105- 

120 X 30-45. Some females from the redcapped 

plover, Charadrius (Alexandrinus) ruficapillus 

Temminck, 1822, in Tasmania had larger 

eggs, up to 168 X 67, that mostly had no 

visible prolongation of the fertilization membrane. 

In most other females examined, however, 

about 80% of the eggs normally had no 

polar prolongation. This extreme variation in the 

polar swelling of the fertilization membrane poses 

taxonomic problems and is clearly not related 

to egg size or maturity. It may be associated 

with host species or with unknown geographical 

factors. 

SPECIMENS EXAMINED: HWMLC 34128, 34747, 

39347, 39374. 

Plagiorhynchus (Plagiorhynchus) paulus Van 

Cleave and Williams, 1951 

Measurements of 2 males and 2 females from 

the varied thrush, Zoothera (=Ixoreus) naevius 

(Gmelin, 1784), in the State of Washington, 

U.S.A., did not agree with the original description. 

For example, testes were longer (anterior 

0.848 X 0.364 mm, posterior 0.666 X 0.364 

mm), proboscis receptacle 1.060 X 0.212 mm in 

1 male and 1.394 X 0.273 mm in 1 female, cement 

glands 0.697 X 0.106 mm to 1.515 X 

0.121 mm and eggs 50-76 (66) X 14-28 (19) 

(n = 8). A few (5-10%) of the eggs showed no 

polar prolongation of the fertilization membrane, 

but most did (Fig. 7). The female gonopore was, 

however, not terminal as would be expected in 

a species placed in Plagiorhynchus. The female 

gonopore was actually subterminal (Fig. 8). No 

reference to the position of the female gonopore 

was made in the original description (Van 

Cleave and Williams, 1951) or in subsequent accounts 

by other authors (e.g., Petrochenko, 

1958). Based on this character alone, this species 

would be assigned to Prosthorhynchus. 

However, the polar prolongation of the egg fertilization 

membrane, among other factors discussed 

below, further complicates the issue. No 

reassignment is made at this time. 


Inclusion of species in the key 

Amin (1985) listed 19 species in the subgenus 

Prosthorhynchus, and Golvan (1994) listed 27, 

while Hoklova (1986) listed 11 species from 

land vertebrates. Part of this discrepancy is because 

of synonyms not acknowledged by Golvan 

(1994) or Hoklova (1986) and hence not included 

in the key. The following species are not recognized 

as valid: P. (P.) formosus, P. (P.) taiwanensis, 

and P. (P.) transversus (synonyms of 

P. (P.) cylindraceus, see this paper; Schmidt, 

1981; Amin, 1985). Other synonyms of P. (P.) 

cylindraceus noted by Golvan (1994) are P. (P.) 

rosai (Porta, 1910) Meyer, 1932, and P. (P.) 

upupae Lopez-Neyra, 1946. Rhadinorhynchus 

asturi Gupta and Lata, 1967, was erroneously 

named Prosthorhynchus asturi by Golvan 

(1994); this species, with a spinose trunk, is 

clearly a rhadinorhynchid. Golvan (1956) proposed 

other synonymies that he later retracted 

(Golvan, 1994). Plagiorhynchus (Prosthorhynchus} 

pupa (von Linstow, 1905) Meyer, 1931, is 

a synonym of Polymorphic pupa (von Linstow, 

1905) Kostylev, 1922 (see Amin, 1992). Golvan 

(1994) removed Prosthorhynchus (Prosthorhynchus} 

limnobaeni Tubangui, 1933, to the subgenus 

Plagiorhynchus despite the fact that this 

species is known from only 2 males. This reassignment 

to Plagiorhynchus is unjustified, and 

the species is retained in the subgenus Prosthorhynchus. 

It is not, however, included in the 

key because of controversy regarding the only 

usable diagnostic trait, the proboscis armature. 

Tubangui (1933) indicated that proboscis hooks 

are "in forty-three alternating anteroposterior 

rows of eight hooks each," but his Plate 5, Figure 

1 shows a proboscis with about 18-20 longitudinal 

rows, each with 30 hooks. Golvan 

(1956) accepted the 43 X 8 formula and Petrochenko 

(1958, after Meyer, 1932-1933) indicated 

16 longitudinal rows of 17 hooks each. Yamaguti 

(1963) quoted both figures, 43 X 8 and 

16 x 17. Both Petrochenko (1958) and Yamaguti 

(1963) retained the species in Prosthorhynchus 

as originally described. Golvan (1956, 

1994) synonymized P. (Prosthorhynchus) rectus 

Sphern, 1942 nee Linton, 1892, with "Prosthorhynchus 

schmidti nom. nov." This entity, 

originally described as Echinorhynchus rectus 



Linton, 1892, was declared incertae sedis by Posterior 1-8 hooks smaller, spine-like, with 

Schmidt 

o i- •_! b»"ock! Sc^1 d Kunt7' 196J 

Proboscis with 1-4 spine-like hooks 6 

(1994) also listed "Prosthorhynchus luehei Tra- 6 Proboscis with 3_4 spine-like hooks having 

vassos, 1916" (=Echinorhynchus spirilla Ru- greatly reduced but definite roots 

dolphi, 1819; E. spirilla Linstow, 1878, 1897; 

P- (P.) malayensis 

Gigantorhynchus spirula Porta, 1908, 1909; (Tubangui, 1935) Schmidt and Kuntz, 1966 

_ , , . , , . „ ir,nr n ; Proboscis with 1-3 spine-like hooks having 

Prosthenorchis luhei Travassos, 1916; Prosthor- underdeveloped, rudimentary, or no roots 7 

hynchus spiralis (Rudolphi, 1809) Schmidt and 7 Adults very long (males 45 mm, females 60 

Kuntz, 1966). The species is considered incertae mm) P. (P.) scolopacidis 

sedis (Schmidt and Kuntz, 1966) and is not in- (Kostylev, 1915) Schmidt and Kuntz, 1966 

eluded in the key because its inadequate descrip- Adults sj°rter (alef UP to 30 mm' females o 

,, . , . . , , up to 40 mm long) 8 

tion does not allow its placement in either of the g Eggs large> 125_i3o x 45-50 ..... P. (P.) pittamm 

2 subgenera of Plagiorhynchus. Another spe- (Tubangui, 1935) Schmidt and Kuntz, 1966 

cies, Plagiorhynchus kuntzi Gupta and Fatma, Eggs smaller than 125-130 x 45-50 9 

1988, is not included in the key because it is not 9- Proboscis with 8 rows of hooks, posterior 

assignable to either subgenus. The position of ho°ks with very short roots; most eggs with 

; , . , , , , . , polar prolongation or fertilization memthe 

female gonopore was described as terminal brane 

or subterminal"; the description was based on .... p. (/>.) ,-usselli (Tadros, 1970) Golvan, 1994 

only 1 female and 1 male (Gupta and Fatma, Proboscis with 14 or more rows of hooks, pos- 

1988). Petrochenko (1958) and Yamaguti (1963) terior hooks with greatly reduced, rudimenlisted 

22 and 21 species of Prosthorhynchus, re- ^ or no roots; most e§§s with Concentric 

, shells 

spectively, but the taxonomic status and assign- 1Q Vaginal sphincter strongly developed on 1 side 

10 

ment of many of these species also has been p. (/>.) asymmetricus Belopolskaja, 1983 

changed since. Vaginal sphincter symmetrical 11 

Based on the above account, 21 species are 1L Lemnisci considerably shorter than proboscis 

considered valid and are included in the follow- receptacle; proboscis with 18 rows, each 

. _ _ , , , /ir> each with 10-22 hooks 12 

cies from the former U.S.S.R., some of which 12' Ventral surface of female gonopore with elevated 

papilla 

are synonyms. p (/)) genitopapillosus Lundstrom, 1942 

No papilla at female gonopore 13 

Key to Species of the Subgenus 13. Proboscis small, 640-770 x 190-230, with 18 

Prosthorhynchus rows of hooks P. (P.) ogati (Fukui 

and Morisita, 1936) Schmidt and Kuntz, 1966 

1. Proboscis with 30 rows of hooks; eggs small Proboscis larger, with 14-20 rows of hooks 14 

(40 X 20); trunk pigmented 14. Proboscis less than 1.0 mm long 15 

P. (P.) pigmentatus Proboscis 1.0 mm long, or longer 16 

(Marval, 1902) Meyer, 1932 15. Proboscis 800-900 X 200 with 16-18 rows of 

Proboscis with 8-21 rows of hooks; eggs larg- 

15-18 hooks each, hooks very small, middle 

er; trunk not pigmented 2 and posterior hooks 23 and 4 long; females 

2. All proboscis hooks of almost uniform size 17 mm long; eggs 70 X 10 P. (P.) rheae 

(50-54 long), with rectangular well-devel- (Marval, 1902) Schmidt and Kuntz, 1966 

oped roots P. (P.) limnobaeni Proboscis 957 X 65 with 16—18 rows of 20— 

(Tubangui, 1933) Golvan, 1956 22 hooks each, middle and posterior hooks 


AMIN ET AL.—PLAGIORHYNCHUS IN SOUTH AFRICA AND REVIEW 131 

39 and 13 long; females 4.6 mm long; eggs 

44-46 X 26-28 P. (P.) rossicus 

(Kostylev, 1915) Schmidt and Kuntz, 1966 

16. Proboscis consistently longer than 1.0 mm ___ 17 

Proboscis length averaging about 1.0 mm ..... 20 

17. Proboscis with 18-20 rows of hooks 18 

Proboscis with 14-16 rows of hooks 19 

18. Proboscis 1.25-1.44 X 0.33 mm with 18-20 

rows of 15 hooks each, middle hooks 58-59 

long, posterior 3 hooks rootless 

- P. (P.) gallinagi (Schachtachtinskaia, 1953) 


Proboscis 1.18 X 0.260-0.033 mm with 20 

rows of 16 hooks each, middle hooks 71-77 

long, posterior 3 hooks with underdeveloped 

but definite roots 

P. (P.) gracilis 

(Petrochenko, 1958) Schmidt and Kuntz, 1966 

19. Proboscis 1.0-1.3 mm long with 16-17 hooks 

per row, 1—3 basal hooks with broadened 

base but no definite root; females 12-15 mm 

long; eggs 80 X 40 P. (P.) reticulatus 

(Westrumb, 1821) Golvan, 1956 

Proboscis 1.1 X 0.3 mm with 14-15 hooks per 

row, posterior hooks spiniform and rootless; 

females 7.0-8.5 mm long; eggs 70 X 35 

P. (P.) nicobarensis (Soota and Kansal, 1970) 

Zafar and Farooqi, 1981 

20. Proboscis 0.96-1.1 X 0.19-0.22 mm with 20 

rows of 19-20 hooks each, most posterior 

hooks rootless; proboscis receptacle 1.8 mm 

long; males 7 X 1.1 mm, females 8X1.1 

mm 

P. (P.) longirostris 

(Travassos, 1927) Amin, 1985 

Proboscis 0.8-1.3 X 0.2-0.36 mm with 14-20 

(usually 14-18) rows of 10-18 (usually 13- 

18) hooks each, posterior 1-3 spiniform 

hooks with greatly reduced or no roots; proboscis 

receptacle 2.0-2.5 mm long; males 

4.5-30 X 0.6-2.4 mm, females 5-40 X 0.4- 

3.2 mm P. (P.) cylindraceus 

(Goeze, 1782) Schmidt and Kuntz, 1966 

Remarks 

Plagiorhynchinae was established by Meyer 

(1931) as a subfamily of Polymorphidae, within 

which he included the genera Plagiorhynchus 

Liihe, 1911, and Prosthorhynchus Kostylew 

1915, as well as Sphaerechinorhynchus Johnston 

and Deland, 1929, and Porrorchis Fukui, 1929. 

Golvan (1956, 1960) erected 2 new subfamilies, 

Porrorchinae and Sphaerechinorhynchinae, to 

accommodate forms with short spheroid proboscides. 

This left only 2 genera, Plagiorhynchus 

and Prosthorhynchus, in the Plagiorhynchinae. 

Petrochenko (1956) established the family Prosthorhynchidae 

to contain Prosthorhynchus, 

among other genera, that infect terrestrial vertebrates 

as adults and terrestrial insects as larvae 

and that have eggs with concentric shells and no 

polar prolongations. Yamaguti (1963) placed 

Plagiorhynchidae Golvan, 1960 emend, in Echinorhynchidea 

Southwell and Macfie, 1925, in 

which adult and larval worms infected aquatic 

vertebrates and crustaceans, respectively, and 

eggs had a polar prolongation of the middle 

membrane. Schmidt and Kuntz (1966) synonymized 

Prosthorhynchus with Plagiorhynchus 

and reduced the 2 genera to subgenera of the 

genus Plagiorhynchus s. lat. Schmidt and Kuntz 

(1966) observed that the only 2 consistent morphological 

differences between the 2 taxa, the 

position of the female genital pore and the presence 

or absence of polar swelling in the egg fertilization 

membrane, were "not invariable." 

Amin (1982, 1985) accepted Schmidt and 

Kuntz's (1966) classification, and additional 

documentation was produced by this study. Hoklova 

(1986) and Golvan (1994), however, preferred 

to retain the original independent status 

of the 2 genera in Polymorphidae. 

In the present work, an examination of many 

specimens and a review of relevant literature 

provided additional documentation and justification 

of Schmidt and Kuntz's (1966) decision 

to reduce Plagiorhynchus s. str. and Prosthorhynchus 

to subgenera of the genus Plagiorhynchus 

s. lat. All characteristics examined were 

found to vary considerably within each taxon, 

and to overlap between the 2 taxa. Characters 

found with some degree of variation and with 

very little but evident overlap include hosts, egg 

membranes, and female gonopore. Species of 

the subgenus Plagiorhynchus s. str. normally infect 

shore and aquatic arthropods (crustaceans 

and insects) as larvae, have a terminal gonopore 

in the female, and have eggs with polar prolongation 

of the fertilization membrane. Species of 

subgenus Prosthorhynchus normally infect terrestrial 

birds and occasionally mammals as 

adults and terrestrial arthropods as larvae, have 

a subterminal gonopore in the female, and have 

eggs with concentric shells showing no prolongation 

of any membrane. Despite Golvan's 

(1994) assertions and Hoklova's (1986) reservations, 

we have found exceptions to each of 

these 3 more stable characteristics, constituting 

an overlap between the concept of Plagiorhynchus 

s. str. and that of Prosthorhynchus. Our P. 

(Prosthorhynchus) cylindraceus specimens from 

South Africa were collected from 5 species of 

shore birds, suggesting an aquatic life cycle in 

the definitive and intermediate hosts. The same 

specimens and many others reported as syno- 



nyms of the same species included females having 

up to 15% of their eggs with polar prolongation 

of the fertilization membrane. Most eggs 

(at least 80%) of the P. (Prosthorhynchus) bullocki 

female specimens examined also had polar 

prolongation of the fertilization membrane. Females 

of P. (Prosthorhynchus) bullocki have a 

definite subterminal gonopore; thus, this taxon 

remains in limbo between the 2 subgenera. Similarly, 

females of P. {Plagiorhynchus) paulus 

with eggs mostly having prolongation of the fertilization 

membrane have a subterminal gonopore. 

Because the eggs vary in size, shape, and 

the presence and degree of polar prolongation 

and because host ecological parameters are not 

consistent within each subgenus, the position of 

the female gonopore becomes the only remaining 

reliable trait distinguishing the 2 subgenera. 

Examples of the limitations to sole use of this 

characteristic include that of P. (P.) paulus and 

the fact that males cannot be keyed out. Variability 

within and between the 2 subgenera in all 

3 characteristics (host, female gonopore, eggs) 

should be considered in toto while considering 

the limitations inherent in each. 

Despite the above documented variations and 

limitations, no new subgeneric diagnoses are 

given or believed necessary; those provided by 

Schmidt and Kuntz (1966) are considered adequate. 


Amin, O. M. 1982. Acanthocephala. Pages 933-941 

in S. P. Parker, ed. Synopsis and Classification of 

Living Organisms. McGraw-Hill Book Company, 

New York. 

. 1985. Classification. Pages 27-72 in D. W. T. 

Crompton and B. B. Nickol, eds. Biology of the 

Acanthocephala. Cambridge University Press, 

London. 

-. 1992. Review of the genus Polymorphus 

Liihe, 1911 (Acanthocephala: Polymorphidae), 

with the synonymization of Hexaglandula Petrochenko, 

1950, and Subcorynozoma Hoklova, 

1967, and a key to the species. Qatar University 

Science Journal 12:115-123. 

Golvan, Y. J. 1956. Acanthocephales d'oiseaux. Troisieme 

note. Revision des especes Europeennes de 

la sous-famille de Plagiorhynchinae A. Meyer 

1931 (Polymorphidae). Annales de Parasitologie 

Humaine et Comparee 31:351-384. 

. 1960. Le phylum des Acanthocephala. Troisieme 

note. La classe de Palaeacanthocephala 

(Meyer 1931). Annales de Parasitologie Humaine 

et Comparee 35:350-386. 

-. 1994. Nomenclature of the Acanthocephala. 

Research and Reviews in Parasitology 54:35-205. 

Gupta, V. and S. Fatma. 1988. On four acanthocephalan 

parasites of vertebrates from Uttar Pradesh 

and Tamil Nadu. Indian Journal of Helminthology 

(1987) 39:128-142. 

Hoklova, I. G. 1986. The Acanthocephalan Fauna of 

Terrestial Vertebrates of S.S.S.R. Nauka Press, 

Moscow. 276 pp. 

Meyer, A. 1931. Neue Acanthocephalen aus dem Berliner 

Museum. Begrundung eines neuen Acanthocephalensystems 

auf Grund einer Untersuchung 

der Berliner Sammlung. Zoologische Jahrbucher, 

Abteilung fiir Systematik, Okologie und Geographic 

der Tiere 62:53-108. 

. 1932-1933. Acanthocephala. Pages 1-582 in 

Dr. H. G. Bronn's Klassen und Ordnungen des 

Tier-Reichs. Vol. 4. Akademisch Verlagsgesellschaft 

MBH, Leipzig. 

Petrochenko, V. I. 1956. Acanthocephala of Domestic 

and Wild Animals. Vol. 1. Izdatel'stvo Academii 

Nauk S.S.S.R., Moscow. 465 pp. (English translation 

by Israel Program for Scientific Translations 

Ltd., 1971) 

. 1958. Acanthocephala of Domestic and Wild 

Animals. Vol. 2. Izdatel'stvo Akademii Nauk 

S.S.S.R., Moscow. 478 pp. (English translation by 

Israel Program for Scientific Translations Ltd., 

1971) 

Schmidt, G. D. 1981. Plagiorhynchus formosus Van 

Cleave, 1918, a synonym of Plagiorhynchus cylindraceus 

(Goeze, 1782) Schmidt and Kuntz, 

1966. Journal of Parasitology 67:597-598. 

, and R. E. Kuntz. 1966. New and little-known 

plagiorhynchid Acanthocephala from Taiwan and 

the Pescadores Islands. Journal of Parasitology 52: 

520-527. 

-, and O. W. Olsen. 1964. Life cycle and development 

of Prosthorhynchus formosus (Van 

Cleave, 1918) Travassos, 1926, an acanthocephalan 

parasite of birds. Journal of Parasitology 50: 

721-730. 

Tubangui, M. A. 1933. Notes on Acanthocephala in 

the Philippines. Philippine Journal of Science 50: 

115-128, 6 plates. 

. 1935. Additional notes on Philippine Acanthocephala. 

Philippine Journal of Science 56:13- 

17, 2 plates. 

Van Cleave, H. J. 1918. The Acanthocephala of North 

American birds. Transactions of the American Microscopical 

Society 37:19-47. 

. 1942. A reconsideration of Plagiorhynchus 

formosus and observations of Acanthocephala 

with atypical lemnisci. Transactions of the American 

Microscopical Society 61:206-210. 

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Japan. Part 29. Acanthocephala, II. Japanese Journal 

of Zoology 13:317-351. 

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Interscience Publishers, New York. 423 

pp. 



66(2), 1999 pp. 133-137 

Sciadocephalus megalodiscus Diesing, 1850 (Cestoda: 

Corallobothriinae), a Parasite of Cichla monoculus Spix, 1831 

(Cichlidae), in the Parana River, State of Parana, Brazil 

AMILCAR ARANDAS REGO,' PATRICIA MIYUKI MACHADO,2 AND GILBERTO CEZAR 

PAVANELLI2-3 

1 Department of Helminthology, Fundacao Institute Oswaldo Cruz (FIOCRUZ), Rua Marques de Valen9a, 25, 

Apt. 1004, 20550-030, Rio de Janeiro, Rio de Janeiro, Brazil (e-mail: arego@openlink.com.br) 

2 Center for Research in Limnology, Ichthyology and Aquaculture (NUPELIA), State University of Maringa, 

87020-900 Maringa, Parana, Brazil (e-mail: gcpavanelli@ppg.uem.br) 

ABSTRACT: Sciadocephalus megalodiscus Diesing, gen. et sp. inquirenda, is redescribed from the tucunare, 

Cichla monoculus Spix, collected in the Parana River, Brazil. The position of the reproductive system of the 

parasite is clarified, thus revalidating the genus and species. Sciadocephalus megalodiscus is recorded from the 

Parana River for the first time. 

KEY WORDS: Cestoda, Proteocephalidae, Sciadocephalus megalodiscus, Cichla monoculus, Cichlidae, Teleostei, 

Parana River, Brazil. 

The basis of the taxonomy of the South American 

cestodes of the Order Proteocephalidea 

Mola, 1928, parasitizing freshwater fishes was 

established by W. N. F. Woodland, who, in a 

series of studies published in the 1930's, described 

numerous proteocephalid parasites of 

fishes of the Amazon basin. Some older species 

were described by Diesing (1850, 1855). Interest 

in these helminths has increased recently, and 

new cestodes are frequently being added to the 

South American species list (Rego et al., 1999). 

Some of the older species were placed as species 

inquirenda, as is the case with Sciadocephalus 

megalodiscus Diesing, 1850, which Diesing 

(1850) described from the tucunare, Cichla monoculus 

Spix, 1831, collected in the state of Mato 

Grosso, Brazil. This parasite was later found by 

Woodland (1933) in Amazonia from the same 

fish species. Because there were doubts as to the 

subfamily to which this species belonged, because 

the position of the reproductive organs (a 

fundamental character in classification of the 

taxon) was unclear, Wardle and McLeod (1952) 

and Rego (1994) preferred to treat it as genus 

and species inquirenda. 

Sciadocephalus megalodiscus had not previously 

been found in the Parana River. It is important 

to note that C. monoculus is not native 

to the Parana River, where it was introduced 

some years ago. Recently, one of us (P.M.M.) 

had the opportunity to collect several specimens 


of this parasite, and with the present description, 

the genus and species are revalidated. 


A total of 136 C. monoculus were caught in the 

Parana River from July 1996 through October 1997. 

After removal from the intestine, the cestodes were 

fixed in 4% hot formalin. Cestodes were stained with 

alcoholic carmine or Dclafield's hematoxylin, dehydrated 

in an alcohol series, cleared in Eugenol® or in 

beech creosote, and mounted in Canada balsam. Cestodes 

for histological sections were embedded in paraffin, 

cut in 8 (Jim cross-sections, and stained with hematoxylin 

and eosin. Illustrations were made with the 

aid of a drawing tube. Measurements are in millimeters 

(mm). Photomicrographs were made with a scanning 

electron microscope (SEM). The terms "prevalence" 

and "mean intensity of infection" are used according 

to Bush et al. (1997). Representative specimens were 

deposited in the Helminthological Collection of the 

Funda?ao Institute Oswaldo Cruz (FIOCRUZ), Rio de 

Janeiro, state of Rio de Janeiro, Brazil, under accession 

numbers 33951, 33952, and 33953a-c. 

Results 

Proteocephalidae La Rue, 1911 

Corallobothriinae Freze, 1965 

Sciadocephalus megalodiscus Diesing, 1850 

(Figs. 1-7) 

Description 

GENERAL (based on 11 specimens): Strobila 

6.1-9.3 (7.9) long X 1.1-1.7 (1.3) wide. Strobila 

comprised of 17—22 proglottids, including 6—8 

(7) immature proglottids, 4-6 (5) mature proglottids, 

8-12 (10) gravid proglottids. All proglottids 

several times wider than long. Scolex 

133 



Figures 1, 2. SEM photomicrographs of Sciadocephalus inegalodiscus Diesing, 1850. 1. Small specimen 

(entire). 2. Scolex and metascolex. Apical view. 

wider than strobila, with umbrella-shaped metascolex 

with borders turned upwards. Scolex 

enveloped by these borders, comprised of 4 

muscular suckers and 1 apical sucker (Figs. 1- 

3). Scolex and metascolex 1.4-2.2 (1.9) long X 

2.8-2.9 (2.8) wide; suckers 0.385-0.515 (0.454) 

in diameter and apical sucker 0.115 in diameter. 

Neck inconspicuous. Immature proglottids wider 

than long, 0.1 X 1.8 to 0.2 X 1.4 (0.2 X 1.6). 

Gravid proglottids wider than long, 0.3 X 1.8 to 

0.9 X 1.4 (0.6 X 1.7). Last few proglottids more 

Figure 3. SEM photomicrograph of the scolex, 

detail of a sucker and apical sucker of Sciadocephalus 

inegalodiscus Diesing, 1850. 

or less rectangular. Genital opening in anterior 

Vs of proglottid, alternating irregularly. Vagina 

opening anterior or posterior to cirrus pouch. 

Vaginal sphincter inconspicuous. Cirrus pouch 

long and narrow, 0.3 X 0.1 to 0.4 X 0.1 (0.4 X 

0.1). Cirrus pouch about 0.2 times width of proglottid. 

Testes about 26, medullar, 0.07 in diameter, 

arranged in 2 distinct fields, separated by 

ovary. Ovary medullar, compact, indistinctly bilobate, 

central, 0.415-0.465 (0.442) in width. 

Vitellaria medullar, diffuse, not forming follicles, 

occupying lateral body region. Uterus medullar, 

rapidly resolving into capsules containing 

varying numbers of eggs. In last segments, some 

capsules not containing eggs and modified in 

form (Figs. 4, 7). Some capsules passing from 

medulla to cortex, opening through tegument. 

Eggs not containing developed embryos. Hexacanth 

hooks not observed. Musculature with numerous 

isolated longitudinal fibers, distributed 

throughout entire proglottid. Demarcation between 

medulla and cortex indicated by delicate 

transverse fibers situated next to longitudinal fibers 

(Fig. 6). Tegument of strobila with 2-4 longitudinal 

sulci (Fig. 5). 

Taxonomic summary 

HOST: Cichla monoculus Spix, 1831 (Cichlidae), 

"tucunare." 

LOCALITY: Parana River, region of Porto 

Rico, State of Parana, Brazil. 

SITE OF INFECTION: Intestine. 


REGO ET AL.—SC/ADOCEPHALUS MEGALODISCUS IN C1CHLA MONOCULUS 135 

Vit ex 

- 

tf 

ex 

Vit 

eoc 

Figures 4—7. Sciadocephalus megalodiscus Diesing, 1850. Scales in millimeters (mm). 4. Entire specimen; 

note that most proglottids are gravid. 5. Small specimen; note small sulci present on tegument (tc). 

6. Cross-section of gravid proglottid, showing vitellaria (Vit), excretory canal (ex), testes (t), transverse 

fibers (tf), uterus (u), ovary (ov), longitudinal fibers (If). 7. Gravid proglottid; note some ovigerous capsules 

with eggs and others without eggs and modified; empty ovigerous capsule (eoc), cirrus pouch (cp). 



PREVALENCE: 13.2%. 

MEAN INTENSITY OF INFECTION: 

8.6. 

Discussion 

This is the third report of S. megalodiscus. 

The species was initially described by Diesing 

(1850) from C. monoculus in the state of Mato 

Grosso, Brazil. Woodland (1933) redescribed it 

from the same fish species in Brazilian Amazonia. 

The latter author's description of the arrangement 

of the reproductive system was incomplete 

in that he did not note whether this 

system is medullar or cortical. Woodland (1933, 

p. 193) stated that "It is important to note that 

a definite band of longitudinal muscle fibres is 

entirely absent, though individual fibres may be 

scattered in the parenchyma. There is no question 

as to organs being medullary or cortical in 

position." The classification system for proteocephalids 

(sensu Freze, 1965) defined 2 families, 

Proteocephalidae and Monticelliidae, according 

to whether the gonads are located in the medullar 

or cortical parenchyma. For this reason, 

some authors (Wardle and McLeod, 1952; Rego, 

1994) considered the genus and species as inquirenda. 

Sciadocephalus megalodiscus have no groups 

of longitudinal fibers separating the cortex from 

the medulla (Woodland, 1933). However, as described 

in the present work (Fig. 6), the isolated 

fibers, together with the transverse fibers, sufficiently 

delimit the medulla from the cortex. We 

can therefore determine that the gonads and the 

vitelline glands are entirely medullar. Vitellaria 

do not form true follicles as in the majority of 

the proteocephalids, but appear as diffuse bodies, 

arranged laterally in the proglottids. 

The metascolex is the most interesting characteristic 

of this species. Its umbrella form is 

different from typical "collar-type" metascolices 

found in genera of proteocephalids such as 

Amphoteromorphus Woodland, 1935; Goezeella 

Fuhrmann, 1916; and Spatulifer Woodland, 

1934. Rego (1999) defined the metascolex as 

"any development of folds and wrinkles in the 

posterior part of the scolex or on the surface of 

the scolex proper, encircling the suckers or not." 

There are several types of metascolex, as many 

as the number of described species with metascolices. 

The scolex of Sciadocephalus has some 

resemblances to that of Corallotaenia Freze, 

1965. Brooks and Deardorff (1980) reported an 

unidentified Corallotaenia sp. from the flatnose 

catfish, Ageneiosus caucanus Steindachner, 

1880, in Colombia. Unfortunately, the authors 

did not provide a formal description of the 

worms. Sciadocephalus differs from Corallotaenia 

by the umbrella-shaped metascolex, the 

disposition of the ovary, the nonfolliculate vitellaria, 

and the uterus resolving into ovigerous 

capsules. It is important to emphasize that the 

other South American genera that possess a metascolex 

have the reproductive systems arranged 

variously, but partly or entirely located in the 

cortical parenchyma. Sciadocephalus megalodiscus 

is an exception; the gonads and vitellaria 

are entirely medullar. 

Brooks and Rasmussen (1984) stated the importance 

of the metascolex to eliminate cases of 

parallel evolution in a cladogram. However, subsequent 

authors did not attribute much importance 

to these structures, probably because of 

difficulties in characterizing the metascolex 

types. Rego et al. (1999) produced a phylogenetic 

analysis of the subfamilies of Proteocephalidea, 

but in regard to the character metascolex, 

they stated: "only two states (presence 

versus absence) were considered until such time 

as the various forms of metascolices are clearly 

defined and distinguished." The preliminary results 

of a phylogenetic analysis of South American 

genera (Rego et al., unpubl.) indicate a 

closer phylogenetic relationship between Sciadocephalus 

and Megathylacus Woodland, 1935. 

It therefore becomes necessary to present a new 

generic diagnosis in order to revalidate the genus. 

Sciadocephalus Diesing, 1850 

GENERIC DIAGNOSIS: Strobila small. Scolex 

wider than strobilus. Metascolex umbrellashaped, 

sometimes with edges turned upwards. 

Suckers muscular, round, and turned upwards. 

Apical sucker conspicuous. Genital openings alternating 

in regular fashion. Ovary compact, 

central. Testes in 2 fields, separated by ovary. 

Vitellaria diffuse, not forming follicles. Cirrus 

pouch elongate. Vaginal opening posterior or anterior 

to cirrus pouch. Uterus rapidly resolving 

into ovigerous capsules, with varying numbers 

of eggs. Eggs not embryonated. Longitudinal canals 

in tegument of strobilus. Gonads and vitellaria 

entirely medullar. Musculature consisting 

of numerous isolated, irregularly arranged longitudinal 

fibers, present in medullar parenchyma, 

but concentrated in cortex/medulla separa- 


REGO ET AL.—SC/ADOCEPHALUS MEGALODISCUS IN CICHLA MONOCULUS 137 

tion. Cortex/medulla separation best characterized 

by presence of transverse fibers. 


We are grateful to Dr. Alain de Chambrier, 

Geneva, Switzerland, for preparing the SEM micrographs, 

and to Dr. Ricardo Massato Takemoto, 

State University of Maringa, for assistance 

in preparing drawings and sectioning proglottid 

material. The editors, Drs. Janet W. Reid 

and Willis A. Reid, Jr., assisted in translating the 

text into English. 


Brooks, D. R., and T. L. Deardorff. 1980. Three proteocephalids 

from Colombian siluriform fishes, including 

Nomimoscolex alovarius sp.n. (Monticelliidae: 

Zygobothriinae). Proceedings of the Helminthological 


, and G. Rasmussen. 1984. Proteocephalidean 

cestodes from Venezuelan siluriform fishes, with 

a revised classification of the Monticelliidae. Proceedings 

of the Biological Society of Washington 

97:748-760. 





Diesing, K. M. 1850. Systema Helminthum. Vol. 1. 

Wilhelm Braumuller, Vindobonae. 679 pp. 

. 1855. Sechzehn Gattungen von Binnewurmen 

und ihre Arten. Denkschriften der Kaiserlichen 

Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche 

Classe 13:556-616. 

Freze, V. I. 1965. Essentials of Cestodology. Vol. 5. 

Proteocephalata in Fish, Amphibians and Reptiles. 

Izdatel'stvo Nauka, Moscow. 538 pp. (In Russian; 

English translation, Israel Program for Scientific 

Translation, 1969.) 

Rego, A. A. 1994. Order Proteocephalidea Mola, 

1928. Pages 257-293 in L. F. Khalil, A. Jones, 

and R. A. Bray, eds. Keys to the Cestode Parasites 

of Vertebrates. Commonwealth Agricultural Bureaux 

International, St. Albans, U.K. 

. 1999. Scolex morphology of proteocephalid 

cestode parasites of neotropical freshwater fishes. 

Memorias do Institute Oswaldo Cruz 94:37-52. 

, J. Chubb, and G. C. Pavanelli. 1999. Ces 

todes in South American freshwater fishes: keys 

to genera and brief descriptions of species. Revista 

Brasileira de Zoologia 16(2):(in press) 

, A. de Chambrier, V. Hanzelova, E. Hoberg, 

T. Scholz, P. Weekes, and M. Zehnder. 1998. 

Preliminary phylogenetic analyses of subfamilies 

of the Proteocephalidea (Eucestoda). Systematic 


Wardle, R. A., and J. A. McLeod. 1952. The Zoology 

of Tapeworms. University of Minnesota 

Press, Minneapolis. 780 pp. 

Woodland, W. N. F. 1933. On the anatomy of some 

fish cestodes described by Diesing from the Amazon. 

Quarterly Journal of Microscopical Science 

76:175-208. 

Obituary Notice 

FRANCIS G. TROMBA 

1920-1999 

Elected to Membership in 1951; 

Recording Secretary, 1957; 

Vice President, 1962 President, 1963; 

Editor, 1967-1970; Life Member, 1983; 

Anniversary Award, 1991 



66(2), 1999 pp. 138-145 

Revisions of Protoancylodiscoides and Bagrobdella, with 

Redescriptions of P. chrysichthes and B. auchenoglanii 

(Monogenoidea: Dactylogyridae) from the Gills of Two Bagrid 

Catfishes (Siluriformes) in Togo, Africa 

DELANE C. KRiTSKY1-3 AND SiM-Dozou KuLO2 

1 College of Health Professions, Campus Box 8090, Idaho State University, Pocatello, Idaho 83209 U.S.A. 

(e-mail: kritdela@isu.edu) and 

2 Laboratoire de Parasitologie, Faculte des Sciences, Universite du Benin, B.P. 1515, Lome, Togo 

ABSTRACT: The generic diagnoses of Protoancylodiscoides Paperna and Bagrobdella Paperna, are emended 

based on the study and redescription of the respective type species: P. chrysichthes Paperna from the gills of 

the bagrid catfishes Chrysichthys nigrodigitatus (Lacepede) and B. auchenoglanii Paperna from the gills of 

Auchenoglanis occidentalis (Cuvier and Valenciennes) collected from Togo, Africa. Protoancylodiscoides is 

characterized by species possessing hook shanks comprised of 2 subunits (proximal subunit variably expanded) 

in hook pairs 1, 6, and 7; a dorsal striated pouch (onchium) through which the extrinsic dorsal muscles extend; 

a sinistral vaginal pore; a V-shaped ventral bar and straight dorsal bar; tandem (or slightly overlapping) gonads 

(germarium pretesticular); and 2 seminal vesicles. Bagrobdella includes species with tandem gonads (germarium 

pretesticular); a sinistral vaginal aperture; hook pairs 1-4, 6, and 7 with shank comprised of 2 subunits (basal 

subunit variably expanded); and straight bars. The ventral bar in species of Bagrobdella possesses a long 

anteromedial projection associated with a lightly sclerotized skirt; the dorsal bar is adorned with a shield-like 

projection originating from the posterior margin of the bar. 

KEY WORDS: Monogenoidea, Dactylogyridae, Protoancylodiscoides, Bagrobdella, Protoancylodiscoides chrysichthes, 

Bagrobdella auchenoglanii, Chrysichthys nigrodigitatus, Auchenoglanis occidentalis, catfish, Siluriformes, 

Bagridae, Pisces, Togo, Africa. 

This paper is a continuation of our series on 

dactylogyrid genera from Africa. Earlier papers 

dealt with Characidotrema Paperna and Thurston, 

1968, Quadriacanthus Paperna, 1961, and 

Schilbetrema Paperna and Thurston, 1968 (see 

Kritsky et al., 1987; Kritsky and Kulo, 1988; 

1992a, respectively). In addition, 2 new genera 

of African Dactylogyridae have been proposed: 

Quadriacanthoides Kritsky and Kulo, 1988 (a 

junior subjective synonym of Paraquadriacanthus 

Ergens, 1988; see Kritsky, 1990), and Schilbetrematoides 

Kritsky and Kulo, 1992 (see Kritsky 

and Kulo, 19925). In the present paper, Protoancylodiscoides 

Paperna, 1969, and Bagrobdella 

Paperna, 1969, are revised, and 

Protoancylodiscoides chrysichthes Paperna, 

1969, and Bagrobdella auchenoglanii Paperna, 

1969, the type species of their respective genera, 

are redescribed from the gills of siluriform fishes 

in Togo, Africa. 


Fish hosts Chrysichthys nigrodigitatus (Lacepede, 

1803) and Auchenoglanis occidentalis (Cuvier and Va- 

Corresponding author. 

lenciennes, 1840) were collected from localities in 

Togo during 1995-1996. Methods of collection, preservation, 

mounting, and illustration of helminths were 

those described by Kritsky et al. (1987). Measurements, 

all in micrometers, were made with a filar micrometer 

according to procedures of Mizelle and Klucka 

(1953), except that length of the male copulatory 

organ (MCO) of P. chrysichthes 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. Flattened specimens 

mounted in Gray and Wess' medium were used 

to obtain measurements of the 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 

synthetic resin. Voucher specimens of P. chrysichthes 

and B. auchenoglanii collected from Togo were deposited 

in the U.S. National Parasite Collection 

(USNPC), the helminth collections of the H. W. Manter 

Laboratory (HWML) of the University of Nebraska 

State Museum, and the Musee Royal de 1'Afrique Centrale 

(MRAC) as indicated in the respective redescriptions. 

For comparative purposes, the following type 

specimens were examined: holotype and 3 paratypes 

(all on 1 slide) of Protoancylodiscoides mansourensis 

El-Naggar, 1987 (British Museum of Natural History 

[BMNH], London, 1985.1.8.1-2); 9 paratypes (all on 

1 slide) of Protoancylodiscoides malapteruri Bilong, 

Birgi, and Le Brim, 1997 (BMNH 1996.4.7.6-7); 17 

138 


KRITSKY AND KULO—MONOGENEANS FROM AFRICAN CATFISHES 139 

paratypes (on 2 slides) of P. malapteruri (Museum National 

d'Histoire Naturelle [MNHN 113 HF], Paris); 

holotype of P. chrysichthes Paperna, 1969 (MRAC 

35.566); holotype of B. auchenoglanii Paperna, 1969 

(MRAC 35.581); holotype of Bagrobdclla fraudidenta 

Euxet and Le Brun, 1990 (MRAC 35.915). 

Results 

Class Monogenoidea Bychowsky, 1937 

Order Dactylogyridea Bychowsky, 1937 

Dactylogyridae Bychowsky, 1933 

Protoancylodiscoides Paperna, 1969 

EMENDED DIAGNOSIS: Body elongate, fusiform, 

comprised of cephalic region, trunk, peduncle, 

haptor. Tegument thin, smooth. Two terminal, 

2 bilateral cephalic lobes; head organs 

present; cephalic glands unicellular, lateral or 

posterolateral to pharynx. Two pairs of eyes; 

granules subspherical. Mouth subterminal, midventral; 

pharynx muscular, glandular; esophagus 

present; 2 intestinal ceca, confluent posterior to 

gonads, lacking diverticula. Genital pore midventral 

near level of intestinal bifurcation. Gonads 

intercecal, tandem or slightly overlapping; 

germarium pretesticular. Vas deferens looping 

left cecum, ascending to level of genital pore 

where it empties into saccate seminal vesicle; 

short duct arises from seminal vesicle dilating 

into large granule-filled vesicle that empties into 

base of male copulatory organ (MCO). Copulatory 

complex comprising nonarticulated tubular 

MCO, accessory piece; accessory piece serving 

as guide for MCO; 2 dorsal glandular masses 

lying immediately posterior to genital atrium; 

prostatic reservoir present. Seminal receptacle 

pregermarial; vaginal aperture sinistral. Vitellaria 

coextensive with intestine, frequently extending 

into peduncle. Haptor with dorsal, ventral 

anchor/bar complexes, 7 pairs of hooks with ancyrocephaline 

distribution (Mizelle, 1936; see 

Mizelle and Price, 1963); hook pairs 1, 6, 7 with 

shanks comprised of 2 subunits, proximal subunit 

expanded; pairs 2-5 with shanks of 1 subunit. 

Dorsal striated tissue pouch (onchium) present. 

Ventral bar V-shaped; dorsal bar straight. 

Parasites of gills of African siluriform fishes. 

TYPE SPECIES: Protoancylodiscoides chrysichthes 

Paperna, 1969, from Chrysichthys nigrodigitatus 

(Bagridae). 

OTHER SPECIES: Protoancylodiscoides malapteruri 

Bilong, Birgi, and Le Brun, 1997, from 

Malapterurus electricus Gmelin, 1789 (Malapteruridae); 

P. mansourensis El-Naggar, 1987, 

from Chrysichthys auratus Geoffrey, 1809 

(Bagridae). 

REMARKS: Paperna (1969) proposed Protoancylodiscoides 

for P. chrysichthes from the 

gills of Chrysichthys nigrodigitatus collected 

from 3 locations in Volta Lake, Ghana. He characterized 

the genus and differentiated it from 

Ancylodiscoides Yamaguti, 1937, by species 

having a "non-sclerotized bar" associated with 

the tip of the superficial root of each dorsal anchor, 

hooks of 2 different morphological types, 

and male reproductive organs shifted to the extreme 

posterior end of the body. Paperna (1969) 

clearly erred when describing the "non-sclerotized 

bars," as these structures represent the 

well-developed dorsal extrinsic muscles that insert 

on the tip of the superficial root of each 

dorsal anchor and extend to the midline of the 

haptor where their direction abruptly curves toward 

their origins in the peduncle or trunk (El- 

Naggar, 1987; Bilong et al., 1997). At the midline 

of the haptor, these muscles extend through 

a superficial dorsal pouch-like structure (onchium) 

before proceeding anteriorly toward their 

origins (Fig. 4). Contraction of the muscles apparently 

results in lateral displacement of the anchor 

points, thereby embedding its tip in host 

tissue during attachment. 

Apparently Paperna (1969) considered 

"hooks of two types" to refer to the hook shank 

being composed of either 1 or 2 subunits, with 

the proximal subunit (when present) dilated to 

varying degrees. However, the presence of multiple 

hook types within species of Dactylogyridae 

is common and should probably not be used 

to differentiate genera without determination of 

the type present in homologous hook pairs. 

Hook types similar to those shown in Figures 5, 

6, 9, and 10 for hook pairs 1, 6, and 7 in Protoancylodiscoides 

chrysichthes are also found in 

some African and Asian species infesting siluriform 

fishes: Quadriacanthus Paperna, 1961 

(pairs 1, 6, and 7; see Kritsky and Kulo, 1988); 

Bychowskyella Achmerow, 1952 (pairs 1, 6, and 

7; see Lim, 1991); and Bagrobdella Paperna, 

1969 (pairs 1-4, 6, and 7). Also, in species of 

Chauhanellus Bychowsky and Nagibina, 1969 

(all marine), and some (but not all) freshwater 

species of Demidospermus Suriano, 1983 (neotropical), 

all of which infest siluriform fishes, 

similar hooks have been reported (pairs 1-4, 6, 

and 7 in Chauhanellus; and pairs 1, 2, and 7 in 

Demidospermus (see Lim, 1994; Kritsky and 



Gutierrez, 1998, respectively). Based on hook 

types, therefore, species of Protoancylodiscoides 

show affinity to those of Quadriacanthus and 

Bychowskyella and perhaps those of Bagrobdella 

and Chauhanellus. 

Although Protoancylodiscoides chrysichthes 

and P. mansourensis have elongate MCOs that 

extend from the level of the ovary to that of the 

esophageal bifurcation, the positions of this and 

other male reproductive organs are not outstanding. 

The only "shifting" of organs posteriorly 

in these 2 species are those of the distal seminal 

vesicle and prostatic reservoir to near the body 

midlength; both shifts are apparently accommodations 

to the posterior position of the base 

of the elongate MCO. In P. malapteruri, with a 

comparatively shorter MCO, these organs lie in 

the usual position of the anterior trunk (Bilong 

et al., 1997). Although Paperna (1969) showed 

the testis far posterior to the germarium in his 

whole-mount drawing of P. chrysichthes, the 

specimen on which the drawing was based was 

clearly distorted and flattened, which may have 

produced the pattern illustrated. In the present 

specimens, including the types of P. mansourensis 

and P. malapteruri, the gonads are tandem 

or slightly overlapping. 

Based on its emended diagnosis, Protoancylodiscoides 

is now characterized by the combined 

presence of 1) hook shanks comprised of 

2 subunits (proximal subunit expanded to varying 

amounts) in hook pairs 1, 6, and 7; 2) a 

striated pouch (onchium) on the dorsal surface 

of the haptor and through which the dorsal extrinsic 

muscles extend; 3) a sinistral vaginal 

pore; 4) a V-shaped ventral bar and a straight 

dorsal bar; 5) tandem (or slightly overlapping) 

gonads; and 6) a proximal saccate seminal vesicle 

followed by a fusiform distal vesicle. 

Protoancylodiscoides chrysichthes Paperna, 

1969 

(Figs. 1-14) 

HOST AND LOCALITY: Gills of Chrysichthys 

nigrodigitatus, Bagridae; Anie River, Kpehoun, 

Togo. 

PREVIOUS RECORDS: Chrysichthys nigrodigitatus 

from 3 localities on Volta Lake, Ghana 

(Paperna, 1969, 1979); C. auratus from Lake 

Tiga, Kano, northern Nigeria (Ndifon and Jimeta, 

1990). 

SPECIMENS STUDIED: Forty-nine voucher 

specimens, USNPC 88263, 88264, 88265, 

88266, 88267, HWML 39924, MRAC 37.422 

(all from Togo). 

REDESCRIPTION: Body 637 (410-884; n = 

29) long; greatest width 90 (73-115; n = 33) 

near midlength. Cephalic region ventrally concave, 

lobes moderately developed, 3 bilateral 

pairs of head organs. Members of posterior pair 

of eyes slightly larger, closer together than those 

of anterior pair; subspherical granules moderately 

large; accessory granules absent or few in cephalic 

region. Pharynx ovate, greatest diameter 

30 (23-43; n = 35); esophagus elongate. Peduncle 

elongate; haptor subhexagonal, 99 (79-140; 

n = 29) long, 94 (74-127; n = 23) wide. Ventral 

anchor 33 (29-38; n = 5) long; with differentiated 

roots connected by delicate or perforated 

web; thickened ridge originating from posterior 

margin of deep root, extending across base of 

shaft; shaft curved, point elongate; base 20 (17- 

22; n = 3) wide. Dorsal anchor 64 (55-69; n = 

10) long, with elongate superficial root with 

curled tip, short truncate deep root, curved shaft, 

elongate point; base 31 (27-36; n = 6) wide. 

Ventral bar 68 (55-80; n = 12) long, 45 (35- 

69; n = 15) between ends, V-shaped, with slightly 

enlarged terminations; dorsal bar 41 (34-46; 

n = 20) long, straight, with short blunt anteromedial 

projection, pair of bilateral sliver-like 

projections frequently present on anterior margin, 

ends enlarged. Hook pairs 1, 6, 7 with shank 

of 2 subunits, proximal subunit lightly sclerotized, 

variably expanded, point delicate; hook 

pairs 2, 3, 4 with shank comprised of 1 subunit, 

slightly expanded; hook pair 5 delicate, with depressed 

thumb. Hook pair 1: 42 (38-45; n = 3); 

hook pairs 2, 3, 4: 16 (14-17; n = 12); hook 

pair 5: 18 (17-19; n = 4); hook pair 6: 23 (20- 

26; n = 6); hook pair 7: 30 (22-35; n = 4) long; 

Figures 1-14. Protoancylodiscoides chrysichthes Paperna, 1969. All figures are drawn to the 25 (Jim 

scale, except Figure 1 (200 u.m scale). 1. Whole mount (ventral, composite). 2. Vagina and distal seminal 

receptacle. 3. Copulatory complex (ventral). 4. Dorsal pouch, dorsal extrinsic muscle and hook pair 7. 5. 

Hook pair 1. 6. Hook pair 1 (variant). 7. Hook pair 5. 8. Hook pair 4. 9. Hook pair 7. 10. Hook pair 6. 

11. Ventral bar. 12. Dorsal bar. 13. Ventral anchor. 14. Dorsal anchor. 



14 



hook pair 1 (variant): 22 (n = 1) long. Filamentous 

booklet (FH) loop extending to proximal 

end of distal subunit of shank. MCO an elongate 

tube winding from base at level of germarium 

to genital atrium near level of intestinal bifurcation, 

base of MCO with sclerotized margin; 

MCO 255 (162-365: n = 5) long. Accessory 

piece variable, comprising 2 or 3 articulated subunits, 

elongate nipple (preputium) guiding distal 

portion of MCO shaft. Testis 50 (32-71; n = 8) 

long, 24 (21-32; n = 8) wide, elongate ovate; 

saccate proximal seminal vesicle subconical, lying 

sinistral to genital atrium, separated from 

distal vesicle by short duct with sphincter-like 

muscle; distal vesicle fusiform; prostatic reservoir 

fusiform, lying ventral to left cecum at midlength 

of body. Germarium fusiform, with irregular 

margins, 85 (61-113; n = 15) long, 31 (21- 

40; n — 15) wide; oviduct, ootype not observed; 

vaginal aperture at body midlength; vagina 

comprising distal thick-walled funnel, proximal 

coiled tube poorly sclerotized with 2-3 rings 

(ring direction counterclockwise proximally, reversing 

to a clockwise direction distally), emptying 

into subovate seminal receptacle overlying 

anterior extremity of germarium; diameter of 

vaginal ring 16 (13-20; n = 26); vitellaria dense 

throughout trunk, extending into peduncle, absent 

in regions of other reproductive organs. 

REMARKS: Protoancylodiscoides chrysichthes 

is very similar to P. mansourensis, and differentiation 

of the 2 species is based on relatively 

few moiphometric characters. Comparison 

with the holotype and 3 paratypes of the latter 

species has revealed the following differences: 

1) in P. chrysichth.es, the coiled vagina has 2-3 

rings (4—5 rings in P. mansourensis); 2) the diameter 

of the rings of the vagina is greater in P. 

mansourensis (24 to 27 u.m) than in P. chrysichthes 

(13 to 20 |xm). 

In addition, El-Naggar (1987) differentiated 

the 2 species utilizing moiphometric features, 

the presence/absence of a "preputium" associated 

with the tip of the MCO, and a haptoral 

funnel-like structure through which the dorsal 

extrinsic muscles extend. However, our measurements 

of the type specimens of P. mansourensis 

showed that body length (497-650 fjim) 

does not differ from that of our specimens of P. 

chrysichthes (410-884 |xm). Indeed, our measurements 

of body length of the flattened holotype 

and paratypes of P. mansourensis did not 

fall within the range (710-1,000 u.m) reported 

by El-Naggar (1987), indicating that some of his 

conversions were in error. Although measurements 

of body length presented by Paperna 

(1969) for P. chrysichthes had only 1 significant 

digit, resulting in difficulty in determining the 

rounding effects, his range (400—500 u,m) falls 

within those reported herein for the types of P. 

mansourensis and for our specimens from Togo. 

With the exception of the total length of the 

dorsal anchor, differences in all other measurements 

of P. chrysichthes and P. mansourensis 

reported herein may be explained by potential 

rounding effects. In specimens of P. chrysichthes 

from Togo, the length of the dorsal anchor 

ranged from 55 to 69 |Jim, whereas our values 

for the type specimens of P. mansourensis 

were 78 to 83 u,m. Paperna (1969) reported 100 

to 110 u,m for this parameter, but this range does 

not necessarily exclude our measurements because 

of possible rounding effects. Therefore, 

dorsal anchor length is problematic in differentiating 

P. mansourensis from P. chrysichthes. 

Although Paperna (1969) described a "preputium" 

associated with the distal end of the 

MCO, we were unable to find this structure in 

our specimens. However, it is likely that Paperna's 

"preputium" refers to a small, elongate, often 

longitudinally striated portion of the accessory 

piece through which the tip of the MCO 

projects. A similar component of the accessory 

piece is also visible in the holotype and paratypes 

of P. mansourensis. Finally, presence of a 

dorsal "funnel-like structure" (of El-Naggar, 

1987) or "onchium" (of Bilong et al., 1997) 

through which the dorsal extrinsic muscles of 

the haptor extend is probably a generic character, 

because it also occurs in our specimens of 

P. chrysichthes. 

It is clear that P. chrysichthes and P. mansourensis 

are poorly differentiated, and they 

may be synonyms. However, we do not feel that 

available information on the 2 forms (species) 

justifies proposal of synonymy at this time. Additional 

collections from throughout the range of 

the host would be necessary to determine intraspecific 

variation within the species. If the 2 species 

are distinct, the record of P. chrysichthes 

from C. auratus in Nigeria (Ndifon and Jimeta, 

1990) must be confirmed. 

Protoancylodiscoides malapteruri is easily 

differentiated from the 2 species discussed 

above by the presence of a elongate proximal 

rod in the accessory piece (absent in P. chrys- 



ichthes and P. mansourensis}. In P. malapteruri, 

the MCO is shorter and less convoluted than that 

of P. chrysichthes or P. mansourensis. 

Bagrobdella Paperna, 1969 

EMENDED DIAGNOSIS: Body robust, fusiform, 

comprised of broad cephalic region, trunk, peduncle, 

haptor. Tegument thin, smooth. Two terminal, 

2 bilateral cephalic lobes; head organs 

present; cephalic glands unicellular, posterolateral 

to pharynx. Two pairs of eyes; granules subspherical. 

Mouth subterminal, midventral; pharynx 

muscular, glandular; esophagus short; 2 intestinal 

ceca, confluent posterior to gonads, lacking 

diverticula. Genital pore dextroventral about 

Vi distance between germarium and intestinal bifurcation. 

Gonads intercecal, tandem; germarium 

pretesticular. Vas deferens looping left cecum; 

seminal vesicle a simple dilation of vas 

deferens. Copulatory complex a coiled tube with 

clockwise rings (see Kritsky et al., 1985), directed 

posteriorly from MCO base, lacking accessory 

piece; prostatic vesicle present. Seminal 

receptacle pregermarial; vaginal aperture sinistral. 

Vitellaria coextensive with intestine. Haptor 

with dorsal, ventral anchor/bar complexes, 7 

pairs of hooks with ancyrocephaline distribution 

(Mizelle, 1936; see Mizelle and Price, 1963); 

pairs 1-4, 6, 7 with shanks comprised of 2 subunits, 

proximal subunit expanded; pair 5 with 

shank of 1 subunit. Ventral bar straight, with 

long anterior projection associated with lightly 

sclerotized skirt; dorsal bar straight, with posterior 

shield-like projection. Parasites of gills of 

siluriform fishes. 

TYPE SPECIES: Bagrobdella auchenoglanii 

Paperna, 1969, from Auchenoglanis occidentalis 

(Bagridae). 

OTHER SPECIES: Bagrobdella fraudulenta Euzet 

and Le Brun, 1990 (syn. B. auchenoglanii of 

Paperna, 1971), B. anthopenis Euzet and Le 

Brun, 1990, both from Auchenoglanis occidentalis. 

REMARKS: Euzet and Le Brun (1990) 

emended the diagnosis of Bagrobdella and corrected 

some initial observations on internal anatomy 

and haptoral sclerites offered by Paperna 

(1969). Our emendation adds to their diagnosis 

the morphologic differences between respective 

hook pairs and details of the coil of the MCO. 

Bagrobdella auchenoglanii Paperna, 1969 

(Figs. 15-24) 

HOST AND LOCALITY: Gills of Auchenoglanis 

occidentalis, Bagridae; Barrage du "Chantier 

Rouge," Kara River, Kara, Togo. 

PREVIOUS RECORDS: Auchenoglanis occidentalis, 

Volta Lake, Ghana (Paperna, 1969, 1979); 

Niger River at Bamako, Mali (Euzet and Le 

Brun, 1990). 

SPECIMENS STUDIED: Forty-four vouchers, 

USNPC 88258, 88259, 88260, 88261, 88262, 

HWML 39925, MRAC 37.423 (all from Togo). 

REDESCRIPTION: Body 457 (361-686; n = 

25) long; greatest width 103 (78-130; n = 25) 

in posterior trunk. Cephalic region broad; cephalic 

lobes well developed. Eyes subequal; 

members of posterior pair farther apart than 

members of anterior pair; granules small; accessory 

granules absent, infrequently few in cephalic 

region. Pharynx subspherical to ovate, 28 

(24-33; n = 24) in greatest diameter. Peduncle 

broad; haptor subhexagonal, 91 (78-113; n = 

25) long, 93 (79-104; n = 27) wide. Ventral 

anchor 42 (37-45; n = 11) long, with short 

roots, evenly curved elongate shaft abruptly 

flexed immediately distal to anchor base; tip of 

point recurved; base 22 (19-24; n = 10) wide. 

Dorsal anchor 56 (50-58; n = 11) long, with 

poorly differentiated roots, curved shaft, long 

point; base 22 (18—25; n = 7) wide. Ventral bar 

46 (42-53; n = 17) long, with bifurcated ends 

surrounding superficial surface of anchor base; 

anteromedial projection 27 (24-31; n = 19) 

long, distally trifid; skirt delicate. Dorsal bar 59 

(53-65; n = 24) long, yoke shaped, with subtrapezoidal 

posterior shield; shield 35 (31-40; n 

= 25) long. Hook pair 1: 35 (30-37; n = 11), 

pairs 2, 3, 4: 21 (20-23; n = 14), pairs 6, 7: 29 

(26-36; n = 10) long, each with truncate thumb, 

delicate shaft, point, proximal subunit of shaft 

variable in length between hook pairs; hook pair 

5: 16-17 (n = 3) long, with delicate point, shaft, 

shank with 1 subunit; FH loop about length of 

distal subunit of shank. MCO 63 (52-74; n = 

11) long, a coil of about 6 rings, proximal 3 

rings poorly defined, distal 3 rings with delicate 

cup-like processes; base expanded, lightly sclerotized. 

Testis 40 (28-53; n = 10) long, 28 (20- 

35; n — 7) wide, ovate; seminal vesicle ovate; 

prostatic reservoir elongate fusiform. Germarium 

pyriform, 44 (35-56; n = 22) long, 29 (20- 

42; n = 22) wide; oviduct broad; ootype not 



Figures 15-24. Bagrobdella auchenoglanii Paperna, 1969. All figures are drawn to the 25 fjim scale, 

except Figure 15 (200 (Jim scale). 15. Whole mount (ventral, composite). 16. Hook pair 1. 17. Hook pair 

5. 18. Hook pairs 2, 3, 4, 7. 19. Hook pair 6. 20. Copulatory complex (ventral). 21. Ventral bar. 22. Dorsal 

bar. 23. Ventral anchor. 24. Dorsal anchor. 

observed; uterus delicate; vagina a simple nonsclerotized 

straight tube; seminal receptacle submedian, 

pregermarial. Vitellaria dense throughout 

trunk, except absent in regions of other reproductive 

organs. 

REMARKS: Measurements of specimens of 

Bagrobdella auchenoglanii from Togo compare 

favorably with those reported by Euzet and Le 

Brun (1990) for their material from Mali. Paperna's 

(1969) measurements are generally greater 

than those reported herein. Reported differences 

between respective studies are not considered 

sufficient to separate the collections into 

separate species and likely represent intraspecific 

variability between geographic localities. 

Because Paperna's (1971) redescription of 

Bagrobdella auchenoglanii from Auchenoglanis 

occidentalis in Lake Albert, Uganda, was based 

on specimens of B. fraudulenta (see Euzet and 

Le Brun, 1990), the Ugandan records reported 



by Paperna (1971, 1979) are for the latter species. 

Bagrobdella auchenoglanii is not known 

from Uganda. 


We are grateful to J.-L. Justine (MNHN), F. 

Puylaert (MRAC), David Gibson (BMNH), and 

Eileen Harris (BMNH) for allowing us to examine 

type specimens in their care. Financial 

support for this study was provided, in part, by 

the Idaho State University Faculty Research 

Committee (award 740). 


Bilong, C. F. B., E. Birgi, and N. Le Brun. 1997. 

Protoancylodiscoides malapteruri n. sp. (Monogenea, 

Dactylogyridea, Ancyrocephalidae), parasite 

branchial de Malapterurus electricus Gmelin 

(Silurifonnes, Malapteruridae), au Cameroun. 

Systematic Parasitology 38:203-210. 

El-Naggar, M. M. 1987. Protoancylodiscoides mansourensis 

n. sp. A monogenean gill parasite of the 

Egyptian freshwater fish Chrysichthys auratus 

Geoffrey, 1809. Arab Gulf Journal of Scientific 

Research, Agricultural and Biological Science B5 

3:441-454. 

Euzet, L., and N. Le Brun. 1990. Monogenes du 

genre Bagrobdella Paperna, 1969 parasites branchiaux 

d'Auchenaglanis occidentalis (Cuvier et 

Valenciennes, 1840) (Teleostei, Siluriformes, Bagridae). 

Journal of African Zoology (Revue de 

Zoologie Africaine) 104:37-48. 

Kritsky, D. C. 1990. Synonymy of Paraquadriacanthus 

Ergens, 1988 and Quadriacanthoides Kritsky 

et Kulo, 1988 (Monogenea Dactylogyridae) and 

their type species. Folia Parasitologica 37:76. 

, 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 Dawestretna 

cycloancistrium Price and Nowlin, 1967 

(Dactylogyridae: Ancyrocephalinae). Proceedings 

of the Biological Society of Washington 98:321- 

331. 

, and P. A. Gutierrez. 1998. Neotropical Monogenoidea. 

34. Species of Demidospermus (Dactylogyridae, 

Ancyrocephalinae) from the gills of 

pimelodids (Teleostei, Siluriformes) in Argentina. 

Journal of the Helminthological Society of Washington 

65:147-159. 

, and S.-D. Kulo. 1988. The African species of 

Quadriacanthus with proposal of Quadriacanthoides 

gen. n. (Monogenea: Dactylogyridae). 

Proceedings of the Helminthological Society of 

Washington 55:175-187. 

, and . 1992a. A revision of Schilbetrema 

(Monogenoidea: Dactylogyridae), with descriptions 

of four new species from African Schilbeidae 

(Siluriformes). Transactions of the American 


, and . 1992b. Schilbetrematoides pseudodactylogyrus 

gen. et sp. n. (Monogenoidea, 

Dactylogyridae, Ancyrocephalinae) from the gills 

of Schilhe intermedium (Siluriformes, Schilbeidae) 

in Togo, Africa. Journal of the Helminthological 


-, and W. A. Boeger. 1987. Resurrection 

of Characidotrema Paperna and Thurston, 

1968 (Monogenea: Dactylogyridae) with description 

of two new species from Togo, Africa. Proceedings 

of the Helminthological Society of 


Lim, L. H. S. 1991. Three new species of Bvchowskyella 

Achmerow, 1952 (Monogenea) from peninsular 

Malaysia. Systematic Parasitology 19:33— 

41. 

. 1994. Chauhanellus Bychowsky & Nagibina, 

1969 (Monogenea) from ariid fishes (Siluriformes) 

of peninsular Malaysia. Systematic Parasitology 

28:99-124. 

Mizelle, J. D. 1936. New species of trematodes from 

the gills of Illinois fishes. American Midland Naturalist 

17:785-806. 

, and A. R. Klucka. 1953. Studies on monogenetic 

trematodes. XIV. Dactylogyridae from 

Wisconsin fishes. American Midland Naturalist 

49:720-733. 

, and C. E. Price. 1963. Additional haptoral 

hooks in the genus Dactylogyrus. Journal of Parasitology 

49:1028-1029." 

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observations of the parasites of Chrysichthys auratus 

Geoffroy in Tiga Lake, Kano, Nigeria. Nigerian 

Journal of Parasitology 9-11:139-144. 

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of the Volta basin and south Ghana. Bulletin de 

1'Institut Francaise d'Afrique Noire (Serie A) 31: 

840-880. 

. 1971. Redescription of Bagrobdella auchenoglanii 

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83:141-146. 

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66(2), 1999 pp. 146-154 

Redescription of Pseudacanthostomum panamense Caballero, Bravo- 

Hollis, and Grocott, 1953 (Digenea: Acanthostomidae), a Parasite of 

Siluriform Fishes of the Family Ariidae, with Notes on Its Biology 

TOMAS ScHOLZ,1-7 LEOPOLDINA AouiRRE-MACEDO,2 GUILLERMO SALGAOO-MALDONADO,3 

JOAQUIN VARGAS-VAZQUEZ,2 VICTOR VlDAL-MARTINEZ,2 JAN WOLTER,4 ROMAN KUCHTA,5 

AND WOLFGANG KoRTiNG6 

1 Institute of Parasitology, Academy of Sciences of the Czech Republic, Branisovska 31, 370 05 Ceske 

Budejovice, Czech Republic (e-mail: tscholz@paru.cas.cz), 

2 Center for Investigation and Advanced Studies of the National Polytechnic Institute (CINVESTAV-IPN) 

Unidad Merida, Carretera Antigua a Progreso Km 6, A.P. 73 "Cordemex," C.P. 97310 Merida, Yucatan, 

Mexico, 

3 Institute of Biology, National Autonomous University of Mexico (UNAM), A.P. 70-153, C.P. 04510, 

Mexico D.F., Mexico, 

4 Wexstrasse 39, 10715 Berlin, Germany, 

5 Faculty of Biology, University of South Bohemia, Branisovska 31, 370 05 Ceske Budejovice, 

Czech Republic, and 

6 Fish Diseases Research Unit, School of Veterinary Medicine, Biinteweg 17, 30559 Hannover, Germany. 

ABSTRACT: The acanthostomid trematode Pseudacanthostomum panamense Caballero, Bravo-Hollis, and Grocott 

is redescribed on the basis of examination of its holotype and new material from Galeichthys (=Ariopsis) 

seemani (Giinther) (type host) from Colombia (new geographical record), and Ariopsis assirnilis (Giinther) and 

Arius guatemalensis (Giinther) (new host records) (all Siluriformes: Ariidae) from the Atlantic and Pacific coasts 

of Mexico (new geographical record). It was found that P. panamense possesses intestinal ceca that are connected 

with the excretory bladder near the posterior extremity and opening outside by an uroproct. The actual number 

of circumoral spines of the holotype is 27; the number of spines is stable, with most specimens possessing 27 

spines and a very few 26 or 28. Pseudacanthostomum floridensis Nahhas and Short, described from Galeichthys 

(= Arius) fells (Linnaeus) from Florida, U.S.A., is considered a synonym of P. panamense. Metacercariae of P. 

panamense from the eleotrid fishes Dormitator latifrons (Richardson) and Gobiomorus maculatus (Giinther) 

from the Pacific coast of Mexico (Jalisco state) are described for the first time. 

KEY WORDS: Pseudacanthostomum panamense, Digenea, metacercariae, Acanthostomidae, taxonomy, catfish, 

Siluriformes, Ariidae, Pisces, Mexico, Colombia. 

During parasitological examination of fish and geographical regions. Metacercariae of this 

from Colombia and Mexico, acanthostomid trematode are described for the first time, and 

trematodes were found, both as adults in catfish the taxonomic status of Pseudacanthostomum 

of the family Ariidae and as metacercariae in floridensis Nahhas and Short, 1965, the only 

eleotrid fish. They were identified as Pseuda- congeneric species, is discussed. 

canthostomum panamense Caballero, Bravo- 

Hollis, and Grocott, 1953, a species described 


from Galeichthys (_= Ariopsis) seemani (Giinther, Trematodes studied were found in Ariopsis seemani 

1864) from Panama (Caballero et al., 1953). Ex- (7 specimens examined) from Colombia (locality not 

animation of the holotype of P. panamense known; May 1996)MnV^,, ///, (Cninther, 1864), 

, , . . . , , .. ., from Laguna Bacalar near the village of Bacalar, Qumshowed 

that its original description had not pro- tana Roo Mexico January 1995 (, specimen)> and 

vided data on some taxonomically important from Chetumal Bay, Quintana Roo, Mexico, October 

features such as the morphology of the intestinal 1996 (96 specimens); and Arius guatemalensis (Giinceca; 

in addition, no information about intraspe- ther' 1864>

SCHOLZ ET AL.—REDESCRIPTION OF PSEUDACANTHOSTOMUM PANAMENSE 147 

Jalisco, Mexico, September 1995 (7 specimens); and 

in Gobiomorus maculatus (Giinther, 1859) from the 

Cuitzmala River at Emiliano Zapata, Jalisco, Mexico, 

January, March, and September 1995 (89 specimens). 

Holotypes of P. panamense from Ariopsis seemani 

from Panama (National Helminthological Collection of 

the Institute of Biology, National Autonomous University 

of Mexico, Mexico City, Mexico-CNHE 947) 

and P. floridcnsis from Galeichthys (= Arius) felis 

(Linnaeus, 1766) from Florida (U.S. National Parasite 

Collection, Beltsville, Maryland, U.S.A.-USNPC 

60087) were compared with the present material. 

Measurements (length and width) of 59 undeformed, 

uncollapsed eggs of P. panamense (from Ariopsis seemani, 

Panama and Colombia and A. assimilis, Bacalar 

and Chetumal, Mexico) and P. floridensis (from Arius 

felis, Florida, U.S.A.) were compared by ANOVA (Tukey's 

HSD for unequal N; Spojotvoll/Stoline test). 

The specimens studied are deposited in the helminthological 

collections of the Institute of Parasitology, 

Ceske Budejovice, Czech Republic (IPCAS D-384); 

Institute of Biology, National Autonomous University 

of Mexico, Mexico City, Mexico (CNHE 3239); Laboratory 

of Parasitology, CINVESTAV-IPN Merida, 

Mexico (CHCM 181); and the U.S. National Parasite 

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

87809, 87810). The nomenclature of the fish hosts 

(catfish) follows that presented by Eschmeyer (1998). 

Measurements are in micrometers unless otherwise 

noted. 

Results 

Comparison of acanthostomid trematodes occurring 

in Ariopsis seemani from Colombia and 

A. assimilis and A. guatemalensis from Mexico 

with the holotype of Pseudacanthostomum panamense 

from A. seemani from Panama revealed 

their conspecificity (Figs. 1, 2; Table 1). All 

specimens, including the holotype of P. panamense 

(Fig. 1), possess long intestinal ceca connected 

near the posterior extremity with the excretory 

bladder, thus forming an uroproct (Figs. 

ID, 2D, F). Vitelline follicles are distributed between 

the ventral sucker and the anterior testis 

(Figs. IB, 2A, C, F, G), ventrally forming 2 separate 

fields and, in the same specimens, are dorsally 

confluent at the ovarian level (Figs. 1F-H, 

2C). The uterine loops are sinuous, filling the 

space between the ventral sucker and the posterior 

extremity (Figs. 1C, 2A, C, G). A thinwalled, 

coiled seminal vesicle is situated posterodextrally 

to the ventral sucker (Figs. IB, 2C, 

F), and a genital pore is located just anterior to 

the ventral sucker (Fig. IB). With the exception 

of 3 specimens, all trematodes (TV = 40), including 

the holotype (Fig. 1A), had 27 circumoral 

spines (Table 2). 

The present study also demonstrated that the 

trematodes studied are identical in all but 1 morphological 

and biometrical character to P. floridensis, 

a species described from Arius felis from 

Florida, U.S.A (Nahhas and Short, 1965; see Table 

1). No significant difference between these 

2 taxa was found in the size (length and width) 

of eggs (Fig. 3). The only difference between P. 

panamense and P. floridensis is the more anterior 

position of the vitelline follicles in the latter 

species. However, the distribution of the vitelline 

follicles is rather variable (Fig. 1E-H), and its 

suitability as a discriminative character between 

P. panamense and P. floridensis is doubtful. 

Consequently, P. floridensis is considered a junior 

synonym of P. panamense. 

Because the original description of P. panamense 

was incorrect in some features (the number 

of circumoral spines, the presence of an uroproct, 

and the spination of the posterior part of 

the body), its redescription based on extensive 

material from 4 fish hosts is provided herein. In 

addition, metacercariae from the eleotrid fishes 

Donnitator latifrons and Gobiomorus maculatus 

from Mexico, considered to be conspecific with 

P. panamense, are described. 

Pseudacanthostomum panamense Caballero, 

Bravo-Hollis, and Grocott, 1953 

(Figs. 1, 2) 

SYNONYMS: Pseudacanthostomum floridensis 

Nahhas and Short, 1965 (new synonymy). 

Pseudacanthostomum sp. of Pineda-Lopez et 

al. (1985) (new synonymy). 

Pelaezia sp. of Scholz and Vargas-Vazquez 

(1998) (new synonymy). 

DESCRIPTION: Adult (measurements in Table 

1): Body elongate, densely covered with fine tegumental 

spines, including post-testicular region. 

Oral sucker terminal, cup-shaped, with large buccal 

cavity; ventral sucker small, pre-equatorial. 

Oral sucker surrounded by 1 row of 27 large, 

straight circumoral spines (Figs. 1A, 2B, J, K); 

exceptionally 26 or 28 spines present (Table 2). 

Prepharynx present and short (Fig. 1A) or absent 

(Fig. 2A); pharynx strongly muscular; esophagus 

very short. Intestinal bifurcation pre-equatorial; 

intestinal ceca long, connected with excretory 

bladder and opening outside by uroproct (Figs. 

ID, 2D). Testes tandem, close to posterior extremity. 

Vas deferens forming numerous loops, 

widened near ventral sucker to form coiled seminal 

vesicle; cirrus-sac lacking, ejaculatory duct 

slightly curved, opening into hermaphroditic 



Figure 1. Pseudacanthostomum panamense. A-D, holotype from Galeichthys (=Arius) seemani, Panama 

(IBUNAM 947), ventral view. A: oral sucker; B: ventral sucker and terminal genitalia; C: anterior part 

of body; note extent of vitelline follicles; D: posterior extremity; note connection of intestinal ceca with 

excretory bladder and presence of uroproct; E-H, acetabular region; note variation in anterior extent of 

vitelline follicles (E, F: specimens from Ariopsis assimilis, Mexico; G, H: specimens from A. seemani, 

Columbia; E: dorsal view, ventral follicles omitted; F, G: ventral view, dorsal follicles dashed; H: ventral 

view but dorsal follicles drawn in full and ventral follicles dashed). Scale bars in millimeters. Abbreviations: 

e, eggs; exb, excretory bladder; gp, genital pore; ic, intestinal ceca; sr, seminal receptacle; sv, seminal 

vesicle; u, uterus; up, uroproct; vf, vitelline follicles; vs, ventral sucker. 

duct; genital pore close to anterior margin of ventral 

sucker (Fig. IB). Ovary transversely elongate, 

slightly lobate (Fig. 1C) or with almost indistinct 

lobes (Fig. 2A), pretesticular. Seminal receptacle 

oval, preovarial or anterolateral to ovary 

(Fig. 1C). Vitelline follicles numerous, dorsally 

filling space between ventral sucker and ovary, 

ventrally forming 2 lateral bands starting at acetabular 

level or posterior to ventral sucker and 

reaching posteriorly to anterior margin of anterior 

testis (Figs. 1E-G, 2G); exceptionally, vitelline 

follicles preacetabular. Uterus sinuous, with numerous 

loops, reaching to body extremity posteriorly 

and completely filling body posterior to 

ovary (Fig. 2A, G, F). Metraterm thin-walled, 

opening into hermaphroditic duct. Eggs operculate, 

rather variable in size (Figs. 3, 4). Excretory 

bladder Y-shaped, long, with anterior branches 

anterolateral to intestinal ceca, reaching to pharynx 

(Figs. 1C, 2A, C, F). 


SCHOLZ ET AL.—REDHSCRIPTION OF PSEUDACANTHOSTOMUM PANAMENSE 149 

Figure 2. Pseudacanthostomum panamense. Adults from Ariopsis seemani, Colombia (A—D, G); nietacercariae 

from Dormltator latifrons, Mexico (E, H, I); adults from A. assimilis, Mexico (F, J, K). A, E, F: 

total view. B, H-K: oral sucker with circumoral spines. B: tegumental spines on only the right side and 

subtegumental gland cells on the left side are illustrated. C: detail of acetabular region with terminal 

genitalia; note connection of dorsal vitelline follicles (dashed) at level of ovary. D: posterior extremity with 

connection of intestinal ceca, opening to the outside, with the excretory bladder (uroproct). G: posterior 

part of body; note vitelline follicles reaching posteriorly to level of anterior testis. Scale bars in millimeters. 



Table 1. Measurements of Pseudacanthostomum panamense from different hosts* (in micrometers). 

Species 

Host 

Locality 

Author 

N 

Caballero 

et al., 1953 

3 

A. seemani 

Panama 

Present 

datat 

1 

P. panamense 

A. assimilis 

Mexico 

Present 

data 

8 

A. seemani 

Colombia 

Present 

data 

4 

P. floridensis 

A. fells 

U.S.A. 

Nahhas and 

Short, 1965 

2 

Present 

datav 

1 

Body length 

Body width 

Oral sucker 

Length 

Width 

Spines (no.) 

Spine length 

Spine width 

Prepharynx 

Pharynx 

Length 

Width 

Esophagus 

Ventral sucker 

Length 

Width 

Sucker ratio 

Anterior testis 

Length 

Width 

Posterior testis 

Length 

Width 

Ovary 

Length 

Width 

Eggs 

Length 

Width 

Uroproct 

2,440-2,540 

332-481 

76-133 

171-228 

26 

30-38 

11 

95-133 

122-171 

95-106 

11-19 

87-114 

106-114 

0.33-0.50 

175-232 

114-194 

194-285 

125-228 

103-129 

1 33-236 

19-21 

11 

absent 

2,784 

360 

21 1 

214 

27 

31-37 

12-13 

154 

125 

99 

14 

83 

86 

0.40 

173 

118 

202 

128 

112 

141 

21.5-25 

12.5-13.5 

present 

2,150-3,650 

230-370 

123-195 

130-238 

26-27 

28-45 

8-13 

30-138 

78-105 

63-98 

13-42 

70-103 

68-103 

0.41-0.68 

1 80-300 

78-180 

180-380 

1 1 5-220 

90-170 

55-190 

20-27.5 

10-14 

present 

1,850-2,580 

408-5 1 2 

186-208 

227-259 

27 

37-54 

9-12 

45-56 

99-122 

85-102 

22—23 

82-108 

83-118 

0.38-0.51 

214-250 

179-256 

208-272 

205-266 

99-122 

230-272 

23-28 

12-14.5 

present 

2,630-3,000 

489-750 

1 80-294 

309-330 

28 

42-60 

18-24 

— 

1 29-206 

— 

v. short 

118-155 

155-170 

0.54 

283-309 

1 80-283 

— 

— 

232-260 

298-309 

20-25 

1 1-14 

present 

3,050 

730 

266 

314 

28 

26-59 

15-19 

15 

218 

144 

— 

154 

170 

0.56 

278 

173 

317 

176 

224 

317 

23-26 

12-13.5 

present 

* Specimens from A. asximili.i from Bacalar, Mexico, are not included because they were flattened during fixation. 

t Measurements of the holotypes (CNHE 947 and USNPC 60087). 

Table 2. Number of circumoral spines of Pseudacanthostomum 

panamense. 

Host and country 

Ariopsix seemani (Panama) 

Ariopsis seemani (Colombia) 

Ariusfelis (U.S.A.) 

Ariopsis assimilis (Mexico) 

Arius gitatemalensis (Mexico) 

Dormitator latifrons* (Mexico) 

Total 

Metacercariae. 

Number 

of spines 

26 27 28 

— 1 — 

— 4 — 

— — 1 

1 14 2 

17 

4 

1 40 3 

Number 

of 

specimens 

1 

4 

1 

17 

17 

4 

44 

HOSTS: Ariopsis seemani (type host), A. assimilis, 

Arius guatemalensis, and A. felis (all Siluriformes: 

Ariidae) (Table 3). 

SITE: Intestine. 

GEOGRAPHIC DISTRIBUTION: Panama Viejo, 

Pacific coast, Panama (type locality); Colombia; 

Mexico (states of Tabasco and Quintana Roo, 

Atlantic coast; state of Jalisco, Pacific coast), 

U.S.A. (state of Florida) (Caballero et al., 1953; 

Nahhas and Short, 1965; Yamaguti, 1971; Pineda-Lopez 

et al., 1985; Scholz and Vargas- 

Vazquez, 1998). 

METACERCARIA: (based on 4 specimens from 

Dormitator latifrons; Fig. 2E, H, I): Body of 

excysted metacercariae elongate, 630-845 long 

by 147-182 wide. Oral sucker terminal, cup- 


SCHOLZ ET AL.—REDESCRIPTION OF PSEUDACANTHOSTOMUM PANAMENSE 15 1 

5 24 

z 

15.5 

14.5 

13.5 

11.5 

10.5 

9.5 

LENGTH 

A.a. MB A.a. MC A.s. C A.s. P A.f. U 

GROUP 

I Min-Max CH 25%-75% D Median value 

WIDTH 

8.5 

A.a. MB A.a. MC A.s. C A.s. P A.f. U 

GROUP 

Figure 3. Length (above) and width (below) of 

eggs of Pscudacanthostomum panamense from different 

hosts and geographical regions. Measurements 

in micrometers. Groups: A.a. MB, Ariopsis 

assimilis, Bacalar, Mexico; A.a. MC, A. assimilis, 

Chetumal Bay, Mexico; A.s. C, A. seemani, Colombia; 

A.s. P, A. seemani, Panama (holotype: CNHE 

947); A.f. \J, Arius felis, Florida, U.S.A. (holotype of 

P. floridensis: USNPC 60087). 

shaped, 111-124 long by 115-147 wide. Ventral 

sucker small, equatorial, 35-44 long by 35-41 

wide. Sucker ratio 1:0.31-0.34. Oral sucker 

armed with 1 circle of 27 spines; spines on dorsal 

side 21-28 long by 4-7 wide; on ventral side 

15-21 long by 4-5 wide. Prepharynx 49-90 

long; pharynx oval, 52-59 long by 36-52 wide; 

esophagus short. Intestinal ceca long, connected 

with excretory bladder near posterior extremity 

and opening outside by uroproct. Primordium of 

ovary postacetabular; testis primordia tandem, 

near posterior extremity. 

HOSTS: Dormitator latifrons and Gobiomorus 

maculatus (both Perciformes: Eleotridae) 

(Table 3). 

SITE: Liver, more rarely musculature of gills, 

mesentery, intestinal wall, occasionally muscles, 

heart, gonads, fins, scales. 

GEOGRAPHICAL DISTRIBUTION: Mexico (state 

of Jalisco, Pacific coast). 

Discussion 

Acanthostomid trematodes from 3 different 

definitive hosts, the ariid catfish Ariopsis seemani, 

A. assimilis, and Arius guatemalensis, and 

2 geographical regions (Colombia and Mexico) 

were found to be conspecinc with Pseudacanthostornum 

panamense. Examination of the holotype 

of P. panamense has shown that the original 

description (Caballero et al., 1953) was incorrect 

in reporting the following characters: 1) 

26 circumoral spines (there are in fact 27 spines 

in the holotype; Fig. 1A); 2) the absence of tegumental 

spines in the post-testicular region, 

which is actually spined; and 3) the absence of 

an uroproct (i.e., a connection of the intestinal 

ceca with the excretory bladder), which is actually 

present (Fig. ID). Consequently, the species 

diagnosis of P. panamense, the type species 

of the genus Pseudacanthostomum Caballero, 

Bravo-Hollis, and Grocott, 1953, is emended accordingly. 

In 1965, Nahhas and Short described another 

species, P. floridensis, to accommodate 2 specimens 

from Galeichthys (= Arius) felis from 

Florida, U.S.A. The authors differentiated this 

species from P. panamense by the number of 

circumoral spines (28 compared with 26), the 

greater extent of the vitellaria, and the presence 

of an uroproct. 

The presence of an uroproct in P. panamense 

was not reported by Caballero et al. (1953), who 

stated that there is no connection between the 

intestinal ceca and excretory bladder ("Los ciegos 

intestinales . . . no se abren en la vesicula 

excretora" [p. 121] and "Los ciegos intestinales 

no desembocan a la vesicula excretora" [p. 

122]). However, this study has demonstrated that 

an uroproct is in fact present in P. panamense 

(Fig. ID). Consequently, P. panamense and P. 

floridensis do not differ in this character (Table 

1). 

Although the number of circumoral spines is 

fairly stable in acanthostomid trematodes and 

can be species-specific (Brooks, 1980), some 



15.5 

15.0 

14.5 

14.0 

13.5 

13.0 

12.5 

JE 12.0 

Q 11.5 

% 11.0 

10.5 

10.0 

9.5 

9.0 

8.5 

« n 

O 0 

o o o 

0 000 

o o o 

o o o 

o 

0 O O 

o 

o o o 

o 

o 

o 

o o 

o 

o o o o 

o o o o o 

o 

o o o 

o 

O O O 0 

18 19 20 21 22 24 25 26 27 28 

LENGTH 

Figure 4. Range of size of eggs (length and width) of Pseudacanthostomum panamense. Measurements 

of all eggs measured (N = 59) grouped together. Values in micrometers. 

o 

o 

variability apparently exists (Brooks and Overstreet, 

1977; Ostrowski de Nunez, 1984; Scholz 

et al., 1995a, b). This is also the case in the 

present material (Table 2). Although a majority 

of specimens (93%) had 27 spines, including the 

holotype of P. panamense (see Results and Fig. 

1A), a few specimens had a different number of 

spines. One trematode from A. assimilis from 

Bacalar (Mexico) possessed 26 spines, and 2 

specimens from the same host (A. assimilis) 

from Chetumal (Mexico) had 28 spines (i.e., the 

identical number reported for P. floridensis) (Table 

2). 

The extent of distribution of vitelline follicles 

in the holotype of P. floridensis is actually more 

anterior than in P. panamense specimens. However, 

there is great variability in this feature. 

Trematodes from Ariopsis seemani have follicles 

reaching to the acetabular level (Fig. 1G) or 

even to the anterior margin of the ventral sucker 

(Fig. 1H), whereas those from A. assimilis have 

vitelline follicles mostly restricted to the postacetabular 

region (Fig. IE, F) with vitelline follicles 

reaching to the posterior border of the ventral 

sucker in only a few specimens. It also 

seems that contraction of the body influences the 

position of follicles; in contracted specimens vitelline 

follicles usually reach to the acetabular 

level (Fig. 1G, H), whereas in protracted worms, 

the follicles start rather far posterior to the ven- 

Table 3. Survey of hosts, localities, dates of collection, and parameters of infection with Pseudacanthostomum 

panamense. 

Host 

Country and locality 

No. of 

fish Mean 

infected/ inten- Minimum- 

Date examined sity maximum 

Adults 

A riopsis see man i 

A riopsis assim His 

A rius guatemalensis 

Metacercariae 

Dormitator latifronx 

Gobiomorus maculatus 

Colombia 

Bacalar, Quintana Roo, Mexico 

Chetumal Bay, Quintana Roo, Mexico 

Marismas Chalacatepec, Jalisco, Mexico 

Marismas Chalacatepec, Jalisco, Mexico 

Rio San Nicolas, Jalisco, Mexico 

Rio Cuitzmala, Jalisco, Mexico 

Rio Cuitzmala, Jalisco, Mexico 

5/96 

1/95 

10/96 

3/95 

3/95 

11/94 

9/95 

9/95 

1/95 

3/95 

9/95 

4/7 

1/1 

39/96 

3/3 

1/24 

1/5 

2/16 

5/7 

0/25 

2/37 

22/31 

1.5 1-2 

12 

7.5 1-30 

24 9-52 

39 39 

52 52 

1 1 

(not counted) 

— — 

3 1-5 

(not counted) 


SCHOLZ ET AL.—REDESCRIPTION OF PSEUDACANTHOSTOMUM PANAMENSE 153 

tral sucker (Fig. IE). It is evident that this character 

is not sufficiently stable and its taxonomic 

importance is questionable. Because P. floridensis 

was described on the basis of only 2 specimens, 

the anterior position of vitellaria should 

be confirmed in much more extensive material. 

Statistical analysis of egg measurements has 

revealed a great intraspecific variability in egg 

length and width (Fig. 4). Nevertheless, this 

analysis has not demonstrated any significant 

differences in the length and width of eggs of 

P. panamense and P. floridensis (Fig. 3). Eggs 

of P. panamense specimens from Colombia 

were larger than those of conspecific worms 

from Mexico, thus being more similar to eggs 

of P. floridensis (Fig. 3). Because of the identity 

of P. floridensis with P. panamense in almost all 

morphological and biometrical characters (the 

distribution of vitelline follicles is considered a 

doubtful and unsuitable taxonomic criterion for 

differentiation of these taxa), the former species 

is synonymized with P. panamense. 

On the basis of the proposed synonymy, the 

genus Pseudacanthostomum becomes monotypic, 

currently containing only 1 species, P. panamense. 

In the presence of an uroproct, P. panamense 

resembles members of the genus Pelaezia 

Lamothe-Argumedo and Ponciano-Rodriguez, 

1986, of the subfamily Acanthostominae 

Nicoll, 1914 (see Lamothe-Argumedo and Ponciano-Rodriguez, 

1986). However, Pelaezia differs, 

as all other genera of the Acanthostominae, 

in that the uterus is never situated posterior to 

the testes (mostly completely preovarial), whereas 

its loops reach to the posterior extremity in 

Pseudacanthostomum, the type genus of the subfamily 

Pseudacanthostominae Yamaguti, 1958. 

In addition, both species of Pelaezia, P. unami 

(Pelaez and Cruz-Lozano, 1953), the type species, 

and P. loossi (Perez-Vigueras, 1957), have 

different numbers of circumoral spines (30 and 

23, respectively; Pelaez and Cruz-Lozano, 1953; 

Perez-Vigueras, 1957; Brooks, 1980; Salgado- 

Maldonado and Aguirre-Macedo, 1991). 

The subfamily Pseudacanthostominae Poche, 

1926 contains only 2 genera, Pseudacanthostomum 

and Pseudallacanthochasmus Velasquez, 

1961, members of which parasitize marine fish 

in the Americas and Southeast Asia, respectively 

(Yamaguti, 1971). This subfamily differs from 

the Acanthostominae in possessing a long prepharynx 

(Yamaguti, 1971, p. 212). However, as 

demonstrated in this study, the prepharynx is 

usually short or even absent (Fig. 2A, F) in 

many P. panamense specimens. Moreover, the 

length of the prepharynx is highly variable, depending 

mainly on the state of contraction of the 

worms. Therefore, this feature should not be 

used as a differential criterion for the diagnosis 

of this subfamily. In other features, the subfamiliar 

diagnosis presented by Yamaguti (1971)— 

i.e., the uterus extending to the posterior extremity 

(different from other acanthostomid subfamilies 

except for Anisocladiinae Yamaguti, 

1958)—the ceca being equal and reaching to the 

posterior extremity, the ventral sucker being 

well apart from the anterior extremity, and the 

vitelline follicles being both anterior and posterior 

to the ovary (differing from Anisocladiinae) 

well characterize the subfamily Pseudacanthostominae. 

Metacercariae found in eleotrid fishes from 

the Pacific coast of Mexico are considered to be 

conspecific with P. panamense because of their 

morphology (Fig. 2E, H, I), in particular the 

presence of 27 circumoral spines (Fig. 2H, I) 

and the morphology of the intestinal ceca, which 

are connected with the excretory bladder near 

the posterior extremity, thus forming an uroproct 

(Fig. 2E). This is the first record of P. panamense 

from the second intermediate host. It can 

be assumed that the life cycle of this taxon resembles 

that of other acanthostomid trematodes 

(Yamaguti, 1975). The first intermediate host is 

a mollusk (snail), in which the cercariae develop; 

the second intermediate hosts are fish in 

which the metacercariae are encysted. The definitive 

host, an ariid catfish, becomes infected 

by ingesting fish with metacercariae. Dormitator 

latifrons and Gobiomorus maculatus are fish living 

in brackish water, i.e., in the same habitat in 

which ariid catfish occur; the latter become infected 

after consuming prey fish harboring metacercariae. 

Pseudacanthostomum panamense seems to be 

a common parasite of catfishes of the family 

Ariidae. Existing records of P. panamense from 

the southern U.S.A. (Florida), Mexico (both Atlantic 

and Pacific coasts), Panama (Pacific 

coast), and Colombia indicate that it is a species 

with a wide distribution in the Neotropical zoogeographical 

region on both the Pacific and Atlantic 

coasts. 


The authors are indebted to Elizabeth Mayen 

Pena, Guillermina Cabanas-Caranza, Juan Ma- 



nuel Caspeta-Mandujano, Rafael Baez-Vale, and 

Isabel Jimenez-Garcia, Institute of Biology, National 

Autonomous University of Mexico 

(UNAM), Mexico City, for help in sampling and 

examining fish in the state of Jalisco and to Raul 

Sima-Alvarez, Clara Margarita Vivas-Rodriguez, 

Ana Maria Sanchez-Manzanilla, Isabel Jimenez-Garcia, 

Sandra Martha Laffon-Leal, Sonia 

Zarate-Perez and Victor Ceja-Moreno, Center 

for Investigation and Advanced Studies of the 

National Polytechnic Institute (CINVESTAV- 

IPN), Unidad Merida, Mexico, for help in collecting 

fish in Quintana Roo. Thanks are due to 

Drs. J. Ralph Lichtenfels and Patricia Pilitt, U.S. 

National Parasite Collection, Beltsville, Maryland, 

U.S.A., and Dr. Rafael Lamothe-Argumedo 

and Luis Garcia-Prieto, Institute of Biology, 

National Autonomous University of Mexico 

(UNAM), Mexico City, for the loan of types of 

Pseudacanthostomum species. Dr. Patricia Pilitt 

is further acknowledged for her valuable help 

with egg size analysis, Martina Borovkova (Institute 

of Parasitology, Ceske Budejovice) for 

excellent technical help, and Luis Garcia-Prieto 

for providing the original description of P. panamense. 


Brooks, D. R. 1980. Revision of the Acanthostominae 

Poche, 1926 (Digenea: Cryptogonimidae). Zoological 

Journal of the Linnean Society 70:313- 

382. 

, and R. M. Overstreet. 1977. Acanthostome 

digeneans from the American alligator in the 

southeastern United States. Proceedings of the Biological 


Caballero y C., E., M. Bravo-Hollis, and R. G. Grocott. 

1953. Helmintos de la Republica de Panama. 

VII. Descripcion de algunos trematodos de peces 

marines. Anales del Institute de Biologfa, Universidad 

Nacional Autonoma de Mexico, Serie 

Zoologia 24:97-136. 

Eschmeyer, W. N. 1998. Catalog of Fishes. Vols. 1, 

2, 3. California Academy of Sciences, San Francisco, 

2905 pp. 

Lamothe-Argumedo, R., and G. Ponciano-Rodriguez. 

1986. Revision de la subfamilia Acanthostominae 

Nicoll, 1914 y establecimiento de dos 

nuevos generos. Anales del Instituto de Biologfa, 

Universidad Nacional Autonoma de Mexico, Serie 

Zoologia 56:301-322. 

Nahhas, F. M., and R. B. Short. 1965. Digenetic 

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de 2 especies de Mexico. Memorias del VII 

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66(2), 1999 pp. 155-174 

Ultrastructure of the Female Reproductive System of the Lesion 

Nematode, Pratylenchus penetrans (Nemata: Pratylenchidae) 

BURTON Y. ENDO', ULRICH ZuNKE2, AND WILLIAM P. WERGiN1-3 

1 U.S. Department of Agriculture, Agricultural Research Service, Plant Sciences Institute, Nematology 

Laboratory, Beltsville, Maryland 20705-2350, U.S.A., and 

2 Universtat Hamburg, Institut fur Angewandte Botanik, Marseiller Str. 7, 20355, Hamburg, Germany 

ABSTRACT: Transmission electron microscopy of the reproductive system of adult females of Pratvlenchus 

penetrans (Cobb) Filipjev and Schuurmans Stekhoven revealed details of oocyte development and the transformation 

of oocytes into eggs. Oogonial cell divisions were not observed; however, oogonial development into 

oocytes was distinctive in that most of the nuclei of ovarian cells were in the pachytene stage (i.e., prophase I 

of meiosis). In the midsection of the ovary, the oocytes increase in number, enlarge, and accumulate in a single 

row. Next, the oocytes enter a muscular oviduct and begin to accumulate lipid bodies and protein granules. The 

plasma membrane of the oviduct becomes plicated and forms cisternae; centralized membrane junctions establish 

openings for oocytes to enter the spermatheca. Spermatozoa traverse the lumen of the uterus and accumulate in 

the spermatheca. Each oocyte then passes through the spermatheca proximally and then traverses between 

columnar cells. The posteriad regions of the columnar cells attach to other uterine cells to form the central 

lumen of the uterus that extends beyond the vaginal opening and into the postvulvar uterine branch of the 

reproductive system. The fertilized egg is deposited to the exterior after passing between cuticle-lined vaginal 

and vulval walls supported by anteriad and posteriad muscle bands, which have ventrosublateral insertions on 

the body wall. 

KEY WORDS: transmission electron microscopy, lesion nematode, female reproductive system, Pratylenchus 

penetrans, Nemata, Pratylenchidae. 

The lesion nematodes, Pratylenchus spp., are 

among the most destructive plant pathogenic 

nematodes world-wide (Mai et al., 1977; Dropkin, 

1989; Zunke, 1990a). Dropkin (1989) reviewed 

the disease symptoms and pathogenesis 

of Pratylenchus species, which occur as single 

parasites or in combination with other pathogens. 

The ectoparasitic and endoparasitic feeding 

behavior of Pratylenchus penetrans (Cobb, 

1917) Filipjev and Schuurmans Stekhoven, 

1941, has been studied using video-enhanced 

contrast light microscopy (Zunke and Institut fiir 

den Wissenschaftlichen Film, 1988; Zunke, 

1990b) and transmission electron microscopy 

(TEM) (Townshend et al., 1989). Light microscopic 

studies also have described embryogenesis 

and postembryogenesis, including the molting 

process and the development of the reproductive 

system, in several species of Pratylenchus 

(Roman and Hirschmann, 1969a, b). In a 

related study of Ditylenchus triformis, Hirschmann 

(1962) illustrated the development of male 

and female reproductive systems during postembryogenesis, 

beginning with the genital primordium. 

Recently, we used TEM to describe the 


general anatomy of P. penetrans (Endo et al., 

1997) and the development of the testis, including 

the production and morphology of spermatozoa 

(Endo et al., 1998). These observations 

complement extensive studies on spermatogenesis 

and sperm ultrastructure of various species 

of cyst nematodes (Shepherd et al., 1973; Cares 

and Baldwin, 1994a, b, 1995). To extend these 

studies, TEM was used to describe the ultrastructure 

of the female reproductive system of 

P. penetrans, with emphasis on oocyte development 

in the ovary and the morphology of the 

oviduct, spermatheca, columnar cells, and central 

uterus. The studies of development of the 

eggs include evaluation of egg shell depositions 

in the uterus and the vaginal and vulval muscle 

morphology as they relate to egg laying. 


Infective and parasitic stages of P. penetrans were 

obtained from root cultures of corn (Zea mays Linnaeus 

'Ichief') grown in Gamborg's B-5 medium without 

cytokinins or auxins (Gamborg et al., 1976). Adults 

and juveniles were collected from infected root segments 

that were incubated in water. The samples were 

prepared for electron microscopy as previously described 

(Endo and Wcrgin, 1973; Wergin and Endo, 

1976). Briefly, nematodes, which were embedded in 

2% water agar or in infected roots, were chemically 

155 



fixed in buffered 3% glutaraldehyde (0.05 M phosphate 

buffer, pH 6.8) at 22°C for 1.5 hr, washed for 1 hr in 

6 changes of buffer, postfixed in buffered 2% osmium 

tetroxide for 2 hr, dehydrated in an acetone series, and 

infiltrated with a low-viscosity embedding medium 

(Spurr, 1969). Silver-gray sections were cut on an ultramicrotome 

with a diamond knife and mounted on 

uncoated 75 X 300 mesh copper grids. The sections 

were stained with uranyl acetate and lead citrate and 

viewed in a Philips 400T® electron microscope operating 

at 60 kV with a 30-|xm objective aperture. 

Results 

The female reproductive system of P. penetrans 

has amphidelphic development during early 

stages of postembryogenesis. However, later 

in the adult development, the posterior region of 

the ovary becomes reduced to a postvulvar uterine 

branch (Fig. 1). This change results in a telogonic 

gonad having a prodelphic orientation 

and a short postvulvar uterine branch that consists 

of epithelial cells. The cells in the anterior 

terminus of the ovary have spheroid nuclei, numerous 

polyribosomes, and high concentrations 

of rough endoplasmic reticulum (RER), mitochondria, 

Golgi, and electron-dense granules 

(Fig. 2 on Foldout 1). These germinal cells are 

completely ensheathed by spindle-shaped epithelial 

cells (Figs. 2, 3, 5, 6 on Foldout 2) that 

lie adjacent to and between the ovarian cells. In 

longitudinal view, the anterior gonad occupies 

about half the diameter of the body cavity (Figs. 

1, 6, 7). Nuclear divisions of oogonia were not 

observed in the specimens studied. However, as 

the ovarian cells increase in number and size, 

the germ cells contribute to a double row of 

overlapping oogonia (Figs. 3-5). Posteriorly, oocytes 

occur in a single row in the ovary and 

attain a slightly larger size than the germinal 

cells in the anterior region (Figs. 6-8 on Foldout 

3). The cellular organelles of the oocytes found 

in the midregion and proximal sites of the ovary 

are similar to those present in the oogonia (Figs. 

2—5). The well-defined nuclei of oocytes in the 

midregion of the ovary contain fragments of 

synaptonemal complexes, indicating that the oocytes 

are at the pachytene stage of prophase I 

(Figs. 4, 5). The synaptonemal complex is a tripartite 

structure consisting of a central scalariform 

element and a pair of lateral elements. This 

complex is surrounded by condensed chromatin 

(Fig. 5). The nucleoli are prominent, large, and 

electron-dense (Figs. 3, 5-7). Nuclei occupy a 

major part of the enlarged volume of oocytes in 

the proximal region of the ovary (Fig. 7). In actively 

reproducing females, oocytes near the anterior 

entrance of the oviduct or within the oviduct 

channel have an accumulation of electrontranslucent 

lipid droplets (Fig. 10). 

Oviduct 

The oviduct (Fig. 11 on Foldout 4) consists 

of a series of irregularly shaped cells having plicated 

plasma membranes. Although adjacent 

cells are generally separated by many intercellular 

spaces, membrane junctions interconnect 

the cells and allow for the extensive opening of 

the oviduct that is required during passage of the 

enlarged oocytes. Muscle filaments are associated 

with most of the cells along the length of 

the oviduct (Fig. 9). Oviduct cells contain mitochondria 

and nuclei with irregularly shaped nuclear 

membranes lined with electron-dense chromatin. 

The cells occupy the ventral region of the 

body cavity and lie adjacent to the intestinal epithelium 

(Fig. 11). In the distal portion of the 

oviduct, the cells are more tightly packed and 

have centrally located membrane junctions (Fig. 

12). In this region, the cells are not associated 

with muscle filaments. These closely arranged 

cells appear to function as a valve for the entry 

of oocytes into the spermatheca. Sperm were not 

observed on this side of the spermatheca. 

Spermatheca 

The terminal cells of the oviduct are attached 

closely to spindle-shaped cells of the spheroid 

spermatheca (Fig. 11). Membranes of the cells 

of the spermatheca are joined together with 

prominent lateral membrane junctions. Spermatozoa 

in the center of spermatheca have prominent 

masses of chromatin that are surrounded by 

clusters of mitochondria and widely dispersed 

fibrillar bundles (Fig. 11). These structures are 

similar to the major sperm protein bodies that 

have been identified and described in other nematode 

species (Shepherd et al., 1973). The spermatozoa 

seem to be suspended in a moderately 

electron-dense fluid similar in appearance to the 

contents of the vas deferens of males. The posteriad 

boundary of the spermatheca joins a series 

of columnar cells of the uterus (Figs. 11, 13). 

Columnar cells of the uterus 

Columnar cells leading posteriad from the 

spermatheca have plicated limiting membranes 

(Fig. 15 on Foldout 5) similar to those of cells 

in the oviduct (Fig. 8) but differing by the ab- 


A 

ENDO ET AL.—ULTRASTRUCTURE OF THE LESION NEMATODE 157 

B 

oviduct 

spermatheca 

columnar cells 

of uterus 

proximal region 


vulva 

$ 

columnar cells 


post-vulvar 

uterine branch 

vagina 

postvulvar 

uterine branch 

anus 

I 

1 

Figure 1. Line drawings of the female reproductive system of Pratylenchus penetrans, illustrating the 

features of pseudomonodelphic reproductive development. (A) Anterior region of the gonad containing 

oogonial cells and oocytes in growth phase. (B) Posterior region of the reproductive system showing a 

postvulvar uterine branch. Posteriad to the oocytes are the oviduct, spermatheca, columnar cells of the 

uterus, and the vaginal-vulval regions. 


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Figure 2. Distal region of the ovary of P. /7cne/raws showing 3 enlarged distal cells. Germinal cells 

(GC) arc precursors to oocyte development. Cells of the gonad epithelium lie adjacent to linearly arranged 

germ cells (i.e., oogonia and oocytes). GEN, gonad epithelium nucleus; M, mitochondria. (Note: In this 

and in later longitudinal figures that are illustrated with fold-outs (Figs. 2, 6, 8, 11, 15, 20), the proximal 

or left axis is toward the head of the nematode, whereas the distal or right axis is toward the tail. In the 

longitudinal sections that are illustrated in the single plates, the head to tail orientation is top to bottom.) 



Figure 3. Longitudinal section through oocytes of P. pcnetrans in the region of their growth phase. 

Nucleoplasm with fragments of chromatin and electron-dense nucleolus (Nu). GEN, gonad epithelium 

nucleus; N, oocyte nucleus. 



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Figure 4. Longitudinal, submedian section of ovary of P. penetrans showing oocytes (O) during initial 

stages of meiosis. M, mitochondria; N, nucleus; SM, somatic muscles. 

13). However, a preformed lumen is not appar- 

ent. In this region, the spermatozoa may be dis- 

placed from the spermatheca as the oocyte 

moves through the central part of the uterus. 

sence of muscle filaments within their cell 

boundaries. Membrane junctions between cells 

near the spermatheca define the region in which 

a lumen may form during oocyte passage (Fig. 



. '~SM$mm^?i•• 

/.r» •' ' '-'-'-^^^ 

yfa *• îv ' ;^;;!^:^"!tS^^?^^^S^^ ^^'^^^P^ff 

Figure 5. Transverse section of midregion of an ovary of P. penetrans, showing oocytes at pachytene 

stage of meiosis. Oocytes (O) are surrounded by gonad epithelial cells (GE), whose cytoplasm extends 

between the germinal cells. GEN, gonad epithelium nucleus; G, Golgi apparatus; M, mitochondria; Nu, 

nucleolus; N, nucleus; SC, synaptonemal complex. 

uterus have dense clusters of mitochondria and 

numerous polyribosomes throughout the cyto- 

plasm (Figs. 13, 15). The distal columnar cells 

of the uterus contain relatively large clusters of 

electron-dense material (Fig. 15). The lumen, 

When this occurs, the invagination of the plasma 

membrane of the columnar cell results in a spermatozoan 

that appears to have a double membrane 

(Fig. 13). Fertilization was not evident in 

the oocytes observed. Columnar cells of the 


.- x 

^- -N 

Figure 6. Longitudinal section of the proximal region of the ovary of P. penetrans, illustrating growth 

stage of oocytes. GE, gonad epithelium; Nu, nucleolus; N, nucleus. 



Figure 7. Longitudinal section of oocytes in proximal region of ovary of P. penetrans. An oocyte lies 

adjacent to the plicated cell membrane of the oviduct (Od). 

which forms as the egg passes into the columella, 

merges with the central, fluid-filled channel 

of the uterus (Fig. 15). The main channel of 

the uterus continues posteriad as a flattened or 

collapsed region that extends across the ventral 

sector of the body, terminating in a postvulvar 

uterine branch (Figs. 17-19). The uterus opens 

ventrally through the cuticle-lined vagina and 

vulva (Fig. 16). 

Egg passage 

The traversing of an oocyte or egg through 

the spermatheca or between columnar cells compresses 

epithelial cells (Figs. 14, 20 on Foldout 

6). In the absence of an egg within the uterus, 

the abundance of mitochondria and ribosomes 

and the occurrence of scattered secretory globules 

suggest that the columnar cells are metabolically 

active (Fig. 15). In the presence of an 

egg in the uterine channel, secretory granules 

occur intracellularly in compressed regions of 

uterine cells and extracellularly in the space between 

the surface of the egg and the limiting 

membrane of the columnar cells (Fig. 20). The 

accumulated secretory granules appear to contribute 

to the electron-dense deposits that form 

the egg shell. These deposits (Figs. 20, 21 on 

Foldout 6) accumulate on the vitelline layer, 

which is derived from the oolemma and has a 

unit membrane-like structure. Just below the vitelline 

layer is a chitinous layer followed by a 

lipid layer. The egg shell appears to be separated 

from the egg cytoplasm by a unit membrane. 

Tangential sections through the egg revealed 


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Figure 8. Longitudinal section of oviduct of P. penetrans. Plicated cell membranes (PCM) form cisternac-like 

invaginations among the enlarged irregularly shaped cells along the oviduct (Od), which lacks a 

preformed lumen. 


162 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 66(2). JULY 1999 

Figure 9. Longitudinal section of P. penetrans showing the junction between an oocyte and the oviduct 

(Od) supported by plicated cell wall membranes (PCM). Some cells with plicated membranes are associated 

with muscle filaments (MF). N, nucleus. 

electron-transparent lipid bodies, numerous electron-dense 

protein granules (Fig. 20), and the 

sperm or egg nucleus, which contains prominent 

chromatin (Figs. 20, 22 on Foldout 6). 

The vaginal-vulvar region 

The wall of the vagina is continuous with the 

body cuticle (Fig. 16). Hemidesmosomes attach 

pairs of broad muscle bands to anteriad and posteriad 

portions of the vulva cuticle. These 4 fiber 

bands extending anteriad are believed to correspond 

to the anterior dilatores vulvae, whereas 

the posteriad muscle fibers are the posterior dilatores 

vulvae (Fig. 16). The muscle bands project 

ventrolaterally and connect with somatic 

muscles along the body cuticle (Fig. 17). Adjacent 

and internal to the vulva wall muscles is a 

broad band of sphincter muscles or the constrictor 

vaginae. Adjacent and dorsal to the constrictor 

muscles are the anterior and posterior dilatores 

vaginae (Fig. 16). The cuticle of the vaginal 

wall is continuous with the ventral lining of 

the uterine channel. 

Anal region 

The body wall cuticle forms the lining of the 

anus and invaginates into the body cavity to 

form the lining of the rectum, which extends 

dorsoanteriad and subterminally into the tail region 

(Fig. 23). Proximally, the cuticular rectal 

channel is flat and broad (Fig. 25); distally it 

becomes elongate and oblong (Fig. 24). The 

noncuticularized region of the lumen is supported 

by rectal cells. The lumen may also be occluded 

by membrane evaginations of rectal cells 

joined laterally by membrane junctions. The H- 

shaped conformation of cells surrounding the 

rectum (Figs. 24, 25) coincides with the position 



mnî* 

10 

Figure 10. Transverse section of an oocyte (O) within the oviduct of P. penetrans. The oocyte is filled 

with large merging lipid droplets (LD) and a few protein granules (PG) that lie within the cytoplasmic 

matrix. 

of the depressor ani muscles that connect the 

dorsal rectal cuticle to the dorsal lateral body 

cuticle via hemidesmosomes. 

Discussion 

In a study of postembryogenesis, Roman and 

Hirschmann (1969a) determined that several 

species of Pratylenchus, including P. vulnus, P. 

coffeae, P. penetrans, P. brachyurus, P. zeae, P. 

neglectus, and P. crenatus, have an amphidelphic 

pattern of gonad development. However, the 

monosexual species P. scribneri follows a monodelphic 

pattern. In the amphidelphic species, 2 

gonads develop until the fourth molt, then the 

posterior gonad deteriorates. The remaining gonad 

is prodelphic, similar to that of P. penetrans. 

The distal end of the telogonic gonad is occupied 

by an ovary with a short germinal zone and 

an elongated growth zone. The germinal zone 

contains oogonial cells that undergo rapid mitotic 

divisions. In the growth zone, the oocytes 

enlarge. The ovary is followed by a narrowly 

folded oviduct that is connected to the spermatheca 

by a 12-celled constriction (Roman and 


11 

Figure 11. Longitudinal section of spermatheca of P. penetrans. The anterior boundary of the spermatheca 

(S) is surrounded by epithelial cells that are joined by membrane junctions (MJ). Spermatozoa 

(Sp) within the spermatheca contain electron-dense chromatin (C), mitochondria, and fihrHlar bundles 

(FB). The posteriad boundary of the spermatheca merges with enlarged columnar cells (CC) of the uterus. 

Columnar cells near the spermatheca contain enlarged electron-dense globules (EDG), numerous mitochondria, 

and ribosomes. 



Figure 12. Transverse section through cells at the proximal region of the oviduct and anterior region 

of the spermatheca of P. penetrans. Membrane junctions (MJ) join adjacent cells so that a lumen is formed 

for the oocyte passage into the spermatheca. 

•^^.^r\&^


1:0 jum 

Figure 14. Longitudinal section of an egg emerging from a spermatheca in a female P. penetrans. 

Spermatozoa (Sp) remaining in spermatheca (S) after oocyte passage appear to be oriented toward the 

emerged egg (E). Their electron-dense nuclei (N) and mitochondria adhere to the internal surface of the 

leading membrane of the spermatozoa. The membrane trailing the major body of the egg is intact and 

clearly separated from the spermatheca and its contents. 


15 

Submedian longitudinal section of columnar cells (CC) that delineate the lumen in the distal 

Figure 15. 

region of the uterus. The uterine channel (UC) posteriad from the columnar cells is filled with electrondense 

granular material (EDGM) that extends from beyond the vagina into the postvulvar uterine region 

of the reproductive system. This submedian section illustrates the continuity of the lining of the vaginal 

lumen (VO) with the body wall cuticle (C), but not with the lumen of the uterus. Tangential sections show 

muscle fibers that belong to the dilatorcs vaginae (DVa) and dilatores vulvae (DVu), which play a major 

role in egg deposition. EDGL, electron-dense globules; MJ, membrane junctions; PCM, plicated cell membranes; 

Vu, vulva. 


166 JOURNAL OF THE HRLMINTHOLOGICAL SOCIETY OF WASHINGTON, 66(2), JULY 1999 

1.0 Jim 

Figure 16. Longitudinal section of the uterus and vagina of P. penetrans. The cuticular lining of the 

vagina is continuous with the body wall cuticle (C) and extends internally to join the uterine channel 

(UC). Hemidesmosomes (H) attach the dilatores vaginae (DVa) and dilatores vulvae (DVu) muscles to the 

cuticle lining the vulva and vagina. Constrictores vaginae (CV) or sphincters surround and attach to the 

cuticle that forms the inner region of the vagina. 


EN DO ET AL.—ULTRASTRUCTURE OF THE LESION NEMATODE 167 

17 

SM . -.-. 

tfPlBFti 

. " , >'> - ', 

Figure 17. Transverse section through columnar cells (CC) of the uterus surrounding the proximal 

end of the uterine channel (UC) of P. penetrans. Muscle elements adjacent to the columnar cells are 

extensions of dilatores vaginae (DVa) or dilatores vulvae (DVu) muscles. Other extensions of these muscles 

(DVa and DVu) contact the laterosubventral somatic muscles. SM, somatic muscles. 

Hirschmann, 1969b). The spermatheca, which is 

composed of about 10 epithelial cells, is followed 

by the uterus that consists of 2 portions. 

The distal portion is composed of 12 large gland 

cells arranged in 4 rows of 4 cells each (tricolumella) 

that could have a role in egg shell deposition. 

The proximal portion is a short tube 

lined with a flat epithelium. This portion enters 

the vagina, which is lined with cuticle and supported 

by muscles and opens through the vulva. 

Specialized muscles dilate the vulva during oviposition 

(Hirschmann, 1971). 

In the present study, the ultrastructural observations 

were of adult specimens of P. penetrans. 

The morphology of the reproductive system that 

we observed is similar to the modified amphidelphic 

mode of development described in previous 

studies. Briefly, in Pratylenchus crenatus 

and P. penetrans (Dickerson, 1962) and in a diverse 

group of Pratylenchus species (Roman and 

Hirschmann, 1969a), the reproductive system is 

comprised of a functional anterior ovary and a 

posterior branch of the ovary reduced to a postvulvar 

uterine branch. The mitotic divisions occur 

in the blunt anterior terminus of the developing 

ovary (Coomans, 1962; Dickerson, 1962; 

Hirschmann, 1962; Yuen, 1964; Roman and 

Hirschmann, 1969a). Mitotic divisions were not 

observed in distal cells of the ovary. These 

events may occur rather quickly and may not 

have been captured at our fixation times. No distinction 

could be made between oogonial and 

oocyte cells in the anterior region of the ovary 

in several mature female specimens. However, 

lipid accumulations were observed among oocytes 

in the oviduct of an actively reproducing 

female. In addition, our observations suggest 

that extracellular lipid or protein granules could 

nourish the oocyte. 

Future work should involve labeling experiments 

to show the movement of secretory granules 

from ovarian epithelial cells across the limiting 

membranes of the oocyte. If this movement 

occurs, it could explain the accumulation of lipids 

and proteins that are associated with oocyte 

enlargement. Changes also appear to occur in 



SM 

v&J'BM 

•M$&L, 

KK^P 

sac «*• 

1.0 jim 

Figure 18. Transverse section of the uterine channel (UC) and muscles associated with the dilation of 

the vagina and vulva during egg deposition by P. penetrans. DVa, dilatores vaginae; DVu, dilatores vulvae; 

SM, somatic muscles. 

the morphology and porosity of the oocyte surface 

as it passes through the spermatheca, becomes 

fertilized by sperm, and begins to receive 

egg shell depositions from columnar cells prior 

to egg deposition. The electron-dense globules 

observed in some cells of the distal region of 

the columnar cells are unusual and are dissimilar 

to secretory granules observed in the cells forming 

the oviduct and proximal regions of the uterus. 

In our study, nuclear divisions were not observed 

in the distal region of the ovary of the 

mature females. This observation is consistent 

with the observations of Roman and Hirschmann 

(1969a), who found that oogonial divisions 

occur in the germinal zone of the ovary of 

fourth-stage juveniles and probably in young females, 

but not in mature, egg-laying females. 

Similarly, oogonial divisions were observed in 

populations of the soybean cyst nematode, Heterodera 

glycines, before and during the fourth 

molt. This species has a normal meiotic cycle 

and reproduces by cross-fertilization (Triantaphyllou 

and Hirschmann, 1962). 

The presence of synaptonemal complexes in 

many of the ovary cells proximal to the anterior 

end indicate that many of the oocytes are in the 

pachytene stage of prophase I. The presence of 

the tripartite synaptonemal complex is consistent 

with observations of nuclei in the testes of P. 

penetrans. This tripartite pattern differs from 

that of most species of Meloidogyne, which have 


ENDO ET AL.— ULTRASTRUCTURE OF THE LESION NEMATODE 169 

uc |jy? 

1.0 jim 

Figure 19. Transverse section through the uterine channel (UC) of P. penetrans showing the broad 

opening for egg passage. The bands of muscles adjacent to the uterine channel are the dilatores vaginae 

(DVa). The bands of muscles midventral and close to the body wall cuticle constitute the vulval wall 

muscles, dilatores vulvae (DVu). I, intestine; U, uterus. 

a bipartite pattern consisting of 2 lateral elements 

but lacking striated central elements 

(Westergaard and von Wettstein, 1972; Goldstein 

and Triantaphyllou, 1995). Whether or not 

the tripartite pattern of the synaptonemal complex 

occurs in most species of Pratylenchus is 

not yet determined. Observations of Caenorhabditis 

elegans show that developing oocytes are 

arranged in single file along the proximal arm 

of the ovary, the site of gametogenesis in a hermaphrodite. 

Oocytes are arrested at diakinesis in 

meiotic prophase I. After the oocyte is fertilized, 

the zygote moves through the spermatheca to the 

uterus, where meiosis is completed (Kimble and 

Ward, 1988). 

In Xiphinema theresiae, the ovary has 2 types 

of cells: the ovarian epithelial cells and the germ 

cells (Van De Velde and Coomans, 1988). The 

ovarian epithelial cells form a thin layer around 

the germ cells and have nuclei between some of 

the germ cells. At some sites, processes of ovarian 

epithelial cells extend inward to form a central 

cytoplasmic mass, which has cytoplasmic 

contact with the germ cells. These cells develop 

2 membrane-derived features, the villi and the 

small coated bulges, which are thought to play 

a role in transport. However, X. theresiae does 

not have a typical rachis, a large, clearly delineated 

structure, around which oogonia are arranged 

and make cytoplasmic contact. 

Bird and Bird (1991) described a typical rachis 

for the telogonic and didelphic reproductive 

system of the female root-knot nematode, Meloidogyne 

javanica. The oogonia are radially arranged 

around a central anucleate rachis to 

which oogonia are attached by cytoplasmic 

bridges. In C. elegans, which is monodelphic, 

mitotic germ cells occupy the distal end of the 

ovary, and meiotic cells occupy the remaining 

portion of the gonad (Kimble and White, 1981). 

A typical rachis was not observed in the female 

reproductive system of P. penetrans. 


SM ,v 

20 

Figures 20-22. Section of an egg of Pratylcnchiis penetrans. 20. Tangential section through an egg within the postvulvar uterine branch. This section is from the same specimen shown 

shows an oocyte in the oviduct. The oocyte cytoplasm is filled primarily with lipid bodies. In contrast, the cytoplasm of the egg contains numerous irregularly shaped electron-translucent lip 

numerous electron-dense protein granules (PG) that generally occur around the lipid droplets. The nucleus (N) is located near one end of the egg. The egg shell (ES) has a well-defined 

vitelline layer and an electron-translucent inner chitinous layer. Electron-dense secretory granules (SG) accumulate on the surface of the egg. Similar granules occur singly or in clusters 

cells of the uterus or supporting cells of the uterine channel. The intercellular electron-dense granules originating in these cells appear to be secreted and deposited on the egg shell. C, 

muscle. 21. Enlargement of a portion of the egg shell shown in Figure 20. Secretory granules (SG) near the surface of the egg shell appear to contribute to the electron-dense outer vitelline 

easily distinguished from the electron-translucent inner chitinous layer (CL). 22. Enlargement of nucleus (N) of egg shown in Figure 20. Chromatin (Cr) occurs within the nucleoplasm. 



Figures 23-25. Section of the rectal region of Pratylenchus penetrans. 23. Longitudinal section of the 

rectal region of an adult female. The complex of membrane junctions denotes part of the rectal valve 

(RV). The rectal channel (RC) extends posteriad and is supported by the cell membranes and cuticle. The 

depressor ani muscles (DM) are located on the dorsal surface of the rectal cuticle near the anal (A) opening. 

SM, somatic muscles; C, cuticle. 24. Transverse section of the rectal channel (RC) supported by rectal 

cells. 25. Transverse section of the rectal channel (RC) near the attachment of the depressor ani muscles 

(DM) to the cuticle lining of the channel. The depressor ani muscles have a dorsosublateral orientation. 



The ovary of P. penetrans has cells that appeal' 

as single or double rows of germ cells enclosed 

by epithelial cells that are characterized 

by irregularly shaped nuclei. These nuclei have 

electron-dense chromatin that tends to accumulate 

along the inner surface of the nuclear membrane. 

Cytoplasmic contact between germ cells 

and epithelial cells appears to be minimal and is 

not similar to that described for other species 

(Hirschmann, 1971). The distinctive morphology 

of epithelial cells of P. penetrans ovaries was 

also noted in the cluster of cells anteriad to the 

spermatheca. These epithelial cells, in conjunction 

with oviduct cell wall, may affect movement 

of oocytes from the oviduct into the spermatheca. 

The plicated membranes of cells lining the 

oviduct and their capacity to expand and accommodate 

the moving oocyte were previously illustrated 

for Rotylenchus goodeyi (Coomans, 

1962) and the Hoplolaiminae (Yuen, 1964). This 

process may also operate in the spermatheca and 

columnar cells. However, a fundamental difference 

occurs in their cellular contents and functions. 

In P. penetrans, the presence of muscle 

filaments, which line the oviduct, suggests that 

they have an active role during oocyte passage 

toward the spermatheca. The cluster of cells, 

which have centralized membrane junctions at 

the anterior region of the spermatheca and are 

described as a 12-celled constriction in Pratylenchus 

spp. (Roman and Hirschmann, 1969b), 

may function as a valve, which opens or closes 

to regulate oocyte passage into the spermatheca. 

The female reproductive system of Xiphinema 

meridianum has an ovarial sac that is muscular 

and an outer membrane that is highly plicated. 

The proximal part of the oviduct is narrow and 

tube-like, but widens into the pars dilatata oviductus. 

The oviduct of X. meridianum lacks a 

preformed lumen except for the pars dilatata 

oviductus, where the lumen is narrow. The ultrastructure 

of the female gonoduct of X. theresiae 

is similar to that described for X. meridianum 

(Van De Velde et al., 1990a, b). In P. penetrans, 

the ultrastructure of the lumen of the 

oviduct and that of the columnar cells in the central 

region is similar to the plicated cell membranes 

described for Xiphinema, which also 

lacks a preformed oviduct lumen. 

Ward and Carrel (1979) described oocyte migration 

in the hermaphroditic species C. elegans. 

In this species, migration is accompanied by 

sporadic contractions of the oviduct walls and 

the oocyte cytoplasm. As contractions of the 

oviduct wall increase, the oocyte moves through 

the spermathecal constriction and into the spermatheca. 

A similar mechanism may propel oocytes 

through the muscular oviduct of P. penetrans. 

The spermatheca of P. penetrans is denned 

by the adjoining columella cells. Columella cells 

are joined by a junctional complex to form a 

continuous lumen between the spermatheca and 

the central uterus. The ultrastructure of the columella 

cells of the uterus is distinctly different 

from the cells forming the oviduct. In the uterus, 

the columella cells have more ribosomes, mitochondria, 

secretory granules, and membrane 

junctions than the cells adjoining the oviduct. In 

the female gonad of Rotylenchus goodeyi, the 

uterus has two regions: the quadricolumella and 

a thin-walled, muscular region that lies between 

the quadricolumella and the vagina (Coomans, 

1962). This muscular region was not observed 

in P. penetrans. However, the muscle bands that 

were found near the vagina and vulva appear to 

have a major role in the movement of the oocyte 

or egg through the genital tract as well as in 

dilation of the vagina and vulva during egg deposition. 

In a study of about 50 females of R. goodeyi, 

Coomans (1962) determined that the quadricolumella 

is a glandular region in the uterus and 

probably secretes the egg shell. The glandular 

region was particularly large and granular when 

a well-developed egg was found in the oviduct. 

As the egg passed into the uterus, the glandular 

cells appeared to empty and a thin layer formed 

around the egg shell. In P. penetrans, the uterus 

with eggs has electron-dense secretory granules 

in the columella cells, and cells of the uterine 

wall are appressed and flattened by passage of 

an egg. At this time, the secretory granules are 

found between the uterine wall and the limiting 

membrane of the egg. 

We concur that the columella cells serve a 

functional role in providing secretions that contribute 

to formation of the egg shell, as proposed 

by Coomans (1962) for R. goodeyi and by investigators 

of other nematode species (Coomans, 

1965; Bleve-Zacheo et al., 1976; McClure and 

Bird, 1976; Bird and Bird, 1991). This hypothesis 

is further supported by ultrastructural examinations 

of cross sections of egg shells of P. 

penetrans (Hilgert, 1976). Our study illustrates 



sites where secretory granules appear to merge 

with the electron-dense outer layer of the egg 

shell. 

Fertilization of the oocyte occurs between the 

oviduct and the uterus, regardless of the presence 

or absence of a spermatheca (Bird and 

Bird, 1991). In a light microscope study, Hung 

and Jenkins (1969) observed oogonial divisions 

at the apical portions of the gonads of young 

females of P. penetrans and P. zeae. In P. penetrans, 

only 1 sperm appears to enter each oocyte 

as it passes through the spermatheca. After 

sperm penetration, the oocyte nucleus moves 

centrally and undergoes maturation divisions. 

After the initial reduction division and the second 

division of meiosis, the egg pronucleus is 

formed, which in turn fuses with a sperm nucleus 

to form the zygote shortly before or after egg 

deposition. In P. penetrans, the chromosome 

number is 2n = 10, whereas in P. zeae, which 

reproduces by mitotic parthenogenesis, 2n = 26. 

In the present ultrastructural study of P. penetrans, 

the stage at which fertilization occurs 

could not be determined, but sperm was observed 

in the developing eggs inside the uterus. 

In Ascaris, Poor (1970) showed that when 

male sperm and oocyte membranes establish 

contact, the membranes appear to fuse. In other 

cases, considerable interdigitation occurs between 

the opposing gamete surfaces. Subsequently, 

the sperm progresses to a position deep 

within the oocyte cytoplasm. In some cases, fusion 

appears to take place between the oolemma 

and the lateral margins of the sperm. After fusion 

of the gamete membranes, the underlying 

interdigitating membranes disappear and the 

contents of the spermatozoan are within the oocyte 

(Poor, 1970). 

In P. penetrans, the ultrastructure of initial 

stages of gamete fusion was not examined. Hung 

and Jenkins (1969) used light microscopy to 

show that the oocyte nucleus of P. penetrans 

undergoes 2 divisions after sperm penetration. 

Roman and Triantaphyllou (1969) studied the 

maturation of oocytes and fertilization in P. penetrans, 

P. vulnus, and P. coffeae. In these species, 

oocytes in the spermatheca contain a small 

number of bivalent chromosomes at prometaphase 

I. One spermatozoan enters each oocyte, 

which then rapidly completes the first division. 

At telophase I, the chromosomes that form the 

first polar body nucleus are discrete and can be 

used to determine the haploid chromosome number. 

A second maturation division follows rapidly, 

and the sperm pronucleus is formed and 

then fuses with the egg pronucleus to form the 

zygote nucleus. Fusion of the pronuclei was observed 

in nondeposited eggs of P. penetrans and 

in eggs laid by P. coffeae. The primary oocyte 

of the dog heartworm, Dirofilaria immitis, completes 

meiosis only after fertilization by a male 

gamete in the seminal vesicle (Delves et al., 

1986). After meioses I and II are completed in 

the oocyte and the 2 polar bodies are extruded, 

the haploid chromosome complement of the female 

unites with that of the male and re-establishes 

the diploid chromosome number in the zygote. 

Oogenesis and the mode of reproduction were 

also studied in populations of the soybean cyst 

nematode, H. glycines. Triantaphyllou and 

Hirschmann (1962) determined that oogonial divisions 

occur before and during the fourth molt. 

Maturation of oocytes in inseminated females 

consists of 2 meiotic divisions and the formation 

of 2 polar nuclei. Nine bivalents are present at 

metaphase I in all populations. Sperm enters the 

oocytes at late prophase or early metaphase I. 

After the second maturation division, sperm and 

egg pronuclei fuse to form the zygote nucleus. 

The vulval walls of P. penetrans are attached 

to 2 sets of dilatores vulvae. Four bands on each 

side of the vulval wall are directed anteriad and 

posteriad and insert ventrolaterally on the body 

wall. This orientation of muscles coincides with 

light microscopic observations of R. goodeyi 

(Coomans, 1962). The dorsally and ventrally located 

dilatores vaginae have been diagrammed 

for P. penetrans (Kisiel et al., 1972; Hilgert, 

1976; Mai et al., 1977). Although the vulval 

muscles were not clearly defined in the latter 

studies, they did appear as prominent muscle 

bands in our study. 

In the hermaphrodite C. elegans stained with 

phalloidin, a photomicrograph clearly showed 4 

of 8 vulval muscle cells that were inserted near 

the vulval opening and at the lateral epidermis 

(Waterston, 1988; Bird and Bird, 1991). Our observations 

of P. penetrans tend to support the 

concept that the dilatores vulvae play a major 

role in egg deposition. 

In conclusion, the ultrastructure of the reproductive 

system of P. penetrans increases our understanding 

of the anatomical, physiological, 

and phylogenetic relations among a vast array of 

nematodes, including many plant parasitic nem- 



atodes. In the future, comparative studies should 

be conducted on reproductive anatomy and 

physiology of sedentary endoparasitic species 

such as Meloidogyne, the cyst nematode species, 

and the migratory and free-living forms, such as 

C. elegans. These observations may provide 

clues for modifying or disrupting nematode reproduction 

and could lead to new methods of 

control for economically destructive species. 


The authors thank Sharon Ochs for technical 

support in specimen preparation for TEM and 

photographic processing, Chris Pooley for preparing 

the final plates, Naeema Latif for maintenance 

and extraction of P. penetrans used in 

the study, Charles Murphy for TEM support 

data, Zafar Handoo for preparing specimens 

used in light microscopic observations of the reproductive 

organs of P. penetrans, and Robert 

Ewing for the illustration used in Figure 1. Mention 

of trade names or commercial products in 

this article is solely for the purpose of providing 

specific information and does not imply recommendation 

or endorsement by the U.S. Department 

of Agriculture. 


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Nematologie 13:331-337. 

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Germany. 

1999-2000 MEETING SCHEDULE OF THE 

HELMINTHOLOGICAL SOCIETY OF WASHINGTON 

13 October 1999 

17 November 1999 

19 January 2000 

12 March 2000 

10 May 2000 

Animal Parasitology Laboratories, Beltsville Agricultural Research Center, 

USDA, Beltsville, MD, 7:30 pm (Contact person: Eric Hoberg, 301- 

504-8588) 

Anniversary Dinner—meeting location TEA 

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 Farrell, 215-898-8561) 



66(2), 1999 pp. 175-179 

Skrjabinodon piankai sp. n. (Nematoda: Pharyngodonidae) and Other 

Helminths of Geckos (Sauria: Gekkonidae: Nephrurus spp.) from 

Australia 

CHARLES R. BURSEYU AND STEPHEN R. GOLDBERG2 

1 Department of Biology, Pennsylvania State University, Shenango Campus, 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@whittier.edu) 

ABSTRACT: Skrjabinodon piankai sp. n. from the large intestine of the Australian gecko Nephrurus laevissimus 

is described and illustrated. It is also reported from Nephrurus levis and Nephrurus vertebralis. Skrjabinodon 

piankai differs from 6 other Australian realm species in the number of tail filament spines and egg shape. Other 

helminths found include Oochoristica piankai, Maxvachonia brygooi, Pharyngodon tiliquae, Physalopteroides 

filicauda, Wanaristrongylus ctenoti, third-stage larvae of Abbreviata sp., third-stage larvae of Physaloptera sp., 

and Raillietiella scincoides. New host records are established for O. piankai and R. scincoides in N. laevissimus; 

M. brygooi and P. filicauda in N. levis; and P. tiliquae in N. vertebralis. 

KEY WORDS: Skrjabinodon piankai sp. n., Pharyngodonidae, helminths, Nephrurus laevissimus, Nephrurus 

levis, Nephrurus vertebralis, Gekkonidae, Sauria, Australia. 

Four species of Skrjabinodon Inglis, 1968 

have been reported previously from reptiles of 

Australia. Parathelandros oedurae Johnston and 

Mawson, 1947, was originally described from 

specimens taken from the robust velvet gecko, 

Oedura robusta Boulenger, 1885, collected in 

southeast Queensland. Inglis (1968) revised Parathelandros 

Diesing, 1861, retaining the genus 

for parasites of Australian amphibians and erecting 

Skrjabinodon as a new genus for parasites 

of reptiles; 7 species, including P. oedurae, were 

placed in the new genus. Skrjabinodon smythi 

Angel and Mawson, 1968 was described from 

the marbled gecko, Christinus (=Phyllodactylus) 

rnarmoratus (Gray, 1845) collected in South 

Australia. Skrjabinodon parasmythi Mawson, 

1971, from the thick-tailed gecko, Underwoodisaurus 

milii (Bory de Saint-Vincent, 1825), and 

Skrjabinodon leristae Mawson, 1971, from a 

skink, Lerista sp., were described from specimens 

collected on Flinders Island, South Australia. 

In addition, 2 species, Skrjabinodon trimorphi 

Ainsworth, 1990, from the common 

skink, Leiolopisma nigriplantara Patterson and 

Daugherty, 1990, and Skrjabinodon poicilandri 

Ainsworth, 1990 from the common gecko, Hoplodactylus 

maculatus Boulenger, 1885, have 

been described from specimens collected in New 

Zealand (Ainsworth, 1990). 


Nephrurus Giinther, 1876, is an endemic Australian 

gecko genus containing arid-adapted species 

characterized by large heads and short, fat 

tails that terminate in a small knob (Cogger, 

1992). The spinifex knobtail gecko, Nephrurus 

laevissimus Mertens, 1958, occurs in southeastern 

Western Australia, northwestern South Australia, 

and southern parts of the Northern Territory; 

the smooth knobtail gecko, Nephrurus levis 

De Vis, 1886, occurs from the central coast of 

Western Australia to the arid parts of all states 

except Victoria; Storr's knobtail gecko, Nephrurus 

vertebralis Storr, 1963, occurs from the lower 

central interior of Western Australia to South 

Australia (Cogger, 1992). The ranges of these 3 

nocturnal species overlap in Western Australia 

(Cogger, 1992). However, they are reported to 

favor different habitats (Pianka, 1972): TV. laevissimus 

is associated with sandridges; N. levis 

occurs on sandplains vegetated with dense 

clumps of perennial grasses of Triodia Brown, 

1810; and N. vertebralis is associated with 

shrubs of Acacia Miller, 1754. 

There are 4 previous reports of nematodes 

from N. laevissimus (Jones, 1985, 1987, 1995a, 

b), 1 report from N. levis (Jones, 1995b), but, to 

our knowledge, no reports from N. vertebralis. 

We describe here a new species of Skrjabinodon 

that was found in the large intestines of TV. laevissimus, 

N. levis, and N. vertebralis from Western 

Australia and the Northern Territory and list 

other helminth parasites found in these hosts. 

175 



Table 1. Prevalence (%) and mean abundance of helminths of Nephrurus laevissimus, N. levis, and N. 

vertebralis from Australia. 

Nephrurus laevissimus (N = 36) Nephrurus levis (N = 13) Nephrurus vertebralis (N = 3) 

Helminth P* (%) A ± SD1 P (%) A ± SD SD 

Cestoda 

Oochoristica piankai 3± 0.14 ±0.83 

Nematoda 

Maxvachonia brygooi — — 

Pharyngodon tiliquae — — 

Physalopteroides filicauda 17 

Skrjabinodon piankai 22:]: 

Wanaristrongylus ctenoti — — 

Abbrcviata sp. (larvae) 5 0.08 ± 0.37 

Physaloptera sp. (larvae) 3 0.03 ± 0.17 

Pentastomatida 

Raillietiella scincoides 5t 0.06 ± 0.23 

31* 

62$ 

8 

31 

16.08 ± 56.47 

53.69 ± 78.69 

0.15 ± 0.56 

0.85 ± 1.95 

33:j 

66:i 

4.00 ± 6.93 

55.33 ± 94.98 

* P = Prevalence (number of hosts infected with a parasite species divided by the number of hosts examined X 100). 

t A ± SD = mean abundance (summation of number of individuals of a parasite species per host divided by the number of 

hosts examined) ± standard deviation. 

$ New host record. 


Thirty-six N. laevissimus, 13 N. levis, and 3 N. vertebralis 

from the collections of the Natural History 

Museum of Los Angeles County (LACM) were examined: 

N. laevissimus, mean snout-vent length (SVL) 

= 64.6 ± 8.5 mm SD, range 51-80 mm, LACM 

57145, 57146, 57156, 57159, 57160, 57162, 57163, 

57165, 57170, 57173-57175, 57177, 57180-57182, 

57189, 57192, 57193, 57196-57198, 57201, 57204, 

57209, 57210, 57213, 57215-57217, 57219, 57220, 

57225-57228, collected 34 km west of Lorna Glen 

homestead, Western Australia (26°14'S, 121°13'E); N. 

levis, SVL = 77.2 ± 10.2 mm SD, range 64-98 mm, 

LACM 57008, 57009, collected 29 km south of Neale 

Junction, Western Australia (28°30'S, 125°50'E), 

LACM 57011-57014, 38 km east of Laverton, Western 

Australia (28°28'S, 122°50'E), LACM 57018, 

57020, 16 km southeast of Renhan's Well, Northern 

Territory (21°24'S, 130°53'E), LACM 57026, 57029, 

11 km south of The Granite, Northern Territory 

(20°38'S, 130°25'E), LACM 57032, 57037, 57039, 13 

km west of Neale Junction, Western Australia 

(28°17'S, 125°40'E); N. vertebralis, SVL = 81.3 ± 7.6 

mm SD, range 73-88 mm, LACM 57047, 6 km east 

of Stony Point, Western Australia (28°05'S, 124°15'E), 

LACM 57049, 57051, 14 km northeast of Millrose 

homestead, Western Australia (26°17'S, 121°00'E). 

These specimens had been collected between October 

1966 and January 1968 for use in an ecological study 

(Pianka and Pianka, 1976). Because the ecological 

study included stomach analysis, only small and large 

intestines remained with the carcasses. Each intestine 

was searched for helminths using a dissecting microscope. 

Cestodes were stained with hematoxylin and 

mounted in balsam for identification; other helminths 

were identified from the glycerol mounts. Measurements 

are in mm unless otherwise indicated. 

Results 

Helminths representing 9 species were found: 

the cestode Oochoristica piankai Bursey, Goldberg, 

and Woolery, 1996; the nematodes Maxvachonia 

brygooi Mawson, 1972, Pharyngodon 

tiliquae Baylis, 1930, Physalopteroides filicauda 

Jones, 1985, Skrjabinodon piankai sp. n. (this 

paper), Wanaristrongylus ctenoti Jones, 1987, 

Abbreviata sp. (third-stage larvae only), Physaloptera 

sp. (third-stage larvae only); and the 

pentastomid Raillietiella scincoides Ali, Riley, 

and Self, 1984. Prevalence and mean abundance 

are given in Table 1. Selected specimens were 

placed in vials of alcohol and deposited in the 

U.S. National Parasite Collection (USNPC). 

These are parasites from N. laevissimus: O. 

piankai, USNPC 88189; P. filicauda, USNPC 

88190; 5. piankai, USNPC 88191; Abbreviata 

sp. (larva), USNPC 88192; Physaloptera sp. 

(larva), USNPC 88193; R. scincoides, USNPC 

88194. N. levis: M. brygooi, USNPC 88195; P. 

filicauda, USNPC 88196; 5. piankai, USNPC 

88197; W. ctenoti, USNPC 88198; Abbreviata 

sp. (larva), USNPC 88199. Nephrurus vertebralis: 

Pharyngodon tiliquae, USNPC 88200; S. 

piankai, USNPC 88201. 

Skrjabinodon piankai sp. n. 

(Figs. 1-8) 

Description 

GENERAL: Oxyurida: Pharyngodonidae Travassos, 

1919, Skrjabinodon Inglis, 1968. Small, 


BURSEY AND GOLDBERG—SKRJABINODON PIANKA1 SP. N. FROM AUSTRALIA 177 

o 

CO 

8 

Figures 1—8. Skrjabinodon piankai sp. n. 1. Female, entire, lateral view. 2. Female, en face view. 3. 

Male, entire, lateral view. 4, Egg, pronuclear stage. 5. Egg, morula stage. 6. Male, posterior end, ventral 

view. 7. Spicule. 8. Male, posterior end, lateral view. 



cylindrical nematodes, extremities tapered in 

both sexes; moderate sexual dimorphism, males 

approximately one-third length of females. Cuticle 

with fine transverse striations along entire 

body. Mouth surrounded by 3 small lips; prominent 

lateral amphids just behind lips. Lateral 

alae present in both sexes. Tail narrowing 

abruptly behind anus to form filamentous appendage. 

MALE (based on 10 specimens): Small, 

white, fusiform nematodes tapering both anteriorly 

and posteriorly, body usually bent to give 

comma-shaped appearance. Length 1.27 (1.19- 

1.40), body length 1.00 (0.97-1.12), tail filament 

0.25 (0.22-0.29). Width at level of excretory 

pore 0.12 (0.10-0.14). Cuticle with striations approximately 

3 |xm apart. Esophagus excluding 

bulb 0.216 (0.204-0.242), bulb length 0.049 

(0.040-0.054), bulb width 0.052 (0.046-0.057). 

Nerve ring 0.118 (0.103-0.125) and excretory 

pore 0.342 (0.306-0.383) from anterior end, respectively. 

Lateral alae 0.012 (0.010-0.015) 

wide, beginning midway between lips and nerve 

ring and ending just anterior to third pair of caudal 

papillae. Spicules 0.055 (0.051-0.057). Tail 

filament with 1 (0-2) small spine. Cloaca and 

associated papillae slightly raised from body 

surface but not on distinct cone. Caudal alae absent, 

3 pairs of sessile papillae, 1 pair precloacal, 

1 pair postcloacal, third pair occurring on base 

of tail filament. Single tubular testis reflexed just 

posterior to excretory pore. 

FEMALE (based on 10 gravid specimens): 

Small, white nematodes tapering anteriorly and 

posteriorly. Length 3.21 (2.80-3.58), body 

length 2.55 (2.21-2.86), tail filament 0.66 (0.58- 

0.71). Width at level of vulva 0.22 (0.18-0.25). 

Lateral alae 2 |xm (2-3 |o,m) wide, doubled, approximately 

50 (Jim apart at midbody, beginning 

in a single point at level of nerve ring, ending 

in a single point just anterior to beginning of tail 

filament. Cuticle with transverse striations approximately 

2 u,m wide. Mouth with 3 lips, each 

lateral lip with 1 small papilla. Esophagus excluding 

bulb 0.295 (0.285-0.310), bulb length 

0.073 (0.068-0.080), bulb width 0.087 (0.080- 

0.094). Nerve ring 0.125 (0.115-0.145), excretory 

pore 0.477 (0.410-0.535), and vulva 0.535 

(0.485-0.610) from anterior end, respectively. 

Thick-walled muscular ovijector extending posteriorly 

0.40 mm, then continuing as thin-walled 

vagina 0.18 mm in length before joining 2 uteri, 

1 directed anteriorly and the other posteriorly. 

Ovarian and uterine coils not extending to vulva. 

In fully gravid females, uterus extending from 

slightly behind vulva to end of body. Egg barrel 

shaped, slightly flattened on 1 side, operculum 

at each end, length 105 fjim (100-108 |xm), 

width 34 (Jim (31-37 (xm). Egg surface finely 

pitted, having a ground-glass appearance. Development 

to morula stage at deposition. Tail 

spines 5 (4-7). 


TYPE HOST: Nephrurus laevissimus Mertens, 

1958. 

ADDITIONAL HOSTS: Nephrurus levis De Vis, 

1886; N. vertebralis Storr, 1963. 

TYPE LOCALITY: 34 km west of Lorna Glen 

homestead, Western Australia (26°14'S, 121°13'E). 

SITE OF INFECTION: Large intestine. 

TYPE SPECIMENS: Holotype, male, U.S. National 

Parasite Collection no. 88186; allotype, 

female, no. 88187; paratypes (9 males, 9 females), 

no. 88188. 

ETYMOLOGY: The specific epithet honors 

Eric R. Pianka, Denton A. Cooley Centennial 

Professor of Zoology, University of Texas at 

Austin, for his pioneering studies on the ecology 

of Australian lizards. 

Remarks 

Skrjabinodon piankai is the seventh species of 

Skrjabinodon to be reported from the Australian 

biogeographical realm; 5 from Australia and 2 

from New Zealand. These species are separated 

on the basis of tail spines and egg shape. Skrjabinodon 

oedurae and S. poicilandri possess 3 

caudal body spines that the other 5 species lack. 

Females of S. oedurae have 19 tail filament 

spines; females of S. poicilandri have 36-44. 

Skrjabinodon leristae, S. parasmythi, S. smythi, 

and 5. trimorphi have spindle-shaped eggs; the 

eggs of S. piankai are barrel-shaped. Eggs of S. 

parasmythi and S. smythi have plugs at each end, 

those of 5. leristae and 5. trimorphi do not. Tail 

filament spines of female 5. parasmythi are slender 

and pointed, those of female S. smythi are 

digitiform. Males of 5. parasmythi have a welldeveloped 

spicule, males of 5. smythi lack a 

spicule. Females of S. leristae have doubled lateral 

alae; females of S. trimorphi have single 

lateral alae. 

Discussion 

Other species of helminths found in this study 

are listed in Table 1. Previously reported hel- 


BURSEY AND GOLDBERG—SKRJAB1NODON PIANKAI SP. N. FROM AUSTRALIA 179 

minths of N. laevissimus include P. filicauda, 

Wanaristrongylus papangawurpae Jones, 1987, 

and cysts containing larvae of physalopterids; 

from N. levis, W. ctenoti and physalopterid larvae 

(Jones, 1985, 1987, 1995a, b). 

Oochoristica piankai was first described from 

specimens taken from the small intestine of the 

thorny devil, Moloch horridus Gray, 1841, collected 

by E. R. Pianka in Western Australia 

(Bursey et al., 1996). Nephrurus laevissimus is 

the second host for this parasite to be reported. 

Maxvachonia brygooi was first described from 

the agamid genus Amphibolurus Wagler, 1830, 

by Mawson (1972); N. levis is a new host record 

for M. brygooi and represents the 10th lizard 

species to harbor this helminth. Pharyngodon tiliquae 

was first described from the skink Tiliqua 

scincoides (White, ex Shaw, 1790) by Baylis 

(1930); N. vertebralis is a new host record for 

P. tiliquae and represents the 10th lizard species 

to harbor this helminth. Physalopteroides filicauda 

was described from specimens taken from 

the stomach of a N. laevissimus collected by E. 

R. Pianka in Western Australia (Jones, 1985). It 

has been found in at least 38 species of Australian 

lizards. Wanaristrongylus papangawurpae 

and W. ctenoti were also described from specimens 

taken from the stomachs of N. laevissimus 

and N. levis, respectively, collected by E. R. 

Pianka in Western Australia (Jones, 1987). Wanaristrongylus 

papangawurpae has been found 

in 8 species of Australian lizards and W. ctenoti 

in 12 species (Jones, 1988, 1995a). Raillietiella 

scincoides was originally described from T. 

scincoides by Ali et al. (1984); N. laevissimus is 

the second reported host. Larvae of Abbreviata 

sp. and Physaloptera sp. are commonly reported 

in Australian reptiles (Jones, 1995a). Larvae of 

Abbreviata sp. have submedian teeth on each 

pseudolabium; such teeth are absent in larvae of 

Physaloptera sp. 

It should be noted that the material examined 

by Jones (1995a, b) and our material were from 

the same collection of lizards by E. R. Pianka; 

the stomachs had been deposited in the Western 

Australia Museum and the carcasses in LACM. 

Further examination of Australian lizards will be 

necessary before the number of hosts for S. 

piankai can be known. 


We thank Robert L. Bezy (Natural History 

Museum of Los Angeles County) for permission 

to examine the geckos; Peggy Firth for the illustrations 

constituting Figs. 1-8; and Cynthia 

Walser and Cheryl Wong for dissection assistance. 


Ainsworth, R. 1990. Male dimorphism in two new 

species of nematode (Pharyngodonidae: Oxyurida) 

from New Zealand lizards. Journal of Parasitology 

76:812-822. 

Ali, J. H., J. Riley, and J. T. Self. 1984. Further observations 

of blunt-hooked raillietiellids (Pentastomaida: 

Cephalobaenida) from lizards with descriptions 

of three new species. Systematic Parasitology 

6:147-160. 

Baylis, H. A. 1930. Some Heterakidae and Oxyuridae 

(Nematoda) from Queensland. Annals and Magazine 

of Natural History, Series 10, 5:354-366. 

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 


215-221. 

Cogger, H. G. 1992. Reptiles and Amphibians of Australia, 

5th ed. Reed Books, Chatswood, New 

South Wales, Australia. 775 pp. 

Inglis, W. G. 1968. Nematodes parasitic in western 

Australian frogs. British Museum (Natural History) 

Bulletin, Zoology 16:161-183. 

Jones, H. I. 1985. Two new species of nematode (Spirurida: 

Physalopteridae) from Australian lizards 

(Reptilia: Scincidae: Gekkonidae). Journal of Natural 

History 19:1231-1237. 

. 1987. Wanaristrongylus gen. n. (Nematoda: 

Trichostrongyloidea) from Australian lizards, with 

descriptions of three new species. Proceedings of 


40-47. 

. 1988. Nematodes from nine species of Varanus 

(Reptilia) from tropical Northern Australia, 

with particular reference to the genus Abbreviata 

(Physalopteridae). Australian Journal of Zoology 

36:691-708. 

. 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 asssociated with physalopterid 

larvae (Nematoda: Spirurida) in the gastric 

tissues of Australian reptiles. Journal of Wildlife 

Diseases 31:299-306. 

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. 

Pianka, E. R. 1972. Zoogeography and speciation of 

Australian desert lizards: an ecological perspective. 

Copeia 1972:127-145. 

, and H. D. Pianka. 1976. Comparative ecology 

of twelve species of nocturnal lizards (Gekkonidae) 

in the Western Australian desert. Copeia 

1976:125-142. 



66(2), 1999 pp. 180-186 

Parapharyngodon japonicus sp. n. (Nematoda: Pharyngodonidae) 

from the Japanese Clawed Salamander, Onychodactylus japonicus 

(Caudata: Hynobiidae), from Japan 

CHARLES R. BURSEYU 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@whittier.edu) 

ABSTRACT: Parapharyngodon japonicus sp. n. from the large intestine of the Japanese clawed salamander, 

Onychodactylus japonicus (Houttuyn), is described and illustrated. Parapharyngodon japonicus is most similar 

to P. tyche in that the anterior cloacal lip is smooth, the ovary is postbulbar, and the eggs are thin-walled and 

oval in outline. These 2 species differ in that the spicule of P. japonicus is half the length of that in P. tyche 

and the lateral alae of P. japonicus end abruptly about 80 u,m anterior to the cloaca, whereas in P. tyche the 

lateral alae continue to the end of the body. Two species are transferred from Parapharyngodon to The land ros 

and represent new combinations: Thelandros awakoyai (Babero and Okpala) comb. n. and T. senisfaciecaiidus 

(Freitas) comb. n. 

KEY WORDS: Parapharyngodon japonicus sp. n., Pharyngodonidae, Onychodactylus japonicus, Hynobiidae, 

Amphibia, salamander, Japan. 

The validity of Parapharyngodon Chatterji, 

1933, has been in question almost since its proposal 

by Chatterji (1933). Baylis (1936) considered 

it to be a synonym of Thelandros Wedl, 

1862; Karve (1938), Garcia-Calvente (1948), 

and Skrjabin et al. (1951) maintained this synonymy. 

Freitas (1957) reinstated the genus; Chabaud 

(1965) returned it to synonymy with Thelandros. 

Sharpilo (1976), on the basis of the 

presence of lateral alae, reinstated Parapharyngodon, 

but Fetter and Quentin (1976) did not 

accept lateral alae as a differential character and 

again synonymized Parapharyngodon with Thelandros. 

Adamson (1981) reestablished Parapharyngodon 

based on the dietary habits of the 

host, genital cone morphology (well developed 

in males of Thelandros, reduced or absent in 

Parapharyngodon), egg morphology (operculum, 

if present, polar in position, larvated at deposition 

in Thelandros; subpolar operculum, deposited 

in early stage of cleavage in Parapharyngodon), 

and morphology of the tail of females. 

Castano-Fernandez et al. (1987) 

supported retention of Parapharyngodon but restricted 

separation of the 2 genera to morphological 

characters, not dietary habits. Males of 

Parapharyngodon lack a genital cone, papillae 

surround the cloaca, the accessory piece is absent, 

and the tail is subterminal and curved dor- 


sally, whereas males of Thelandros have a narrow, 

elongated genital cone (sometimes with an 

accessory piece), papillae are outside the genital 

cone, and the tail is terminal. Females of Parapharyngodon 

have a conical tail ending in a 

short spike and the eggs have a subterminal 

operculum and are in the early stages of cleavage 

when released. Females of Thelandros have 

various caudal morphologies; in some species 

the tail is conical, tapering evenly from the anus, 

whereas in others it is rounded and supports a 

short filiform appendage. The eggs of Thelandros 

have a terminal operculum and are larvated 

at deposition. 

The Japanese clawed salamander, Onychodactylus 

japonicus (Houttuyn, 1782), is restricted to 

mountainous areas of Honshu and Shikoku Islands, 

Japan, where it inhabits coniferous and 

broad-leafed deciduous forests 20-2,000 m 

above sea level (Kuzmin, 1995). The ancestors 

of O. japonicus supposedly reached Japan from 

continental Asia by way of the Korean peninsula 

(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) 

180 


BURSEY AND GOLDBERG—PARAPHARYNGODON JAPONICUS SP. N. 181 

( = Capillaria filiformis (Linstow, 1885)), 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). To our 

knowledge there are no reports of Paraphaiyngodon 

from Japanese salamanders, although 

Hasegawa (1988) reported an unidentified species 

of Parapharyngodon from the scincid lizard, 

Ateuchosaurus pellopleurus Hallowell, 

1860, from Okinawa, Japan. The purpose of this 

paper is to describe a new species of nematode, 

Parapharyngodon japonicus from a salamander 

Onychodactylus japonicus from Japan, and to 

provide a current list of species assigned to the 

genus Parapharyngodon. 


Sixty-eight Onychodactylus japonicus, mean snoutvent 

length = 62.4 ± 4.3 mm (range 43-72 mm), were 

collected by hand and fixed in neutral buffered 10% 

formalin, preserved in 70% alcohol, examined for intestinal 

helminths, then deposited in the Natural History 

Museum of Los Angeles County (LACM). Sixtyfive 

were from Hineomata Village (37°01'N, 

139°23'E), 1,100-1,200 m elevation, Fukushima Prefecture, 

Honshu Island, Japan (LACM 143245- 

143260, collected 13 June 1995; LACM 143715- 

143736, 19 June 1996; LACM 144266-144292, 7 June 

1997), and 3 were from Hakone Mountain (35°12'N, 

139°00'E), ca. 800 m elevation, Hakone, Kanagawa 

Prefecture, Honshu Island, Japan (LACM 143714, 28 

May 1980; LACM 143712, 13 May 1986; LACM 

143713, 8 June 1993). The body cavity was opened 

by a longitudinal incision from vent to throat and the 

gastrointestinal tract was removed and opened longitudinally. 

Nematodes were removed, placed in undiluted 

glycerol, allowed to clear, and examined under a 

light microscope. Measurements are given in micrometers. 

Results 

Parapharyngodon japonicus sp. n. 

(Figs. 1-6) 

Description 

GENERAL: Robust nematodes with prominent 

annulations beginning just behind cephalic extremity 

and continuing to anus. Moderate sexual 

dimorphism. Triangular oral opening surrounded 

by 3 bilobed lips. One small, pedunculate amphid 

on each ventrolateral lip. Lateral alae present 

in males, absent in females. Males without 

caudal alae; caudal filament directed dorsally. 

Females with conical tail terminating in short, 

stiff spike. 

MALE (holotype and 9 paratypes; mean and 

range): Length 789 (620-1,170). Width 131 

(115—153). Lateral alae beginning near level of 

esophagus isthmus, increasing gradually in 

width and ending abruptly about 80 u,m anterior 

to cloaca. Annulations about 2 |xm apart. Esophagus 

160 (131-177), bulb length 45 (40-51), 

bulb width 43 (37-48). Nerve ring 116 (86- 

143), excretory pore 57 (40-74) from anterior, 

respectively. Tail 27 (23—34), reduced to a slim 

appendage inserted dorsally and directed 

obliquely to longitudinal axis of body. Spicule 

53 (45-57). Testis reflexed behind esophagus. 

Three pairs of caudal papillae: 1 pair ventral, 

precloacal; 1 pair sublateral, postcloacal; 1 pair 

on caudal appendage. Posterior cloacal lip thickened 

centrally. 

FEMALE (allotype and 9 paratypes; mean and 

range): Length 2,493 (1,820-3,250). Without 

lateral alae. Width at vulva 469 (306-714). 

Esophagus 298 (257-336), bulb length 85 (68- 

100), bulb width 92 (72-114). Nerve ring 206 

(125-239), excretory pore 718 (459-969), vulva 

1,207 (765-1,785) from anterior, respectively. 

Tail 91 (57—114). Amphidelphic; uteri divergent; 

anterior uterus directed anteriorly, posterior uterus 

directed posteriorly; ovaries reflexed, remaining 

below level of esophageal bulb; muscular 

ovijector, nonsalient vulva. Egg oval, in profile 

slightly flattened on 1 side, 92 (77-100) by 42 

(34-48), thin-shelled, with subterminal operculum. 

Eggs in ovijector at pronucleus stage of 

development. 


TYPE HOST: Onychodactylus japonicus 

(Houttuyn, 1782). 

TYPE LOCALITY: Hineomata, Fukushima Prefecture, 

Honshu Island, Japan, 37°01'N, 

139°23'E. 

SITE OF INFECTION: Small intestine. 

TYPE SPECIMENS: Holotype: male, U.S. National 

Parasite Collection, Beltsville, Maryland, 

USNPC 88238; allotype, female, USNPC 

88239; paratypes (9 males, 9 females), USNPC 

88240. 

ETYMOLOGY: The new species is named in 

reference to the country of origin. 

Discussion 

We consider the most significant character for 

separation of Parapharyngodon and Thelandros 

to be egg morphology. Based on egg morphology, 

as defined by Castano-Fernandez et al. 



E n 

o 

CM 

50pm 

40|jm 

O 

m 

Figures 1-6. Parapharyngodon japonicus sp. n. 1. Female, entire, lateral view. 2. Male, entire, lateral 

view. 3. Female, en face view. 4. Egg, pronuclear stage. 5. Male, posterior end, lateral view. 6. Male, 

posterior end, ventral view. 


Egg s 

83-95 

88-96 

75-90 

109-119 

90-99 

115 

84-108 

not 

90-110 

85-98 

78-87 

82-90 

80-85 

72-82 

110-129 

77-126 

78-82 

80-100 

91-92 

86-102 

80-91 

127-135 

88 

99 

Table 1. 

Current list and selected characters of species assigned to Parapharyngodon. 

Biogeographical realm 

Species of Parapharyngodon 

Spicule (u,m) 

Cloacal lip 

Ovary 

Australian Realm 

P. anomalus Hobbs, 1996 

P. fitzroyi Jones, 1 992 

P. kartana (Johnston and Mawson, 1941) 

Ethiopian Realm 

P. adramitana Adamson and Nasher, 1984 

P. bulbosus (Linstow, 1 899) 

P. rneridionalis (Chabaud and Brygoo, 1962) 

P. rotundatus (Malan, 1939) 

P. rousseti (Tcheprakoff, 1966) 

Nearctic Realm 

P californiensis (Read and Amrein, 1952) 

P. iguanae (Telford, 1965) 

Neotropical Realm 

P. alvarengai Freitas, 1957 

P. cubensis (Barus and Coy-Otero, 1969) 

P. garciae Schmidt and Whittaker, 1975 

P. largitor Alho and Oliveira-Rodrigues, 1963 

P. osteopili Adamson, 1981 

P. scleratus (Travassos, 1923) 

P. verrucosus Freitas and Dobbin, 1959 

Oriental Realm 

P. alrnoriensis (Karve, 1949) 

P. calotis (Johnson, 1966) 

P. kasauli (Chatterji, 1935) 

P. rnaplestonei Chatterji, 1933 

Palaearctic Realm 

P. dogieli Markov and Bogdanov, 1965 

P. echinatus (Rudolphi, 1819) 

P. lilfordi Castano-Fernandez, Zapatero-Ramos, Solera-Puertas, 

and Gonzalez-Santiago, 1987 

P. japonicus sp. n. 

P. micipsae (Seurat, 1917) 

P. pavlovskyi Markov, Ataev, and Bogdanov, 

1968 

P. psamrnodromi Roca and Lluch, 1986 

P. skrjabini Vakker, 1 969 

P. tyche Sulahian and Schacher, 1968 

63 

80-92 

55 

80-86 

51-63 

80 

96-140 

110 

53-76 

43 

80-100 

77 

30-45 

54-68 

53-61 

80-109 

55-63 

85-105 

31 

94-114 

76-90 

93-110 

74-112 

67-85 

45-57 

88 

74-87 

absent 

139-176 

100-110 

echinate 

echinate 

smooth 

echinate 

smooth 

echinate 

smooth 

echinate 

smooth 

echinate 

smooth 

smooth 

smooth 

smooth 

echinate 

smooth 

smooth 

echinate 

smooth 

smooth 

smooth 

echinate 

echinate 

smooth 

smooth 

echinate 

echinate 

smooth 

smooth 

smooth 

prebulbar 

prebulbar 

not given 

prebulbar 

postbulbar 

postbulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

prebulbar 

postbulbar 

prebulbar 

not stated 

prebulbar 

prebulbar 

postbulbar 

prebulbar 

postbulbar 

prebulbar 

prebulbar 

77-100 

91 

91_100 

prebulbar 

prebulbar 

postbulbar 

88-104 

82-93 

90-100 



(1987), the species harbored by Onychodactylus 

japonicus is assigned to the genus Parapharyngodon. 

The most recent list of species of Parapharyngodon 

is that of Baker (1987), in which 33 

species are listed. Parapharyngodon aegyptiacus 

Moravec, Barus, and Rysavy, 1987, has 

since been transferred to Skrjabinodon Inglis, 

1968, by Moravec and Barus (1990). Six species 

on Baker's list have eggs with terminal opercula; 

thus, based on the criteria of Castano-Fernandez 

et al. (1987), these species should be assigned 

to Thelandros, namely, T. awokoyai (Babero and 

Okpala, 1962) comb, n.; T. bicaudatus Read and 

Amrein, 1952; T. maculatus Caballero, 1968; T. 

pseudothaparius Lucker, 1951; T. senisfaciecaudus 

(Freitas, 1957) comb, n.; and T. xantusi 

Lucker, 1951. The egg morphology has not been 

described for 4 species from Baker's list, P. bulbosus 

(Linstow, 1899) Freitas, 1957; P. garciae 

Schmidt and Whittaker, 1975; P. kartana (Johnston 

and Mawson, 1941) Adamson, 1981; and 

P. mabouia (Rao and Hiregauder, 1962) Adamson, 

1981. We were able to examine a specimen 

of P. kartana (USNPC 88241), the eggs of 

which had subterminal opercula. Specimens of 

P. bulbosus, P. garciae, and P. mabouia were 

not available for examination. Until egg morphology 

is described, we will provisionally retain 

P. bulbosus and P. garciae; P. mabouia is 

inadequately described and is to be considered 

a species inquirendae. Five additional, recently 

described species should be added to Baker's 

list, namely P. psamrnodromi Roca and Lluch, 

1986; P. lilfordi, Castano-Fernandez, Zapatero- 

Ramos, Solera-Puertas, and Gonzalez-Santiago, 

1987; P. fitzroyi Jones, 1992; P. anomalus 

Hobbs, 1996; and P. japonicus sp. n. A revised 

list of Parapharyngodon is given in Table 1. 

In addition to the species in Table 1, 10 species 

assigned to Parapharyngodon are considered 

species inquirendae: females are unknown 

for P. szczerbaki Radchenko and Sharpilo, 1975; 

males are unknown for P. cincta (Linstow, 

1897) Freitas, 1957, P. megaloon (Linstow, 

1906) Adamson, 1981, and P. waltoni (Read and 

Amrein, 1952) Adamson, 1981; inadequately 

described are P. aspiculus, Khera, 1961, P. cameroni 

(Belle, 1957) Adamson, 1981, P. evaginatus 

Fotedar, 1974, P. fotedari Kalyankar and 

Palladwar, 1977, P. macrocerca Fotedar, 1974, 

and P. seurati (Sandground, 1936) Freitas, 1957. 

Species of Parapharyngodon are distinguished 

on the basis of the morphology of the 

anterior cloacal lip, the location of the ovary, 

and geographical distribution (Table 1). Of the 

30 species in Table 1, with the exception of P. 

anomalus, P. garciae, and P. japonicus, all are 

parasites of lizards. Of the 9 species reported 

from the Palaearctic Realm, Parapharyngodon 

japonicus is most similar to P. tyche in that the 

anterior cloacal lip is smooth, the ovary is postbulbar, 

and the eggs are thin-walled and oval in 

outline. These 2 species differ in that the spicule 

of P. japonicus is half the length of that in P. 

tyche, and the lateral alae of P. japonicus end 

abruptly about 80 (Jim anterior to the cloaca, 

whereas in P. tyche, the lateral alae continue to 

the end of the body. 

Hasegawa (1988) reported an unidentified 

species of Parapharyngodon from the lizard 

Ateuchosaurus pellopleurus Hallowell, 1860 

from Okinawa, Japan. This species differs from 

P. japonicus in that its ovarian coils are prebulbar, 

the tail of the female is conical, and the egg 

has a pitted, thick wall and is somewhat triangular 

in outline. 


We thank Tatsuo Ishihara (Hakone Woodland 

Museum, Hakone, Japan) for the samples of Onychodactylus 

japonicus, Peggy Firth for the illustrations 

constituting Figures 1—6, Hay Cheam 

and Cynthia Walser for assistance with dissections, 

and Serge Ferleger for Russian translation. 


Adamson, M. L. 1981. Parapharyngodon osteopili n. 

sp. (Pharyngodonidae: Oxyuroidea) and a revision 

of Parapharyngodon and Thelandros. Systematic 


, and A. K. Nasher. 1984. Pharyngodonids 

(Oxyuroidea; Nematoda) of Agama adramitana in 

Saudi Arabia with notes on Parapharyngodon. 


Alho, J. R., and H. Oliveira-Rodrigues. 1963. Nova 

especie do genero Parapharyngodon Chatterji, 

1933 (Nematoda, Oxyuroidea). Atas da Sociedade 

de Biologia do Rio de Janeiro 7:10-12. 

Baker, M. R. 1987. Synopsis of the Nematoda parasitic 

in amphibians and reptiles. Memorial University 

of Newfoundland, Occasional Papers in 

Biology 11:1-325. 

Barus, V. 1973. Some remarks on the neotropical species 

of the genera Parapharyngodon and Batracholandros 

(Oxyuridae). Folia Parasitologica 

(Prague) 20:131-139. 

, and A. Coy-Otero. 1969. Nematodes del genero 

Parapharyngodon Chatterji, 1933 (Oxyuridae), 

en Cuba. Torreia 7:1-10. 


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Baylis, H. A. 1936. Nematoda. I. Ascaridoidea and 

Strongyloidea. The Fauna of British India. Taylor 

and Francis, London. 408 pp. 

Castano-Fernandez, C., L. M. Zapatero-Ramos, 

and M. A. Solera-Puertas. 1987. Revision de los 

generos Parapharyngodon Chatterji, 1933 y Thelandros 

Wedl, 1862 (Oxyuroidea, Pharyngodonidae). 

Revista Iberica de Parasitologia 47:271-274. 

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n. sp. (Oxyuroidea, Pharyngodonidae) en 

Podarcis lilfordi (Reptilia, Lacertidae) de las islas 

Baleares. Revista Iberica de Parasitologfa 47:275- 

281 

Chabaud, A. G. 1965. Ordre des Ascaridida. Pages 

932-1180 in P. P. Grasse, ed. Traite de Zoologie. 

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Paris. 

, and E.-R. Brygoo. 1962. Nematodes parasites 

de Cameleons malgaches. Deuxieme note. 

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37:569-602. 

Chatterji, R. C. 1933. On a new nematode, Parapharyngodon 

maplestoni gen. nov., sp. nov., from 

a Burmese lizard. Annals of Tropical Medicine 

and Parasitology 27:131-134. 

. 1935. Nematodes from a common Indian lizard 

(Uromastix hardwicki) with remarks on Kalicephalus 

parvus Maplestone, 1932. Records of the 

Indian Museum 37:29-36. 

Freitas, J. F. T. 1957. Sobre os generos Thelandros 

Wedl, 1862 e Parapharyngodon Chatterji, 1933, 

com descrigao de Parapharyngodon alvarengai 

sp. n. (Nematoda, Oxyuroidea). Memorias do Instituto 

Oswaldo Cruz 55:21-45. 

, and J. E. Dobbin, Jr. 1959. Nova especie do 

genero Parapharyngodon Chatterji, 1933 (Nematoda, 

Oxyuroidea). Anais da Sociedade de Biologia 

de Pernambuco 16:23-33. 

Garcfa-Calvente, I. 1948. Revision del genero Pharyngodon 

y descripcion de nuevas especies. Revista 

Iberica de Parasitologfa 8:367-410. 

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

Pharyngodonidae) collected from the lizard, 

Ateuchosaurus pellopleurus (Sauria: Scincidae), 

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

(In Japanese.) 

Hobbs, R. P. 1996. Parapharyngodon anomalus sp. 

n. (Oxyuridae, Pharyngodonidae) from the Australian 

echidna Tackyglossus aculeatus, with notes 

on the Thelandroinae. Journal of the Helminthological 


Johnson, S. 1966. A new oxyurid nematode of the 

genus Thelandros from Calotes versicolor (Daud.) 

from India, with a key to the Indian species of the 

genus from Calotes. Indian Journal of Helminthology 

18:123-127. 

Johnston, T. H., and P. M. Mawson. 1941. Some 

nematodes from Kangaroo Island, South Australia. 

Records of the South Australian Museum 7: 

145-148. 

Jones, H. I. 1992. Gastrointestinal nematodes in the 

lizard genera Tiliqua and Cyclodomorphus (Scincidae) 

in Western Austalia. Australian Journal of 

Zoology 40:115-126. 

Karve, J. N. 1938. Some nematode parasites of lizards. 

Pages 251—258 in Livro Jubilar do Prof. 

Lauro Travassos. Rio de Janeiro, Brazil. 

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Agama tuberculata Gray. Journal of the University 

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conservation. Westarp Wissenschaften, Magdeburg, 

Germany. 108 pp. 

Malan, J. R. 1939. Some helminths of South African 

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Moravec, F., and V. Barus. 1990. Some nematode 

parasites from amphibians and reptiles from Zambia 

and Uganda. Acta Societatis Zoologicae Bohemoslovenicae 

54:177—192. 

, , and B. Rysavy. 1987. On parasitic 

nematodes of the families Heterakidae and Pharyngodonidae 

from reptiles in Egypt. Folia Parasitologica 

34:269-280. 

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

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japonicus in Shikoku. Biosphaera 2:33-37. 

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

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the Nematode Parasites of Vertebrates. No. 4. 

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Agricultural Bureaux, Farnham Royal, 

U.K. 30 pp. 

Read, C. P., and Y. U. Amrein. 1952. Some new 

oxyurid nematodes from southern California. 


Roca, V., and J. Lluch. 1986. Parapharyngodon 

psammodromi n. sp. (Nematoda: Pharyngodonidae), 

parasite de Psatnmodromus hispanicus Fitzinger, 

1826 (Reptilia: Lacertidae) en Valencia 

(Espafia). Rivista di Parassitologia 3:17-22. 

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of Poekilostrongylus gen. nov. (Trichostrongylidae). 


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66(2), 1999 pp. 187-193 

Paraochoterenetta javanensis gen. et sp. n. (Filarioidea: 

Onchocercidae) from Rana cancrivora (Amphibia: Anura) in 

West Java, Indonesia 

PURNOMO AND MICHAEL J. BANGS1 

U.S. Naval Medical Research Unit No. 2, Box 3, APO AP 96520-8132, U.S.A. 

ABSTRACT: Paraochoterenella javanensis gen. et sp. n. (Filarioidea: Onchocercidae) is described from the mesentery 

of the frog Rana cancrivora Gravenhorst in West Java, Indonesia. Paraochoterenella javanensis presently 

represents the only species in this newly created genus. Three of 13 frogs contained mature male and female 

worms and microfilariae. Paraochoterenella is distinguished from the other 4 genera, Foleyellides Caballero, 

Ochoterenella Caballero, Madochotera Bain and Brunhes, and Paramadochotera Esslinger in the subfamily 

Waltonellinae Bain and Prod'hon by the presence of cuticularized parastomal structures in both sexes, a distinct 

cuticularized buccal capsule, the lack of both lateral and caudal alae, and the presence of scattered (nonoriented) 

minute bosses on the cuticle of the midbody region. The microfilariae are unsheathed and slightly narrowed at 

the caudal extremity, with a 10:1 length to width ratio. Paraochoterenella represents the second genus in the 

subfamily Waltonellinae present in southern Asia and the first report of a filarial species in the subfamily from 

an Indonesian amphibian. A revised key to the genera is presented in light of this new addition to the subfamily. 

KEY WORDS: Filarioidea, Onchocercidae, Waltonellinae, Paraochoterenella javanensis gen. et sp. n., taxonomic 

key, Rana cancrivora, Amphibia, Anura, Ranidae, morphology, Java, Indonesia. 

The majority of the species contained in the 

subfamily Waltonellinae Bain and Prod'hon, 

1974 (Filarioidea: Onchocercidae) have been described 

from the Western Hemisphere, particularly 

neotropical areas. Esslinger (1986a, b) provided 

redescriptions of type material of Ochoterenella 

Caballero, 1944, and Foleyellides Caballero, 

1935, and revisions of the 4 related genera in 

the subfamily. Species previously assigned to the 

genus Waltonella Schacher, 1975, were transferred 

into the genera Foleyellides and Ochoterenella, 

the name Waltonella was placed as a junior 

synonym of Foleyellides, and the subfamily 

designation Waltonellinae was retained (Esslinger, 

1986a, b). Members of this filarial assemblage 

have only been found in the body cavities 

of anuran amphibians, with the exception of 1 

subcutaneous parasite, Foleyellides confusa 

(Schmidt and Kuntz, 1969; see Anderson and 

Bain, 1976). The subfamily members are parasites 

of toads and frogs in the families Bufonidae, 

Leptodactylidae, Racophoridae, and Ranidae. 

Three of 13 frogs identified as Rana cancrivora 

Gravenhorst, 1829 (Anura: Ranidae), and 

collected from Bekasi, West Java, Indonesia, 

were examined and discovered to harbor adults 

and microfilariae of an Ochoterenella-like nem- 

1 Corresponding author. Address reprint requests to 

Publications Office, U.S. Naval Medical Research Unit 

No. 2, Box 3, Unit 8132, APO AP 96520-8132, U.S.A. 

atode. Microfilariae found in the blood and adult 

male and female worms removed from the mesentery 

belong to a previously unknown genus 

and species as described herein. 


Live frogs were obtained from a local food dealer 

residing in Jakarta. All had been captured from the 

same locality along drainage ditches, approximately 5 

km east of the city of Jakarta proper. Live adult worms 

were removed from the mesentery, relaxed in 0.6% 

saline solution, fixed in hot 70% ethanol, and preserved 

in 70% ethanol/5% glycerine. All specimens 

were cleared and temporarily mounted and examined 

in lactophenol. Microfilariae were obtained from 

blood. Thick blood films were processed with Giemsa's 

stain diluted 1:15 with pH 7.2 sodium phosphate 

buffer for 15 min. Drawings and measurements were 

made with the aid of a camera lucida. All measurements 

are expressed as means followed by the range 

in parentheses and are given as length by width in 

micrometers (|xm) unless otherwise indicated. 

Results 

Paraochoterenella gen. n. 

DIAGNOSIS: Onchocercidae (Leiper, 1911) 

Chabaud and Anderson, 1959; Waltonellinae 

Bain and Prod'hon, 1974. Cephalic end with 

pair of lateral flap-like cuticularized parastomal 

structures. Cephalic plate with lateral axis slightly 

longer than dorsoventral axis; 4 pairs cephalic 

papillae, broad basally and tapered with nonarticulated 

distal portion. Distinct cuticularized 

187 



buccal cavity. Lateral and caudal alae lacking. 

Esophagus divided into a short anterior muscular 

region and a long, wider posterior glandular portion 

(muscular to glandular ratio: 6.1). Vulva in 

posterior region of glandular portion of esophagus 

near esophageal-intestinal junction. Two 

pairs of preanal, 4 pairs of postanal papillae. Cuticular 

bosses minute (

PURNOMO AND EA.NGS—PARAOCHOTERENELLA JAVANENSIS GEN. ET SP. N. FROM RANA CANCRIVORA 189 

/ ^ ^ ^ 5 

Figures 1-7. Adults and microfilaria of Paraochoterenella javanensis gen. et sp. n. 1. Generalized en 

face view of female showing arrangement of 4 pairs of suhmedian papillae and 2 lateral amphids. 2. 

Transversely striated cuticle of female. 3. Anterior region of female, lateral view. 4. Caudal end of female, 

lateral view. 5. Microfilaria from blood. 6. Caudal end of male, lateral view showing left and right spicules, 

cloaca, and caudal papillae. 7. Caudal end of male, ventral view showing arrangement of caudal papillae. 

All scale bars in urn. 



8 

5O/u 

11 

14 

12 15 

13 16 17 

Figures 8-17. Paraochoterenella javanensis gen. et sp. n. 8. Cephalic extremity of female, dorsal view 

showing cuticularized buccal capsule. 9. Cephalic extremity of female, en face view showing arrangement 

of papillae, amphids, and parastomal structures. 10. Cephalic extremity of female, lateral view. 11, 12, 13. 

Minute bosses on female, lateral views of cervical region (11), midbody (12), and anal region (13). 14, 15, 

16. Minute bosses on male, lateral view, cervical region (14), midbody (15), and anal region (16). 17. Detail 

of area rugosa of male, ventral view. Scale bars = 50 urn (Figs. 8-10) and 200 u,m (Figs. 11-17). 

TYPE LOCALITY: Indonesia, West Java, Bekasi. 

SITE OF INFECTION: Mesentery. 

DATE OF COLLECTION: AUGUST 1990. 

DEPOSITED SPECIMENS: Holotype male, 

USNPC 82165; allotype female, USNPC 82166; 

paratypes, 2 females, USNPC 82167 in 70% ethanol/5% 

glycerine; 1 blood slide, Giemsastained 

microfilariae (syntypes), USNPC 82168, 

deposited in the U.S. National Parasite Collec- 


PURNOMO AND BANGS—PARAOCHOTERENELLA JAVANENSIS GEN. ET SP. N. FROM RANA CANCRIVORA 191 

tion (USNPC), Beltsville, Maryland. Preserved 

frog specimens have been retained at U.S. Naval 

Medical Research Unit-2 in 10% formalin. 

ETYMOLOGY: The specific epithet is derived 

from the type locality of the new species. 

Remarks and Discussion 

The finding of Paraochoterenella javanensis 

sp. n. from the mangrove frog, Rana cancrivora, 

in Bekasi, West Java, represents the first report 

of a filarial species in the subfamily Waltonellinae 

from an Indonesian amphibian. The subfamily 

members are parasites of toads and frogs 

in Bufonidae, Leptodactylidae, Racophoridae, 

and Ranidae. Of the Waltonellinae, only Foleyellides 

and Paraochoterenella have been definitively 

described from ranid frogs (Anderson and 

Bain, 1976). Geographically, Ochoterenella appears 

restricted to the Neotropical Region. Species 

of Foleyellides have been recorded predominantly 

in the Western Hemisphere, whereas species 

of both Madochotera Bain and Brunhes, 

1968, and Paramadochotera Esslinger, 1986, 

have been described only from Madagascar 

(Bain and Brunhes, 1968, Esslinger, 1986a). 

Based on described morphological measures 

and structures of adults and microfilariae, together 

with information on definitive hosts and 

geographic localities, the generic name Paraochoterenella 

is proposed to accommodate the 

new species, P. javanensis. The specific characters 

deemed important in distinguishing genera 

in the subfamily Waltonellinae, as revised by 

Esslinger (1986a, b), are the presence or absence 

of caudal alae and parastomal structures, the appearance 

and arrangement of the cuticular bosses, 

and the morphology of the microfilariae. 

Paraochoterenella gen. n. shares various characters 

with the other 4 genera, including paired 

cephalic papillae without articulated tips, cuticularized 

parastomal structures, the absence of 

lateral and caudal alae, a distinct buccal formation, 

the vulva near the base of the glandular 

esophagus, a thin, elongated (left) spicule shaft, 

and being a parasite of an anuran (Anderson and 

Bain, 1976). The principal characters that separate 

Paraochoterenella from other genera are the 

unsheathed microfilaria and the appearance and 

arrangement of the cuticular bosses. 

Of the 4 previously recognized genera in the 

subfamily, Paraochoterenella appears most 

closely aligned with Ochoterenella. However, 

Esslinger (1986a, 1988) concluded that all Ochoterenella 

species are a morphologically uniform 

group, restricted to the Neotropical Region. 

With the exception of only 2 species, both recovered 

from leptodactylid frogs, all have been 

found only in the toad Bufo marinus Linnaeus, 

1758 (Esslinger, 1988). Before Esslinger's 

(1986a) detailed reassessment, only 3 species of 

Ochoterenella Caballero, 1944 (Caballero, 1944; 

Johnston, 1967), in the subfamily (Bain and 

Prod'hon, 1974) had been assigned to the genus. 

Ochoterenella digiticauda Caballero, 1944, has 

been found in Mexico, Guatemala, and Paraguay 

(Lent et al., 1946; Yamaguti, 1961). Ochoterenella 

papuensis Johnston, 1967, found in the 

frog Platymantis ( — Cornufer} papuensis Meyer, 

1875 has been reported only from New Guinea 

(Johnston, 1967), whereas Ochoterenella guibei 

Bain and Prod'hon, 1974 from a racophorid 

frog, appears in Madagascar. 

Esslinger (1988) included 14 members in 

Ochoterenella, partially the result of a previous 

transfer of 8 species in the genus Waltonella to 

Ochoterenella (Esslinger, 1986a). Ochoterenella 

guibei from Madagascar was placed in a new 

genus Paramadochotera. Ochoterenella papuensis 

from New Guinea, as described by Johnston 

(1967), was considered incertae sedis and was 

removed from the genus until more material 

could be fully described (Esslinger, 1986a). An 

incompletely described Ochoterenella species 

from northern Viet Nam (Moravec and Sey, 

1985) is also considered incertae sedis for the 

present. Specific identification of the Viet Nam 

filariid was not possible because of the absence 

of males and the poor condition of the 5 female 

specimens. It is also noted that both Asian populations 

assigned to Ochoterenella lacked a distinct 

buccal cavity and the microfilariae were 

unsheathed, characters present in all known 

members of Ochoterenella (Esslinger, 1986a, b). 

However, because O. papuensis and the Viet 

Nam specimens represent the only purported 

members of the genus described from the Asian 

region, both are briefly mentioned in this discussion. 

Paraochoterenella javanensis can be distinguished 

from O. digiticauda (the type species), 

O. papuensis, and Ochoterenella from Viet Nam 

(VN) by the following characters: adult male 

and female worms are shorter in body length 

(except VN sp.), the longer (left) spicule is nearly 

4 times as long as the right (male not described 

for VN sp.), and the spicule ratio (3.7: 



1) is greater (1.7:1 and 2:1, respectively). Unlike 

all recognized members of Ochoterenella, the 

microfilariae of P. javanensis are unsheathed in 

blood. On average, the microfilariae are shorter 

in length, but have a distinctly smaller length to 

width body ratio (10:1) compared to O. digiticauda 

and O. papuensis (—30:1) and Ochoterenella 

VN (—20:1). The tip of the microfilaria 

tail is slightly narrowed versus the rounded, usually 

bulbous appearance in O. digiticauda. The 

VN microfilariae were described as unsheathed. 

In Ochoterenella, the appearance and length 

of individual bosses in both sexes are considered 

consistent within a species (Esslinger, 1986a). 

Depending on the site of measurement, the individual 

bosses of O. digiticauda ranged in 

mean size from 8.7 |xm at the midbody to 4 (xm 

at the midportion of the area rugosa (Esslinger, 

1986a). The scattered appearance of minute 

bosses on the cuticle, in the size range of 2—3 

(xm, clearly set P. javanensis apart from Ochoterenella 

species. Ochoterenella papuensis female 

worms apparently lack surface tubercles, 

and tubercles were not described for the VN 

specimen. 

The arrangement of male preanal and caudal 

papillae differs among the 4 descriptions. Paraochoterenella 

javanensis has 2 pairs of preanal 

and 4 pairs of postanal papillae, and O. digiticauda 

has 2 pairs of preanal and 3 pairs of postanal 

(Caballero, 1944) or 1 pair of preanal and 

3 pairs of postanal papillae as reported by Lent 

et al. (1946) and Esslinger (1986a). Paraochoterenella 

javanensis also lacks a median ventral 

preanal plaque. Ochoterenella papuensis has 2 

single preanal papillae in tandem, 2 adanal papillae, 

and 3 pairs of postanal papilla. Paraochoterenella 

javanensis has 4 pairs of anterior 

submedian papillae, 2 lateral cephalic amphids, 

and parastomal structures similar to those of O. 

digiticauda and the VN Ochoterenella sp. The 

position of the vulva is very near the glandular 

esophagointestinal junction, similar to that in O. 

digiticauda. In O. papuensis, the vulva was indistinct, 

lying slightly behind the musculoglandular 

esophageal junction, whereas Ochoterenella 

(VN) had it positioned at about the midpoint 

of the glandular esophagus. Unlike all 

members of Ochoterenella, P. javanensis has a 

distinct cuticularized buccal capsule, presently 

found elsewhere only in the genus Paramadochotera. 

Paraochoterenella represents a second genus 

in the subfamily present in southern Asia. The 

distribution and host range of this monotypic genus 

is not known. To date, only Foleyellides 

( = Waltonella) confusa from the Philippines and 

Foleyellides ( = Waltonelld) malayensis (Petit 

and Yen, 1979) from peninsular Malaysia have 

been described. It is possible that specimens described 

from Viet Nam and New Guinea may be 

members of Paraochoterenella, because their 

microfilariae also lacked a cuticular sheath; 

however, a decision regarding this possibility 

awaits full descriptions. The limited number of 

species described outside the Western Hemisphere 

may be more reflective of the lower relative 

number of investigations on amphibians 

and their nematodes from other areas of the 

world (Esslinger, 1986b). Given the wide range 

and species diversity of anuran amphibian species 

present in the Asian Region, this would not 

seem unreasonable. 

Nothing is known of the biology or transmission 

of Paraochoterenella javanensis. Larval 

stages have only been described from a few species 

of Foleyellides ( = Waltonelld), based primarily 

on experimental infections (Bain and 

Chabaud, 1986). Larval stage development has 

been observed in adipose and muscle tissue of 

mosquitoes. Likewise, the natural intermediate 

hosts of Waltonellinae are poorly known except 

for a few Foleyellides. Vectors are presumed to 

be blood-feeding dipterans, most likely various 

culicine mosquitoes (Diptera: Culicidae). In general, 

as more information becomes available on 

species morphology, biological variability, distribution, 

and natural host range of this group of 

filariids, the diagnostic significance of certain 

characters used to separate genera and species 

will become better understood. A revised simplified 

key to the genera is presented in light of 

this new addition to the subfamily. 

Key to the Genera of the Subfamily 

Waltonellinae 

la. Cuticularized parastomal structures present 

2 

Ib. Cuticularized parastomal structures absent 

Paramadochotera (Madagascar) 

2a. Lateral and caudal alae present 3 

2b. Lateral and caudal alae absent 4 

3a. Cuticle with transversely oriented ridges 

and bosses .. Madochotera (Madagascar) 

3b. Cuticle smooth, generally lacking bosses 

Foleyellides (worldwide) 


PURNOMO AND BANGS—PARAOCHOTERENELLA JAVANENSIS GEN. ET SP. N. FROM RANA CANCRIVORA 193 

4a. Cuticle of midbody with annular bands 

of longitudinally oriented bosses; microfilaria 

sheathed with tip of tail 

rounded, often bulbous 

Ochoterenella (Neotropics) 

4b. Cuticle of midbody with scattered minute 

bosses; microfilaria unsheathed 

with tip of tail slightly narrowed 

Paraochoterenella (Indonesia) 


The Naval Medical Research and Development 

Command, Navy Department, supported 

this study under Work Unit 3M161102BS13. 

AD410. The opinions and assertions contained 

herein are those of the authors and do not purport 

to reflect those of the U.S. Naval Service 

or the Indonesian Ministry of Health. 


Anderson, R. C., and O. Bain. 1976. Keys to the 

genera of the order Spirurida (No. 3), Part 3. Diplotriaenoidea, 

Aproctoidea and Filarioidea. Pages 

59-116 in R. C. Anderson, A. G. Chabaud, and 

S. Willmont, eds. CIH Keys to the Nematode Parasites 

of Vertebrates. Commonwealth Agricultural 

Bureaux, Farnham Royal, Buckinghamshire, U.K. 

Bain, O., and J. Brunhes. 1968. Un nouveau genre 

de filaire, parasite de grenouilles malgaches. Bulletin 

du Museum National d'Histoire Naturelle, 

Paris, 2nd ser. 40:797-801. 

, and A. G. Chabaud. 1986. Atlas des larves 

infestantes de filaires. Tropical Medicine and Parasitology 

37:301-340. 

, and J. Prod'hon. 1974. Homogeneite des filaires 

de batraciens des genres Waltonella, Ochoterenella 

et Madochotera; creation de Waltonellinae 

n. subfam. Annales de Parasitologie Humaine 

et Comparee 49:721—739. 

Caballero, E. C. 1944. Estudios helmintologicos de la 

region oncocercosa de Mexico y de la Repiiblica 

de Guatemala. Nematoda: Primeira parte. Filarioidea. 

I. Anales del Institute de Biologia, Universidad 

de Mexico 15:87-108. 

Esslinger, J. H. 1986a. 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 

of Washington 53:210-217. 

. 1986b. Redescription of Foleyellides striatus 

(Ochoterena and Caballero, 1932) (Nematoda: Filarioidea) 

from a Mexican frog, Rana montezumae, 

with reinstatement of the genus Foleyellides 

Caballero, 1935. Proceedings of the Helminthological 


. 1988. Ochoterenella figueroai sp. n. and O. 

lamothei sp. n. (Nematoda: Filarioidea) from the 

toad Bufo marinus. Proceedings of the Helminthological 


Johnston, M. R. L. 1967. Icosiella papuensis n. sp. 

and Ochoterenella papuensis n. sp. (Nematoda: 

Filarioidea), from a New Guinea frog, Cornufer 

papuensis. Journal of Helminthology 41:45-54. 

Lent, H., J. F. Teixeira de Freitas, and M. C. Proenca. 

1946. Alguns helmintos de batraquios colecionados 

no Paraguai. Memorias do Institute Oswaldo 

Cruz 44:195-214. 

Moravec, F., and O. Sey. 1985. Some nematode parasites 

of frogs (Rana spp.) from North Viet Nam. 

Parasitologia Hungarica 18:63-77. 

Petit, G., and P. Yen. 1979. Waltonella malayensis n. 

sp., une nouvelle filaire de batracien, en Malaisie. 

Bulletin du Museum National d'Histoire Naturelle, 

Paris 1, Sect. A 1:213-218. 

Schmidt, G. D., and R. E. Kuntz. 1969. Nematode 

parasites of Oceania. VI. Foleyella confusa sp. n., 

Icosiella hoogstraali sp. n. (Filarioidae), and other 

species from Philippine amphibians. Parasitology 

59:885-889. 

Yamaguti, S. 1961. Systema Helminthum. Vol. 3. The 

Nematodes of Vertebrates. Parts I and II. Interscience 

Publishers, Inc., New York. 1261 pp. 



66(2), 1999 pp. 194-197 

Research Note 

New Records, Hosts, and SEM Observations of Cercaria owreae 

(Hutton, 1954) from the Mexican Caribbean Sea 

DEL CARMEN GOMEZ DEL PRAoo-RosAS,1'4 JOSE N. ALVAREZ-CADENA,2 LOURDES 

SEGURA-PUERTAS,2 AND RAFAEL LAMOTHE-ARGUMEDO3 

1 Universidad Autonoma de Baja California Sur, Departamento de Biologia Marina, Apartado Postal 19-B, 

C.P. 23080, La Paz, Baja California Sur, Mexico (e-mail: mcgomez@calafia.uabcs.mx) 

2 Universidad Nacional Autonoma de Mexico, Institute de Ciencias del Mar y Limnologia, Estacion Puerto 

Morelos, Apartado Postal 1152, C.P. 77501, Canctin, Quintana Roo, Mexico, and 

3 Universidad Nacional Autonoma de Mexico, Institute de Biologia, Apartado Postal 70-153, C.P. 04510, 

Mexico, D.F., Mexico. 

ABSTRACT: Digenetic trematode larvae identified as 

Cercaria owreae (Hutton) were recorded in the coela 

of the following chaetognath species: Flaccisagitta enflata 

(Grassi), Serratosagitta serratodentata (Krohn), 

Ferosagitta hispida (Conant), and Sagitta helenae Ritter-Zahony. 

The hosts and parasites were collected during 

4 oceanographic cruises in February, March, May, 

and August 1991. The low prevalence of infection (average 

0.11%) was comparable with previous records. 

The intensity was restricted to 1 parasite. Ferosagitta 

hispida and Sagitta helenae are recorded for the first 

time as hosts of Cercaria owreae, and the Mexican 

Caribbean Sea is reported as a new locality for the 

geographical distribution of this parasite. 

KEY WORDS: Cercaria owreae, SEM, scanning 

electron microscopy, chaetognaths, new records, Caribbean 

Sea, Mexico. 

Cercaria owreae (Hutton, 1954) has been reported 

parasitizing species of Sagitta in the Atlantic 

Ocean and the Caribbean Sea (Hutton, 

1952, 1954; Suarez-Caabro, 1955; Dawes, 1958, 

1959). However, parasites of holoplanktonic organisms 

such as chaetognaths have not been 

studied in the vicinity of the Mexican Caribbean 

Sea. The main possible reasons for this lack of 

information are that the larval parasites have 

been mistaken for food remains or the holoplanktonic 

organisms are seldom investigated as 

hosts; thus, their importance as intermediate 

hosts has been underestimated and frequently 

overlooked. 

The purpose of this study is to describe larvae 

of the digenetic trematode Cercaria owreae with 

the aid of scanning electron microscopy (SEM), 

to determine the prevalence and mean intensity 

of parasitism in chaetognaths, and to report the 

Corresponding author. 

chaetognaths Ferosagitta hispida and Sagitta 

helenae as new hosts and the Mexican Caribbean 

Sea as a new locality record. 

Zooplankton samples were collected during 

scientific cruises of the Mexican Navy (Secretaria 

de Marina) during February, March, May, 

and August 1991 (cruises I to IV) in the Mexican 

Caribbean Sea (Fig. 1). The material was 

intended for studies of the composition, abundance, 

and species distribution of the major zooplankton 

groups, and it was during its analysis 

that trematode larval parasites were observed in 

the coela of some chaetognaths. 

Sampling was carried out from 50 m to the 

surface in oblique tows with a square-mouth 

standard net 0.45 m per side (330 fjim mesh). 

Zooplankton material was fixed in 4% buffered 

(lithium carbonate) formalin. All chaetognaths 

were sorted from approximately 22 samples 

from each cruise. Prevalence and mean intensity 

were calculated according to Margolis et al. 

(1982). Parasitized chaetognaths were stained 

with Hams' hematoxylin and acetic carmine, 

cleared with methyl salicylate, and mounted on 

permanent slides in synthetic resin. Some chaetognaths 

were dissected and parasites were extracted 

for SEM. Twenty-two specimens were 

mounted on permanent slides and examined using 

a compound microscope, and 2 specimens 

were observed and photographed using SEM 

techniques. Measurements (mm) of 5 parasites 

are given as the range and mean (in parentheses). 

Specimens of the parasites are deposited in 

the Coleccion Nacional de Helmintos (CNHE), 

Institute de Biologia, Universidad Nacional Autonoma 

de Mexico, Mexico City, under the catalogue 

number 3185 for parasites of Flaccisa- 

194 


RESEARCH NOTES 195 

Table 1. Prevalence and intensity of Cercaria 

owreae infecting chaetognaths from the Mexican 

Caribbean Sea. 

Chaetognath species 

analyzed 

Cercaria owreae* 

N P %P 

I 

Flaccisagitta enflata 

Serratosagitta serratodentata 

Ferosagitta hispida 

Sagitta helenae 

14,583 

3,638 

1,015 

288 

18 

1 

1 

2 

0.12 

0.05 

0.09 

0.69 

I 

1 

1 

1 

* N, total number of chaetognaths analyzed; P, total number 

of chaetognaths parasitized; %P, percentage of chaetognaths 

infected; I, intensity of parasitism. 

Figure 1. Study area with the locations of the 

stations sampled in February, March, May, and 

August 1991. Geographical positions of the stations 

were similar for the 4 cruises. 

gitta enflata and number 3186 for parasites of 

Serratosagitta serratodentata. Specimens from 

the other 2 species were used for the SEM and 

are deposited in the SEM laboratory of the In- 

stituto de Ciencias del Mar y Limnologia, Universidad 

Nacional Autonoma de Mexico, Mexico 

City. 

A total of 19,524 chaetognaths (prevalence 

0.11%) belonging to 4 species were analyzed: 

Flaccisagitta enflata (Grassi, 1881), Serratosagitta 

serratodentata (Krohn, 1853), Ferosagitta 

hispida (Conant, 1891), and Sagitta helenae Ritter-Zahony, 

1911, had 1 trematode larva per host 

(Table 1). Ferosagitta hispida and S. helenae are 

reported as hosts for the first time, and the Mexican 

Caribbean Sea is reported as a new locality. 

Cercaria owreae has an oval to pyriform 

body 0.166-0.575 (0.333) long and 0.087-0.235 

(0.154) wide and 2 posterior cylindrical appendages 

0.066-0.131 (0.107) long (Fig. 2). The tegument 

has deep circular furrows and dermal pa- 

Figure 2. Cercaria owreae: ventral view (SEM) of entire specimen; 1 appendage is missing. Scale 50 p, 

Figure 3. Cercaria owreae: oral and ventral suckers (SEM) showing dermal papillae. Scale 50 u.m. 



pillae in the anteroventral and anterodorsal body 

regions extending to the acetabulum. The oral 

sucker, 0.041-0.079 (0.060) long and 0.041-0.1 

(0.065) wide, has a subterminal mouth and is 

strongly muscular, with 11 papillae encircling it 

and another 5 distributed irregularly (Fig. 2). 

The acetabulum, 0.045-0.108 (0.104) length and 

0.045-0.133 (0.090) width, in a preequatorial 

position, also has 13 papillae encircling it and 5 

to 6 papillae nearby (Fig. 3). The average ratio 

of the diameters of the oral and ventral suckers 

is 1:1.7, and there is a slit-like opening anterior 

to the acetabulum. The muscular pharynx, which 

is round to oval, leads to a short esophagus and 

thence to a cecal bifurcation. The esophageal or 

cecal diverticula were not observed. The intestinal 

cecum is unbranched and passes into the 2 

appendages. No vitelline glands or gonads were 

observed. The excretory vesicle is Y-shaped and 

does not enter the posterior appendages. Its lateral 

excreting tubules join together dorsally to 

the pharynx. The excretory pore is terminal. 

Dermal papillae in the oral and ventral suckers 

are reported here for the first time; papillae 

in the anterodorsal and anteroventral body regions 

were reported in the family Accacoeliidae 

by Odhner (1911). Subcuticular tissues from the 

deep fold facing the acetabulum, which are 

"thickenings producing small papillae," were 

reported by Dawes (1959), but the papillae encircling 

the suckers have not been reported. 

Cercaria owreae has been previously reported 

in the Florida Current, parasitizing the chaetognaths 

Flaccisagitta enflata, Flaccisagitta hexaptera 

(d'Orbigny, 1836) and Flaccisagitta lyra 

(Krohn, 1853) (see Hutton, 1952, 1954) in the 

Caribbean Sea between Jamaica and Cuba 

(Dawes, 1958, 1959) and in Cuban waters in the 

north (Suarez-Caabro, 1955). It parasitizes Zonosagitta 

pulchra (Doncaster, 1902) northwest 

of Madagascar; Serratosagitta serratodentata 

var. atlantica and Sagitta bipunctata Quoy and 

Gaimard, 1828, in Mauritania; F. hexaptera in 

Cabo Frio and west of Mossamedes in Angola; 

and F. enflata off Gabon, Mauritania, and Liberia 

(Furnestin and Rebecq, 1966). 

Prevalence and mean intensity values of infection 

in the present study were low, comparable 

to those obtained by Hutton (1954) and 

Furnestin and Rebecq (1966), even though the 

host species are different. To date, 7% is the 

highest prevalence reported (Dawes, 1959). 

The parasites reported here are the smallest 

reported until now (0.166-0.575). The largest 

(0.245-2.200) were those reported by Furnestin 

and Rebecq (1966). These authors reported 

length variability between posterior appendages 

and body length. They noted that the perforating 

trematode larvae emerging from the first intermediate 

host (a benthic coastal mollusk) were 

small parasites with similarly small appendages 

and that both the body of the larva and the appendages 

would not grow proportionately. 

Cercaria owreae has been found in the tropical-subtropical 

zones (Furnestin and Rebecq, 

1966) off the coast of Miami, Florida, in the 

Caribbean Sea, and in the east and northwest of 

Africa. However, this distribution does not 

match that of the chaetognath species; for example, 

Flaccisagita enflata is distributed worldwide 

(Alvarino, 1964, 1965). No one has recorded 

a holoplanktonic intermediate host; thus, 

it seems more plausible that the Cercaria 

owreae distribution recorded until now has been 

determined by the initial intermediate host, the 

benthic mollusk (Furnestin and Rebecq, 1966). 

According to Dawes (1959), Cercaria owreae 

should be placed within the genus Accacladocoelium 

Odhner, 1928. The length of the ceca 

going into the posterior appendages suggests 

that they could correspond to the anal openings 

ending in the excretory vesicle walls in the case 

of the adult; this feature is present in several 

families, but it has also been observed in 7 genera 

of the family Accacoeliidae. Additionally, 

the presence of 6 diverticula in the anterior region 

of the intestinal ceca on each side resembles 

the situation in 1 of the genera of the family. 

Dawes (1959) mentioned that Accacladocoeliurn 

petasiporum Odhner, 1928 does not belong 

to this trematode larval stage because this species 

has a conspicuous acetabulum, which does 

not correspond with Cercaria owreae. The other 

3 species, Accacladocoelium nigroflavum (Rudolphi, 

1819), Accacladocoelium macrocotyle 

(Diesing, 1858) sensu Monticelli, 1893, and Accacladocoelium 

alveolatum Robinson, 1943, remain 

to be studied. It is worth mentioning that 

these 3 species have been reported as parasites 

of the sunfish Mola mola (Linnaeus, 1758), 

which could indicate that Cercaria owreae may 

parasitize this fish species. 

Whatever the course of discussions in relation 

to the taxonomic position of this trematode, the 

presence of papillae circling both the oral and 

ventral suckers in Cercaria owreae is a distinc- 



live feature not reported previously in any species 

of Accacladocoelium. This feature raises the 

possibility of an undescribed species within the 

genus. 

We thank Yolanda Hornelas of the Institute 

de Ciencias del Mar y Limnologfa, UNAM, for 

helping with the SEM photomicrographs. Rebeca 

Gasca and Eduardo Suarez-Morales, of El 

Colegio de la Frontera Sur-Unidad Chetumal 

kindly supplied the biological material. 


Alvarino, A. 1964. Bathymetric distribution of chaetognaths. 

Pacific Science 18:64-82. 

. 1965. Chaetognaths. in Harold Barnes, ed. 

Annual Review of Oceanography and Marine Biology. 

3:115-195. 

Dawes, B. 1958. Sagitta as a host of larval trematodcs, 

including a new and unique type of cercaria. Nature 

182:960-961. 

. 1959. On Cercaria owreae (Hutton, 1954) 

from Sagitta hexaptera (d'Orbigny) in the Caribbean 

plankton. Journal of Helminthology 33:209- 

222. 

Furnestin, M. L., and J. Rebecq. 1966. Sur 1'ubiquite 

de Cercaria owreae (R. F. Hutton, 1954). Annales 

de Parasitologie 41:61-70. 

Hutton, R. F. 1952. Schistosome cercariae as the 

probable cause of seabather's eruption. Bulletin of 

Marine Science of the Gulf and Caribbean 2:346- 

359. 

. 1954. Metacercaria owreae n. sp. an unusual 

trematode larvae from the Florida Current. Chaetognaths. 

Bulletin of Marine Science of the Gulf 

and Caribbean 4:104-109. 

Odhner, T. 1911. Zum natiirlichen System dcr digenen 

Trematoden. Zoologischer Anzeiger 4:513— 

531. 

Margolis, L., G. W. Esch, J. C. Holmes, A. M. Kuris, 

and G. A. Schad. 1982. The use of ecological 

terms in parasitology. Journal of Parasitology 68: 

131-133. 

Suarez-Caabro, J. A. 1955. Quetognatos de los mares 

Cubanos. Memorias de la Sociedad Cubana de 

Historia Natural 22:125-180. 


66(2), 1999 pp. 197-201 

Research Note 

New Host and Locality Records for Three Species of Glypthelmins 

(Digenea: Macroderoididae) in Anurans of Mexico 

U. RAZO-MENDIVIL,' J. P. LACLETTE,2 AND G. PEREZ-PONCE DE LEON1-3 

1 Laboratorio de Helmintologla, Institute de Biologfa, Universidad Nacional Autonoma de Mexico, Ap. Postal 

70-153, C.P. 04510, Mexico D.F., Mexico (e-mail: ppdleon@servidor.unam.mx), and 

2 Departamento de Inmunologia, Institute de Investigaciones Biomedicas, Universidad Nacional Autonoma de 

Mexico, Ap. Postal 70228, C.P. 04510, Mexico D.F., Mexico 

ABSTRACT: During an inventory of the helminth parasites 

of amphibians from several localities in Mexico, 

trematode parasites of the genus Glypthelmins from 5 

species of frogs were studied. Three species of Glypthelmins 

were collected from Rana montezumae, Rana 

dunni, Rana neovolcanica, Rana megapoda, and Rana 

vaillanti. New host and locality records for Glypthelmins 

quieta and Glypthelmins californiensis in anurans 

from Mexico are established, and we report Glvpthelmins 

facioi for the first time from R. vaillanti from Los 

Tuxtlas, Veracruz State. Diagnostic characters for each 

parasite species and sister-group relationships are presented. 

KEY WORDS: Digenea, Macroderoididae, Glypthelmins 

spp., anurans, systematics, frogs, Rana spp., 

Mexico. 

' Corresponding author. 

The genus Glypthelmins was established by 

Stafford (1905) to include Distomum quietum 

Stafford, 1900, parasitic in Rana catesbeiana 

Shaw, 1802, Rana virescens Kalm, 1878, and 

Hyla pickeringll Holb, 1890, all from Canada. 

At the present time there is controversy about 

the species comprising the genus Glypthelmins, 

primarily because the original description of the 

type species of Glypthelmins was incomplete. 

This, and some degree of intraspecific morphological 

variability among some members of the 

genus, have led to taxonomic uncertainty concerning 

the species. This confusion has resulted 

in investigators creating nonphylogenetic 

groups, and some species that should be included 

in Glypthelmins were assigned to other gen- 



Table 1. Prevalence and mean abundance of 3 species of Glypthelmins in 5 species of frogs from Mexico. 

Glypthelmins 

califomiensis 

Host 

Local ity* 

Aft 

quieta 

facioi 

Rana montezumae 

Rana dunni 

Rana megapoda 

Rana neovolcanica 

Rana vaillanti 

CLE 

LZA 

LPA 

LCU 

MCO 

LAE 

89 

73 

18 

46 

34 

34 

330±/23.6§ (3.7)|| 

273/46.6 (3.7) 

4/22.2 (1) 

— 

— 

— 

1034/39.3 (11.6) 

39/15 (3.5) 

180/50 (20) 

6/8.7 (0.13) 

231/31.7 (5.6) 

— 

— 

— 

— 

31/41.2 (0.91) 

:i: CLE = Cienaga de Lerma; LZA = Lago de Zacapu; LPA = Lago de Patzcuaro; LCU = Lago de Cuitzeo; MCO 

Manantiales de Cointzio; LAE = Laguna Escondida. 

t N = sample size. 

:|: Number of worms collected. 

§ Prevalence of infection (expressed as %). 

|| Mean abundance of infection (mean no. of worms per host examined). 

era such as Margeana Cort, 1919, Microderma 

Mehra, 1931, Choledocystus Pereira and Cuocolo, 

1941, Rauschiella Babero, 1951, Reynoldstrema 

Cheng, 1959, and Repandum Byrd and 

Maples, 1963 (Miller, 1930; Caballero, 1938; 

Cheng, 1959; Byrd and Maples, 1963). In Mexico, 

at least 4 species of the genus have been 

reported from frogs and toads: Glypthelmins califomiensis 

(Cort, 1919) Miller, 1930, Glypthelmins 

quieta (Stafford, 1900) Stafford, 1905, 

Glypthelmins intermedia (Caballero, Bravo, and 

Zerecero, 1944) Yamaguti, 1958 (=Choledocystus 

intermedia), and Glypthelmins tineri (Babero, 

1951) Brooks, 1977 (=Rauschiella tineri) 

(see Lamothe-Argumedo et al., 1997; Brooks, 

1977). As part of an ongoing inventory of the 

helminth parasites of amphibians from different 

localities in Mexico, we establish herein new 

host and locality records for 3 species of Glypthelmins. 

During this study, we examined the 

species of Glypthelmins deposited at the Coleccion 

Nacional de Helmintos (CNHE) and produced 

a revised list of hosts and species in Mexico. 

Between 1996 and 1997, individuals of 18 

species of frogs and toads were collected from 

9 localities in Mexico. Only at 5 of these localities 

(Cienaga de Lerma, Estado de Mexico 

[CLE], 19°17'N, 99°30'W; Lago de Patzcuaro, 

Michoacan [LPA], 19°30'N, 101°36'W; Lago de 

Zacapu, Michoacan [LZA], 19°49'N, 101°47'W; 

Manantiales de Cointzio, Michoacan [MCO], 

19°35'N, 101°14'W; and Laguna Escondida, Los 

Tuxtlas, Veracruz [LAE], 20°37'N, 98°12'W), 

and only in 5 of the 18 species of frogs and 

toads studied were several specimens of Glypthelmins 

recovered from the intestines of their 

hosts. Anurans were captured by hand, and in 


and an I- or Y-shaped excretory vesicle. Glypthelmins 

quieta is characterized by having 2 

groups of prominent peripharyngeal glands on 

each side of the pharynx extending to the cecal 

bifurcation, with gland ducts opening at the posterior 

border of the oral sucker. Vitelline follicles 

extend from the posterior border of the pharynx 

and occasionally from the midlevel of the esophagus, 

reaching far beyond the posterior border 

of the testes. In addition, G. quieta possesses 

cecal, intracecal, and extracecal uterine loops. 

The original description of G. californiensis 

by Cort (1919), based on live specimens, indicated 

the absence of peripharyngeal glands. We 

have studied specimens identified as G. californiensis 

from CNHE (nos. 3280-3284) and from 

the personal collection of Dr. Daniel Brooks 

from Rana aurora Baird and Girard, 1852, from 

British Columbia, Canada. These specimens 

possess reduced peripharyngeal glands that surround 

the pharynx both ventrally and dorsally. 

Because the location of the holotype of this species 

is not known, we are unable to confirm this 

characteristic until a neotype is assigned and 

studied. However, our observations agree with 

those made by O'Grady (1987) who described 

G. californiensis from British Columbia, naming 

these glands as medial glands. Glypthelmins californiensis 

has vitelline follicles that extend anteriorly 

to the level of the posterior border of the 

pharynx and occasionally to the posterior border 

of the oral sucker with follicles confluent dorsally 

at the cecal bifurcation. The vitellaria extend 

to the posterior border of the testes. Uterine 

loops are completely intracecal. In contrast, G. 

facioi is characterized by lacking peripharyngeal 

glands, vitelline follicles extending anteriad 

from the cecal bifurcation just beyond the posterior 

border of the left testis, by having oblique 

rather than symmetric testes, cecal and intracecal 

uterine loops, and by having tegumentary spines 

that extend only along the anterior % of the 

body. 

These 3 species of Glypthelmins constitute a 

monophyletic clade, according to the phylogenetic 

hypothesis proposed by Brooks (1977) and 

Brooks and McLennan (1993). Glypthelmins facioi 

is the sister species of the species pair G. 

quieta + G. californiensis. Glypthelmins facioi 

was originally described from R. pipiens Schreber, 

1782, from Costa Rica by Brenes et al. 

(1959), and later redescribed by Sullivan (1976). 

Herein, we report G. facioi for the first time 

from Mexico, thus establishing a new host and 

locality record. Based on previous geographical 

records, this species is apparently restricted to 

the neotropics. Glypthelmins quieta, the type 

species of the genus, is widely distributed in 

North America, including the eastern U.S.A., 

Canada, and Central Mexico, parasitizing at 

least 21 species of anurans in 5 genera (Acris 

Dumeril and Bibron, 1841, Bufo Laurenti, 1768, 

Hyla Laurenti, 1768, Pseudacris Fitzinger, 1843, 

and Rana Linnaeus, 1758). In Mexico, this species 

was previously recorded from R. montezumae 

from Xochimilco and Texcoco lakes, both 

in the vicinity of Mexico City (Lamothe-Argumedo 

et al., 1997). In this report we add 4 new 

locality records (CLE, LPA, LZA, MCO), and 3 

host records, all belonging to the R. pipiens 

complex (leopard frogs) including R. dunni, R. 

neovolcanica, and R. megapoda. 

Glypthelmins californiensis also occurs in the 

Nearctic Region but has a different geographic 

distribution than the type species; it occurs in 

North America, but is known only from 6 species 

of Rana and 1 species of Hyla. Its range 

extends through the western U.S.A. and Canada, 

converging with G. quieta in frogs from the central 

region of Mexico in localities of the Transverse 

Neovolcanic Axis, at the boundary between 

the Nearctic and Neotropical biogeographic 

zones. Previously, this species was reported 

in Mexico from R. montezumae and R. 

pipiens from Mexico City and Lerma (Caballero, 

1942; Caballero and Sokoloff, 1934; Leon- 

Regagnon, 1992) and from R. dunni from Lake 

Patzcuaro (Pulido, 1994). Herein, we establish 

Lake Zacapu as a new locality record for G. californiensis. 

Guillen (1992) recorded G. californiensis 

as a parasite of Rana berlandieri Baird, 

1854, and R. vaillanti from Los Tuxtlas, Veracruz 

State. We examined specimens deposited at 

the CNHE (no. 1514, 5 specimens). Based on 

our diagnoses of the 3 species, we believe these 

were misidentified because in them the vitellaria 

extend anteriorly to the level of cecal bifurcation, 

and posteriorly they extend to the posterior 

border of the testes. The specimens do have 

oblique testes, and the uterine loops are intraand 

extracecal. In our opinion, they are G. facioi. 

As can be generally expected, the close phylogenetic 

relationship between G. quieta and G. 

californiensis (see Brooks, 1977; Brooks and 

McLennan, 1993) determines some degree of 



Table 2. Species of Glypthelmins recorded from anurans from Mexico. 

Species 

Host 

Locality 

Reference 

Glypthelmins califomiensis* 

Glypthelmins facial* 

Glypthelmins intermedia']"^ 

Glypthelmins quieta* 

Glypthelmins tineri* 

* Intestine. 

t Liver. 

$ Gall bladder. 

§ Bile ducts. 

|| Locality not determined. 

Rana montezumae, 

Rana pipiens 

R. montezumae, R. 

pipiens 

Rana dunni 

Rana vaillanti, Rana 

berlandieri 

Bufo marinus 

R. dunni 

Rana megupoda 

Rana neovolcanica 

R. montezumae 

"Green frog" 

Mexico, Distrito Federal 

Xochimilco, Distrito Federal 

Cienaga de Lerma, Estado de Mexico 

Lago de Patzcuaro, Michoacan 

Lago de Zacapu, Michoacan 

Laguna Escondida, "Los Tuxtlas", 

Veracruz 

Rio Huixtla, Chiapas 

Tuxtepec, Oaxaca 

Lago de Patzcuaro and Lago de Zacapu, 

Michoacan 

Lago de Cuitzeo, Michoacan 

Manantiales de Cointzio, Michoacan 

Cienaga de Lerma, Estado de Mexico 

San Pedro Tlaltizapan, Estado de 

Mexico 

Xochimilco, Distrito Federal and Texcoco, 

Estado de Mexico 

Mexico|| 

Caballero and Sokoloff ( 1 934) 

Caballero (1942) 

Pulido (1994) 

This work 

This work; Guillen (1992) 

Caballero et al. (1944) 

Bravo (1948) 

This work 

This work 

This work 

This work 

Leon-Regagnon ( 1 992) 

Lamothe-Argumedo et al. 

(1997) 

Babero ( 1 95 1 ) 

morphological similarity. Detailed examination 

of diagnostic characters allowed us to review the 

taxonomic status of species of Glypthelmins deposited 

at the CNHE. We examined specimens 

from the following lots: lot no. 1561 representing 

10 specimens from R. dunni from Lake Patzcuaro, 

identified by Pulido (1994) and labeled as 

G. calif orniensis (1 individual is actually G. 

quieta); lot no. 1461, represented by 8 specimens 

from R. montezumae identified by Leon- 

Regagnon (1992) from Lerma, and labeled as G. 

californiensis, are G. quieta; lot no. 1181, 17 

specimens from R. montezumae from Lerma, 

collected and identified by Caballero (1942); and 

lot no. 2495, represented by 8 specimens from 

R. montezumae from Lake Xochimilco, identified 

by Dr. Eduardo Caballero, were correctly 

identified as G. californiensis; lots no. 1562 (3 

specimens) and 1563 (4 specimens), from R. 

montezumae from Lake Xochimilco and Lake 

Texcoco, respectively, were correctly identified 

as G. quieta. 

In Table 2, we present an updated and revised 

list of species of Glypthelmins in anurans from 

Mexico. Adding previous records to the results, 

we conclude the genus Glypthelmins is currently 

represented in Mexico by 5 species (G. quieta, 

G. calif orniensis, G. facioi, G. intermedia, and 

G. tineri) from at least 7 species of Rana and 1 

species of Bufo. The most common of these are 

G. californiensis and G. quieta, both found in 

different species of frogs in localities of the 

Mesa Central of Mexico. Whether or not these 

are all the species of Glypthelmins that occur in 

anurans from Mexico will be determined once 

further research on the helminth fauna of different 

species of amphibians in the country is finished. 

The species composition of the genus Glypthelmins, 

as well as its taxonomic position and 

relationships to other closely related genera, are 

still uncertain. Yamaguti (1971) recognized 23 

valid species; Brooks (1977) in his phylogenetic 

analysis of species of Glypthelmins, considered 

19 species to be valid. Prudhoe and Bray (1982) 

proposed that some species, allocated originally 

to other genera, should be transferred to Glypthelmins, 

and then included 27 species in the genus. 

A complete revision of the genus is necessary 

to clarify the taxonomic composition of 

this group of parasites as well as to update the 

phylogenetic hypotheses of Brooks (1977) and 

Brooks and McLennan (1993). We are currently 

obtaining DNA sequences of 18S ribosomal 


201 

genes as an additional source of characters. Preliminary 

results show an agreement of sistergroup 

relationships among the 3 species discussed 

here. 

We thank Luis Garcia, Agustm Jimenez, Berenit 

Mendoza, and Angelica Sanchez for their 

help collecting specimens, and Dr. Virginia Leon 

(CNHE) and Dr. Scott L. Gardner (HWML) for 

critical reviews of the manuscript. The critical 

reviews and comments made by 2 anonymous 

reviewers are appreciated. We gratefully acknowledge 

Dr. Daniel Brooks (University of Toronto) 

for the loan of specimens of Glypthelmins 

from his personal collection. This study was 

funded by the Program PAPIIT-UNAM nos. 

IN201396 and IN219198, and CONACYT 2676 

PN to G.P.P.L., and CONACYT LOO42-M9607 

and PAPIIT-UNAM IN-207195 to J.P.L. 


Babero, B. B. 1951. Rauschiella tineri n. g., n. sp. a 

trematode (Plagiorchiinae) from a frog. Journal of 


Bravo, H. M. 1948. Descripcion de dos especies de 

trematodos parasites de Bufo marinus L. procedentes 

de Tuxtepec, Oaxaca. Anales del Institute 

de Biologfa, Universidad Nacional Autonoma de 


Brenes, M. R., G. S. Arroyo, O. Jimenez-Quiroz, 

and E. Delgado-Flores. 1959. Algunos trematodos 

de Rana pipiens. Descripcion de Glypthelmins 

facioi n. sp. Revista de Biologfa Tropical 72:191- 

197. 

Brooks, R. D. 1977. Evolutionary history of some plagiorchioid 

trematodes of anurans. Systematic Zoology 

26:277-289. 

, and D. McLennan. 1993. Parascript: Parasites 

and the Language of Evolution. Smithsonian 

Institution Press, Washington, D.C. 429 pp. 

Byrd, E. E., and W. P. Maples. 1963. The glypthelminths 

(Trematoda: Digenea), with a redescription 

of one species and the erection of a new genus. 

Zeitschrift fur Parasitenkunde 22:521-536. 

Caballero, C. E. 1938. Contribucion al conocimiento 

de la helmintofauna de Mexico. Tesis Doctoral, 

Facultad de Filosoffa y Estudios Superiores, Universidad 

Nacional Autonoma de Mexico. 149 pp. 

. 1942. Trematodos de las ranas de la Cienaga 

de Lerma, Estado de Mexico. III. Redescripcion 

de una forma norteamericana de Haematotoechus 

y algunas consideraciones sobre Glypthelmins californiensis 

(Cort, 1919). Anales del Institute de 

Biologfa, Universidad Nacional Autonoma de 

Mexico, Serie Zoologia 13:71—79. 

, M. H. Bravo, and C. Zerecero. 1944. Estudios 

helmintologicos de la region oncocercosa de 

Mexico y de la Republica de Guatemala. Trematoda 

I. Anales del Instituto de Biologfa, Universidad 

Nacional Autonoma de Mexico, Serie Zoologia 

15:59-72. 

, and D. Sokoloff. 1934. Tercera contribucion 

al conocimiento de la parasitologfa de Rana montezumae. 

Anales del Instituto de Biologfa, Universidad 

Nacional Autonoma de Mexico, Serie Zoologia 

5:337-340. 

Cheng, T. C. 1959. Studies on the trematode family 

Brachycoeliidae, II. Revision of the genera Glypthelmins 

(Stafford, 1900) Stafford, 1905, and Margeana 

Cort, 1919; and the description of Reynoldstrema 

n. g. (Glypthelminae, n. subfam.). American 

Midland Naturalist 61:68-88. 

Cort, W. W. 1919. A new distome from Rana aurora. 

University of California Publications in Zoology 

8:283-298. 

Guillen, H. S. 1992. Comunidades de helmintos de 

algunos anuros de "Los Tuxtlas", Veracruz. Master's 

Thesis, Facultad de Ciencias, Universidad 

Nacional Autonoma de Mexico. 90 pp. 

Lamothe-Argumedo, R., L. Garcia-Prieto, D. Osorio-Sarabia, 

and G. Perez-Ponce de Leon. 1997. 

Catalogo de la Coleccion Nacional de Helmintos. 

Instituto de Biologfa, Universidad Nacional Autonoma 

de Mexico, CONABIO, Mexico. 211 pp. 

Leon-Regagnon, V. 1992. Fauna helmintologica de 

algunos vertebrados acuaticos de la Cienaga de 

Lerma, Estado de Mexico. Anales del Instituto de 

Biologfa, Universidad Nacional Autonoma de 


Miller, E. L. 1930. Studies on Glypthelmins quieta 

Stafford. Journal of Parasitology 16:237-243. 

O'Grady, R. T. 1987. Phylogenetic systematics and 

the evolutionary history of some intestinal flatworm 

parasites (Trematoda: Digenea: Plagiorchioidea) 

of anurans. Ph.D. Thesis, University of 

British Columbia, Vancouver, B.C., Canada. 210 

pp. 

Prudhoe, S., and R. A. Bray. 1982. Platyhehninth 

parasites of the Amphibia. Oxford University 

Press, Great Britain. 217 pp. 

Pulido, F. G. 1994. Helmintos de Rana dunni, especie 

endemica del Lago de Patzcuaro, Michoacan, 

Mexico. Anales del Instituto de Biologfa, Universidad 

Nacional Autonoma de Mexico, Serie Zoologfa 

65:205-207. 

Stafford, J. 1905. Trematodes from Canadian vertebrates. 

Zoologischer Anzeiger 28:681-694. 

Sullivan, J. J. 1976. The trematode genus Glypthelmins 

Stafford, 1905 (Plagiorchioidea: Macrodcroididae) 

with a redescription of G. facioi from 

Costa Rican frogs. Proceedings of the Helminthological 


Yamaguti, S. 1971. Synopsis of Digenetic Trematodes 

of Vertebrates I. Keigaku Publishing Co., Tokyo, 

Japan. 1,074 pp. 



66(2), 1999 pp. 202-205 

Research Note 

Radiographic Imaging of the Rat Tapeworm, Hymenolepis diminuta 

KIMBERLY M. DEINES, DENNIS J. RICHARDSON,' GERALD CONLOGUE, RONALD G. BECKETT, 

AND DAN M. HOLIDAY 

The Bioanthropology Research Institute at Quinnipiac College, Quinnipiac College, 275 Mount Carmel 

Avenue, Hamden, Connecticut 06518, U.S.A. 

ABSTRACT: The model of Hymenolepis diminuta Rudolphi 

in laboratory rats was used to investigate potential 

applications of radiographic imaging in the diagnosis 

and/or study of tapeworm infections. Radiographic 

imaging successfully demonstrated the presence 

of H. diminuta in the rat intestine in the presence 

of a water-soluble iodinated radiographic contrast medium, 

Gastrografin®. Even single worms and small 

segments of proglottids could be detected. Optimal imaging 

was achieved with an exposure factor of 3.75 

mAs at 54 kVp with mammography film. Visualization 

was improved by fasting the rat host to effect the elimination 

of food and fecal shadows. Elaboration of this 

methodology may prove useful in basic research and 

the incidental diagnosis of human tapeworm infection 

by permitting rapid diagnosis of prepatent infection, 

thereby providing a useful tool in efficacy testing of 

anthelmintics when assessing prepatent success and 

temporal aspects of drug activity. 

KEY WORDS: radiographic imaging, tapeworm, Cestoda, 

Hymenolepis diminuta, laboratory rat, diagnosis, 

Gastrografin, x-ray. 

Hymenolepis diminuta Rudolphi, 1819, is a 

cosmopolitan tapeworm of rats that occasionally 

infects humans. A closely related species, Hymenolepis 

nana Siebold, 1852 (syn. Vampirolepis 

nana (Siebold, 1852) Spassky, 1954), is one 

of the world's most common tapeworms and is 

especially prevalent among children, with prevalences 

of up to 97.3% having been reported 

among humans (Roberts and Janovy, 1996). Although 

light infections of H. nana are asymptomatic, 

heavy infections may be characterized 

by abdominal pain, diarrhea, headache, dizziness, 

anorexia, and various other nonspecific 

symptoms characteristic of intestinal cestodiasis 

(Markell et al., 1999). Sehr (1974) indicated that 

roentgenological recognition of Hymenolepis 

spp. in humans is relatively difficult and that radiographic 

findings are mostly negative or that 

1 Corresponding author 

(e-mail: richardson@quinnipiac.edu). 

202 

only nonpathognomonic changes can be seen in 

the mucosal pattern of the intestine. Gold and 

Meyers (1977) reported the radiographic diagnosis 

of a human infection with the beef tapeworm, 

Taenia saginata Goeze, 1782, in the 

small intestine of a 34 year old male patient. 

Following a barium enema, "small bowel examination 

clearly outlined an intraluminal, essentially 

continuous linear filling defect in the 

distal jejunum and ileum extending into the 

proximal descending colon" (Gold and Meyers 

1977, p. 493). In this instance, the worm extended 

into the proximal descending colon. It 

was concluded that tapeworm infection may be 

initially recognized on barium enema study. Unfortunately, 

barium enema studies would seldom 

be expected to be of great value in diagnosis 

because tapeworms are normally restricted to the 

small intestine. Aside from this information, little 

is known about radiographic imaging of tapeworm 

infections and, specifically, infection with 

Hymenolepis spp., although infections with other 

helminth species such as Schistosoma haematobium 

(Bilharz, 1852) Weinland, 1858, Ancylostoma 

duodenale (Dubini, 1843) Creplin, 

1845, and Ascaris lumbricoides Linnaeus, 1758, 

are sometimes diagnosed in the course of routine 

radiographic examination (Reeder and Palmer, 

1989). We utilized the laboratory model of Hymenolepis 

diminuta in rats to investigate potential 

applications of radiographic imaging in the 

diagnosis and/or study of Hymenolepis spp. The 

goals of this study were to determine whether 

infection of H. diminuta in rats can be diagnosed 

using radiography, to determine the optimal 

methodology for visualization of worms, and to 

determine what information can be obtained 

from radiographs of infected animals. 

Laboratory infection of rats was accomplished 

by feeding 3 female Wistar rats 10, 10, and 30 

cysticercoids, respectively, of H. diminuta taken 

from our laboratory colony of the grain beetle, 



Tenebrio molitar Linnaeus, 1758. Radiographic 

studies were conducted at 21 days postinfection. 

Baseline methodologies were established using 

an uninfected control rat. Each rat was lightly 

anesthetized with the inhalation anesthesia Halothane® 

(Halocarbon Laboratories, River Edge, 

New Jersey), and a 1.5 cc bolus of a water-soluble 

iodinated radiographic contrast medium, 

diatrizoate meglumine sodium solution (Gastrografin®; 

Squibb Diagnostics, Princeton, New 

Jersey), was administered through a 6 French 

teflon catheter inserted into the rat's stomach. X- 

rays were taken at various exposure factors and 

with various films to determine the optimal radiographic 

technique. Optimal imaging was 

achieved with an exposure factor of 3.75 mAs 

at 54 kVp with Kodak Min-R® single-emulsion 

mammography film. The rat was placed in a 

posterior-anterior or dorsal-ventral position and 

x-rays were taken at 5-min intervals to establish 

the length of time required for the contrast medium 

to reach the ileocecal junction. By 30 min, 

Gastrografin had filled the entire small intestine. 

Food material and fecal shadows were evident 

in the control rat. Next, Gastrografin was administered 

to Rat I, which had been fed 10 cysticercoids. 

At 30 min, posterior-anterior and lateral 

x-rays were taken. Based on the lateral projections, 

worms were evident in the anterior portion 

of the small intestine (Fig. 1). Rat I was 

killed in a carbon dioxide chamber, and the entire 

gastrointestinal tract, excluding the esophagus, 

was removed, coiled onto a mammography 

cassette, and x-rayed. From the x-ray, predictions 

were made concerning the position and relative 

abundance of worms. The intestine was 

then longitudinally dissected and the locations of 

the 10 adult tapeworms were noted and compared 

to the predictions. It was concluded that 

even in the presence of food in the intestine, 

infection can be diagnosed and inference made 

regarding the location and relative abundance of 

worms. 

Twenty-four hours after administration of 

Gastrografin to another infected rat, x-rays were 

taken to determine whether the contrast medium 

was taken up by or had adhered to the worms, 

thereby creating an outline of the worms in the 

alimentary canal, as may be the case with A. 

lumbricoides (Reeder and Palmer, 1989). Worms 

could not be visualized in x-rays of the small 

intestine when Gastrografin was lacking, suggesting 

that worms do not absorb the contrast 

medium. This is consistent with the observations 

of Gold and Meyers (1977) regarding human infection 

with T. saginata in association with a 

barium enema. 

To determine whether fasting would improve 

the conditions for visualization of worms, rats 

were not fed for 24 hr prior to the administration 

of Gastrografin and radiographic examination 

using the methodologies outlined above. After 

fasting, the control rat exhibited gas bubbles, but 

food and fecal shadows were lacking. Radiologic 

examination of Rat II, which had been fed 10 

cysticercoids, revealed that visualization of 

worms was improved by fasting because of the 

elimination of food and fecal shadows. The posterior-anterior 

projection of Rat II is shown in 

Figure 2. Interestingly, x-rays suggested that 

worms were present in the cecum. Postmortem 

examination confirmed this x-ray finding. The 

rat was killed and the intestine was removed and 

coiled onto a mammography cassette. Based on 

the x-ray (Fig. 3), predictions were made concerning 

the position and relative abundance of 

worms. The intestine was longitudinally dissected 

and the numbers and locations of worms were 

confirmed. The procedure was repeated with Rat 

III, which had been fed 30 cysticercoids. Even 

small sections of proglottids could be detected 

in the large intestine. 

We have shown that radiographic imaging can 

successfully demonstrate the presence of H. 

diminuta in the rat intestine. It is possible that 

these findings can be extended to human infections 

of H. nana. If so, this could be useful in 

the incidental diagnosis of human infection in 

the course of routine radiographic imaging. This 

could be especially valuable in areas of high parasite 

prevalence, such as Moscow, where prevalences 

as high as 97.3% have been reported 

(Karnaukov and Laskovenko, 1984; see Roberts 

and Janovy, 1996). Because of the size differences 

of the hosts and the worms, more information 

concerning the radiographic imaging of 

Hymenolepis spp. in humans is warranted to better 

define the radiographic presentation of human 

infection and the utility of this methodology 

in diagnosis. 

In addition to potential human clinical applications, 

this technique provides rapid diagnosis 

of prepatent infection without having to kill the 

animal. This may prove useful in studying the 

basic biology of H. diminuta, which exhibits 

complex emigrations and migrations within the 



Figures 1-3. Radiographic imaging of Hymenolepis diminuta. Scale is actual size. 1. Lateral projection 

of Rat I showing infection of Hymenolepis diminuta. Arrows indicate aggregation of worms in the small 

intestine. 2. Posterior-anterior projection of Rat II showing infection of Hymenolepis diminuta. Arrows 

indicate worms in cecum. 3. Radiograph of intestine removed from Rat II, showing infection of Hymenolepis 

diminuta. Arrows indicate worms in a substantial portion of the small intestine. 



rat intestine (Mettrick and Podesta, 1974). This 

may also be a useful tool in efficacy testing of 

anthelmintics when assessing prepatent success 

and temporal aspects of drug activity. 


Gold, B. M., and M. A. Meyers. 1977. Radiologic 

manifestations of Taenia saginata infestation. 

American Journal of Roentgenology 128:493- 

494. 

Karnaukov, V. K., and A. I. Laskovenko. 1984. 

Clinical picture and treatment of rare human helminthiasis 

(Hymenolepis diminuta and Dipylidium 

caninum). Meditsinskaya Parazitologiya i Parasitarnye 

Bolezni 4:77-79. 

Markell, E. K., D. T. John, and W. A. Krotoski. 

1999. Markell and Voge's Medical Parasitology, 

8th ed. W. B. Saunders Co., Philadelphia, Pennsylvania. 

501 pp. 

Mettrick, D. F., and R. B. Podesta. 1974. Ecological 

and physiological aspects of helminth—host interactions 

in the mammalian gastrointestinal canal. 

Advances in Parasitology 12:183-278. 

Reeder, M. M., and P. E. S. Palmer. 1989. Infections 

and infestations. Pages 1475-1542 in A. R. Margulis 

and H. J. Burhenne, eds. Alimentary Tract 

Radiology, 4th ed. C. V. Mosby, St. Louis, Missouri. 

Roberts, L. S., and J. Janovy, Jr. 1996. Gerald D. 

Schmidt and Larry S. Roberts' Foundations of 

Parasitology, 5th ed. Wm. C. Brown Publishers, 

Dubuque, Iowa. 659 pp. 

Sehr, M. A. 1974. The radiology of parasitic diseases. 

Acta Universitatis Carolinae Medica, Monographia 

LXIII, Universita Karlova, Praha (Charles 

University, Prague). 119 pp. 


66(2), 1999 pp. 205-208 

Research Note 

Helminths of Two Lizards, Barisia imbricata and Gerrhonotus 

ophiurus (Sauria: Anguidae), from Mexico 

STEPHEN R. GOLDBERG,1-4 CHARLES R. BuRSEY,2 AND JOSE L. CAMARiLLO-RANGEL3 

1 Department of Biology, Whittier College, Whittier, California 90608, U.S.A. (e-mail: 

sgoldberg@whittier.edu), 

2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, 

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

' Laboratorio y Coleccion de Herpetologfa, Conservacion y Mejoramiento del Ambiente, Escuela Nacional de 

Estudios Profesionales Iztacala, Universidad Nacional Autonoma de Mexico, A.P. 314, Tlalnepantla, Estado de 

Mexico, Mexico (e-mail: herpetol@servidor.unam.mx) 

ABSTRACT: The gastrointestinal tracts of 37 Barisia 

imbricata (Wiegmann) and 54 Gerrhonotus ophiurus 

Cope from Mexico were examined for helminths. The 

helminth fauna of B. imbricata consisted of 4 species 

of nematodes: Cosrnocercoides variabilis (Harwood), 

Oswaldocruzia pipicns Walton, Physaloptera retusa 

Rudolphi, and Raillietnema brachyspiculatum Bursey, 

Goldberg, Salgado-Maldonado, and Mendez-de la 

Cruz. Gerrhonotus ophiurus harbored 1 trematode species, 

Brachycoelium salamandrae (Frolich), and 2 

nematode species, Cosrnocercoides variabilis and Physaloptera 

retusa. All represent new host records. With 

the exception of R. brachyspiculatum, all these helminths 

are generalists, which are widely distributed in 

other amphibian and reptile hosts. 

KEY WORDS: lizards, Sauria, Barisia imbricata, 

Gerrhonotus ophiurus, Anguidae, Trematoda, Brachy- 


coelium salamandrae, Nematoda, Cosmocercoides 

variabilis, Oswaldocruzia pipiens, Physaloptera retusa, 

Raillietnema brachyspiculatum, Mexico. 

Barisia imbricata (Wiegmann, 1828) occurs 

in highland pine forests throughout Mexico west 

of the Isthmus of Tehuantepec (Good, 1988). 

Gerrhonotus ophiurus Cope, 1866, occurs in the 

Mexican states of Hidalgo, Puebla, San Luis Potosi, 

and Veracruz (Good, 1994). There are, to 

our knowledge, no reports of helminths from 

these species. We report here the helminths from 

populations of B. imbricata and G. ophiurus. 

Thirty-seven B. imbricata deposited in the 

herpetology collection (ENEPI) of the Escuela 

Nacional de Estudios Profesionales Iztacala, 

Universidad Nacional Autonoma de Mexico 

(UNAM) were examined: 23 from Estado de 



Mexico, snout-vent length (SVL) =104 mm ± 

14.8 SD, range = 68-124 mm, ENEPI numbers 

11, 12, 393, 616, 699, 730, 3873, 3874 (collected 

1984-1985) and 4939, 5436, 5587-5591, 

6333-6340 (collected 1990-1991); 14 from Hidalgo, 

SVL = 89 mm ± 20.5 SD, range = 61- 

123 mm, ENEPI numbers 4321, 4834-4836, 

5841-5850 (collected 1990-1991). Fifty-four G. 

ophiurus, SVL = 112 mm ± 12 SD, range = 

80-136 mm, were collected near San Antonio 

Ixtatetla, Municipio de Huayacocotla, Veracruz, 

(20°43'N, 98°22'W) during 1991, ENEPI numbers 

6252-6262, 6264-6295, 6297-6303, 6305, 

6306, 6308, 6309. 

The abdominal cavities were opened and the 

gastrointestinal tracts were excised by cutting 

across the esophagus and rectum. The digestive 

tracts were each slit longitudinally and examined 

under a dissecting microscope. Each helminth 

was removed to a drop of undiluted glycerol on 

a glass slide for study; trematodes were regressively 

stained with hematoxylin and mounted in 

Canada balsam. 

Because a statistically significant difference 

was found for the SVL between the Estado de 

Mexico and Hidalgo populations of B. imbricata 

(Kruskal-Wallis test = 4.87, 1 df, P < 0.05) and 

because of community similarity differences 

(Jaccard's coefficient, 0.75; Morisita's index, 

0.73), data for the 2 populations were not combined. 

The helminth fauna of the Estado de 

Mexico population of B. imbricata consisted of 

3 species of nematodes: Cosmocercoides variabilis 

(Harwood, 1930), Oswaldocruzia pipiens 

Walton, 1929, and Raillietnema brachyspiculatum 

Bursey, Goldberg, Salgado-Maldonado, and 

Mendez-de la Cruz, 1998. The helminth fauna 

of the Hidalgo population of B. imbricata consisted 

of 4 species of nematodes: C. variabilis, 

O. pipiens, Physaloptera retusa Rudolphi, 1819, 

and R. brachyspiculatum. Helminths of G. 

ophiurus consisted of 1 species of trematode, 

Brachycoelium salamandrae (Frolich, 1789), 

and 2 species of nematodes, C. variabilis and P. 

retusa, all representing new host and locality records. 

Terminology is in accordance with Bush 

et al. (1997). Representative specimens were 

placed in vials of 70% ethanol and deposited in 

the U.S. National Parasite Collection, Beltsville, 

Maryland (USNPC): Barisia imbricata: Cosmocercoides 

variabilis, USNPC 88291; Oswaldocruzia 

pipiens, USNPC 99292; Physaloptera 

retusa, USNPC 88293; Raillietnema brachyspiculatum, 

USNPC 88294. Gerrhonotus ophiurus: 

Brachycoelium salamandrae, USNPC 87245; 

Cosmocercoides variabilis, USNPC 87246; Physaloptera 

retusa, USNPC 87247. Helminths 

from Barisia imbricata were also deposited in 

the Coleccion Nacional de Helmintos (CNHE), 

Instituto de Biologia de la Universidad Nacional 

Autonoma de Mexico, Mexico, Distrito Federal, 

Mexico: Cosmocercoides variabilis, CNHE 

3384; Oswaldocruzia pipiens, CNHE 3387; Physaloptera 

retusa, CNHE 3385; Raillietnema brachyspiculatum, 

CNHE 3386. 

The number of infected lizards, number of 

helminths, prevalence, mean intensity ± SD, and 

range and mean abundance ± SD are presented 

in Table 1. Both lizard species harbored C. variabilis 

and P. retusa. Brachycoelium salamandrae 

was found only in G. ophiurus; O. pipiens 

and R. brachyspiculatum were found only in B. 

imbricata. 

Brachycoelium salamandrae, the only trematode 

species found in this study, was found in 

the small intestines of 2 G. ophiurus. There has 

been controversy surrounding the assignment of 

species to the genus Brachycoelium. Rankin 

(1938) reduced all the American species to synonymy 

with B. salamandrae, a European species 

and the type species of the genus. However, 

Parker (1941) and Cheng (1958) did not accept 

the synonymy and recognized 7 and 10 species 

of the genus, respectively. Later Cheng and 

Chase (1960) and Couch (1966) described additional 

species, bringing to 13 the number of 

species assigned to the genus. Prudhoe and Bray 

(1982) favored a monospecific genus. Regardless 

of confusion in the taxonomy, the specimens 

collected in this study most closely resemble 

B. salamandrae as described by Cheng 

(1958), in that they were elongate distomes, approximately 

3 mm in length, more than twice 

the length of any other species assigned to the 

genus, and the vitellaria extended beyond the 

ceca and did not join on the midline. The North 

American host list for B. salamandrae includes 

salamanders, anurans, lizards, and snakes (see 

Prudhoe and Bray, 1982). Gerrhonotus ophiurus 

is added to this host list. 

As in the case of the identity of species of 

Brachyocoelium, some uncertainty also exists 

for North American species of Cosmocercoides. 

Cosmocercoides variabilis, originally described 

as Oxysomatium variabilis by Harwood (1930) 

from Bufo valliceps Wiegmann, 1833, collected 



Table 1. Helminths from the anguid lizards, Barisia imbricata and Gerrhonotus ophiurus, from Mexico. 

Lizard species 

Helminth species 

Number 

of Number Prevainfected 

of lence 

lizards helminths (%) 

Mean intensity ± SD 

(range) 

Mean abundance 

± SD 

Barisia imbricata (Estado de Mexico, TV = 23) 

Nematoda 

Cosmocercoides variabilis 3 4 13 1.3 ± 0.6 (1—2) 

Oswaldocruzia pipiens 3 6 13 2.0 ± 1.7 (1-4) 

Raillietnema brachyspiculaturn 1 83 4 83 

Barisia imbricata (Hidalgo, N = 14) 

Nematoda 

Cosmocercoides variabilis 2 6 1 5 3.0 ± 2.8 (1-5) 

Oswaldocruzia pipiens 11 86 79 7.8 ±6.1 (1-15) 

Physaloptera retusa 6 18 43 3.0 ± 3.2 (1-8) 

Raillietnema brachyspiculatum 1 93 7 93 

Gerrhonotus ophiurus (Veracruz, /V = 54) 

Trematoda 

Brachycoelium salamandrae 2 5 4 2.5 ± 2.1 (1-4) 

Nematoda 

Cosmocercoides variabilis 17 21 31 1.2 ± 0.6 (1—3) 

Physaloptera retusa 10 65 19 6.7 ± 12.0 (1-40) 

0.4 ± 1.3 

6.1 ± 6.3 

1.2 ± 2.5 

6.6 ± 24.9 

0.4 ± 0.7 

1.2 ± 5.6 

at Houston, Texas, was considered a synonym 

of the molluscan parasite Cosmocercoides dukae 

(Roll, 1928) by Ogren (1953), who presumed 

that amphibians acquired C. dukae infections by 

ingesting infected mollusks. Cosmocercoides 

dukae was first described by Holl (1928) from 

the salamander Notophthalmus viridescens (Rafinesque, 

1820) from North Carolina. Wilkie 

(1930) established the genus Cosmocercoides, 

and Travassos (1931) included both C. dukae 

and C. variabilis in his monograph on the Cosmocercidae. 

Vanderburgh and Anderson (1987) 

demonstrated that these 2 species of Cosmocercoides 

are distinct. The major difference in the 

2 species is the number of rosette papillae of the 

male: C. dukae with 12 pairs and C. variabilis 

with 14-20. Specimens collected in our study 

had 16-18 papillae. The host list includes salamanders, 

anurans, lizards, snakes, and turtles 

(see Baker, 1987). Barisia imbricata and G. 

ophiurus are added to this list. 

All North American specimens of the genus 

Oswaldocruzia have been referred to O. pipiens 

by Baker (1987). This species is widely distributed 

in North America and has been reported 

from anurans, salamanders, lizards, and tortoises 

(see Baker, 1987). Barisia imbricata is added to 

this host list. 

Physaloptera retusa is a common parasite of 

North American lizards (see Baker, 1987). Both 

Barisia imbricata and G. ophiurus are added to 

this host list. 

Raillietnema brachyspiculatum was recently 

described from the xantusiid lizard, Lepidophyma 

tuxtlae Werler and Shannon, 1957, from Veracruz, 

Mexico, by Bursey et al. (1998). Barisia 

imbricata is a new host record, and the states of 

Hidalgo and Mexico are new locality records for 

this nematode. 

The results reported here support previous 

studies on North American anguids (see Goldberg 

et al., 1999), which have shown that lizards 

of this family appear to harbor depauperate communities 

comprised of generalist helminths. As 

can be seen by the host lists above, with the 

exception of the recently described R. brachyspiculatum 

(for which there is insufficient information 

to categorize), the helminth species harbored 

by B. imbricata and G. ophiurus are generalists. 

Although host lists can easily be constructed 

and host distributions mapped, parasite 

distribution patterns are more difficult to evaluate. 

Reasons for varying infection rates among 

host populations are not understood; for example, 

there is a significant difference between the 

Estado de Mexico and Hidalgo populations of 

B. imbricata for O. pipiens (chi-square = 15.8, 

1 df, P < 0.001). Additional work will be required 

to understand the factors influencing 



prevalence patterns of helminths in anguid lizards. 


Baker, M. R. 1987. Synopsis of the Nematoda parasitic 

in amphibians and reptiles. Memorial University 

of Newfoundland, Occasional Papers in 

Biology 11:1-325. 

Bursey, C. R., S. R. Goldberg, G. Salgado-Maldonado, 

and F. R. Mendez-De La Cruz. 1998. Raillietnema 

brachyspiculatum sp. n.(Nematoda: Cosmocercidae) 

from Lepidophyma tuxtlae (Sauria: 

Xantusiidae) from Mexico. Journal of the Helminthological 






Cheng, T. C. 1958. Studies on the trematode family 

Dicrocoeliidae. I. The genera Brachycoelium (Dujardin, 

1845) and Leptophallus Luhe, 1909, (Brachycoeliinae). 

American Midland Naturalist 59: 

67-81. 

, and R. S. Chase, Jr. 1960. Brachycoelium 

stablefordi, a new parasite of salamanders; and a 

case of abnormal polylobation of the testes of 

Brachycoelium storeriae Harwood, 1932 (Trematoda: 

Brachycoeliidae). Transactions of the American 


Couch, J. A. 1966. Brachycoelium ambystomae sp. n. 

(Trematoda: Brachycoeliidae) from Ambystoma 

opacum. Journal of Parasitology 52:46-49. 

Goldberg, S. R., C. R. Bursey, and H. Cheam. 1999. 

Helminths of the Madrean alligator lizard, Elgaria 

kingii (Sauria: Anguidae) from Arizona. Great Basin 

Naturalist 59:198-200. 

Good, D. A. 1988. Phylogenetic relationships among 

gerrhonotine lizards. An analysis of external morphology. 

University of California Publications in 

Zoology 121:1-139. 

. 1994. Species limits in the genus Gerrhonotus 

(Squamata: Anguidae). Herpetological Monographs 

8:180-202. 

Harwood, P. D. 1930. A new species of Oxysomatium 

(Nematoda) with some remarks on the genera Oxysomatium 

and Aplectana, and observations on 

the life history. Journal of Parasitology 17:61-73. 

Holl, F. J. 1928. Two new nematode parasites. Journal 

of the Elisha Mitchell Scientific Society 43:184- 

186. 

Ogren, R. E. 1953. A contribution to the life cycle of 

Cosmocercoides in snails (Nematoda: Cosmocercidae). 

Transactions of the American Microscopical 

Society 72:87-91. 

Parker, M. V. 1941. The trematode parasites from a 

collection of amphibians and reptiles. Journal of 

the Tennessee Academy of Science 16:27-45. 

Prudhoe, S. P., and R. A. Bray. 1982. Platyhelminth 

Parasites of the Amphibia. British Museum (Natural 

History), Oxford University Press, Oxford, 

U.K. 217 pp. + 4 microfiches. 

Rankin, J. S., Jr. 1938. Studies on the trematode genus 

Brachycoelium Duj. I. Variation in specific 

characters with reference to the validity of the described 

species. Transactions of the American Microscopical 

Society 57:358—375. 

Travassos, L. 1931. Pesquizas helminthologicas realizadas 

em Hamburgo. IX. Ensaio monographico 

da familia Cosmocercidae Trav., 1925 (Nematoda). 

Memorias do Institute Oswaldo Cruz 25:237- 

298. 

Vanderburgh, D. J., and R. C. Anderson. 1987. The 

relationship between nematodes of the genus Cosmocercoides 

Wilkie, 1930 (Nematoda: Cosmocercoidea) 

in toads (Bufo amcricanux) and slugs 

(Deroceras laevae). Canadian Journal of Zoology 

65:1650-1661. 

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

. Japanese Amphibia. Annals and Magazine of Natural 

History, Series 10, 6:606-614. 



66(2), 1999 pp. 209-210 

Anniversary Award 

The Helminthological Society of Washington 

SHERMAN S. HENDRIX 

J. Ralph Lichtenfels, right, presents 

the 1998 Anniversary Award to Sherman S. Hendrix 

Ladies and Gentlemen, in 1989 my longtime friend, Sherm Hendrix, presented the Anniversary 

Award to me after I completed a term as Editor of our journal. Nine years later, it is my pleasure 

to switch roles and (in your behalf) honor Sherm as he completes his term as Editor. 

Sherm was born June 1, 1939 in Bridgeport, Connecticut and grew up in Connecticut near Long 

Island Sound, where he developed an interest in biology and the marine environment. He received 

a B.A., with Departmental Honors, in Biology from Gettysburg College in 1961. 

Shortly after graduating from Gettysburg, Sherm married his college sweetheart, Carol Seibel. 

Carol and Sherm have raised 2 children, Mark, an Assistant Professor of Geology at the University 

of Montana, and Robin, a teacher who has taken time off to raise 2 children, Anna (5) and Rachel 

(2). Carol is an ordained Lutheran pastor, currently serving as Assistant to the Bishop for Congregational 

Care. 

Sherm was introduced to Parasitology at Florida State University, in courses taught by Rhodes 

"Buck" Holliman and Robert B. Short. Sherm received an M.S. degree from Florida State University 

in 1964 working under Bob Short. His thesis was titled, "Aspidogastrids from Northeastern 

Gulf of Mexico river drainages". While at Florida State University, he was a member of a 61-day 

Antarctic Scientific Cruise in 1964, on the Pacific side, out of Valparaiso. 

Later that year, he returned to his alma mater, Gettysburg College, as Instructor in Biology. 

While continuing his teaching career at Gettysburg, Sherm decided to pursue a Ph.D. at the 

University of Maryland and became a Graduate Teaching Assistant there in 1969, working under 

the guidance of Leo Jachowski. His doctoral dissertation, entitled, "The biology, ecology and taxonomy 

of Plagioporus hypentelii, a parasite of the hog sucker in the Monocacy River basin of 

Maryland and Pennsylvania", and his Ph.D. degree, were completed in 1972. He was an NIH 

Interamerican Fellow in Tropical Medicine at Louisiana State University in 1973 while on sabbatical 

from Gettysburg. By this time, Sherm had already been promoted to Assistant Professor at Gettysburg 

(in 1970). He became Associate Professor in 1977, and Professor in 1990, serving several 

terms as Chairman, Department of Biology, including a current term as Chair, begun in 1997. 

Sherm has developed and managed an almost idyllic career that is a balanced blend of teaching, 

209 



research, administration and service. Now you know why he is always pleasant and looks so young! 

He has taught a range of courses from Introductory Biology to Electron Microscopy, including such 

interesting titles as Parasitology, Biostatistics, Virology, Biological Control, and Microtechniques 

and Histochemistry. I encourage you to visit Sherm's excellent homepage (www.gettysburg.edu/ 

—shendrix) to learn more about his courses. He has also developed a homepage for HelmSoc 

(www.gettysburg.edu/~shendrix/helmsoc). 

His research has centered on the morphology, systematics and zoogeography of Monogenea and 

Trematoda of fish and molluscans. In 1987, an NSF Grant provided an opportunity for more research 

support (specifically, an illustrator) which resulted in several important papers on Monogenea of 

fishes, including a landmark, 107-page key and monograph, "Marine Flora and Fauna of the Eastern 

United States. Platyhelrninths: Monogenea." (NOAA Technical Report NMFS 121 of the Fisheries 

Bulletin). More recently he has traveled to Africa to study parasites of fish in Lake Malawi. A fullyear 

Sabbatical in 1994-1995 provided the time to initiate the Lake Malawi research with collaborator 

Jay Stauffer of Penn State. 

The service activities of a college Professor are many and varied, and Sherm has been recognized 

for outstanding service at Gettysburg College with the Alpha Phi Omega Service Award in 1979, 

and the Theta Chi Fraternity Chapter Service Award in 1987. Among his scientific societies, Sherm 

has been most active in the Pennsylvania Academy of Science and the Helminthological Society 

of Washington. He served as President of the Academy (1990—1992) and received its 1998 Lifetime 

Achievement Award. 

Professor Sherman S. Hendrix has brought honor and credit to the Helminthological Society of 

Washington in every leadership role possible. He was Corresponding Secretary Treasurer (1979- 

1982), President (1984), and Editor (1993-1998). In recognition of this outstanding, dedicated 

service the Society bestows its highest honor, The Anniversary Award, on Professor Sherman S. 

Hendrix. 


November 18, 1998 



66(2), 1999 pp. 211-212 

MINUTES 

Six Hundred Sixty-First Through 

Six Hundred and Sixty-Fifth Meeting 

661st Meeting: Walter Reed Army Institute of 

Research, Washington, DC, 14 October, 1998. 

The President opened the meeting and announced 

a slate of nominations for society officer 

positions: Eric P. Hoberg for President, Ronald 

Neafie for Vice President, Pat Carney for 

Recording Secretary, Nancy Pacheco for Corresponding 

Secretary-Treasurer, and Willis A. 

Reid, Jr. and Janet W. Reid for Editors. He also 

discussed the rationale for changing the name of 

the journal and suggestions that had been made 

for changing the format of meetings. The meeting 

was then turned over to Dr. Joan Jackson 

who introduced the speakers: Dr. Naomi Aronson 

spoke on "Clinical aspects of leishmaniasis"; 

Dr. Ed Rowton presented his paper on 

"The vector in leishmaniasis", and Dr. Jackson 

provided an overview of her studies on "Drug 

research in leishmaniasis." 

662'"' Meeting: Sabang Indonesian Restaurant, 

Wheaton, MD, 18 November 1998. The Anniversary 

Dinner Meeting and Program were presided 

over by the President, Dr. Eric Hoberg. 

The membership in attendance approved the 

slate of officers for 1999. Dr. J. Ralph Lichtenfels 

introduced the recipient of the Anniversary 

Award, Dr. Sherman S. Hendrix, Gettysburg 

College. In his acceptance comments, Dr. Hendrix 

reviewed his teaching and research career 

at Gettysburg College and shared highlights of 

field expeditions in search of marine parasites. 

663rd Meeting: Armed Forces Institute of Pathology, 

Washington, DC, January 18, 1999. 

The President welcomed members and visitors. 

He advised the membership that the Executive 

Committee had voted unanimously for changing 

the name of the Journal of the Helminthological 

Society of Washington to Comparative Parasitology 

at their September, 1998 meeting, and 

that an amendment to the Constitution of the Society 

was prepared and presented in writing to 

the general membership at the Anniversary 

Meeting in November, 1998. A motion to 

change the name of the journal to "Comparative 

Parasitology" was passed unanimously by the 

general membership. The membership was provided 

with a draft of the Society's "Mission and 

Vision" statements for review and comment. 

The meeting was then turned over to Vice President 

Ronald Neafie who introduced the speakers. 

Drs. Dennis Richardson and Richard Clopton 

jointly discussed "The counterpoint hypothesis: 

opposing forces in natural selection in parasite 

evolution." Dr. Mary Klassen's paper was 

entitled "Imitators of infectious diseases" in 

which she illustrated a series of artifacts that can 

be confused with agents of infectious diseases. 

Dr. Peter McEvoy gave a "case presentation" 

on nodular cutaneous microsporidiosis in a patient 

with AIDS. 

664"' Meeting: Uniformed Services University 

of the Health Sciences, Bethesda, MD, March 

10, 1999. The President opened the general 

meeting and welcomed members and their 

guests. The President then discussed the rationale 

for developing clear Mission and Vision 

statements and his intent to have them in place 

when the name of the Journal changes in January 

2000. The meeting was turned over to Dr. 

John Cross who introduced the speakers. Dr. 

Richard Andre provided an overview of "Applications 

of geographic information systems 

(GIS) for malaria control in Belize." Dr. Allen 

Richards reviewed research he had conducted on 

"Tumor necrosis factor (TNF) and associated 

cytokines in the host's response to malaria." Dr. 

Cross presented the final paper on his ongoing 

studies of "Cyclosporosis in Nepal." 

665th Meeting: University of Pennsylvania, New 

Bolton Center, Kennett Square, PA, May 8, 

1999. The President opened the general meeting 

and welcomed members and guests. The President 

then turned the meeting over to Dr. Jay Farrell. 

Dr. Farrell welcomed members and guests 

on behalf of the University of Pennsylvania and 

the New Jersey Society for Parasitology and introduced 

each of the speakers. Dr. Phillip Lo- 

Verde presented a paper on "Sex in schisto- 

211 



somes: a novel interplay." His presentation was 

followed by Dr. Phillip Cooper who discussed 

"The modulation of allergic inflammation by 

helminth infections." The final speaker was Dr. 

Joseph Urban who described the role of "Counter-regulatory 

properties of IL4/IL-13 and IFNgamma 

in controlling resistance to gastrointestinal 

nematodes." Following the meeting a wine 

and cheese reception was held in the Allam 

House with support from Pfizer Animal Health 

and the Laboratory of Parasitology, University 

of Pennsylvania. 

Respectfully submitted, 

W. Patrick Carney 

Recording Secretary 


662, 1999 pp. 212 

AUTHOR INDEX FOR VOLUME 66 

Aguirre-Macedo, L., 146 

Akahane, H., 41 

Alvarez-Cadena, J. N., 194 

Amin, O., 47, 123 

Bangs, M. J., 187 

Barnes, D. K., 70 

Bauer, A. M., 78 

Beck, C. A., 67 

Beckett, R. G., 202 

Blaney, L. M., 70 

Brugni, N. L., 92 

Bursey, C. R., 37, 78, 89, 175, 180, 

205 

Caillot, C., 95 

Camarillo-Rangel, J. L., 205 

Camp, J. W., 70 

Canaris, A. G., 123 

Cezar, A. D., 14, 81 

Cezar, G., 133 

Cheam, H., 78 

Ching, H. L., 25 

Conlogue, G., 202 

Deines, K. M., 202 

Dronen, N. O., 21 

Dvojnos, G. M., 56 

Endo, B. Y., 155 

Faliex, E., 95 

Fiorillo, R. A., 101 

Font, W. F, 101 

Forrester, D. J., 1, 7 

Garcia-Prieto, L., 41 

Gillilland, M. G., Ill, 73 

Goldberg, S. R., 37, 78, 89, 175, 

180, 205 

Gomez del Prado-Rosas, M. C., 

194 

Hendrix, S. S., 47 

Hernandez, S., 89 

Holiday, D. M., 202 

Kamiya, M., 28 

Kharchenko, V. A., 56 

Kinsella, J. M., 1,7, 123 

Koga, M., 41 

Korting, W., 146 

Kritsky, D. C., 138 

Kuchta, R., 146 

Kulo, S.-D., 138 

Laclette, J. P., 197 

Lamothe-Argumedo, R., 41, 194 

Lichtenfels, J. R., 56 

Luque, J. L., 14, 81 

Machado, P. M., 133 

Madhavi, R., 25 

Marchand, B., 95 

Martinez-Cruz, J. M., 41 

Matsuo, K., 28 

Mignucci-Giannoni, A. A., 67 

Montoya-Ospina, R. A., 67 

Morand, S., 95 

Muller-Graf, C. M., 95 

Muzzall, P. M., 73, 115 

Ogata, K., 41 

Oku, Y., 28 

Osorio-Saraiba, D., 41 

Perez-Ponce de Leon, G., 197 

Pilitt, P. A., 56 

Purnomo, 187 

Razo-Mendivil, U., 197 

Rego, A. A., 133 

Richardson, D. J., 202 

Rossi, P. R., 33 

Salgado-Maldonado, G., 146 

Scholz, T., 146 

Segura-Puertas, L., 194 

Sepulveda, M. S., 7 

Smales, L. R., 33 

Spalding, M. G., 7 

Tehrany, M. R., 21 

Turner, H. M., 86 

Vargas-Vazquez, J., 146 

Vidal-Martinez, V, 146 

Viozzi, G. P., 92 

Walker, D. J., 82 

Wardle, W. J., 21 

Wergin, W.. P., 155 

Williams, E. H., Jr., 67 

Wittrock, D. D., 82 

Wolter, J., 146 

Yabsley, M. J., Ill 

Ganzorig, S., 28 

Noblet, G. P., Ill 

Zunke, U., 155 



662, 1999 pp. 213-216 

KEYWORD AND SUBJECT INDEX FOR VOLUME 66 

Abbreviate! sp., 89, 175 

Abundance, 1, 7, 14, 28, 70, 73, 78, 

89, 92, 101, 115,175, 197, 

Acanthocephala, 7, 47, 70, 95, 101, 

111, 123 

Acanthocephalus dims, 70 

Acanthogyrus (Acanthosentis) tilapiae, 

47 

Acanthogyrus (Acanthosentis) 

malawiensis sp. n., 47 

Acanthostomidae, 146 

Acuaria rnultispinosa, 7 

Africa, 123, 138 

Alaeuris geochelone sp. n., 28 

Allodiscocotylidae, 81 

Alloglossoides caridicola, 86 

Amauroronis phoenicums, 123 

Amphibia, 73, 180, 187, 197 

Amphimenis arcticus, 1 

Anatomy, 155 

Andracantha gravida, 1 

Anguidae, 205 

Anguilla anguilla, 95 

Anguillicola crassus, 95 

Anniversary Award, 209 

Anura, 187, 197 

Anuretes anurus, 14 

Apharyngostrigea pipientis, 7 

Apophallus brevis, 1 

Arborophilia crudigularis, 123 

Ardca albus, 1 

Argentina, 92 

Arhymorhynchus pumilirostris, 1 

Ariidae, 146 

Ariopsis assimilis, 146 

Ariopsis seemani, 146 

Aristochromis christyi, 47 

Arius fe Us, 146 

Arius guatemalensis, 146 

Arkansas, U.S.A., 86 

Armadoskrjabini rostellata, 1 

Arthrocephalus lotoris, 111 

Ascocotyle gemina, 1 

Ascocotyle mcintoshi, 7 

Ascocotyle temiicollis, 1 

Ascocotyle (Phagicola) diminuta, 1 

Ascocotyle (Phagicola) nana, 1, 7 

Atlantic spadefish, 14 

Auchenoglanis occidentalis, 138 

Australia, 33, 89, 123, 175 

Austrobilharzia terrigalensis, 1 

Aves, 1, 7, 123 

Avioserpens galliardi, 7 

Bagridae, 47, 138 

Bagrobdella, 138 

Bagrobdella aiichenoglanii, 138 

Bagrus meridionalis, 47 

Bandicoot, 33 

Barbulostomum cupuloris, 101 

Barisia imbricata, 205 

Barnacle, 67 

Bathyclarias nyasensis, 47 

Birds, 1, 7, 123 

Blacksmith plover, 123 

Bolbogonotylus corkumi, 82 

Bolbophorus confusus, 21 

Borneo, 123 

Bothriocephalus claviceps, 95 

Brachycoelium salamandrae, 205 

Brazil, 14, 81, 133 

Brown pelican, 21 

Bursacetabulus macrobursus sp. n., 

21 

Bursacetabulus pelecanus sp. n., 21 

Caecidotea spp., 70 

Calidris ferruginea, 123 

Caligus minimus, 96 

Caligus mutabilis, 14 

Caligus haemulonis, 14 

Carnallanus oxycephalus, 101 

Capillaria herodiae, 7 

Capillaria mergi, 1 

Carangidae, 81 

Caribbean Sea, 67, 194 

Catfish, 138, 146 

Centrarchidae, 101 

Centrorhynchus conspectus, 111 

Cercaria owreae, 194 

Cestoda, 7, 73, 78, 95, 123, 133, 

175, 202 

Chaetognath, 194 

Chaetopterus faber, 14 

Chandler'onema longigutterata, 7 

Charadriiformes, 123 

Charadrius alexandrinus, 123 

Charadrius rnarginatus, 123 

Charadrius pallidus, 123 

Charadrius pccuarius, 123 

Charadrius ruficapillus, 123 

Charadrius tricollaris, 123 

Chelonibia manati, 67 

Chetumal, Mexico, 146 

Chicken, 92 

Chiorchis fabaceus, 67 

Chrysichthys nigrodigitatus, 138 

Cichla monoculus, 133 

Cichlidae, 47, 133 

Clarias rnossambicus, 47 

Clariidae, 47 

Clinostomum sp., 73 

Clinostomum attenuatum, 7 

213 

Clinostomum complanatum, 7 

Coastal zone, 14 

Cochleotrerna cochleotrema, 67 

Collared bush-robin, 123 

Colombia, 146 

Colorado, U.S.A., 123 

Columnar cells, 155 

Commensals, 67 

Common loon, 1 

Component community, 101 

Community structure, 14, 101 

Contracaecum multipapillatum, 7 

Contracaecum sp., 1, 115 

Cook Islands, 37 

Copepoda, 14, 95 

Copidochrornis cf. thinos, 47 

Corallobothriinae, 133 

Coronocyclus coronatus, 56 

Coronocyclus sagittatus, 56 

Corsica, 95 

Cosmocephalus obvelatus, 1, 7 

Cosmocercoides dukae, 73 

Cosmocercoides variabilis, 205 

Cotylurus erraticus, 1 

Cotylurus platycephalus, 1 

Crayfish, 86 

Crepidostomum cornutum, 101 

Crustacea, 14, 70, 86, 95 

Cryptogonimidae, 82 

Cryptogonimus chyli, 82 

Ctenopharynx (Otopharynx) pictus, 

47 

Ctenotus leonhardii, 86 

Ctenotus quattuordecimlineatus, 89 

Cucullanus sp., 95 

Curlew sandpiper, 123 

Cyathostoma phenisci, 1 

Cyathostominea, 56 

Cyclustera ibisae, 1, 7 

Cyprinidae, 47 

Cyst, 73, 78, 82, 95 

Dactylogyridae, 138 

Dasyuridae, 33 

Day gecko, 78 

Deformities, 73 

Dendritobilharzia pulverulenta, 1 

Dendrouterina ardeae, 7 

Denmark, 56 

Deropristis inflata, 95 

Desmidocercella numidica, 7 

Desportesius invaginatus, 7 

Desportesius larvae, 7 

Desportesius trianuchae, 7 

Diagnosis, 202 

Diagnostic parasitology course, 40 



Diasiella diasi, 7 

Dicentrarchus labrax, 95 

Dichelyne cotylophora, 115 

Didymozoidae, 25 

Digenea, 14, 25, 67, 70, 95, 146, 

197 

Dimidiochrornis kiwinge, 47 

Dioctophymatoidea, 92 

Diplectanum aequens, 95 

Diplostomidae, 21 

Diplostominae, 21 

Diplostomum gavium, 1 

Diplostomurn immer, 1 

Diplostomum ardeae, 1 

Diplostomum sp., 70 

Distribution, 86 

Dog, 41 

Dormitator latifrons, 146 

Echeneis neucratoides, 67 

Echinochasmus skrjabini, 1 

Echinochasmus dietzevi, 7 

Echinonematinae, 33 

Ectoparasites, 95 

Editors' Acknowledgments, 110 

Eggshell surface, 47 

Egret, 7 

Egypt, 56 

Electron microscopy, 28, 41, 82, 

133, 155, 194 

Eleotridae, 146 

Emended diagnosis, 138 

Endoparasites, 95 

Ephippidae, 1 

Equus caballus, 56 

Ergasilus lizae, 95 

Ergasilus gibbus, 95 

Erschoviorchis lintoni, 1 

Estado de Mexico, Mexico, 197, 

205 

Estuary, 101 

Etheostoma flabellare, 82 

European eel, 95 

Eustrongylides sp., 70, 93 

Eustrongylides tubifex, 1,115 

Eustrongylides ignotus, 1 

Euthynnus affinis, 25 

Experimental infection, 41, 92, 202 

Fantail darter, 83 

Female reproductive system, 155 

Ferosagitta hispida, 194 

Fibricola sp., 73 

Fibrocyte, 83 

Filarioidea, 187 

Fishes, 14, 25, 47, 70, 81, 82, 92, 

95, 101, 115, 133, 138, 146 

Flaccisagitta enflata, 194 

Flathead gray mullet, 95 

Florida, U.S.A., 1, 7, 146 

Formosan hill partridge, 123 

France, 95 

French Polynesia, 37 

Frog, 73, 187, 197 

Froglets, 73 

Galaxias maculatus, 92 

Galaxiidae, 92 

Galeichthys (=Ariopsis) seemani, 

146 

Galveston, Texas, 21 

Gastrografin, 202 

Gavia immer, 1 

Gecko, 37, 78, 175 

Gehyra oceanica, 33 

Gekkonidae, 37, 78, 175 

Genarchella sp., 101 

Genychromis mento, 47 

Geochelone elegans, 25 

Gerrhonotus ophiurus, 205 

Glossocercus caribaensis, 7 

Glycocalyx, 83 

Glypthelmins californiensis, 197 

Glypthelmins facioi, 197 

Glypthelmins quieta, 197 

Gnathostoma, 41 

Gnathostoma cf. binucleatum, 41 

Gnathostoma procyonis, 111 

Gnathostomiasis, 41 

Gobiidae, 70 

Gobiomorus maculatus, 146 

Golden plover, 123 

Gorgodera amplicava, 73 

Great Lakes (Laurentian), 70, 115 

Great egret, 7 

Gulf of Mexico, 21 

Haplosplanchnus pachysornus, 95 

Haplosporus sp., 95 

Hawaii, 123 

Helminths, 1, 7, 67, 70, 73, 78, 

101, 111, 123, 133, 138, 146, 

155, 175, 180, 187, 194, 197, 

202, 205 

Heterocheilus tunicatus, 67 

Hidalgo, Mexico, 205 

Himantopus himantopus, 123 

Himasthia alincia, 1 

Histochemistry, 82 

Holopterus arrnatus, 123 

Horse, 56 

Hymenolepis diminuta, 202 

Hypnobiidae, 180 

Ignavia venusta, 7 

Illinois, U.S.A., 70 

Indian star tortoise, 25 

Indiana, U.S.A., 70, 115 

Indonesia, 25, 123, 187 

Infracommunity, 101 

Inglechina virginiae, sp. n., 33 

Intensity, 1, 7, 14, 28, 70, 73, 78, 

89, 92, 95, 205, 111, 115, 146, 

194 

Introduced species, 70 

Isoodon macrourus, 33 

Isopoda, 70, 95 

Israel, 123 

Jalisco, Mexico, 146 

Japan, 28, 56, 180 

Japanese clawed salamander, 180 

Java, 187 

Kansas, U.S.A., 123 

Kentish plover, 123 

Kittlitz' plover, 123 

Labeo cylindricus, 47 

Labeotropheus fullerborni, 47 

Labidochromis vellicans, 47 

Laboratory rat, 202 

Labratrema minimus, 96 

Lake Huron, 115 

Lake Malawi, 47 

Lake Maurepas, 101 

Lake Michigan, 70, 115 

Lake Nyasa, 47 

Lake Ponchartrain, 101 

Larva, 194 

Laurentian Great Lakes, 115 

Lecithocladium chaetodipteri, 14 

Lepomis miniatus, 101 

Leptorhynchoides thecatus, 101 

Lernanthropus kroyeri, 95 

Lernanthropus pupa, 14 

Lesion nematode, 155 

Lichnochromis acuticeps, 47 

Ligophorus rnugilinus, 95 

Ligophorus chabaudi, 95 

Lizard, 205 

Lobatocystis euthynni sp. n., 25 

Loon, 1 

Louisiana, U.S.A., 86, 101 

Mackerel tuna, 25 

Macracanthorhynchus ingens, 111 

Macroderoididae, 86, 197 

Malawi, 47 

Mammalia, 67, 111, 202 

Manatee, 67 

Mangrove frog, 187 

Marine fish, 14 

Maritrema sp., 1 

Maritrema sp. near eroliae, 1 

Marsupialia, 33 

Masked lapwing, 123 


INDEX 215 

Mastacembelidae, 52 

Mastacembelus shiranus, 52 

Maxvachonia brygooi, 175 

Maxvachonia chabaudi, 89 

Maxvachonia dimorpha, 78 

Meeting Minutes, 211 

Meeting Schedule, 174 

Mehdiella microstoma, 28 

Melanochromis cf. melanopterus, 

47 

Melanochromis heterochromis, 47 

Melanochromis auratus, 47 

Melanosis, 92 

Membership application, 99 

Mesocestoides sp., 73 

Mesorchis denticulatus, 1, 7 

Mesostephanus appendiculatoides, 1 

Message from the editors, 20 

Metacamopia oligoplites, 81 

Metacamopiella euzeti, 81 

Metacercaria, 73, 82, 146 

Metamicrocotyla cephalus, 95 

Metriaclima zebra, 47 

Metriaclima zebra "redtop", 47 

Mexico, 47, 146, 194, 197, 205 

Michigan, U.S.A., 73, 115 

Michoacan, Mexico, 197 

Microcotyle mugilis, 95 

Micropai-yphium facetum, 1, 7 

Microphallus spp., 1 

Microphallus forresteri, 1 

Microphallus nicolli, 1 

Microsomacanthus pseudorostellatus, 

1 

Mississippi, U.S.A., 86 

Mitochondria, 83 

Molineus barbatus, 111 

Mollusca, 70 

Mongolia, 56 

Monogenea, 14, 81, 95 

Monogenoidea, 138 

Moorea, 37 

Morphology, 47, 56, 187, 194 

Morphometry, 56 

Mugil cephalus, 95 

Multitestis (Multitestis) inconstant, 14 

Multitestis (Multitestoides) brasiliensis, 

14 

Myxosporidia, 95 

Myxozoa, 95 

Namibia, 78 

Nebraska, U.S.A., 123 

Nematoda, 7, 28, 33, 37, 56, 67, 

70,73,89,93,95, 101, 111, 115, 

155, 175, 205 

Neoechinorhynchus agilis, 95 

Neoechinorhynchus cylindratus, 101 

Neogobius melanostornus, 70 

Neovalipera parvispinae, 1 

Nephrurus laevissirnus, 175 

Nephrurus levis, 175 

Nephrurus vertebralis, 175 

Nerocila orbignyi, 95 

New books available, 55 

New combination(s), 180 

New genus, 21, 187 

New geographical record(s), 1, 7, 

14, 21, 28, 47, 56, 67, 70, 73, 78, 

83, 86,89,92,95, 111, 123, 133, 

138, 146, 194, 197, 205 

New Hampshire, U.S.A., 123 

New host record(s), 7, 21, 28, 47, 

78, 89, 175, 194, 197, 205 

New species, 21, 25, 28, 33, 37, 47, 

175, 180, 187 

New synonym, 81, 146 

New York, U.S.A., 123 

Nipergasilus bora, 95 

Northern Territory, Australia, 33, 

175 

Northern leopard frog, 73 

Northern brown bandicoot, 33 

Obituary notice, Richard M. Sayer, 24 

Oceanic gecko, 37 

Odhneria odhneri, 1 

Oligoplites palometa, 81 

Onchocercidae, 187 

Onychodactylus japonicus, 180 

Oochoristica piankai, 175 

Oochoristica truncata, 78 

Oocyte development, 155 

Oregon, U.S.A., 123 

Oreochromis sp., 47 

Oswaldocruzia pipiens, 205 

Oswaldocruzia priceae, 73 

Oxyuroidea, 37 

Pacific islands, 37 

Panama, 56, 146 

Paracuaria adunca, 1 

Parana River, Brazil, 133 

Parancylodiscoides sp., 14 

Parapharyngodon japonicus sp. 

n., 180 

Parapharyngodon kartana, 89 

Parapharyngodon rotundatus, 78 

Paraochoterenella javanensis gen. 

et sp. n., 187 

Parasite ecology, 14 

Parorchis acanthus, 1 

Parvatrerna sp., 1 

Patagonia, 92 

Pathology, 92, 115 

Pelaezia sp., 146 

Pelecanidae, 21 

Pelecanus occidentalis, 21 

Pelecanus erythrorhynchos, 41 

Pelican, 21, 41 

Pentastomida, 175 

Peramelidae, 33 

Perca flavescens, 115 

Percidae, 115 

Perciformes, 70, 146 

Petrotilapia genalutea, 47 

Phagicola longa, 1 

Pharyngodon oceanicus sp. n., 37 

Pharyngodon tiliquae, 175 

Pharyngodonidae, 28, 37, 78, 89, 

175, 180 

Philometra cylindracea, 115 

Pholeter ante routerus, 7 

Physaloptera rara, 111 

Physaloptera retusa, 205 

Physaloptera sp., 175 

Physalopteroides filicauda, 89, 175 

Physalopteroides impar, 78 

Physocephalus sp., 78 

Pisces, 14, 25, 47, 70, 81, 82, 92, 

95, 101, 115, 133, 138, 146 

Placidochromis johnstoni, 47 

Placidochromis johnstoni "gold", 47 

Plagiorchidae, 73 

Plagiorhynchus s. lat., s. str., 123 

Plagiorhynchus (Plagiorhynchus) 

charadrii, 123 


paulus, 123 


sp., 123 

Plagiorhynchus (Prosthorhynchus), 

123 


bullocki, 123 


cylindraceus, 123 


golvani, 123 


gracilis, 123 


malayensis, 123 

Plerocercoid, 7 

Plotnikovia fodiens, 1 

Pluvialis dominica, 123 

Polymorphus brevis, 1, 7 

Posthodiplostomum boydae, 1 

Posthodiplostomum opisthosicya, 7 

Posthodiplostomum minimum, 1, 7 

Posthodiplostomum macrocotyle, 7 

Posthodiplostomum sp., 1, 7 

Pratylenchidae, 155 

Pratylenchus penetrans, 155 

Prevalence, 7, 14, 28, 47, 70, 73, 

86, 89, 92, 95, 101, 111, 115, 

175, 194, 197, 205 

Procarnbarus acutus, 86 



Procyon lotor, 111 

Prosogonotrema bilabiatum, 14 

Prosthogonimus ovatus, 1 

Prosthorhynchus, 123 

Proteocephalidae, 133 

Protoancylodiscoides, 138 

Protoancylodiscoides chrysichthes, 

138 

Protomelas annectens, 47 

Protomelas cf. taeniolatus, 47 

Pseudacanthostomum floridensis, 

146 

Pseudacanthostomum panamense, 

146 

Pseudacanthostomum sp., 146 

Pseudocaligus apodus, 95 

Pseudodactylogyrus anguillae, 95 

Pseudotropheus tropheops "broadmouth", 

47 

Pseudotropheus tropheops "orange 

chest", 47 

Pseudotropheus elongatus "aggressive", 

47 

Puerto Rico, 67 

Quadrigyridae, 47 

Quintana Roo, Mexico, 146 

Raccoon, 111 

Radiographic imaging, 202 

Raillietnema brachyspiculatum, 205 

Raillietnema sp., 73 

Raillietiella scincoides, 175 

Rana berlandieri, 197 

Rana cancrivora, 187 

Rana dunni, 197 

Rana megapoda, 197 

Rana montezumae, 197 

Rana neovolcanica, 197 

Rana pipiens, 73 

Rana vaillanti, 197 

Ranidae, 73, 187, 197 

Rarotonga, 37 

Rat, 202 

Rat tapeworm, 202 

Red cheeked dunnart, 33 

Redworm, 115 

Remora, 67 

Renicola pollaris, 1 

Renicola sp., 7 

Report of the Brayton H. Ransom 

Memorial Trust Fund, 186 

Reptilia, 28, 37, 78, 89, 175, 205 

Rhabdias ranae, 73 

Rhoptropus afer, 78 

Rhoptropus barnardi, 78 

Ribeiroia ondatrae, 1, 7 

Rio de Janeiro, Brazil, 14, 81 

Round goby, 70 

Russia, 56 

Saginaw Bay, U.S.A., 115 

Sagitta helenae, 194 

Salamander, 180 

Sauria, 37, 78, 89, 175, 205 

Scanning electron microscopy, 41, 

28, 133, 194 

Sciadiocara rugosa, 1 

Sciadocephalus megalodiscus, 133 

Scincidae, 89 

Sculpins, 70 

Sea bass, 95 

Seasonal dynamics, 101 

SEM, 41, 28, 133, 194 

Serranicotyle labracis, 95 

Serratosagitta serratodentata, 194 

Seuratidae, 33 

Shore birds, 123 

Siluriformes, 138, 146 

Sirenia, 67 

Skinks, 89 

Skrjabinodon piankai sp. n., 175 

Sminthopsis virginiae, 33 

Smooth knobtail gecko, 175 

Society Islands, 37 

South Africa, 123 

South Carolina, U.S.A., Ill 

Southwellina hispida, 1 

Spauligodon petersi, 78 

Spermatheca, 155 

Spinifex knobtail gecko, 175 

Spinitectus carolini, 101 

Spiroxys sp., 73 

Splendidofilaria fallisensis, 1 

Spotted sunfish, 101 

Sprostoniella sp., 14 

State of Parana, Brazil, 133 

State of Rio de Janeiro, Brazil, 14 

Stegophorus diomedeae, 1 

Stictodora lariformicola, I 

Stigornatochromis woodi, 47 

Stilt, 123 

Storr's knobtail gecko, 175 

Streptocara formosus, 1 

Streptocara crassicauda longispiculatus, 

1 

Strigeidae, 73 

Subgenus, 123 

Sulawesi Island, Indonesia, 25 

Survey, 1, 7, 14, 21, 28, 47, 67, 70, 

73, 78, 86, 89, 95, 205 

Tachygonetria conica nicollei, 28 

Tachygonetria dentata quentini, 28 

Tachygonetria macrolaimus dessetae, 

28 

Taeniolethrinops praeorbitalis, 47 

Tahiti, 37 

Taiwan, 123 

Tanaisia fedtschenkoi, 1 

Tapeworm, 202 

Tarsiger johnstoniae, 123 

Tasmania, 123 

Taxonomic description, 25, 28, 33, 

37, 47, 123, 133, 138, 146, 175, 

180, 187 

Taxonomic key, 123, 187 

Teleostei, 14, 81, 133 

TEM, 82, 155 

Tenebrio molitar, 202 

Testudinidae, 28 

Tetrabothrius macrocephalus, 1 

Tetrameres microspinosa, 7 

Tetrameres sp., 7 

Texas, U.S.A., 21, 86 

Thelandros awakoyai comb, n., 

180 

Thelandros senisfaciecaudus comb. 

n., 180 

Thubunaea fitzsimonsi, 78 

Timoniella praeteritum, 95 

Togo, 138 

Tortoise, 28 

Trachinotus carolinus, 81 

Transmission electron microscopy, 

82, 155 

Trematocranus placodon, 47 

Trematoda, 7, 73, 82, 86, 101, 194, 

205 

Trichechus manatus, 67 

Triple-banded plover, 123 

Tuna, 25 

Tucunare, 133 

Tyrannochromis nigriventer, 47 

Tyrannochromis macrostoma, 47 

Ultrastructure, 28, 41, 82, 133, 155, 

194 

U.S.A., 1, 7, 21, 67, 70, 73, 82, 86, 

101, 111, 115 

Vanellus miles, 123 

Varied thrush, 123 

Veracruz, Mexico, 197, 205 

Waltonellinae, 187 

Wanaristrongylus ctenoti, 89, 175 

Washington state, U.S.A., 123 

Western Australia, 33, 89, 175 

Whitefin remora, 67 

White-fronted sand plover, 123 

Wisconsin, U.S.A., 82 

X-ray, 202 

Yellow perch, 115 

Zebra mussels, 70 

Zoonoses, 111 

Zoothera naevius, 123 


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MISSION & VISION STATEMENTS 

May 7, 1999. 

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218 


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J998 

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T995 

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CHARTER MEMBERS 1910 

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\t Hassall 

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*Jesse R. Christie 

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*Elois

JULY 1999 

CONTENTS 

(Continued from Front Cover) 

BURSEY, C. R., AND S. R. GOLDBERG. Skrjabinodon piankai sp. n. (Nematoda: Pharyngodonidae) and 

Other Helminths of Geckos (Sauria: Gekkonidae: Nephrurus spp.) from Australia >. -__ 175 

BURSEY, C. R., AND S. R. GOLDBERG. Pampharyngodon japonicus sp. n. (Nematoda: Pharyngodoni- 

-dae) from the Japanese Clawed Salamander, Onychodactylus japonicus (Caudata: Hynobiidae), 

from Japan /——; ..- . i II -. -— ..„ '. . 180 

PURNOMO, AND M. J. BANGS. Paraochoterenella javanensis gen. et sp. n. (Filarioidea: Onchocercidae) 

from Rana cancrivora (Amphibia: Anura) in West Java, Indonesia .„ r . 187 

: - RESEARCH NOTES 

GOMEZ DEL PRADO-ROSAS, M. DEL C:, J. N. ALVAREZ-CADENA, L. SEGURA-PUERTAS, AND R. LAMOTHE- 

ARGUMEDO. New Records, Hosts, and SEM Observations of Cercaria owreae (Hutton, 1954) 

from the Mexican Caribbean Sea ^_ ... . 194 

RAZO-MENDIVIL, U., J. P. LACLETTE, AND G. PEREZ-PONCE DE LEON. New Host and Locality Records 

for Three Species of Glypthelmins (Digenea: Macroderoididae) in Anurans of Mexico : „_ 197 

DEINES, K. M.,'D. J. RICHARDSON, G. CONLOGUE, R. G. BECKETT, AND D. M. HOLIDAY. Radiographic 

Imaging of the Rat Tapeworm, Hymenolepis diminuta ^ „_ 202 

GOLDBERG, S. R., C. R. BURSEY, AND J/L. CAMARILLO-RANGEL. Helminths of Two Lizards, Barisia 

imbricata and Gerrhonotus ophiurus (Saurja: Anguidae), from Mexico 205 

ANNOUNCEMENTS 

EDITORS' ACKNOWLEDGMENTS -__.__ ~~-l ^.— IL— , '. . . 110 

ANNOUNCEMENT OF JOURNAL NAME CHANGE __. : . "~ ._„: 122 

OBITUARY NOTICE ; i___^_ , : . •, r 137 

MEETING SCHEDULE

The Helminthological Society of Washington - Peru State College

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