ARQUIPÉLAGO
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Cover design: E. Arand - Photo: Sancus acoreensis (Wunderlich), Azores - Pedro Cardoso
Diversity and distribution of arthropods in native forests
of the Azores archipelago
CLARA GASPAR1,2, PAULO A.V. BORGES1 & KEVIN J. GASTON2
Gaspar, C., P.A.V. Borges & K.J. Gaston 2008. Diversity and distribution of
arthropods in native forests of the Azores archipelago. Arquipélago. Life and
Marine Sciences 25: 01-30.
Since 1999, our knowledge of arthropods in native forests of the Azores has improved
greatly. Under the BALA project (Biodiversity of Arthropods of Laurisilva of the Azores),
an extensive standardised sampling protocol was employed in most of the native forest
cover of the Archipelago. Additionally, in 2003 and 2004, more intensive sampling was
carried out in several fragments, resulting in nearly a doubling of the number of samples
collected. A total of 6,770 samples from 100 sites distributed amongst 18 fragments of
seven islands have been collected, resulting in almost 140,000 specimens having been
caught. Overall, 452 arthropod species belonging to Araneae, Opilionida,
Pseudoscorpionida, Myriapoda and Insecta (excluding Diptera and Hymenoptera) were
recorded. Altogether, Coleoptera, Hemiptera, Araneae and Lepidoptera comprised the
major proportion of the total diversity (84%) and total abundance (78%) found. Endemic
species comprised almost half of the individuals sampled. Most of the taxonomic,
colonization, and trophic groups analysed showed a significantly left unimodal distribution
of species occurrences, with almost all islands, fragments or sites having exclusive species.
Araneae was the only group to show a strong bimodal distribution. Only a third of the
species was common to both the canopy and soil, the remaining being equally exclusive to
each stratum. Canopy and soil strata showed a strongly distinct species composition, the
composition being more similar within the same stratum regardless of the location, than
within samples from both strata at the same location. Possible reasons for these findings are
explored. The procedures applied in the sampling protocol are also discussed.
Key words: Biodiversity, canopy, endemism, Laurisilva, soil
1
Clara Gaspar (e-mail: cgaspar@ennor.org), Paulo A.V. Borges, Azorean Biodiversity
Group, Departamento de Ciências Agrárias, Universidade dos Açores, Terra-Chã,
PT-9700-851 Angra do Heroísmo, Terceira, Portugal; Kevin J. Gaston, 2BIOME group,
Department of Animal and Plant Sciences, University of Sheffield, S10 2TN Sheffield,
United Kingdom.
INTRODUCTION
Studies focusing on ecological patterns of
diversity and distribution of arthropods in the
Azores have a very recent history. The islands
have been explored since 1850 and some studies
on the biogeography and systematics of arthropods
were undertaken (e.g. Drouët 1859; Wallace 1872;
Fig. 1). However, probably due to the low
diversity and inconspicuous fauna, arthropods
from the Azorean islands were mostly disregarded
until late in the last century (Fig. 2).
From 1975 to 1990, some autoecological studies
were carried out focusing on agricultural pests and
on their parasites, such as Mythimna unipuncta
Haworth (Lepidoptera, Noctuidae; Tavares 1979);
Popillia
japonica
Newman
(Coleoptera,
Scarabaeidae; Simões & Martins 1985) and
Trichogramma
sp.
(Trichogrammatidae,
Hymenoptera; Oliveira 1987). But it was only in
1990 that understanding of the ecology of
arthropod communities started to develop in the
1
Systematics
Ecology
Appl. Entomol.
Biogeography
Fig. 1. Number of studies published regarding arthropods in the Azores archipelago
through time, discriminated by subjects: Systematics, Ecology, Applied Entomology
and Biogeography.
Fig. 2. Cumulative number of arthropod species recorded for the Azores archipelago
(columns) in relation to the number of publications on arthropods through decades (line).
archipelago (Borges 1990, 1991a, 1991b, 1992;
Fig. 1).
The arthropod fauna of native forests, in
particular, had been neglected until less than a
decade ago. Since 1999, a considerable effort has
been made to study arthropod diversity and
distribution across Azorean native forests. An
extensive standardised sampling protocol was
applied in most of the remnant forest fragments of
the archipelago. The first years of field and
laboratory work (1999-2002) involved a
2
considerable number of researchers (see also
Acknowledgments) and were developed under the
BALA project (Biodiversity of Arthropods of
Laurisilva of the Azores), headed by P. Borges.
Later years of more intensive sampling effort
(2003 and 2004) in poorly prospected forest
fragments were developed under another research
project headed by CG and resulted in almost a
duplication of the previous number of samples
(3,140 samples against 3,640 samples from
previous years).
Several studies based on these data have been
published since then, focused on the distribution
of insect herbivores (Ribeiro et al. 2005), selection
of areas for conservation based on endemic
(Borges et al. 2000) and soil arthropods (Borges et
al. 2005a), relationship between endemic and
introduced species (Borges et al. 2006),
performance of species richness estimators (Hortal
et al. 2006), abundance, spatial variance and
occupancy of arthropods (Gaston et al. 2006) and
a proposed biotic integrity index (Cardoso et al.
2007).
Yet none of these studies has explored the
whole diversity, and the vertical and horizontal
distribution of different arthropod groups in these
native forests. It is important to look for such
general patterns before additional studies are
planned and resources used. Also, the outcome
will be helpful to complement further conservation
studies focused on the assessment of diversity and
on the selection and management of areas. Here,
arthropod data from the extensive standardised
sampling protocol applied in native forests of the
Azores archipelago are used to evaluate their
diversity and distribution a) per taxonomic,
colonization and trophic group, b) across sites,
fragments and islands, c) between soil and canopy
strata. Consideration was given to the sampling
protocol design adopted in this study.
MATERIAL AND METHODS
STUDY AREA
The remote Azores archipelago extends for 615
km in the North Atlantic Ocean (37-40º N, 25-31º
W), 1,584 km to the east (south Europe) and 2150
km to the west (north America) from the nearest
mainland (Fig. 3). It comprises nine islands and
islets of recent volcanic origin, ranging between
0.30 and 8.12 million years old (França et al.
2003). The archipelago is crossed by the MidAtlantic ridge and lies at the confluence of the
American, Eurasian and African continental
plates, resulting in frequent volcanic and seismic
activities in the islands (Azevedo et al. 1991;
Azevedo & Ferreira 1999). At sea level the
climate is temperate humid (mean average
temperature of 17 ºC, annual precipitation less
than 1000mm), and at upper altitudes is cold
oceanic (9 ºC, 4000mm) (IM 2005). Humidity is
high, reaching 95% at higher altitudes and there
are only relatively small temperature fluctuations
throughout the year (8.5 ºC).
Native forest in the Azores is characterized by
an association of native (many endemic) evergreen
shrub and tree species (Table 1; Borges et al.
2005b). Commonly known as Laurisilva, due to
the presence of Laurel species (Lauraceae family),
this type of forest also occurs in other islands of
the Macaronesia region (comprising Madeira,
Savage, Canaries and Cape Verde archipelagos). It
has been considered a relict of the Laurel forest
that originally covered the Mediterranean basin
and northwest of Africa during the Tertiary, but
other studies support a more recent origin
(Emerson 2002). It is distinguished from other
Laurisilva forests of Macaronesia by a dense tree
and shrub cover of small stature (trees have an
average height of 3 m), closed canopy, high levels
of humidity and low understorey light. Bryophytes
are very abundant and cover vascular plants,
volcanic rocks and soil to a great extent (Gabriel
& Bates 2005).
Documents from the 15th century suggest that
the Laurisilva covered all the islands 550 years
ago, when the first human settlements were
established in the archipelago. However, clearing
for wood, agriculture and pasture, has markedly
reduced its area and the native forest is now
mostly restricted to high and steep areas where
there are no economic interests (corresponding to
less than 3% of the overall surface area of the
archipelago). The smallest islands, Corvo and
Graciosa, do not preserve native forest due to total
clearance in mid 20th century.
SAMPLING PROTOCOL
Eighteen native forest fragments distributed across
seven of the nine islands were sampled in this
study (Fig. 4, Table 2). Altogether, they represent
most of the native forest cover of the Azores,
excluding highly fragmented, small patches (less
than five hectares), located at low altitudes and/or
strongly disturbed by exotic plants or cattle, which
were not sampled.
During the summers of 1999 to 2004, transects
150 m long and 5 m wide were established in 100
sites (usually one transect per site). A linear
direction was followed whenever possible but
3
frequent deviations were needed
due to uneven ground and very
dense vegetation. All efforts
were made to progress towards
the core of the forest to avoid
margin effects. Transects were
marked with ropes to facilitate
recognition.
Along
each
transect,
arthropods from the soil (mainly
epigean)
and
herbaceous
vegetation were surveyed with a
set of pitfall traps, while
arthropods from woody plant
species were sampled using a
beating tray. Pitfall traps
consisted of plastic cups with
4.2 cm diameter and 7.8 cm
deep. Thirty pitfall traps were
used per transect. Half of the
traps were filled with a non……………………………………………………………………………………………………………………….
attractive solution (ethylene
.
Fig. 3 (above). Location of islands and native forest fragments of the glycol antifreeze solution), and
the remaining with a general
Azores archipelago. Fig. 4 (below). Location of the 100 sites from the
18 native forest fragments studied in the Azores. Precise positions and
attractive solution (Turquin),
distances among fragments were changed for clarity. Forest fragments
prepared mainly with dark beer
were delimited using DIVA-GIS software (Hijmans et al. 2005) and
and some preservatives (for
combined information on cartographic maps provided by IGP (see
further details see Turquin 1973,
Acknowledgments), aerial photographs when available, and field data.
Codes of fragments as in Table 2.
and Borges 1992).
4
Table 1. The most common woody plant species (trees and shrubs) present in Azorean native forests, ordered by
the number of sites (out of 100) where each species was sampled; Col. – Colonization, E - Endemic, N – Native,
I – Introduced.
N sites
Code
Species
FAMILY
Structure
Col.
74
45
45
43
38
20
8
3
3
2
2
1
JUN
LAU
ILE
VAC
ERI
MYS
CAL
FRA
PIT
PIC
CLE
MYC
Juniperus brevifolia (Seub.) Antoine
Laurus azorica (Seub.) Franco
Ilex perado Aiton ssp. azorica (Loes.) Tutin
Vaccinium cylindraceum Sm.
Erica azorica Hochst. ex Seub.
Myrsine africana L.
Calluna vulgaris (L.) Hull
Frangula azorica V. Grubov
Pittosporum undulatum Vent.
Picconia azorica (Tutin) Knobl.
Clethra arborea Aiton
Myrica faya Aiton
Cupressaceae
Lauraceae
Aquifoliaceae
Ericaceae
Ericaceae
Myrsinaceae
Ericaceae
Rhamnaceae
Pittosporaceae
Oleaceae
Clethraceae
Myricaceae
Tree
Tree
Tree
Shrub
Tree/shrub
Shrub
Shrub
Tree
Tree
Tree/shrub
Tree/shrub
Tree/shrub
E
E
E
E
E
N
N
E
I
E
I
N
Table 2. Main characteristics of the Azorean islands (bold) and native forest fragments considered in this study,
including the area (hectares), the highest point (altitude, metres), distance to the nearest island/fragment
(isolation, kilometres) and the oldest geological age of the soil (lava) substrate (million years BP).
_
Island
Fragment
Flores
Morro Alto e Pico da Sé
Caldeiras Funda e Rasa
Faial
Caldeira do Faial
Cabeço do Fogo
Pico
Mistério da Prainha
Caveiro
Lagoa do Caiado
S.Jorge
Topo
Pico Pinheiro
Terceira
S. Bárbara e M. Negros
Biscoito da Ferraria
Guilherme Moniz
Terra Brava
Pico do Galhardo
S.Miguel
Pico da Vara
Graminhais
Atalhada
S.Maria
Pico Alto
a
Code
Areaa
Altitudea
FL
FLMO
FLFR
FA
FACA
FACF
PI
PIMP
PICA
PILC
SJ
SJTO
SJPI
TE
TESB
TEBF
TEGM
TETB
TEPG
MI
MIPV
MIGR
MIAT
MA
MAPA
14102
1331
240
17306
190
36
44498
689
184
79
24365
220
73
40030
1347
557
223
180
38
74456
306
15
10
9689
9
911
911
773
1043
934
597
2350
881
1077
945
1053
946
717
1021
1021
809
487
726
655
1105
1105
930
500
587
579
Isolationb
236.43
6.02
6.02
34.26
4.67
4.67
32.42
2.92
4.61
2.92
32.42
15.13
15.13
71.67
7.20
3.03
2.70
2.70
2.79
97.53
3.42
4.02
3.42
97.53
92.21
Agec
2.16
2.16
2.16
0.73
0.73
0.60
0.30
0.26
0.27
0.28
0.55
0.55
0.55
3.52
1.24
0.10
0.41
0.10
0.10
4.01
3.20
3.20
4.01
8.12
8.12
b
based on the delimitation of forest fragments showed in Fig. 4. determined by a geographic matrix of centroids using the
c
DIVA-GIS software (Hijmans et al. 2005). according to França et al. 2003 and J.C. Nunes (personal communication).
5
Table 3. Total number of sites, transects (including additional transects with only beating samples, defined as B)
and samples considered for each forest fragment, island and for the overall archipelago. The number of plant
species sampled (S), and the dominant plant species considered are also presented. Codes of plants are presented in
Table 1, codes of fragments and islands in Table 2.
A few drops of liquid detergent were added to
both solutions to reduce surface tension. The traps
were sunk in the soil (with the rim at the surface
level) every 5 m, starting with a Turquin trap and
alternating with the ethylene traps. They were
protected from rain using a plastic plate, about 5
cm above surface level and fixed to the ground by
two pieces of wire. The traps remained in the field
for two weeks.
Canopy sampling was conducted during the
period that pitfall traps remained in the field, when
the vegetation was dry. A square 5 m wide was
established every 15 m (10 squares in total per
transect). In each square, a replicate of the three
6
MYC
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
● ● ●
● ● ●
● ● ●
● ●
● ● ●
● ● ●
●
●
● ● ● ● ● ● ●
● ●
● ●
●
●
●
●
●
●
● ● ●
● ● ●
● ● ●
●
●
● ●
● ●
● ●
● ● ●
● ● ●
● ● ●
●
●
● ● ●
● ● ●
● ● ●
● ●
● ● ●
● ●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
●
CLE
12
7
6
4
7
5
4
6
6
5
5
7
4
7
8
7
8
3
6
4
7
5
5
3
5
5
PIT
3350
270
200
70
150
90
60
530
240
150
140
220
110
110
1810
790
460
110
300
150
270
100
100
70
100
100
PIC
3420
360
240
120
240
120
120
480
240
120
120
240
120
120
1620
690
300
150
330
150
360
120
120
120
120
120
FRA
6770
630
440
190
390
210
180
1010
480
270
260
460
230
230
3430
1480
760
260
630
300
630
220
220
190
220
220
CAL
S
MYS
Can.
ERI
Soil
ILE
Total
VAC
Sites Transects
100
114+15B
12
12
8
8
4
4
8
8
4
4
4
4
16
16+4B
8
8+1B
4
4+1B
4
4+2B
8
8
4
4
4
4
40
54+10B
16
23+5B
8
11+5B
4
5
8
11
4
4
12
12+1B
4
4+1B
4
4
4
4
4
4
4
4
JUN
Code
AZ
FL
FLMO
FLFR
FA
FACA
FACF
PI
PIMP
PICA
PILC
SJ
SJTO
SJPI
TE
TESB
TEBF
TEGM
TETB
TEPG
MI
MIPV
MIGR
MIAT
MA
MAPA
Plant species sampled
LAU
Samples
●
●
●
●
●
●
●
●
●
● ●
●
● ●
● ● ●
● ●
● ● ●
●
●
●
●
●
● ●
● ●
most abundant woody plant species was sampled.
In most of the study sites, three species clearly
dominated over the remaining plants and the
choice was evident. However, in some transects,
less than three were present and only those were
considered. For each selected plant, a branch was
chosen at random and a beating tray placed
beneath. Five beatings were made using a stick.
The tray consisted of a cloth inverted pyramid 1 m
wide and 60 cm deep (adapted from Basset 1999),
with a plastic bag at the end.
A total of 6,770 samples (3,420 pitfall traps
and 3,350 beating samples) were collected.
Samples were sorted and the specimens preserved
in 70% alcohol with glycerine. The selection of
the arthropod taxa considered in this study was
made taking into account the available
taxonomists and the taxa which were readily
separable by morphological criteria. All Araneae,
Opilionida, Pseudoscorpionida, Myriapoda and
Insecta (excluding Diptera and Hymenoptera)
were assigned to morphospecies through
comparison with a reference collection. Various
taxonomists (see Acknowledgments) checked the
assignment
to
morphospecies,
made
identifications and supplied additional ecological
information.
Considerable efforts have been made to avoid
lumping and splitting errors (see discussion), so it
may be assumed in this study, with reasonable
confidence, that morphospecies accurately
represent species, and will be considered as
species hereafter. All specimens and types are
deposited in the Arruda Furtado entomological
collection at the Department of Agrarian Science
(University of the Azores).
DATA ANALYSES
Abundance matrices of arthropod species per
island, fragment and site were used to compare the
composition and abundance of different arthropod
groups across areas. Arthropods were grouped by
categories: taxonomic (orders Araneae, Blattaria,
Chordeumatida,
Coleoptera,
Dermaptera,
Ephemeroptera, Geophilomorpha, Hemiptera,
Julida, Lepidoptera, Litobiomorpha, Microcoryphia, Neuroptera, Opilionida, Orthoptera,
Polydesmida, Pseudoscorpionida, Psocoptera,
Scolopendromorpha, Thysanoptera, Trichoptera),
trophic (Herbivores, Predators, Saprophages,
Fungivores), colonization (Introduced or nonindigenous - arrived as a result of human
activities; Native - arrived by long distance
dispersal, indigenous minus endemic; Endemic only occur in the Azores as a result of speciation
in the archipelago or extinction in other areas,
indigenous minus native) and stratum preference
(soil, canopy).
The modality in the frequency of species for
each arthropod group across sites, fragments and
islands was evaluated using the statistical test
proposed by Tokeshi (1992; see also Barreto et al.
2003). Left (occurring in only one site, fragment
or island) and right (occurring in all sites,
fragments or islands) modality of the speciesrange distribution was evaluated and the null
hypothesis of random or uniform distribution was
rejected at p<0.05.
Hierarchical, agglomerative cluster analyses
(Ward’s linkage method, 1-sorensen dissimilarity
measure) were conducted using the Community
Analysis Package (Seaby et al. 2004) to identify
dissimilarities in the species composition for the
canopy and soil strata across sites, fragments and
islands studied.
Paired-sample t-tests were performed to look
for differences in the species richness and
abundance per site between canopy and soil strata.
Also, one-way ANOVAs were conducted to
evaluate the effect of plant species on the average
number of species and individuals of arthropods
found per sample. Abundance data were log (x+1)
transformed to satisfy the assumption of normal
distribution of data. Paired-sampled t-tests and
ANOVAs were performed using MINITAB v13
(2000).
RESULTS
A total of 139,476 identifiable specimens,
distributed amongst 21 orders, at least 106
families, 261 genera and representing 452 species
were collected in the native forests of the Azores.
A detailed list of the species recorded is presented
in Appendix. Adults (69,300 individuals, 50%)
and immatures (67,096 indiv., 48%) contributed in
similar proportions to the total number of
individuals recorded. The majority of the genera
recorded (210 of 261 genera identified) were only
represented by a single species, most of the
remaining genera (34 of 51 genera remaining)
being represented by two species per genus.
SPECIES RICHNESS AND ABUNDANCE PER
TAXONOMIC, TROPHIC AND COLONIZATION GROUP
The great majority of the species (379 spp, 84% of
the overall species richness) belonged to four
taxonomic orders (Fig. 5). Altogether, Coleoptera,
Hemiptera, Araneae and Lepidoptera also
comprised the major proportion of the total
abundance found (108,634 individuals, 78%).
Coleoptera, with the highest number of species
7
(137 spp) had the lowest number of individuals of
the four most diverse taxa (7,196 indiv., Fig. 5).
On the other hand, Araneae with 74 species, had
the highest abundance overall (40,938 indiv.,
Fig. 5). The remaining 17 orders had very low
species richness (Fig. 5). In fact, all except
Psocoptera (21 spp), Thysanoptera (18 spp) and
Julida (9 spp) were represented by three or less
species (Fig. 5). However, the abundance of some
of those taxa was relatively high, such as the
Opilionida, represented by only two species but
with more than 6,700 individuals collected, a
number close to the abundance of the most diverse
order (Fig. 5).
Araneae was one of the taxa with the lowest ratios
of adults per immatures (1:3; 9,358 adults against
31,564 immatures). Overall, Araneae contributed
to 47% of the total number of immatures found in
this study.
The herbivore species were slightly more
diverse and abundant (208 spp, 67,047
individuals) than predators (165 spp, 56,666
indiv.; Fig. 6a). Together, they represented 83% of
the species and 89% of the individuals found
(Fig. 6a). The remaining species were mostly
saprophages (64 spp, 13,932 indiv.). Fungivores
were the least well represented in this study (13
spp, 1,829 indiv.; Fig. 6a).
Fig. 5. Contribution of each taxon (order) to the overall number of species and individuals found (COL Coleoptera, HEM - Hemiptera, ARA - Araneae, LEP - Lepidoptera, PSO - Psocoptera, THY - Thysanoptera,
JUL - Julidae, POL - Polydesmida, PSE - Pseudoscorpionida, DER - Dermaptera, GEO - Geophilomorpha,
LIT - Lithobiomorpha, MIC - Microcoryphia, OPI - Opilionida, ORT - Orthoptera, TRI - Trichoptera, BLA Blattaria, CHO - Chordeumatida, EPH - Ephemeroptera, NEU - Neuroptera and SCO - Scolopendromorpha).
Grouped by colonization categories, more than
half of the species (257 spp, 57%) were
indigenous (endemic plus native, Fig. 6b). Of
those, native species were more diverse (149 spp)
but less abundant (54,669 indiv.) than endemics
(108 spp, 68,138 indiv.; Fig. 6b). Endemic species
alone comprised nearly half of the overall
8
abundance found (Fig. 6b). Grouped with natives,
indigenous species included 88% of the total
number of individuals (Fig. 6b). The abundance of
non-indigenous species (15,956 indiv., 11%) was
relatively low when compared with native or
endemic species, but the species richness (155 spp,
34%) was considerably higher (Fig. 6b).
Fig. 6a (above). Contribution of each trophic group,
and Fig. 6b (below), colonization group, to the overall
number of species and individuals found (H-herbivores,
P-predators, S-saprophages, F-fungivores; I-introduced,
N-native, E-endemic, ?-unknown origin).
SPECIES RICHNESS AND ABUNDANCE ACROSS
SITES, FOREST FRAGMENTS AND ISLANDS
A high proportion of the species occurred in only
one island (45% of the species, Fig. 7a), one
fragment (38%, Fig. 7b) or even one site (31%,
Fig. 7c). The Tokeshi (1992) test for modality
supports this finding showing a strong left
unimodal distribution of species for the three
spatial scales analysed (Pl < 0.001 and Pr > 0.98).
All fragments and islands had locally restricted
species although the fragment MAPA and Terceira
Island had the highest number of exclusive species
(Table 4). In fact, a considerable proportion of the
total number of species (167 spp, 37%) was
considered to be very rare (doubletons: 51 spp,
11%; singletons: 116 spp, 26%).
The general pattern of strong left unimodality
was also observed when species were grouped by
taxa, trophic and colonization categories, whether
at the island, fragment or site scale (Table 5). The
only exception was for the species distribution of
the Araneae, which was found to be strongly
bimodal across islands (Table 5, Fig. 8).
Fig. 7. Distribution range of the species for the (a)
seven islands, (b) 18 fragments and (c) 100 sites studied
(for the latter, the x-axis was transformed on an octave
scale for clarity).
That is, most of the species of Araneae, when
restricted in their distribution, occurred in only
one island; while those that had a wide distribution
tended to occur in all islands (Fig. 8).
SPECIES RICHNESS AND ABUNDANCE IN CANOPY
AND SOIL
The canopy and soil samples captured similar
proportions of the overall number of species
recorded (304 spp, 67% and 296 spp, 65%
respectively; Table 6), although only a third of the
species (148 spp, 33%) was common to both
9
Table 4. Ranking of the Azorean fragments and islands
according to the number of exclusive species (Excl.);
the number of exclusives that were endemic (End.) is
also presented. Codes of fragments as in Table 2
Fragment
All frag.
MAPA
TESB
FLFR
TETB
FLMO
MIAT
PIMP
TEPG
SJPI
TEBF
FACF
MIGR
MIPV
TEGM
PICA
PILC
SJTO
FACA
Excl.
173
31
18
15
15
13
11
10
7
7
6
6
6
6
5
5
5
5
2
End.
33
10
2
0
1
6
1
3
1
1
0
2
0
4
0
1
0
1
0
Island
All isl.
TE
FL
MA
MI
PI
SJ
FA
Excl.
202
65
33
31
26
24
14
9
End.
48
8
10
10
6
7
4
3
Table 5. Significance values for the modality test
(Tokeshi 1992) of the species distribution grouped by
taxa, trophic and colonization categories, with
respective subgroups, across islands, fragments and
sites (** p<0.001, * p<0.01); P l – Left, P r - right.
Island
Taxa
P l
Pr
Fragment
Pl
Pr
Site
Pl
Pr
Coleoptera
**
1.000
**
1.000
**
0.748
Hemiptera
**
0.955
**
0.976
**
0.630
Araneae
**
*
**
0.120
**
0.525
Lepidoptera
**
0.668
**
0.338
**
0.500
Herbivores
**
0.970
**
0.946
**
0.876
Predators
**
0.669
**
0.816
**
0.810
Saprophages
**
0.711
**
0.697
**
0.474
Trophic
Colonization
Introduced
**
1.000
**
0.993
**
0.789
Endemic
**
0.085
**
0.394
**
0.662
Native
**
0.653
**
0.727
**
0.776
strata (Fig. 9). Most of the individuals (104,716
indiv., 75%) were found in the canopy (Table 6).
The strata had a similar fraction of rare species
(singletons and doubletons; canopy: 124 spp, 41%,
_
10
Fig. 8. Distribution range of the species across islands,
grouped by the four most dominant taxonomic orders
(ARA-Araneae, COL-Coleoptera, HEM-Hemiptera and
LEP-Lepidoptera).
soil: 116 spp, 39%). But considering the species
that were exclusive to each stratum, canopy had a
higher proportion of rare species than soil
(canopy: 93 spp, 60%; soil: 69 spp, 47%). The
species common to both methods only showed a
small proportion of doubletons (5 spp, 3%).
Grouped by taxonomic orders, a higher number
of species and a major proportion of individuals of
Araneae, Hemiptera and Lepidoptera were found
in the canopy, while Coleoptera showed a higher
number of species and much more abundance on
the soil (Table 6). In fact, most of the species of
Coleoptera were found exclusively in the soil
stratum (Fig. 9). Instead, Hemiptera and
Lepidoptera had more species exclusively from
the canopy. Species of Araneae were mostly
common to both soil and canopy (Fig. 9).
Herbivore species were more dominant (in
number of species and individuals) in canopy
(Table 6), and most of them were exclusive to
canopy (Fig. 9).
Fig. 9. Percentage of the number of species that were exclusively from soil, canopy,
or that were common to both soil and canopy samples. Results are shown for the
total number of species (TOT) and grouped by taxa (COL-Coleoptera, HEMHemiptera, ARA-Araneae, LEP-Lepidoptera), trophic (H-Herbivores, P-Predators,
S-Saprophages) and colonization (I-Introduced, N-Native, E-Endemic) groups.
Table 6. Number of species and individuals found in
canopy and soil strata. Data are presented for the
overall arthropods collected (Total) and separated by
taxonomic, trophic and colonization categories.
Canopy
Soil
Total
Taxonomic
Coleoptera
Hemiptera
Araneae
Lepidoptera
Trophic
Herbivores
Predators
Saprophages
Colonization
Introduced
Native
Endemic
Species
richness
x
x
304 296
104716
x
34760
64
81
57
48
99
55
52
43
942
28688
34187
27669
6254
2310
6751
1833
158
105
36
118
122
42
57950
35079
11628
9097
21587
2304
108
94
74
94
104
80
5856
36746
61834
10100
17923
6304
Abundance
x
Conversely, predators were more dominant in soil
rather than in canopy (Table 6) and few species
were exclusive to canopy (Fig. 9).
Non-indigenous had a higher number of species
in the canopy than on soil, contrary to endemics or
natives (Table 6). The abundance of nonindigenous in the canopy was smaller than in soil
(Table 6). Endemic species were more abundant in
the canopy (Table 6). Most of the non-indigenous
species were exclusive to the canopy, while most
of the endemics were common to both strata (Fig.
9).
The local number of species and individuals
found per site was significantly higher in the
canopy stratum than in the soil (paired-sample ttests, species richness: t=8.40, d.f.=98, p<0.001;
abundance:
t=10.16,
d.f.=98,
p<0.001).
Notwithstanding, canopy and soil strata showed a
strongly distinct species composition, the
composition being more similar within the same
stratum regardless of the location, than within
samples from both strata at the same location. This
pattern was clear when comparing the two strata
across islands (canopy and soil samples with a
1-sorensen dissimilarity measure of d=1.76,
Fig. 10), across fragments (d=4.54, not presented)
or even across sites (d=26.4, not presented).
11
Fig. 10. Hierarchical, agglomerative cluster analysis (Ward’s linkage, 1-sorensen dissimilarity
measure) for the canopy and soil strata across the seven islands studied. Code of islands as in Table 2.
The mean number of arthropod species and
individuals collected per sample was found to be
significantly different among plant species
(ANOVA, species richness: F=47.9, p<0.001,
d.f.=11, 3,338; abundance: F=143.6, p<0.001,
d.f.=11, 3,338). Erica azorica and Juniperus
brevifolia were two of the plant species with the
highest species richness and abundance per sample
while Calluna vulgaris had the lowest number of
species and individuals (Fig. 11).
Despite the effect of plant species on the
number of species and individuals of arthropods
found per sample, the composition of arthropods
did not seem to be related with plant species,
instead, samples tended to be more similar within
each island rather than grouped per plant species
(Fig. 12).
Fig. 11. Mean number of species (dark grey) and individuals (light grey,
log10 transformed) per sample for each plant species studied. Standard
errors are presented. Codes of plant species as in Table 1.
12
Fig. 12. Hierarchical, agglomerative cluster analysis (Ward’s linkage, 1-sorensen dissimilarity measure) for
the samples of the 12 plant species across the seven islands studied. Codes of islands are presented in Table 2,
codes of plant species in Table 1.
DISCUSSION
As in the majority of terrestrial habitats
worldwide, the arthropods are the most diverse
and abundant animals in the Azores. However,
their diversity in these islands (2,209 spp of which
267 spp are endemic, Borges et al. 2005b) is
relatively low compared with the other
archipelagos of the Macaronesia region (e.g. the
Canary islands with 6,843 spp of which 2,704 spp
are endemic, Martín et al. 2001). This is likely a
consequence of the greater isolation from the
mainland and the more recent geological origin
(Borges & Brown 1999; Borges et al. 2005b).
Also, the poor knowledge of highly diverse taxa in
the Azores, such as Hymenoptera, may underestimate to some extent the overall diversity of
this archipelago (Borges et al. 2005b).
Arthropod diversity in Azorean native forests in
particular is low (452 spp). The fragments of
native forest are likely to be influenced not only
by physical factors such as the isolation,
geological age and area of the islands themselves,
but also by the fragmentation and shrinkage that
have shaped the fragments directly over the last
550 years. Nonetheless, the arthropod diversity of
the native forests still represents one third of the
arthropod species ever recorded (which includes
extinct species) in all habitats of the archipelago
(1297 spp listed for the same taxonomic orders
considered in this study, Borges et al. 2005b),
including 104 of the 162 endemic arthropod
species listed for the overall archipelago.
The relatively low arthropod diversity in the
Azores meant that a large sampling scheme could
be implemented resulting in more than 6,700
samples from 100 sites distributed amongst 18
fragments of seven islands. The most
representative terrestrial arthropod orders present
in these forests were considered (except Diptera,
Hymenoptera, Acari and Collembola) resulting in
nearly 140,000 specimens being identified.
Despite the low diversity, the protocol required a
considerable effort that had never been made
before in these islands. The uneven volcanic
ground and the closed canopy made the progress
13
through the forests difficult. The isolation of the
islands was also a logistical constraint. The effort,
however, was valuable: it is at present the largest
standardised database of arthropods available for
the Macaronesia region and one of the few
worldwide for arthropods at a regional scale.
The extensive sampling effort and high number
of specimens caught, along with the poor
knowledge of arthropods in Azorean native forests
when the BALA project started, made
indispensable the use of a rapid and efficient
shortcut for identification. The use of
morphospecies has become a common strategy to
include poorly known taxa in conservation studies
(Oliver & Beattie 1994; Derraik et al. 2002; Krell
2004). However, errors caused by splitting and
lumping often occur. It is believed that accuracy in
assignment to morphospecies may vary greatly
among different groups of arthropods (Derraik et
al. 2002) and with different life stages or sexes
considered (Oliver & Beattie 1993). Yet, errors
may be considerably reduced if some precautions
are taken, namely: (1) some previous training is
given to the parataxonomists (Oliver & Beattie
1994; Derraik et al. 2002), (2) the same
parataxonomists are used throughout the process,
(3) some tools to assist parataxonomists are
available (Oliver & Beattie 1997; Beattie & Oliver
1999; Oliver et al. 2000) and (4) taxonomic
validation is applied in a further step (Borges et al.
2002). In this study, all of these precautions were
taken. A senior researcher trained several students,
and checked the assignment to morphospecies
made by students for all specimens. Identification
keys were made by taxonomists or students (and
then checked by the senior researcher) to ease
distinction of many morphotypes. A conservative
approach was adopted, and when in doubt a new
morphotype was created. All morphotypes were
checked by taxonomists, with most of them
identified to the species (301) and genus level
(53). For those that still remain unnamed at a
species or genus level (most of them are new
records for the archipelago or new species to
science and waiting to be described by
taxonomists), precautions were taken to ensure
that they corresponded to unique species, distinct
from others unnamed or described in the
collection. With such a considerable effort to
avoid lumping and splitting, it is believed that
14
morphospecies accurately represent species.
Diptera, Hymenoptera and Acari and
Collembola orders were not considered in this
sampling protocol since their assignment to
morphospecies, besides being more time
consuming than for other orders, results in many
lumping and splitting errors. More taxonomic
expertise is required and a greater investment
needs to be made to train parataxonomists.
Moreover, the sampling methods used here were
not adequate for these particular orders. While
other flying insects, such as Coleoptera and
Hemiptera, tend to fall or remain still when taking
a beating sample, Diptera and Hymenoptera are
very agile and tend to escape easily from the
beating tray before closing the collecting bag.
Malaise traps would be preferable but they are
difficult to set in the field due to dense understorey
vegetation in these native forests. Likewise,
Collembola and Acarina orders would be more
effectively sampled using extracting methods of
soil and litter. Berlese funnels were used
experimentally in several transects but they proved
to be ineffective, probably due to the high water
saturation of the soil (further discussion of
sampling methods by Gaspar et al. is under
scientific scrutiny at the moment). It is widely
recognised that the species diversity recorded in a
given site will greatly depend on the sampling
effort and on the sampling methods applied in the
field (Moreno & Halffter 2001; Longino et al.
2002; Romo et al. 2006). The influence of the
sampling methods used in this study on the results
here obtained will be explored in detail elsewhere
in future work. However, regardless of the
sampling methods used, a standardised protocol
allows accurate comparability among places
sampled, which was the main aim of this work.
The use of immatures in diversity studies has
been criticized due to common lumping and
splitting errors. However, in the Azores, as the
diversity is low (Borges et al. 2005b) and most of
the genera are monospecific (80%), identification
errors are less likely to occur (Borges et al. 2002).
Furthermore, and as a result of the large number of
individuals caught, the Azorean collection
includes voucher specimens to account for the
polymorphism that has been observed across
islands, and much expertise has been gained
during the process and from previous studies as
well (e.g., Borges 1990; Borges 1999; Borges &
Brown 2001). Araneae, in particular, which
accounted for nearly half of the overall abundance
of immatures, is one of the arthropod groups that
has received more attention from taxonomists in
the Azores (e.g. Berland 1917; Bacelar 1937;
Machado 1982; Wunderlich 1994; Borges &
Wunderlich 2008). Apart from all these
precautions, only late instars were considered to
avoid any errors.
Although corresponding to the same type of
habitat (Laurisilva), each site has a particular
composition and structure (relative abundance) of
woody plant species. This is a consequence of
local climatic conditions, past geological events
and vegetation succession processes (Dias 1996;
Gabriel 2000). As a result, it was not possible to
compare directly the diversity and distribution of
arthropods for a given plant species across all
sites. Instead, each site was compared with others
based on the combined dominant plant species
present. Actually, results showed that the
arthropod diversity for a given plant species was
more similar to the arthropod composition of other
plant species within the same site than to
composition of the same plant species from
different sites. In a previous study, Ribeiro et al.
(2005) found the same pattern except for Erica
azorica, which showed a characteristic arthropod
diversity across the archipelago. In this study,
using more data, not even Erica azorica was an
exception. In fact, the particular structure and
composition of the combined plant species within
each site is expected to have an effect on the
proportion of organic matter and acidity of the
soil, in the intensity of light, density of the
understorey vegetation and humidity inside the
forest, and thus, may influence the composition
and abundance of arthropods. This supports the
use of arthropod data from plant species combined
rather than using the arthropod information for
each plant species independently. The differences
in the arthropod diversity collected using
dominant or non-dominant plant species will be
evaluated in detail in the near future.
Araneae species had the highest abundance of
the 21 arthropod orders studied, corresponding to
30% of the overall abundance found. Also, it was
the only group of the four most diverse orders to
show a bimodal distribution of occurrences. This
is likely a result of the high dispersal ability
(ballooning capacity of species from the
Linyphiidae family, 34 spp) and low habitat
specificity of many species of Araneae.
Indigenous species, including native and
endemic, corresponded to more than half of the
species recorded and almost 90% of the abundance
found. The low abundance of non-indigenous
species may suggest that some of these species
may be vagrants in native forests, dispersing from
surrounding habitats, such as pastures or exotic
forests. The proportion of singletons and
doubletons for non-indigenous species (45%),
however, was not much higher than that for
indigenous species (31%) and even lower than for
the group with unknown colonization (55%). A
study is being developed comparing the arthropod
diversity and abundance within native forests and
from surrounding habitats that will hopefully help
to clarify this (Borges et al. in press).
The arthropod composition in soil and canopy
strata seems to be considerably different. Canopy
and soil strata shared only a third of common
arthropod species, and arthropod composition
seems to aggregate more strongly per stratum than
per location (islands, fragments or even sites).
This is surprising, taking into account the
particular characteristics that each site presents, as
discussed above. Both strata have a prevalence of
species with high dispersal ability (65% for soil
and 70% for canopy), so this may be a result of
dissimilar niche requirements rather than a
constraint in dispersal ability of soil arthropods.
Also, due to the uneven ground, it is common to
see canopy strata at the ground level, and still,
despite the opportunity given to soil arthropods to
disperse to canopy both strata remain distinct in
their arthropod composition.
More than one third of the arthropod species
occurred in only one island, one fragment or one
site, being the exclusive species distributed across
all fragments and islands. Thus, each site has a
unique contribution to the overall diversity found.
This finding has important implications to the
selection and management of areas for arthropod
conservation in the archipelago. This outcome and
possible factors that may be driving it (e.g.
differential colonization, extinction, speciation,
habitat specificity) will be explored in different
perspectives elsewhere. Notwithstanding, further
15
studies are needed to effectively evaluate
processes that may be driving this general pattern
in the Azores.
ACKNOWLEDGEMENTS
We are grateful to all researchers that
collaborated in the field and laboratory: Álvaro
Vitorino, Anabela Arraiol, Ana Rodrigues, Artur
Serrano, Carlos Aguiar, Catarina Melo, Emanuel
Barcelos, Fernando Pereira, Francisco Dinis,
Genage André, Hugo Mas, Isabel Amorim, João
Amaral, Joaquín Hortal, Lara Dinis, Paula
Gonçalves, Pedro Cardoso, Sandra Jarroca,
Sérvio Ribeiro and Luís Vieira. The Forest
Services provided local support in each island.
Acknowledgments are due to all the taxonomists
who assisted in the identification of the
morphotypes: Andrew Polaszek, António Sousa,
Artur Serrano, Arturo Baz, Fernando Ilharco,
Henrik Enghoff, Jordi Ribes, José Quartau, Jörg
Wunderlich, Mário Boieiro, Ole Karsholt, Pedro
Cardoso, Richard Strassen, Volker Manhert and
Virgílio Vieira. Enésima Mendonça kindly helped
to review past literature on Azorean arthropods.
We thank Jon Sadler and Owen Petchey for
helpful discussions and suggestions. CG was
funded by Fundação para a Ciência e a
Tecnologia (FCT) of the Portuguese Ministry of
Science, Technology and Higher education
(BD/11049/2002).
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Accepted 5 June 2008.
APPENDIX
Table 1. List of the arthropod species recorded in the Azorean native forests, ordered alphabetically by
major taxon (Order). Col. - Colonization group (I-Introduced, N-Native, E-Endemic); Tro. - Trophic group
(P-Predator, H-Herbivore, S-Saprophage, F-Fungivore); Disp. - Dispersal ability (High, Low). Taxa with no
information or followed by ? are waiting for identification or confirmation, but were recognized by
taxonomists as different taxonomic units. Endemic species are highlighted in grey.
Order FAMILY
Araneae
Species
Col.
Tro.
Disp.
I
I?
E
I
P
P
P
P
Low
Low
Low
Low
I
E
E
N
I?
I
I?
P
P
P
P
P
P
P
Low
Low
Low
Low
Low
Low
Low
ARANEIDAE
Araneus sp.
Gen. sp.
Gibbaranea occidentalis Wunderlich
Mangora acalypha (Walckenaer)
CLUBIONIDAE
Cheiracanthium erraticum (Walckenaer)
Cheiracanthium floresense Wunderlich
Cheiracanthium jorgeense Wunderlich
Clubiona decora Blackwall
Clubiona genevensis L. Koch
Clubiona terrestris Westring
Gen. sp.
18
Table 1. Arthropod species from Azorean native forests (continuation, 2/13)
Order
FAMILY
Species
Col.
Tro.
Disp.
E
N
I
P
P
P
Low
Low
Low
I
P
Low
E
E
I
E
E
?
E
I
I
I
I
I
I
I
I
?
E?
?
E
I
I
N
E
I
I
I
N
I
E
I
E
N
I
E
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
E
P
Low
I
P
Low
I
P
Low
E
P
Low
DICTYNIDAE
Dictyna (Emblyna) acoreensis (Wunderlich)
Lathys dentichelis (Simon)
Nigma puella (Simon)
DYSDERIDAE
Dysdera crocata C.L. Koch
LINYPHIIDAE
Acorigone acoreensis (Wunderlich)
Acorigone zebraneus Wunderlich
Agyneta decora (O.P.-Cambridge)
Agyneta depigmentata Wunderlich
Agyneta rugosa Wunderlich
Agyneta sp.
Araeoncus n. sp.
Eperigone bryantae Ivie & Barrows
Eperigone fradeorum (Berland)
Eperigone sp. 1
Eperigone sp. 3
Eperigone trilobata (Emerton)
Erigone atra (Blackwall)
Erigone autumnalis Emerton
Erigone dentipalpis (Wider)
Erigone sp.
Gen. sp. 1
Gen. sp. 2
Lepthyphantes acoreensis Wunderlich
Lessertia dentichelis (Simon)
Meioneta fuscipalpis (C.L. Koch)
Microlinyphia johnsoni (Blackwall)
Minicia floresensis Wunderlich
Neriene clathrata (Sundevall)
Oedothorax fuscus (Blackwall)
Ostearius melanopygius (O.P.-Cambridge)
Palliduphantes schmitzi (Kulczynski)
Pelecopsis parallela (Wider)
Porrhomma borgesi Wunderlich
Prinerigone vagans (Audouin)
Savigniorrhipis acoreensis Wunderlich
Tenuiphantes miguelensis Wunderlich
Tenuiphantes tenuis (Blackwall)
Walckenaeria grandis (Wunderlich)
LYCOSIDAE
Pardosa acorensis Simon
MIMETIDAE
Ero furcata (Villers)
OECOBIIDAE
Oecobius navus Blackwall
OONOPIDAE
Orchestina furcillata Wunderlich
19
Table 1. Arthropod species from Azorean native forests (continuation, 3/13)
Order
FAMILY
Species
Col.
Tro.
Disp.
Pisaura acoreensis Wunderlich
E
P
Low
Macaroeris cata (Blackwall)
Macaroeris sp.
Neon acoreensis Wunderlich
Pseudeuophrys vafra (Blackwall)
N
I?
E
I
P
P
P
P
Low
Low
Low
Low
I
E
P
P
Low
Low
I
I
E?
?
?
E
I
E
I
N
I
P
P
P
P
P
P
P
P
P
P
P
Low
Low
Low
Low
Low
Low
Low
Low
Low
Low
Low
N
I
P
P
Low
Low
I
P
Low
N
S
High
N?
S
Low
?
S/H
High
I
S
High
N
N
I
I
E
E
E
N
N?
I
E
P
P
P
P
P
P
P
P
P
P
P
High
High
High
High
Low
Low
Low
High
High
High
Low
PISAURIDAE
SALTICIDAE
TETRAGNATHIDAE
Metellina merianae (Scopoli)
Sancus acoreensis (Wunderlich)
THERIDIIDAE
Achaearanea acoreensis (Berland)
Argyrodes nasicus (Simon)
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Lasaeola oceanica Simon
Neottiura bimaculata (Linnaeus)
Rugathodes acoreensis Wunderlich
Steatoda grossa (C.L. Koch)
Theridion musivivum Schmidt
Theridion sp.
THOMISIDAE
Xysticus cor Canestrini
Xysticus nubilus Simon
ZODARIIDAE
Zodarion atlanticum Pekár & Cardoso
Blattaria
POLYPHAGIDAE
Zetha vestita (Brullé)
Chordeumatida
HAPLOBAINOSOMATIDAE
Haplobainosoma lusitanum Verhoeff
Coleoptera
Fam ?
Gen. sp.
ANTHICIDAE
Gen. sp.
CARABIDAE
Acupalpus dubius Schilsky
Acupalpus flavicollis (Sturm) ?
Amara aenea (De Geer)
Anisodactylus binotatus (Fabricius)
Calathus lundbladi Colas
Cedrorum azoricus azoricus Borges & Serrano
Cedrorum azoricus caveirensis Borges & Serrano
Laemosthenes complanatus Dejean
Ocys harpaloides (Audinet-Serville)
Paranchus albipes (Fabricius)
Pseudanchomenes aptinoides Tarnier
20
Table 1. Arthropod species from Azorean native forests (continuation, 4/13)
Order
FAMILY
Species
Pseudophonus rufipes (DeGeer)
Pterostichus (Argutor) vernalis (Panzer)
Pterostichus aterrimus aterrimus (Herbst)
Stenolophus teutonus (Schrank)
Trechus terrabravensis Borges, Serrano & Amorim
CERAMBYCIDAE
Crotchiella brachyptera Israelson
CHRYSOMELIDAE
Chaetocnema hortensis (Fourcroy)
Epitrix hirtipennis Melsham
Gen. sp.
CIIDAE
Atlantocis gillerforsi Israelson
COCCINELLIDAE
Clitostethus arcuatus (Rossi)
Coccinella undecimpunctata undecimpunctata L.
Gen. sp.
Rhyzobius lophanthae (Blaisdell)
CORYLOPHIDAE
Gen. sp.
Sericoderus lateralis (Gyllenhal)
CRYPTOPHAGIDAE
Cryptophagus sp. 1
Cryptophagus sp. 2
Cryptophagus sp. 3
Cryptophagus sp. 4
Cryptophagus sp. 5
Gen. sp.
CURCULIONIDAE
Calacalles subcarinatus (Israelson)
Caulotrupis parvus Israelson
Coccotrypes carpophagus (Hornung)
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Drouetis borgesi Machado
Otiorhynchus rugosostriatus (Goeze)
Phloeosinus gillerforsi Bright
Pseudechinosoma nodosum Hustache
Pseudophloeophagus tenax (Wollaston)
Sitona discoideus Gyllenhal
Sitona sp.
Tychius sp.
Xyleborinus saxesenii (Ratzeburg)
DRYOPHTHORIDAE
Sitophilus oryzae (Linnaeus)
Sphenophorus abbreviatus (Fabricius)
DRYOPIDAE
Dryops algiricus Lucas
Dryops luridus (Erichson)
Col.
Tro.
Disp.
I
I
N
I
E
P/H
P
P
P
P
High
High
High
High
Low
E
H
High
I
I
I?
P
H
H
High
High
High
E
F
Low
I
I
I
I
P
P
P
P
High
High
High
High
?
I
P
P
High
High
I
I
I
I
I
I
S
S
S
S
S
S
High
High
High
High
High
High
E
E
I
I?
I
?
E
N
E
E
N
I
I
I?
I
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
High
Low
High
High
High
High
Low
Low
High
Low
High
High
High
High
High
I
I
H
H
High
High
N
N
H
H
High
High
21
Table 1. Arthropod species from Azorean native forests (continuation, 5/13)
Order
FAMILY
Species
Col.
Tro.
Disp.
N
E
E
P
P
P
High
High
High
E
E
E
S
H
H
High
High
High
I
I
S
S
High
High
N?
N
P
P
High
High
I
E?
?
I
E
S
S
S
S
S
High
High
High
High
High
N
S
High
I
F
High
I
I
I
I
I
I
I
I
S
S
S
H
H
H
S
S
High
High
High
High
High
High
High
High
I?
N
S
S
High
High
N?
I
S
S
High
High
I
S
High
N
H
High
N?
S
High
I
P
High
I
N
P
P
High
High
DYTISCIDAE
Agabus bipustulatus (Linnaeus)
Agabus godmani Crotch
Hydroporus guernei Régimbart
ELATERIDAE
Aeolus melliculus moreleti Tarnier
Alestrus dolosus (Crotch)
Athous pomboi Platia & Borges
HYDROPHILIDAE
Cercyon haemorrhoidalis (Fabricius)
Sphaeridium bipustulatum (Fabricius)
LAEMOPHLOEIDAE
Gen. sp.
Placonotus sp. 1
LATHRIDIIDAE
Cartodere (Aridius) nodifer (Westwood)
Gen. sp. 1
Gen. sp. 2
Lathridius australicus (Belon)
Metophthalmus occidentalis Israelson
LEIODIDAE
Catops coracinus coracinus Kellner
MYCETOPHAGIDAE
Typhaea stercorea (Linnaeus)
NITIDULIDAE
Carpophilus fumatus Boheman
Carpophilus hemipterus (Linnaeus)
Carpophilus sp. 2
Epuraea biguttata (Thunberg)
Meligethes aeneus (Fabricius)
Meligethes sp. 2
Meligethes sp. 3
Stelidota geminata (Say)
PHALACRIDAE
Gen. sp.
Stilbus testaceus (Panzer)
PTILIIDAE
Acrotrichis sp. 1
Ptenidium pusillum (Gyllenhal)
SCARABAEIDAE
Onthophagus taurus (Schreber)
SCRAPTIIDAE
Anaspis proteus (Wollaston)
SCYDMAENIDAE
Cephennium distinctum Besuchet
SILVANIDAE
Cryptamorpha desjardinsii (Guérin-Méneville)
STAPHYLINIDAE
Aleochara bipustulata (Linnaeus)
Aloconota sulcifrons (Stephens)
22
Table 1. Arthropod species from Azorean native forests (continuation, 6/13)
Order
FAMILY
Species
Col.
Tro.
Disp.
Amischa analis (Gravenhorst)
Anotylus nitidifrons (Wollaston)
Anotylus sp. 2
Atheta amicula (Stephens)
Atheta atramentaria (Gyllenhal)
Atheta dryochares Israelson
Atheta fungi (Gravenhorst)
Atheta sp. 3
Atheta sp. 4
Carpelimus corticinus (Gravenhorst)
Cilea silphoides (Linnaeus)
Cordalia obscura (Gravenhorst)
Gabrius nigritulus (Gravenhorst)
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Gen. sp. 4
Habrocerus capillaricornis (Gravenhorst)
Medon sp. 2
Ocypus (Pseudocypus) aethiops (Waltl)
Ocypus olens (Muller)
Oligota parva Kraatz
Philonthus sp.
Phloeonomus n. sp. ?
Phloeonomus sp. 1
Phloeonomus sp. 3
Phloeonomus sp. 4
Phloeopora sp. 1
Phloeopora sp. 4
Phloeostiba azorica (Fauvel)
Proteinus atomarius Erichson
Quedius curtipennis Bernhauer
Quedius simplicifrons (Fairmaire)
Rugilus orbiculatus orbiculatus (Paykull)
Scopaeus portai Luze
Sepedophilus lusitanicus (Hammond)
Stenus guttula guttula Müller
Tachyporus chrysomelinus (Linnaeus)
Xantholinus longiventris Heer
Xantholinus sp.
I
I
I
I
I
E
I?
E
E?
N
I
I
I
N?
N?
E?
N
N
N
N
N
I
N?
E
N
I
?
N
N?
E
N
N
N
N
N?
N
N
I
I
I
P
P
P
P
P
P
F
P
P
P
P
P
P
P
P
P
H
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
P
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
E
E
E
E
E
E
E
E
F
F
F
F
F
F
F
F
Low
Low
Low
Low
Low
Low
Low
Low
ZOPHERIDAE
Tarphius acuminatus Gillerfors
Tarphius azoricus Gillerfors
Tarphius depressus Gillerfors
Tarphius pomboi Borges
Tarphius rufonodulosus Israelson
Tarphius serranoi Borges
Tarphius tornvalli Gillerfors
Tarphius wollastoni Crotch
23
Table 1. Arthropod species from Azorean native forests (continuation, 7/13)
Order FAMILY
Dermaptera
Species
ANISOLABIDIDAE
Euborellia annulipes (Lucas)
FORFICULIDAE
Forficula auricularia Linnaeus
Col.
Tro.
Disp.
I
P
Low
I
P
Low
N?
H
High
N
P
Low
N?
P
Low
E?
H
High
N?
N?
?
?
?
E?
E?
E?
E?
E?
E?
E?
E?
H
H
H
H
H
H
H
H
H
H
H
H
H
High
High
High
High
High
High
High
High
High
High
High
High
High
I
N
N
P
P
P
High
High
High
N
N
N
?
N
I
I
I?
I?
I
I
I
I
I
N
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
High
High
High
High
High
High
High
High
High
High
High
High
High
High
High
Ephemeroptera
BAETIDAE
Cloeon dipterum (Linnaeus)
Geophilomorpha
GEOPHILIDAE
Geophilus truncorum Bergsoe & Meinert
LINOTAENIIDAE
Strigamia crassipes (C.L. Koch)
Hemiptera
Fam ?
Gen. sp.
ALEYRODIDAE
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Gen. sp. 4
Gen. sp. 5
Gen. sp. 6
Gen. sp. 7
Gen. sp. 8
Gen. sp. 9
Gen. sp. 10
Gen. sp. 11
Gen. sp. 12
Gen. sp. 13
ANTHOCORIDAE
Brachysteles parvicornis (A. Costa)
Buchananiella continua (White)
Orius (Orius) laevigatus laevigatus (Fieber)
APHIDIDAE
Acyrthosiphon pisum Harris
Amphorophora rubi (Kaltenbach) sensu latiore
Aphis craccivora Koch
Aphis sp.
Aulacorthum solani (Kaltenbach)
Covariella aegopodii (Scopoli)
Dysaphis plantaginea (Passerini)
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Longiunguis luzulella Hille Ris Lambers ?
Myzus cerasi (Fabricius)
Neomyzus circumflexus (Buckton)
Pseudacaudella rubida (Borner)
Rhopalosiphonimus latysiphon (Davidson)
24
Table 1. Arthropod species from Azorean native forests (continuation, 8/13)
Order
FAMILY
Species
Col.
Tro.
Disp.
Rhopalosiphum insertum (Walker)
Rhopalosiphum padi (Linnaeus)
Rhopalosiphum rufiabdominalis (Sasaki)
Toxoptera aurantii (Boyer de Fonscolombe)
Uroleucon erigeronense (Thomas)
I
I
I
I
N?
H
H
H
H
H
High
High
High
High
High
N?
H
High
I?
E
E
?
N?
H
H
H
H
H
High
High
High
High
High
E
E
E
E
E
E
E
E
E
H
H
H
H
H
H
H
H
H
High
High
High
High
High
High
High
High
High
?
?
?
?
N
?
N?
H
H
H
H
H
H
H
Low
Low
Low
Low
Low
Low
Low
N?
H
High
N?
?
N
N
N?
N?
H
H
H
H
H
H
High
High
High
High
High
High
I
N
H
H
High
High
N
H
High
N
H
High
N?
I
H
H
High
High
CERCOPIDAE
Philaenus spumarius (Linnaeus)
CICADELLIDAE
Anoscopus albifrons (Linnaeus)
Aphrodes hamiltoni Quartau & Borges
Eupteryx azorica Ribaut
Gen. sp.
Opsius stactogallus Fieber
CIXIIDAE
Cixius azofloresi Remane & Asche
Cixius azomariae Remane & Asche
Cixius azopifajo azofa Remane & Asche
Cixius azopifajo azojo Remane & Asche
Cixius azopifajo Remane & Asche
Cixius azoricus azoricus Lindberg
Cixius azoricus azoropicoi Remane & Ashe
Cixius azoterceirae Remane & Asche
Cixius insularis Lindberg
COCCIDAE
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Gen. sp. 4
Gen. sp. 5
Gen. sp. 6
Gen. sp. 7
CYDNIDAE
Geotomus punctulatus (Costa)
DELPHACIDAE
Gen. sp. 1
Gen. sp. 2
Megamelodes quadrimaculatus (Signoret)
Muellerianella sp. 1
Muellerianella sp. 2
Muellerianella sp. 3
DREPANOSIPHIDAE
Anoecia corni (Fabricius)
Theriaphis trifolii (Monell)
FLATIDAE
Cyphopterum adcendens (Herr.-Schaff.)
LACHNIDAE
Cinara juniperi (De Geer)
LYGAEIDAE
Beosus maritimus (Scopoli)
Gastrodes grossipes grossipes (De Geer)
25
Table 1. Arthropod species from Azorean native forests (continuation, 9/13)
Order
FAMILY
Species
Col.
Tro.
Disp.
Heterogaster urticae (Fabricius)
Kleidocerys ericae (Horváth)
Microplax plagiata (Fieber)
Nysius atlantidum Horváth
Plinthisus brevipennis (Latreille)
Plinthisus minutissimus Fieber
Scolopostethus decoratus (Hahn)
N?
N
I?
E
N
N
N?
H
H
H
H
H
H
H
High
High
High
High
High
High
High
?
?
?
H
H
H
Low
Low
Low
I
I
H
H
High
High
N?
N
N
N
E
N
H
H
P
H
H
H
High
High
High
High
High
High
N
P
High
I
H
High
I
I
E
H
H
H
High
High
High
N?
P
High
I
H
High
N
H
High
N
H
High
I?
I
N?
N?
S
S
S
S
Low
Low
Low
Low
I?
N?
N?
N
I?
S
S
S
S
H
Low
Low
Low
Low
Low
MARGARODIDAE
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
MICROPHYSIDAE
Loricula (Loricula) elegantula (Bärensprung)
Loricula (Myrmedobia) coleoptrata (Fallén)
MIRIDAE
Campyloneura virgula (Herrich-Schaeffer)
Closterotomus norwegicus (Gmelin)
Heterotoma planicornis (Pallas)
Monalocoris filicis (Linnaeus)
Pinalitus oromii J. Ribes
Polymerus (Poeciloscytus) cognatus (Fieber)
NABIDAE
Nabis pseudoferus ibericus Remane
PENTATOMIDAE
Nezara viridula (Linnaeus)
PSYLLIDAE
Acizzia uncatoides (Ferris & Klyver)
Cacopsylla pulchella (Low)
Strophingia harteni Hodkinson
REDUVIIDAE
Empicoris rubromaculatus (Blackburn)
SALDIDAE
Saldula palustris (Douglas)
TINGIDAE
Acalypta parvula (Fallén)
TRIOZIDAE
Trioza (Lauritrioza) laurisilvae Hodkinson
Julida
BLANIULIDAE
Blaniulus guttullatus (Fabricius)
Choneiulus palmatus (Nemec) ?
Nopoiulus kochii (Gervais)
Proteroiulus fuscus (Am Stein)
JULIDAE
Brachyiulus pusillus (Leach)
Brachyiulus sp.
Cylindroiulus latestriatus (Curtis)
Cylindroiulus propinquus (Porat)
Ommatoiulus moreletii (Lucas)
26
Table 1. Arthropod species from Azorean native forests (continuation, 10/13)
Order FAMILY
Lepidoptera
Species
Col.
Tro.
Disp.
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Gen. sp. 4
Gen. sp. 5
Gen. sp. 6
Gen. sp. 7
Gen. sp. 8
Gen. sp. 9
Gen. sp. 10
Gen. sp. 11
Gen. sp. 12
Gen. sp. 13
Gen. sp. 14
Gen. sp. 15
Gen. sp. 16
Gen. sp. 17
Gen. sp. 18
Gen. sp. 19
?
?
?
N?
?
N?
E?
?
I?
E?
N?
N?
N?
N
N
N?
N?
N?
N?
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
Low
High
Low
Low
Low
Low
Low
High
Low
Low
Low
Low
Low
Low
Low
Low
Low
Low
Low
I?
I
?
H
H
H
High
High
High
E
H
High
E
E
E
E?
N
E
H
H
H
H
H
H
Low
Low
Low
Low
Low
Low
I
E
I
H
H
H
High
High
High
E
E
H
H
High
High
N
N
N
?
N?
N?
N?
N?
H
H
H
H
H
H
H
H
High
Low
Low
High
Low
Low
Low
Low
Fam ?
BLASTOBASIDAE
Blastobasis sp. 1
Blastobasis sp. 3
Neomariania sp.
GELECHIIDAE
Brachmia infuscatella Rebel
GEOMETRIDAE
Ascotis fortunata azorica Pinker
Cyclophora azorensis (Prout)
Cyclophora pupillaria granti Prout
Gen. sp.
Orthomana obstipata (Fabricius)
Xanthorhoe inaequata (Warren)
GRACILLARIIDAE
Caloptilia schinella (Walsingham)
Micrurapteryx bistrigella (Rebel)
Phyllocnistis citrella Stainton
NIMPHALYDAE
Hipparchia azorina occidentalis (Sousa)
Hipparchia miguelensis (Le Cerf)
NOCTUIDAE
Agrotis ipsilon (Hufnagel)
Agrotis sp.
Chrysodeixis chalcites (Esper)
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Gen. sp. 4
Gen. sp. 5
27
Table 1. Arthropod species from Azorean native forests (continuation, 11/13)
Order
FAMILY
Species
Col.
Tro.
Disp.
Gen. sp. 6
Gen. sp. 7
Mesapamea storai (Rebel)
Mythimna unipuncta (Haworth)
Phlogophora interrupta (Warren) ?
Xestia c-nigrum (Linnaeus)
N?
I
E
N
E
N
H
H
H
H
H
H
Low
Low
High
High
Low
High
Eudonia luteusalis (Hampson)
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Scoparia coecimaculalis Warren
Scoparia semiamplalis Warren
Scoparia sp. 1
Scoparia sp. 2
Scoparia sp. 3
Scoparia sp. 4
E
N?
?
?
E
E
E
E?
?
E
H
H
H
H
H
H
H
H
H
H
High
Low
High
High
High
High
Low
High
High
High
I
I
?
H
H
H
High
High
High
I
I
I
I
I
N?
I
H
H
H
H
H
H
H
Low
Low
Low
Low
Low
Low
High
E
H
High
N
N
P
P
Low
Low
N
E
S
S
Low
Low
E
P
High
N
N
P
P
Low
Low
I
S
High
PYRALIDAE
TINEIDAE
Oinophila v-flava (Haworth)
Opogona sacchari (Bojer)
Opogona sp.
TORTRICIDAE
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
Gen. sp. 4
Gen. sp. 5
Gen. sp. 6
Rhopobota naevana Huebner
YPONOMEUTIDAE
Argyresthia atlanticella Rebel
Litobiomorpha
LITHOBIIDAE
Lithobius pilicornis pilicornis Newport
Lithobius sp.
Microcoryphia
MACHILIDAE
Dilta saxicola (Womersley)
Trigoniophthalmus borgesi Mendes et al.
Neuroptera
HEMEROBIIDAE
Hemerobius azoricus Tjeder?
Opilionida
PHALANGIIDAE
Homalenotus coriaceus (Simon)
Leiobunum blackwalli Meade
Orthoptera
GRYLLIDAE
Gryllus bimaculatus (De Geer)
28
Table 1. Arthropod species from Azorean native forests (continuation, 12/13)
Order
FAMILY
Species
CONOCEPHALIDAE
Conocephalus chavesi (Bolivar)
Col.
Tro.
Disp.
N?
H
High
I
S
Low
N
N
S
S
Low
Low
N
N
P
P
Low
Low
I
P
Low
?
?
?
S
S
S
High
High
Low
N
N
S
S
High
High
N
N
S
S
High
High
E
E
N
S
S
S
High
High
High
N
S
High
N
N
N
S
S
S
High
High
High
N
S
High
N
S
High
E
E?
E
N?
N
S
S
S
S
S
Low
Low
Low
Low
Low
N?
P
Low
Polydesmida
PARADOXOSOMATIDAE
Oxidus gracilis (C.L. Koch)
POLYDESMIDAE
Brachydesmus superus Latzel
Polydesmus coriaceus Porat
Pseudoscorpionida
CHTHONIIDAE
Chthonius ischnocheles (Hermann)
Chthonius tetrachelatus (Preyssler)
NEOBISIIDAE
Neobisium maroccanum Beier
Psocoptera
Fam ?
Gen. sp. 1
Gen. sp. 2
Gen. sp. 3
CAECILIUSIDAE
Valenzuela burmeisteri (Brauer)
Valenzuela flavidus (Stephens)
ECTOPSOCIDAE
Ectopsocus briggsi McLachlan
Ectopsocus strauchi Enderlein
ELIPSOCIDAE
Elipsocus azoricus Meinander
Elipsocus brincki Badonnel
Bertkauia lucifuga (Rambur)
LACHESILLIDAE
Lachesilla greeni (Pearman)
PERIPSOCIDAE
Peripsocus milleri (Tillyard)
Peripsocus phaeopterus (Stephens)
Peripsocus subfasciatus (Rambur)
PSOCIDAE
Atlantopsocus adustus (Hagen)
TRICHOPSOCIDAE
Trichopsocus clarus (Banks)
TROGIIDAE
Cerobasis cf sp. A
Cerobasis n. sp.
Cerobasis sp. A
Gen. sp.
Lepinotus reticulatus Enderlein
Scolopendromorpha
CRYPTOPIDAE
Cryptops hortensis Leach
29
Table 1. Arthropod species from Azorean native forests (continuation, 13/13)
Order FAMILY
Thysanoptera
Species
AEOLOTHRIPIDAE
Aeolothrips collaris Priesner
Aeolothrips gloriosus Bagnall
PHLAEOTHRIPIDAE
Apterygothrips ? canarius (Priesner)
Apterygothrips n. sp. ?
Eurythrips tristis Hood
Gen. sp.
Hoplandrothrips consobrinus (Knechtel)
Hoplothrips corticis (De Geer)
Hoplothrips ulmi (Fabricius)
Nesothrips propinquus (Bagnall)
THRIPIDAE
Aptinothrips rufus Haliday
Ceratothrips ericae (Haliday)
Frankliniella sp.
Heliothrips haemorrhoidalis (Bouché)
Hercinothrips bicinctus (Bagnall)
Isoneurothrips australis Bagnall
Thrips atratus Haliday
Thrips flavus Schrank
Col.
Tro.
Disp.
N
I
P
P
High
High
I
E
I
?
I
N
N
I
H
H
H
H
H
F
F
H
High
High
High
High
High
High
High
High
N
N
N
I
I
I
N
N
H
H
H
H
H
H
H
H
High
High
High
High
High
High
High
High
?
P
Low
E
P
High
Trichoptera
Fam ?
Gen. sp.
LIMNEPHILIDAE
Limnephilus atlanticus Nybom ?
30
Distribution and abundance of arthropod species in
pasture communities of three Azorean islands
(Santa Maria, Terceira and Pico)
PAULO A.V. BORGES
Borges, P.A.V. 2008. Distribution and abundance of arthropod species in pasture
communities of three Azorean islands (Santa Maria, Terceira and Pico).
Arquipélago. Life and Marine Sciences 25: 31-41.
This work provides evidence that the "hollow curve" is a consistent pattern in the range size
distribution of taxonomic and ecological groups of arthropod pasture dwelling species.
Many of the inconsistent results relating range size to herbivores diet breadth are probably
due to historical constraints in the colonization of the islands and particular characteristics
of the habitats studied (e.g. types of resources available). The positive relationship between
range size and abundance may be explained by the "resource usage model". However, the
slope of the regression line relating distribution to abundance was similar for different
groups which suggests there is no difference in the way that the species’ local abundance
scales with distribution in the four assemblages of species studied and that there is a close
relationship between the trophic groups studied. This suggests that the “resource
availability model” could be the explanation for the distribution and abundance of pasture
spider and insect species. More work needs to be conducted in order to evaluate the
relationship between diet breadth, habitat specialization and range size in the islands.
Key words: range size, functional groups, herbivore, predator, resource availability model
Paulo A.V. Borges (e-mail: pborges@uac.pt), Universidade dos Açores, Departamento de
Ciências Agrárias (CITA-A; Azorean Biodiversity Group), Terra-Chã, PT-9700-851 Angra
do Heroísmo, Terceira, Açores, Portugal.
INTRODUCTION
Since the classic work of Andrewartha & Birch
(1954) on the distribution and abundance of
animals, the study of distribution has become one
of the key issues in ecological studies, and is
intrinsic to the concept of "Ecology" (Krebs
1994).
One way to examine patterns of distribution is
to plot the frequency histogram of species
distributions, that is, a species-range-size
distribution (Gaston 1994a; Brown 1995). The
results of most previous studies suggest that,
within a particular taxon or assemblage of
species, the untransformed geographic ranges of
species are distributed according to a "hollow
curve" (Schoener 1987; Gaston 1994b). Thus,
most species have a narrow range while a few are
more widespread, distributed throughout all the
measured range (Gaston & Blackburn 2000).
In some cases, the species-range-size
distribution shows a bimodal pattern (Hanski
1982; Gaston 1994a; Brown 1984, 1995), in
which to the left hand mode is added a right hand
mode generated by the widespread group of
species that occur in almost all sampled sites. The
"hollow curve" pattern has important implications
in terms of conservation biology, since a large set
of the species in any community that shows it,
can be regarded as rare in terms of the extent of
their distribution (Gaston & Blackburn 2000). As
restricted distribution and low abundance are
commonly positively correlated (see also below)
(Hanski 1982; Brown 1984, 1995; Gaston 1994a,
31
1996; Gaston & Blackburn 2000), a great
proportion of the species of a particular
assemblage are therefore likely to be prone to
extinction (Lawton 1993; Gaston 1996; Gaston &
Blackburn 2000).
Range size is commonly correlated with
several other variables. Gaston et al. (1997) list
and discuss eight mechanisms that have been
proposed to, or might possibly, generate positive
relationships between the local abundance and
regional distribution of species. In the “sampling
artefact” model the relationship arises as a
consequence of a systematic under-estimation of
the range sizes of species with lower local
abundances.
The
“phylogenetic
nonindependence” model, also considers that the
positive relationship between abundance and
distribution of species might be artefactual and
results from non-independence of species as data
points for statistical analysis (i.e. phylogenetic
relatedness) (Harvey 1996). The "core and
satellite species hypothesis" (Hanski 1982) and
the "resource usage model" (Brown 1984, 1995)
were proposed to explain the finding that a few
species are regionally common (widespread) and
locally abundant (the "core" species in Hanski’s
model; the generalists or broad-niched species in
Brown’s model), while most species can be
regarded as having low ranges and low local
abundances (the "satellite" species in Hanski’s
model; the specialists or narrow-niched species in
Brown’s model). In Brown’s model (“breadth of
resource usage” sensu Gaston et al. 1997) there is
an attainment of higher local abundances and
wider distributions by species with greater
resource breadths. A positive abundance - range
size relationship is an assumption of the "core and
satellite species hypothesis" (Hanski 1982;
Hanski et al. 1993), but other metapopulation
models also predict this pattern (Gaston et al.
1997).
Other explanations for the positive abundance range size relationship are: the "habitat
availability model" (Venier & Fahrig 1996), in
which the positive relationship between
abundance and distribution arises on a patchy
landscape if individual species have differences in
habitat use and consequently different amounts of
habitat are available to them on the same
landscape (“habitat selection” model sensu
32
Gaston et al. 1997); the "population model" (Holt
et al. 1997) (= “vital rates” sensu Gaston et al.
1997) in which, assuming that all species are
similar in their response to density-dependent
factors but differ to their response to densityindependent factors affecting birth and death
rates, then a positive relationship between
distribution and abundance is obtained using a
simple demographic model. To the six models
already listed, two other are also summarized in
Gaston et al. (1997) (see also Lawton 2000;
Gaston 2003): “range position”, i.e. species closer
to the edges of their geographic ranges have
lower abundances in, and occupy a smaller
proportion of, study areas; “resource availability”,
i.e. attainment of higher local abundances and
wider distributions by species with greater
resource availability (see also Gaston 1994a).
We demonstrated elsewhere that in the Azores
natives, endemics and exotics are part of the same
plot in testing the non independence between
abundance and range size for arthropods (see
Gaston et al. 2006), that is, they all lie on the
same bivariate abundance - occupancy
relationship. Therefore, here we will analyse the
community without separating species into their
colonization status. Here we go further and study
patterns of distribution and abundance of different
functional arthropod groups in human altered
grassland habitats, i.e. old semi-natural pastures
and recent intensive pastures. The aims of the
current paper are: i) to give an integrated picture
of distribution patterns in several ecological
functional arthropod groups; ii) test the non
independence between abundance and range size
in human-modified habitats and clarify the
mechanisms generating it.
MATERIAL AND METHODS
SITES AND EXPERIMENTAL DESIGN
Two replicates (“cerrados”) of recently sown
pastures (SP) and old semi-natural pastures (SNP)
were selected in three Azorean islands (Santa
Maria, Terceira and Pico) at a high-altitude level
(see Borges 1999; Borges & Brown 1999, 2001,
2004). The present study includes one habitat
subject to high grazing pressure (sown pastures)
and another with lower grazing management
(semi-natural pastures); it also includes drier
pastures (sown sites of Santa Maria and Terceira)
and highly moist soils of low pH (natural sites
from the three islands. Having taken into account
that the islands have different maximum altitude,
Santa Maria being the lowest altitude island and
Pico the highest Azorean island, the range of
altitudes of the 12 field sites lays between 290
and 800 m (see Appendix I in Borges 1999 for a
detailed description). In all the 12 pastures (3
islands x 2 pasture types x 2 replicates) an area of
at least 900 m2 was fenced during January and
February 1994 with posts and barbed wire. A
preliminary study indicated that rabbit grazing
was unequal in the studied system. Consequently,
rabbit fences to avoid differential rabbit grazing
pressure were erected in April 1994. After the
field sites were fenced, in each of them 20 3x3
(9 m2) plots were marked with coloured small
wood posts. All field sites were grazed regularly
by dairy and beef cattle, thereby maintaining the
traditional management of the sites (see Appendix
1 in Borges 1999). Sampling occurred always
three weeks after a grazing event.
ARTHROPOD DATA SET
The main data set with the arthropod distributions
in the 12 studied field sites used in Borges (1999)
was also used here. For each of the 237 arthropod
species (128 herbivores and 117 predators; note
that some species were listed as both herbivores
and predators), information was gathered on diet
breadth for the herbivores. As stated before
(Borges 1999; Borges & Brown 2001, 2004), the
sources of information were independent for each
taxonomic group, being mainly given by the
taxonomists that identified the morphospecies
who are experts in the Macaronesian faunas (see a
detailed list of contributions in Borges & Brown
1999).
SPECIES ABUNDANCE DATA SETS
For the study of the relationship between
abundance and range size, summer samples were
selected because the vegetation is at its maximum
productivity at this time. The summer of 1994
was chosen in preference to that of 1995 because
the latter was an atypical year (one of the rainiest
years in the Azores of the last 10 years). The
arthropod abundance was assessed with the Vortis
suction apparatus and is given as the number of
specimens per square meter. The range size
obtained for each species is that obtained from
presence/absence data matrices generated from
the Summer 1994 samples, using the Vortis
suction machine for the arthropods, and is given
as the number of occupied sites from a maximum
of 12. Therefore, for the range size - abundance
relationship, the range sizes do not include the
pitfall data used elsewhere (see Borges & Brown
1999).
DATA ANALYSIS
Species range sizes of arthropods were measured
in terms of number of sites occupied with a
maximum occupancy of 12. To have a measure of
the shape of the frequency distribution of species,
its skewness and kurtosis were calculated. As
numbers of species differ between groups of
species, in figures the proportion of species was
used instead of number of species occurring in
each range size category. Moreover, we also
evaluate the occurrence frequency distribution of
species in the various sites using the Tokeshi
statistical test for bimodality (Tokeshi 1992;
Barreto et al. 2003), that allows the calculation of
the probability under the null hypothesis of the
presence of larger numbers of species in the two
extreme classes (one site only vs. all sites).
The range size - diet breadth relationship is
investigated separately for sucking and chewing
herbivores. Each species of herbivore was
allocated to one of four diet categories, species or
genus
monophages,
family
monophages,
oligophages and polyphages. In the cases where
information was not available, the species was not
used in the analysis. For the 2x2 contingency
table analysis, the diet categories were simplified
in order to avoid overdispersion of the data.
Without such modification, some cells would
have had expected frequencies less than five. For
such smaller samples, the recommended
statistical test is the Fisher’s exact test. However,
as in most cases the expected frequencies were so
small that they could easily be a result of chance,
a more robust test was used. The G-test was
chosen since is the most reliable means of
analysing frequency data (Crawley 1993). The
33
new categories were for diet breadth: the four
categories mentioned above were reduced to only
two by grouping the species/genus and family
monophages as "specialists" and the oligophages
and polyphages as "generalists".
For the arthropods, abundance was measured
as the logarithm of the mean number of
individuals per square meter in each field site. As
the frequency distribution of abundance within
each species was shown to be right skewed, the
geometric mean was chosen instead the arithmetic
mean, since it provides a much more accurate
representation of the central tendency (Zar 1984).
The sites used to calculate the regressions were
only those where a species occurred. I examined
the relationship between abundance and range
size for all arthropod species, herbivores,
predators and spiders with ordinary least-squares
(OLS) regression and compared the fits using
range size with both untransformed and
logarithmic transformed values. The best fit was
considered to be that resulting in the higher r2
value. Finally, data was plotted from the best
model.
All statistics, including G-test, Spearman’s
rank correlation and OLS regression analyses
were performed using the STATVIEW 512+
Macintosh statistical package. The graphs were
created using a Macintosh package (Cricket
Graph III).
RESULTS
SPECIES-RANGE-SIZE DISTRIBUTIONS
The Tokeshi test for modality shows a strong left
unimodal distribution of species for the several
groups of arthropods analysed ( pl < 0.001 and
pr n.s.; Fig. 1). However there are differences
within each of these arthropod subsets. Spiders,
chewers and predatory insects showed
particularly interesting range size distributions.
Almost half of the 50 species of Araneae
occurred at only one site, giving the highest skew
and kurtosis values in comparison with the other
groups of species studied. This is due to the
presence of very rare endemic species and
because a high proportion of the species can be
considered as vagrants, occurring only in one of
the sampling periods with very low abundance.
Chewers and predatory insects showed an inverse
pattern with a high proportion of the species
having a wide range. This is due to the broad
distribution of most species of moths, carabids,
staphylinids and chrysomelids, which tend to
occur in three or more sites. Most of them are
polyphagous herbivores (noctuid moth larvae)
and polyphagous predators (carabids and
staphylinids) with high vagility and colonization
abilities. The smallest values of skew and kurtosis
obtained for chewers and predatory insects mean
not only that those groups are more widely
distributed but also that the proportion of species
in each range size category is more similar.
RANGE SIZE AND HERBIVORE DIET BREADTH
Table 1 shows the distribution of the number of
species in each diet category throughout three
range size categories. In the suckers, lumping the
species into specialists and generalist, the
distribution is contrary to the theoretical
expectation, since a high proportion of specialist
species have a wide range, while a large
proportion of the generalists occupy few sites
(G = 5.638, d.f. = 1, p = 0.02).
Table 1. Distribution of the number of herbivore species in each diet category throughout 3 range size categories.
Specialists
Range size
a) Suckers
1 to 4
5 to 8
9 to 12
b) Chewers
1 to 4
5 to 8
9 to 12
34
Generalists
Genus and species monophage
Family monophage
Oligophage
Polyphage
1
0
0
13
7
4
14
3
2
13
0
0
5
0
0
6
3
2
4
3
0
19
6
6
THE MAJOR TAXA GROUPS
a) All arthropods (n=237)
0.3
0.
0.2
s=2.33
k=6.35
0.
0.1
0.
0.3
b) All insects (n=172)
s=1.96
k=4.54
0.2
c) All non-insects (n=65)
0.4
s=2.86
k=8.96
0.3
0.2
0.1
0.1
0.0
0
0
Proportion of species
1 2
HERBIVORES
d) All species (n=128)
0.3
0.3
0.2
0.4
s=2.00
k=4.71
0.2
0.1
0
e) Suckers (n=63)
0.25
s=2.42
k=7.02
0.3
0.2
0.1
0.0
PREDATORS
g) All species (n=117)
0.3
0.
0
s=2.52
k=7.37
0.2
0.
0.1
0.
0.0
0
h) Spiders (n=50)
0.4
0.25
s=3.00
k=9.66
0.3
2 3 4 5 6 7 8 9 10 11 12
0.2
i) Insects (n=58)
s=1.46
k=2.79
0.15
0.2
0.1
0.1
0.05
0
1
1 2 3 4 5 6 7 8 9 10 11 12
1 2 3 4 5 6 7 8 9 10 11 12
0.5
s=1.31
k=0.86
0.2
0.15
0.05
0
1 2 3 4 5 6 7 8 9 10 11 12
f) Chewers (n=65)
0.1
0.1
0
1 2 3 4 5 6 7 8 9 10 11 12
1 2 3 4 5 6 7 8 9 10 11 12
3 4 5 6 7 8 9 10 11 12
0
1 2 3 4 5 6 7 8 9 10 11 12
1 2 3 4 5 6 7 8 9 10 11 12
Field sites
Fig. 1. Frequency histograms showing the proportion of species of several groups of arthropods
occupying the 12 field sites; "n" gives the number of species. Values of skewness (s) and kurtosis (k)
are given for each frequency distribution (see also text).
For chewers, there is no significant pattern in the
distribution of the specialist-generalist species
among the range size categories (G = 0.331, d.f. =
1, n.s.). All the sucker and chewer species of
species/genus monophages consistently occurred
in less than five sites, but there are few species
and they are mainly restricted, so this distribution
may not differ from random expectation (Table
1a) and b).
RANGE SIZE AND LOCAL ABUNDANCE
As Table 2 and Figure 2 show, for arthropods,
there is a clear positive relationship between the
range size of a species and its local abundance.
Wide-ranging species tend to be, on average,
more abundant locally, while narrowly distributed
species tend to have low densities where they
occur. The log-linear model explained slightly
more variance than the log-log model for all
arthropods and herbivores (Table 2). In the
predators and spiders, the fit of the log-log and
log-linear models was very similar, but slightly
better in the former. For arthropods (Fig. 2) the
range of the r2’s is 0.39 - 0.48 (Table 2), with the
best fit for spiders (Table 2; see also Fig. 2d).
Within each model, the slopes of the arthropods
curves look very similar (pairwise t-tests for the
differences between these slopes showed that
none is significant), suggesting that there is no
difference in the way that the species’ local
abundance scales with distribution in the four
groups of species studied.
35
Table 2. Statistics for linear regressions between abundance and range size distribution in the Summer 1994 for all
arthropods, herbivores, all predators and spiders. The higher r2 values are in bold; “n” gives the number of species;
**p < 0.001; *** p < 0.0001.
2
Regression type
Equation
All arthropods (n = 96)
log-untransformed model
log-log model
log y = -1.06+0.094x
log y = -1.07+0.86 log x
0.41
0.38
64.93***
58.06***
Herbivores (n = 50)
log-untransformed model
Log-log model
log y = -1.098+0.112x
log y = -1.108+1.02 log x
0.46
0.42
41.26***
34.43***
All predators (n = 50)
log-untransformed model
log-log model
log y = -1.043+0.079x
log y = -1.106+0.73 log x
0.37
0.39
28.50***
30.38***
Spiders (n = 22)
log-untransformed model
log-log model
log y = 1.013+0.082x
log y = -0.99+0.74 log x
0.48
0.48
18.47**
18.76**
a) All arthropods (n=96)
Log (geometric mean abundance within occupied sites)
2
2
1
1
0
0
-1
-1
r
F
b) Herbivores (n=50)
-2
-2
0 1 2 3 4 5 6 7 8 9 10 11 12
0 1 2 3 4 5 6 7 8 9 10 11 12
Number of sites occupied
c) All predators (n=50)
1
d) Spiders (n=22)
0.5
0
0
-0.5
-1
-1
-1.5
-2
0
0.5
1
1.5
0
0.5
1
1.5
Log (number of sites occupied)
Fig. 2. Relationship between the logarithm of the geometric mean abundance within occupied
sites and the number of sites occupied for a) all arthropods, b) herbivores, and the logarithm of the
geometric mean abundance within occupied sites and the logarithm of the number of sites
occupied for c) predators and d) spiders, in the Summer 1994. Note, several data points overlie
one another. Statistics are presented in Table 2; “n” gives the number of species.
36
Moreover, in the arthropods, there are no
differences in the average abundance of species
within each group (geometric mean of mean
species abundances: all species = 0.21; herbivores
= 0.22; predators = 0.19; spiders = 0.22).
Of course, there are some outliers. Some
species occur in only a small proportion of sites,
but are very abundant where they occur. This is
the case for certain introduced species that occur
in only some sites in the pastureland (e.g. the
linyphiid spiders Erigone atra and Oedothorax
fuscus). However, there are no cases of species
occurring in only one site and being locally
abundant. Moreover, all species that are
widespread (occurring in 11 and 12 field sites of a
maximum of 12) are locally abundant.
DISCUSSION
The present study considers patterns in regional
occurrences of arthropod species (see also Borges
& Brown 2001, 2004) rather than the entire
geographic range of species (a more
biogeographic approach). Therefore, this work
covers only part of the geographic range of the
species ("partial analyses" sensu Gaston &
Blackburn 1996), as range size was measured in
terms of number of sites occupied by each
species.
The general result was a "hollow curve",
repeated for several taxonomic and ecological
(e.g. feeding groups) functional groups. The
bimodal pattern was tested statistically and the
right-hand mode was clearly not statistically
significant. Narrowly distributed arthropod
species are mainly endemic and tourist (or
vagrant) species (note that some endemics can
also be considered as tourists in the studied
habitats). Moreover, for both endemics and
tourists, local density is generally low (Gaston
1994a), a rule that was also confirmed in the
present study. The low densities of endemics are
probably due to a lack of adaptation to pasture
management. However, some endemic species
are persistent throughout the sampling periods,
and some were indicator species of pasture
communities (see Borges 1999). Nevertheless,
endemic species are doubly at risk of extinction,
because occupy few sites and attain low densities
where occur (Lawton 1993). However, the real
range of those species is larger than obtained in
the present study (see Borges et al. in press), and
therefore the current results may be a
consequence of a pasture being a sink habitat.
This is probably true for the tourist species, a
large group of species which are either habitat
generalists (occupy several habitats in the islands)
(e.g. some millipedes, moths, spiders and beetles)
or habitat specialists (e.g. Olisthopus inclavatus
and Tarphius depressus endemic forest dwellers)
that accidentally colonize pastureland. For
endemic species, at least in Santa Maria, the
pastureland seems to be an alternative habitat as a
result of the virtual absence of true natural areas
(see Borges et al. 2005). Hence, the observed
range probably accurately reflects their actual
range. That is, those species genuinely occupy
few sites at low densities. Concerning the tourist
species, there are difficulties in correctly
identifying them without having a total picture of
their distribution in all the available habitats in
the studied islands (but see Borges et al. in press,
for a complete picture for Terceira Island). Their
dynamics as "sink species" (Shmida & Wilson
1985) greatly increases the number of rare species
in the community, which creates an artefactual
increase in the left-hand mode of the frequency
distributions of species (Gaston 1994b).
Species with wider distributions are
predominantly habitat generalists, namely a)
species with wide environmental tolerance, or b)
species with high dispersal capacities (Brown
1984; Hanski et al. 1993; Lawton 2000).
Considering habitat generalists, most species
were also found to be abundant in both sown and
semi-natural pastures, but there are exceptions.
For instance, the endemic lycosid spider Pardosa
acoreensis occurs in all the 12 sites but is mainly
abundant in the semi-natural sites of Santa Maria
and Pico ("source populations" sensu Shmida &
Wilson 1985). Moreover, most of the
species/genus monophage herbivores occur in a
few sites, where they are never abundant. This
result supports the "resource usage theory"
(Brown 1984, 1995), but cannot rule out the 5th
(resource availability) and 6th (habitat selection)
models of Gaston et al. (1997), i.e. how generalist
would a species have to be in these habitats to
occupy all?; a) Species with wide environmental
37
tolerance: in accordance with the positive
relationships found between range size and local
abundance, arthropod species that are spatially
ubiquitous (occur in 10-12 sites) must be highly
tolerant to a wide array of environmental
conditions. Such species also conform to the
predictions of the "resource usage theory", being
the generalist or broad-niched species of Brown
(1984, 1995); b) Species with high dispersal
capacities: most of the widespread and abundant
predator species in these pasture communities are
linyphiid spiders and staphylinids known for their
good dispersal capacities. In the herbivores,
dominant species are flying insects (e.g.
leafhoppers, aphids and moths) also having good
dispersal abilities.
The higher r2 obtained for the spiders in the
range size/abundance relationship (Fig. 2d) is a
consequence of the fact that spiders are a more
closely related ecological group of species than
the predator or herbivore assemblages (Brown
1984; Gaston 1994a). In fact, within the spider
assemblage, there are only two main ways of
using resources, the "web-building way" and the
"wandering way". The predator assemblage, as it
was designed in the present study, includes the
spider foraging strategies mentioned above and
also the feeding behaviours of centipedes,
ground-beetles and rove-beetles. The herbivore
assemblage includes sucker and chewer species
and within these two main groups there are
different ways of using resources (e.g. rootfeeders, leaf-feeders, xylem sap feeders, phloem
sap feeders, pollen feeders, etc.). However, the
fact that the correlation obtained with the
predators was the weakest of the four computed
correlations for the arthropods may reflect a
sampling artefact, since estimates of abundance
were based on a suction method (Vortis machine)
that is not suitable for the larger predatory species
(e.g. centipedes, night-dwelling ground-beetles
and rove-beetles, and larger spiders). However,
the inclusion of pitfall data implies the inclusion
of additional errors for the herbivorous functional
groups and was not considered (see Methods).
Gaston et al. (1997) proposed eight
mechanisms that govern the positive relationship
between abundance and range size (see also
Introduction). Metapopulation models assume
that distance between patches (or sites) should be
38
small enough in order for all species to move
between them (see also Gaston 1994a). This
condition is not fulfilled in the case of oceanic
islands separated by sea, where over-water
dispersal is very low. Moreover, this study was
not designed to test the phylogenetic nonindependence, range position, habitat selection
and vital rate models, and will not be further
considered. As previously suggested in this
manuscript, the "resource usage model" fits very
well with the characteristics of the species/genus
monophage herbivores and wide ranging species.
Brown’s (1984) model also predicts that
“consumers” (e.g. predators) should use the
environment on a larger spatial scale with lower
densities but wider distributions than “producers”
(e.g. herbivores). Despite the fact that on average
the widespread herbivores are more abundant
than the widespread predators (geometric mean of
the mean abundances of the species that occur in
eight or more sites: herbivores = 1.31 m-2;
predators = 0.51 m-2), which conforms with the
model, when the slopes of curves are compared,
there was no evidence to suggest that the
predators have a wider distribution than the
herbivores. Moreover, looking for Figures 1d)
and 1g), and for the skew and kurtosis values
therein, contrary to the prediction, herbivore
species are more widely distributed than the
predators. However, this is largely a consequence
of the spider distribution pattern, since the
predatory insects showed very low values of
skewness and kurtosis and therefore some
tendency for wider distributions. As a great
proportion of the spiders can be considered tourist
species, probably Brown’s (1984) predictions are
best applied to the arthropod community under
study.
As mentioned above, the slopes of the
regression lines relating abundance to range size
were very similar for the different assemblages of
species. This is a very important result (Gregory
& Gaston 2000). Since the slope of the regression
line relating distribution to abundance increases
as the number of resources per locality increases
(Maurer 1990), the similar slopes obtained for the
several assemblages of species may imply a tight
connection between the different trophic groups.
The unexpected result obtained with the sucker
species (viz. a high proportion of specialist
species have a wide range, while a large
proportion of the generalists occupy few sites),
may be explained because a great proportion of
the sucker species are family monophages
adapted to feed on Leguminosae and perennial
grasses common throughout all the measured
range. Hence, patterns in the distribution of the
lower trophic level are constraining the
distribution of herbivore sucker species. On the
other hand, the reason why a large proportion of
the generalist sucker species occupy few sites
may be related to the fact they need a variety of
resources not available in all the measurable
range, or they are recent introduced species and
therefore, they have a more limited distribution
(Gaston 1994a). This conforms with the “resource
availability model” (Gaston et al. 1997), that is,
attainment of higher local abundances and wider
distributions by species with greater resource
availability.
CONCLUDING REMARKS
With this study it is clear that even in humanaltered habitats two commonly ecological
patterns are found for arthropods: i) narrowly
distributed species dominate and very few species
are widespread, and this was repeated for several
taxonomic and ecological (e.g. feeding groups)
functional groups; ii) there is a positive
relationship between mean abundance and the
distribution of species. Moreover, the slopes of
the regression lines relating abundance to range
size were very similar for the different
assemblages of species, which supports the
“resource availability model”.
These results call attention for the fact that
arthropod communities in the Azorean pastures
are well structured and that in spite of most
species being exotic, the communities are
commonly dominated by rare species and the few
widespread species attain high local densities.
We suggest that more work needs to be
conducted in order to evaluate the relationship
between arthropod diet breadth, habitat
specialization and range size in the islands in
several types of habitats.
ACKNOWLEDGEMENTS
I wish to thank Prof. Valerie K. Brown for her
friendship and extreme dedication on the
supervision of my Ph.D. Project (1003-1997).
The arthropod morphospecies were identified by
several taxonomists who also gave valuable
advice on the feeding habits, colonization status
and geographical distribution of each species:
Diplopoda (Prof. H. Enghoff, Zoologisk Museum,
University
of
Copenhagen,
Denmark);
Heteroptera (J. Hollier, Glebe, U.K.; J. Ribes,
Barcelona, Spain); Homoptera-Auchenorrhyncha
(J. Hollier, Glebe, U.K.; Prof. J.A. Quartau,
“Faculdade de Ciências de Lisboa”, Portugal);
Coccoidea (Dr. G. Watson, International Institute
of Entomology, London, U.K.); Aphididae
(Prof. F. Ilharco, “Estação Agronómica
Nacional”, Portugal; Dr. R. Blackman, The
Natural History Museum, London, U.K.);
Thysanoptera (Dr. G.J. du Heaume, International
Institute of Entomology, London, U.K.;
Prof. R. zur Strassen, “Forschungsinstitut und
Naturmuseum
Senckenberg”,
Frankfurt,
Germany); Lepidoptera (V. Vieira, “Departamento de Biologia da Universidade dos
Açores”, Portugal); Chrysomelidae (D. Erber,
Giessen-Lahn, Germany); Curculionidae (Dr. R.
Booth, International Institute of Entomology,
London, U.K.; Dr. A. Serrano, “Faculdade de
Ciências de Lisboa”, Portugal); Araneae
(J. Wunderlich, Straubenhardt, Germany); and
Neuroptera (Dr. V. J. Monserrat, “Universidad
Complutense de Madrid”, Spain). To all them our
sincere thanks.
This research was supported by JNICT (“Junta
Nacional
de
Investigação
Científica
e
Tecnológica”, Lisboa, Portugal) who gave
financial support to the author for the work at
Silwood Park in the form of a three year (October
1993 - September 1996) postgraduate grant
(Science Program - Ph.D Grant BD-2706-93RN). Special thanks are also due to the
“Secretaria Regional da Agricultura e Pescas”
(Azores), that provided financial support for all
field and laboratory work in the Azores. Finally,
the "Science Program" (JNICT) gave the financial
support necessary for the acquisition of two
VORTIS suction samplers.
39
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atlantica (Warren, 1905) has been determined and deposited in the NCBI GenBank under
the Accession number AY600452. Complete and partial COI sequences of other
Lepidoptera have been collected and used to reconstruct a phylogeny with both the
Neighbor-Joining and the Maximum Likelihood methods. A molecular clock calibrated for
our models indicate a divergence time between Noctua atlantica and Noctua pronuba of
4.7-5.9 Million years, consistent with the geological age of the Azores and suggesting that
the speciation process of N. atlantica occurred in this archipelago.
Key words: divergence, endemic, Neighbor-Joining tree, Noctua pronuba, sequences
Rafael Montiel (e-mail: montiel@uac.pt), V. Vieira, T. Martins, N. Simões & L. Oliveira.
Universidade dos Açores, Universidade dos Açores, Departamento de Biologia, CIRN, Rua
da Mãe de Deus, PT- 9501-801 Ponta Delgada, Açores, Portugal.
INTRODUCTION
The Azorean archipelago consists of nine
volcanic islands of variable geological ages
ranging from 0.037 to 8.12 million years (Queiroz
1990). It is situated in the Atlantic Ocean at 1500
km from mainland Portugal. These characteristics
make it very interesting model systems to study
colonization, radiation and even speciation
process of invertebrate and vertebrate taxa. In the
Azores there have been identified 38 Lepidoptera
endemic species, eight of which are Noctuidae
(Karsholt & Vieira 2005).
Noctua atlantica (Warren, 1905) is an endemic
species of Azores (Warren 1905; Meyer 1991;
Vieira & Silva 1994; Hacker & Schmitz 1996;
Vieira 1997) that inhabit all the Azores islands,
excepting Santa Maria Island (Carvalho et al.
1999; Karsholt & Vieira 2005). It is found in
natural ecosystems of “Laurisilva” (ancient native
evergreen forest found in Macaronesia) (Oliveira
et al. 2004) and has been catalogued as an
endangered species, affected mainly by the
specificity of its habitat. On the other hand,
N. pronuba (Linnaeus, 1758), of palaearctic
origin and also found in the Azores, has a less
specific habitat and a more diverse geographic
distribution. Noctua atlantica is morphologically
very similar to N. pronuba, having a smaller
wingspan and wings with a less shining color
(Carvalho et al. 1999). Thus, it is very interesting
to analyze the genetic relationship of these two
species in the context of lepidopteran genetic
variability to address evolutionary hypotheses and
to help in developing conservation planning.
Sequences from the cytochrome c oxidase
subunit I (COI) have been used to address
phylogenetic problems at a wide range of
hierarchical levels, from species to orders
(Caterino & Sperling 1999). Hebert et al. (2003a)
43
proposed that a DNA barcoding system for
animal life could be based upon sequence
diversity in COI and have applied this method to
lepidopterians successfully (Hebert et al. 2003a;
2003b; although see also Will & Rubinoff 2004).
Furthermore, Gaunt & Miles (2002) found that
the COI is better suited to conduct studies based
on the molecular clock assumption than other
gene sequences, such as 16S, 18S, cytochrome b
(cob) or elongation factor 1α (EF-1α). The
molecular clock hypothesis is the basis of the
modern molecular phylogenetic approach for
dating and resolving evolutionary divergence
(Gaunt & Miles 2002).
This is the first report on a DNA sequence of
N. atlantica. We present its complete COI gene
sequence that is compared with COI sequences of
other lepidoptereans, including N. pronuba. Also,
by calibrating a molecular clock, we determine an
approximate time of divergence for these species
and its relationship with the geological history of
the archipelago. This represent a first step to
develop studies aimed to understand how does
genetic variation in N. atlantica compare with
levels observed in other non-endemic Azorean
lepidoptera.
MATERIAL AND METHODS
Noctua atlantica specimens were collected at
Monte Escuro (800 m altitude) in São Miguel
Island. Specimens were reproduced in laboratory
and a 3rd-instar larva (from first generation) was
selected for analysis.
For DNA extraction, larva was grinded under
liquid nitrogen, re-suspended in 500 µl of
digestion buffer (100 mM Tris HCl pH 8.0, 80
mM EDTA, 1% SDS, 160 mM sucrose) and
digested overnight at 37 ºC with 25 µg proteinase
K. After centrifugation, the supernatant was
extracted once with phenol:chloroform:isoamyl
alcohol
(25:24:1)
and
once
with
chloroform:isoamyl alcohol (24:1). DNA was
ethanol precipitated and re-suspended in 100 µl
of H20.
Conserved primers TY-J-1460 and TL2-N3014 (Simon et al. 1994) were used to PCR
amplify a segment between genes for tRNA-Tyr
44
and tRNA-Leu encompassing the complete gene
for the mitochondrial cytochrome oxidase I
(COI). The amplified fragment was cloned into a
TOPO-TA vector (Invitrogen) and three clones
were selected for direct sequencing. Universal
primers T3 and T7 were used for ends
sequencing, and primers NaCOXI-F104 (5'ATTTTTGGAATTTGAGCTGG-3') and NaCOXIR777 (5'-ATATAAACTTCTGGATGACC-3') were
used for internal sequencing.
Fifteen COI sequences from species
representing 4 Lepidopterean families, taken from
the NCBI GenBank, were used for comparison
(Table 1). For some species (as N. pronuba) the
complete COI sequence was not available. For
these reason our alignment was limited to 615 pb
of the 5’ end. Ten out of these 15 sequences were
from Noctuidae (seven Noctuinae). Sequences
were aligned with Clustal W (Thompson et al.
1994) and used to construct Maximum
Likelihood (ML) trees with Treepuzzle (Schmidt
et al., 2002) and Neighbor-Joining trees using the
Tamura-Nei gamma distance with Mega2 (Kumar
et al. 2001). Treepuzzle was used to estimate the
gamma parameter alpha. The standard errors for
the Tamura-Nei distances were estimated
analytically, and for the ML distances they were
derived from the standard errors of the ML
branch lengths. The robustness of the resulting
trees was assessed by bootstrapping (1000
resamplings) and by quartet puzzling (10,000
puzzling steps) for the Neighbor-Joining and ML
trees, respectively. The divergence time between
Tegeticula synthetica and T. yuccasella (32.4
My), estimated from COI sequence data by Gaunt
& Miles (2002), was used to calibrate the
molecular clock for our data.
RESULTS
After remove the primer sequences, we obtained
1579 base pairs (bp) of good quality sequence
(without ambiguities) from the three clones
analyzed. Blast search (Altschul et al. 1997) at the
NCBI GenBank allowed us to identify the
complete gene for the cytochrome c oxidase
subunit I (COI) of Noctua atlantica, from
position 11 to 1555 and comprising 1545 bp. The
Table 1. COI sequences used in this study. a NCBI GenBank. b Economically important
c
pest according to Zhang (1994). Present in the Azores archipelago.
Acession No.
Taxa
a
Pest
b
Distribution
Family NOCTUIDAE
Subfamily Noctuinae
Agrotis ipsilon
Agrotis volubili
c
Anaplectoides prasina
Feltia jaculifera
Feltia tricosa
Noctua atlantica
yes
Cosmopolitan
yes
Nearctic
AF549765
U60990
AF549766
yes
yes
no
Palaearctic
Nearctic
Nearctic
c
AY600452
no
Azores (endemic)
c
AF549752
yes
Palaearctic
AF549755
AJ420361
AJ420369
yes
yes
no
Nearctic
Palaearctic
Palaearctic
Noctua pronuba
Subfamily Plusiinae
Allagrapha aerea
Diachrysia chrysitis
Diachrysia tutti
Family NYMPHALIDAE
Subfamily Nymphalinae
Nymphalis californica
Vanessa cardui
AF549736
AF549702
c
Vanessa virginiensis
Family HESPERIIDAE
Subfamily Pyrginae
Pyrgus communis
c
Family PRODOXIDAE
Tegeticula sintetica
Tegeticula yuccasella
AY248789
yes
Nearctic
AY248782
yes
Cosmopolitan
AY248783
no
Nearctic
AF170857
no
Nearctic
AY327144
AY488835
no
no
Nearctic
Nearctic
10 bp located upstream correspond to the 3’ end
of the gene for tRNA-Tyr and the 24 bp
downstream comprise the 5’ end of the tRNALeu gene. The COI start codon is ATA and the
stop codon is TAA. As expected for insect
mitochondrial genomes this gene has a high A+T
content (73.07%). The N. atlantica sequence data
has been deposited in the NCBI GenBank, under
the Accession number AY600452.
We estimated Tamura-Nei and ML distances
from the sequences used for comparison (Table 2,
see the end of manuscript). Figure 1 shows the
unrooted Neighbor-Joining tree obtained from the
Tamura-Nei distances.
DISCUSSION
We have shown that Noctua pronuba is the
closest species to N. atlantica, showing little
divergence between them (Fig. 1). Assuming that
the genetic distances observed between T.
synthetica and T. yuccasella, were produced in
32.4 My, the divergence time between Noctua
atlantica and N. pronuba is 4.9 (± 2.1) My for the
45
Agrotis ipsilon
0.048 0.142 0.081 0.149 0.137 0.092 0.083 0.090
0.099 0.177 0.213 0.347 0.284 0.203 0.197
0.146 0.080 0.150 0.141 0.081 0.077 0.083
0.089 0.202 0.198 0.311 0.311 0.189 0.208
0.125 0.098 0.097 0.149 0.147 0.144
0.155 0.220 0.247 0.358 0.325 0.216 0.206
0.134 0.123 0.092 0.093 0.056
0.064 0.204 0.206 0.358 0.296 0.195 0.201
0.008 0.167 0.161 0.148
0.153 0.212 0.249 0.319 0.300 0.231 0.204
Agrotis volubilis
0.055
Allagrapha aerea
0.160 0.148
Anaplectoides prasina
0.116 0.091 0.141
Diachrysia chrysitis
0.160 0.147 0.104 0.138
Diachrysia tutti
0.151 0.141 0.107 0.130 0.009
Feltia jaculifera
0.100 0.083 0.151 0.098 0.167 0.155
Feltia tricosa
0.094 0.082 0.153 0.108 0.159 0.147 0.036
Noctua atlantica
0.106 0.087 0.157 0.064 0.148 0.142 0.129 0.126
Noctua pronuba
0.125 0.097 0.178 0.078 0.156 0.149 0.146 0.143 0.014 a
Nymphalis californica
0.196 0.204 0.251 0.230 0.220 0.213 0.207 0.171 0.203
0.156 0.148 0.140
0.145 0.202 0.241 0.299 0.277 0.218 0.193
0.031 0.124
0.134 0.198 0.234 0.365 0.331 0.204 0.221
0.116
0.125 0.169 0.208 0.319 0.297 0.198 0.211
0.013 b 0.196 0.187 0.304 0.280 0.207 0.219
0.198 0.209 0.311 0.295 0.223 0.239
0.207
0.239 0.309 0.289 0.135 0.137
Pyrgus communis
0.244 0.201 0.276 0.228 0.254 0.252 0.248 0.217 0.203
0.237 0.281
Tegeticula synthetica
0.398 0.325 0.392 0.440 0.341 0.326 0.405 0.340 0.320
0.335 0.314 0.317
Tegeticula yuccasella
0.305 0.315 0.361 0.328 0.324 0.301 0.342 0.303 0.288
0.316 0.300 0.274 0.093
0.286 0.261 0.225 0.213
0.076 0.375 0.366
0.341 0.343
Vanessa cardui
0.230 0.208 0.242 0.218 0.231 0.223 0.218 0.216 0.225
0.259 0.164 0.246 0.450 0.356
Vanessa virginiensis
0.208 0.216 0.225 0.221 0.203 0.196 0.229 0.221 0.233
0.274 0.160 0.231 0.425 0.357 0.065
Tamura-Nei distance, and 5.5 (± 3) My for the
ML distance. In order to confirm this result we
estimated, using the same methods, the distances
between Pachliopta neptunus and Papilio
garamas (data not shown), with an estimated
divergence time of 89.1 My (Gaunt & Miles
2002). Using this data we obtained divergence
times for N. atlantica and N. pronuba of 5.1 (± 2)
My and 5.7 (± 3.2) My for the Tamura-Nei and
ML distances, respectively.
These divergence times were obtained using
the most conservative estimations reported by
Gaunt & Miles (2002), and therefore can be
considered to be near to the upper limit. Also it
must be considered that the gene divergence
usually predates species divergence (Nei 1987;
Nichols 2001). Thus, our estimations are
consistent with the Azorean origin of N. atlantica.
The divergence coincides with the geological age
46
V. virginiensis
V. cardui
T. yuccasella
T. synthetica
P. communis
N. californica
N. pronuba
N. atlantica
F. tricosa
F. jaculifera
D. tutti
D. chrysitis
A. prasina
A. aerea
A. volubilis
A. ipsilon
Table 2. Neighbor-Joining gamma distances (below diagonal) and Maximum Likelihood distances (above)
a
b
estimated from COI sequences; Standard error = 0.006; Standard error = 0.007.
0.056
of the Azorean archipelago either occurring just
after formation of the first Island (Santa Maria) or
subsequently, following the conformation of the
archipelago due to volcanic phenomena. Even,
the speciation could be related to the appearing of
São Miguel, that occurred 4.01 My ago (Queiroz
1990).
An alternative hypothesis could be that N.
atlantica occupied a broad geographical range in
ancient times and ultimately become confined to
the Azores due to ecological changes and niche
reduction. This hypothesis could be supported if
N. atlantica arose as species before the formation
of the Azores archipelago, however, if these
hypothetical climatic changes occurred more
recently, this alternative hypothesis could also be
consistent with a recent speciation of N. atlantica.
In this study we analyzed the divergence between
N. atlantica and N. pronuba, however, further
Fig. 1. Unrooted Neighbor-Joining tree constructed from Tamura-Nei gamma distances
(alpha parameter = 0.23). The tree topology was identical for the ML tree. Numbers in
branches are bootstrap (and quartet puzzling) support values.
insights into the age of these species could be
obtained from the analysis of other Noctua
species from Macaronesia, like N. carvalhoi (also
an Azorean endemic species), N. teixeirai
(endemic in Madeira), and N. noacki (endemic in
Canary islands), and comparing their genetic
distances relatively to N. pronuba, since this
widely distributed species could be the ancestor
of all the endemic Noctua species from
Macaronesia. Also intra-specific variability in
these species should be assessed.
ACKNOWLEDGEMENTS
Rafael Montiel received a postdoctoral fellowship
from the Fundação para a Ciência e a Tecnologia,
Portugal (SFRH/BPD/13256/2003).
47
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Martins, L. Silva and V. Vieira (Eds.). A list of the
terrestrial fauna (Mollusca and Arthropoda) and
flora
(Bryophyta,
Pteridophyta
and
Spermatophyta) from the Azores.. Direcção
Regional de Ambiente e do Mar dos Açores and
Universidade dos Açores, Horta, Angra do
Heroísmo and Ponta Delgada. 318 pp.
Kumar, S., K. Tamura, I. Jakobsen & M. Nei 2001.
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Tempe, Arizona, USA.
Meyer, M. 1991: Les Lépidoptères de la region
macaronésienne. II-Liste des Macro-Hétérocères
observes en juillet-août 1990 aux Açores
(Lepidoptera:
Geometridae,
Sphingidae,
Noctuidae). Linneana Belgica 13: 117-134.
[Lepidoptera from the Macaronesia region; in
French]
48
Nei, M. 1987. Molecular Evolutionary Genetics.
Columbia University Press, New York. 512 pp.
Nichols, R. 2001. Gene trees and species trees are not
the same. Trends in Ecology and Evolution 16:
358-364.
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of temperature on the biology of Noctua atlantica
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423-426.
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Accepted 5 November 2008.
Acoetidae (Annelida, Polychaeta) from the Iberian
Peninsula, Madeira and Canary islands, with description
of a new species
ANA M. PALMERO, A. MARTÍNEZ, M.C. BRITO & J. NÚÑEZ
Palmero, A.M., A. Martínez, M.C. Brito & J. Núñez 2008. Acoetidae (Annelida,
Polychaeta) from the Iberian Peninsula, Madeira and Canary islands, with
description of a new species. Arquipélago. Life and Marine Sciences 25: 49-62.
Six species of acoetid polychaetes are reported from the Iberian Peninsula and
Macaronesia: Euarche tubifex Ehlers, 1887, Euarche cristata Núñez, n. sp., Eupanthalis
kinbergi McIntosh, 1876, Eupolyodontes gulo (Grube, 1855), Polyodontes maxillosus
(Ranzani, 1817), and Panthalis oerstedi (Kinberg, 1856). Material was collected during
several sublittoral benthic surveys. Descriptions, figures, and a key for the six species are
included. The new species Euarche cristata is characterized by its prostomium with cristate
or serrated posterior margin.
Key words: Euarche cristata, Macaronesia, identification key, northeast Atlantic, sublittoral
Ana María Palmero (e-mail:anitapalmero@gmail.com), Alejandro Martínez, María del
Carmen Brito & Jorge Núñez, Laboratorio de Bentos, Departamento de Biología Animal
(Zoología), Facultad de Biología, Universidad de La Laguna. ES-38206 La Laguna,
Tenerife, Islas Canarias, Spain.
INTRODUCTION
Acoetidae is a widespread family of marine
scaleworms, with 9 genera and 43 species
described (Hutchings 2000). Members of this
family usually occur in soft sediments in selfmade permanent tubes built by specialized
notopodial spinning glands. Mucous and fibrous
secretions are mixed with sediment and sand
debris to make a tube. They are carnivorous ‘sitand-wait’ predators, not leaving their tubes more
than partially when they feed. The family was
revised by Pettibone (1989), who renamed it from
Polyodontidae Augener, 1918, a family name
already used for fishes. Other important revisions
from the Mediterranean Sea are Ben-Eliahu and
Fiege (1994), Barnich and Fiege (2003). Campoy
(1982) recorded three species from the Iberian
Peninsula: Euarche tubifex Ehlers, 1887 [non
Eupanthalis kinbergi McIntosh, 1876 sensu
Pettibone, 1989], Panthalis oerstedi Kinberg,
1856 and Polyodontes maxillosus (Ranzani,
1817). Four species were previously recorded
from the Canary islands: Euarche tubifex,
Eupanthalis kinbergi, Eupolyodontes gulo, and
Polyodontes maxillosus (Núñez et al. 2005;
Martínez et al. 2007).
Generally, acoetids are quite rare in benthic
samples, hence the low number of publications on
the family. On account of their life strategy, they
are mainly taken by dredging and most of them
are known only from fragments. Despite of being
widely distributed and present in the low
intertidal zone, acoetids are more abundant from
moderate depths down to 1500 m (Pettibone
1989). This also explains the lack of knowledge
about their life cycles and ecology.
In the present paper, recently collected material
from Madeira, Canaries and the Iberian Peninsula
is investigated; it comprises six species, of which
one is new to science i.e. Euarche tubifex,
Euarche cristata n. sp., Eupanthalis kinbergi,
49
Eupolyodontes gulo, Panthalis oerstedi and
Polyodontes maxillosus.
MATERIAL AND METHODS
The material was collected during several
sampling expeditions to the Iberian Peninsula and
the Macaronesian archipelagos of Madeira and
Canaries, between 1975 and 2003. The specimens
from the Iberian Peninsula were collected during
the Capbreton 1988 Cruise and the Fauna Ibérica
II Expedition 1991 Cruise to the Northern Iberian
Peninsula, using Marinovich and Bou de Varas
trawls. Material from the Macaronesia region was
collected during the Taliarte 9709-1997 Cruise to
South-Western Fuerteventura with trawl nets, and
during several biodiversity surveys to Lanzarote
in 2000 and 2001 with a Can-Foster dredge.
Specimens from Tenerife were collected in 1975,
1989 and 1991, associated with the deep coral
community of Dendrophyllia ramea, recovered as
by-catch of fishermen’s trammel nets and from
shallow soft bottom, using vacuum dredges.
Material from Madeira Island was collected
during a sampling expedition in 2003 with a van
Veen grab.
Samples were fixed with a solution of 10%
formaldehyde for 48 hours, and selected
specimens were subsequently preserved in 70%
alcohol for storing. Drawings of complete
specimens were made using a camera lucida
mounted on an Olympus SZX9 stereomicroscope.
Studied parapodia were mounted on a slide in
glycerine gel and drawn using a camera lucida on
a Leica DMLB microscope equipped with
Nomarski interference contrast optics. Scanning
electron microscope studies (SEM, Jeol JSM6300), were also made, after critical point drying
and gold sputtering the samples. All specimens
were deposited at the collection of the
Departamento de Biología Animal (Zoología),
Universidad de la Laguna (DBAULL).
SYSTEMATICS
Aphroditoidea Kinberg, 1856
Acoetidae Kinberg, 1856
50
Euarche tubifex Ehlers, 1887
(Fig. 1)
Euarche tubifex Ehlers, 1887: 54, pl. 12, figs. 1-7,
pl. 13, fig. 1; Pettibone 1989: 14, figs. 1-5; BenEliahu & Fiege 1994: 154, figs. 6-8e; Imajima
1997: 117, figs. 57-59; Barnich & Fiege 2003: 95,
fig. 49.
Eupanthalis sp. A, Wolf, 1984: 22-10, figs. 22-5,
22- 6.
Material examined: Fauna Ibérica II Expedition,
Ribadeo (Northern Spain), station 108, beginning
43º42'51''N - 6º59'30''W, ending 43º42'82''N 7º01'10''W, 125 m depth, muddy sand, 1 median
fragment, 75 mm length, 11 mm width.
Macaronesian Archipelago: Madeira, station
16/22, 32º38'07''N - 16º50'00''W, 75 m depth,
medium and fine sand, 1 specimen, 26 mm
length, 4 mm width. Canary islands: Lanzarote,
station 489, 28º54'22''N - 13º42'27''W, 48 m
depth, medium sand, 2 specimens, 23 and 20 mm
length, 3 and 2 mm width; station 766,
28º51'11''N - 13º48'33''W, 20-40 m depth, fine
sand, 1 specimen, 6 mm length, 1 mm width.
Description: Body long, dorsoventrally flattened,
yellow coloured with darker transversal bands on
dorsum of living specimens, in fixed specimens
pigmented bands less intense. Prostomium oval,
with two pairs of sessile eyes, anterior pair
slightly larger than posterior pair. Three antennae
smooth and tapering, lateral pair attached to
anterior margin of prostomium, shorter than
palps. Median antenna inserted posteriorly on
prostomium. Tapering papillate palps. Tentacular
segment with smooth, dorsal nuchal lobe and
paired tentaculophores lateral to protomium, each
with a bundle of capillary chaetae on
tentaculophores and a pair of smooth cirri (Fig.
1A). Anteriormost parapodia biramous with
numerous capillary notochaetae, the following
parapodia subbiramous with reduced notopodia
and without notochaetae. (Fig. 1B-C). Parapodia
of second chaetiger with first, largest pair of
elytra, overlapping prostomium, small notopodia,
larger neuropodia, and long ventral cirri. Elytra
translucent without lateral pouches, except for
Fig. 1. Euarche tubifex. A. Anterior end, dorsal view. B. Mid-body elytrigerous parapodium. C. Mid-body
cirrigerous parapodium. D. Spiked neurochaeta of the upper bundle. E. Distally spinous neurochaeta of the upper
bundle. F. Acicular neurochaeta of the middle bundle. G. Curved, spinous neurochaeta of the lower bundle.
Scale bar: A = 1 mm; B, C = 0.2 mm; D-G = 0.05 mm.
51
first pair, small, leaving middorsum uncovered.
Dorsal and ventral cirri smooth and tapering,
shorter than neurochaetae. Middle and posterior
parapodia with reduced achaetous notopodia and
spinning gland present from chaetiger 9.
Neuropodia well-developed, with neurochaetae
distributed in three bundles. Upper bundle with
two kinds of neurochaetae: short, capillary with
rows of strong spinules (spiked chaetae) (Fig.
1D), and long capillary chaetae, distally densely
spinous (Fig. 1E). Middle bundle with smooth
acicular chaetae, showing a thick and large,
hooked tip with subdistal hairs (Fig. 1F), and with
or without aristae. Lower bundle with numerous
curved, spinous chaetae (Fig. 1G).
Discussion: The examined specimens agree with
the descriptions given in Imajima (1997) for
Japan, and Barnich & Fiege (2003) for the
Mediterranean Sea. Regarding the chaetal types,
Barnich and Fiege do not describe acicular
aristate chaetae for E. tubifex, while according to
Imajima acicular chaetae are with or without
aristae. In our material, most acicular chaetae are
without and only some with aristae.
Distribution: Temperate and subtropical Atlantic
Ocean, from North Carolina to south Brazil in the
west, and Iberian Peninsula to West Africa in the
east, Mediterranean Sea, Arabian Sea and Japan.
Euarche cristata Núñez n. sp.
(Fig. 2)
Material examined: Madeira, station 17/18,
32º38'11''N - 16º48'92''W, 75 m depth, coarse
sand. Holotype (DBAULL- PO 17/18), 16 mm
length, 4 mm width.
Description: Holotype incomplete posteriorly,
with 33 segments. Body dorsoventrally flattened,
unpigmented, without marked bands; second
segment with small dorsal papillae. Prostomium
oval, with two pairs of sessile eyes, anterior pair
slightly larger than posterior pair. Two lateral
antennae on short ceratophores, styles tapering.
Posterior border of prostomium typically cristate
or serrated (Fig. 2A). Palps short, thick and
tapered, with regularly arranged five rows of long
filiform papillae. Tentacular segment indistinct
52
dorsally, paired tentaculophores lateral to
prostomium, each with a bundle of capillary
chaetae and a pair of tentacular cirri, dorsal and
ventral cirri subequal, longer and stouter than
antennae and shorter than palps. Elytra delicate,
transparent, first pair larger than following and
overlapping prostomium, following pairs rounded
to oval in outline, without ornamentation, not
overlapping middorsally. Segment two (buccal
segment) with first pair of elytrophores and small
notopodia with capillary notochaetae, larger
neuropodia and long ventral cirri. Parapodia of
segment three with dorsal cirri longer than
following, small notopodia with capillary
notochaetae, and larger neuropodia, ventral cirri
shorter than on segment two. From segment 9
subbiramous parapodia with reduced notopodia
without notochaetae (Fig. 2B, C) and spinning
glands with thread-like fibres. Neuropodia with
three bundles of chaetae: upper neurochaetae of
two types, short spiked chaetae (Fig. 2D) and
long distally spinous chaetae (Fig. 2E), middle
bundle consisting of 8-16 acicular chaetae with a
large, hooked tip with subdistal hairs (Fig. 2F);
lower bundle consisting of curved, spinous
chaetae (Fig. 2G). Pygidium and pharynx
unknown.
Discussion: Most of the species that belong to the
genus Euarche are characterized by a prostomium
with two pairs of sessile eyes, two lateral and one
median occipital antennae, a pair of papillate
palps,
tentaculophores
with
numerous
notochaetae, segments 2-8 with biramous
parapodia and four kinds of chaeta from segment
9: spiked chaetae, long distally spinous chaetae,
acicular chaetae with hooked tip with or without
distal arista, and curved, spinous chaetae. The
specimen described above is close to Euarche
tubifex, but differs in the presence of a
prostomium with cristate posterior margin the
absence of a median antennae, and the second
segment with small dorsal papillae, not present in
E. tubifex. Parapodial and chaetal characters do
not differ significantly from E. tubifex.
Distribution: Madeira Island.
Etymology: The species is named for its
characteristic cristate posterior margin of the
protomium, (Latin: crista = crest).
Type locality: Caniço Baixo, Madeira.
Fig. 2. Euarche cristata n. sp.; A. Anterior end, dorsal view. B. Mid-body elytrigerous parapodium. C. Mid-body
cirrigerous parapodium. D. Spiked neurochaeta of the upper bundle. E. Distally spinous neurochaeta of the upper
bundle. F. Acicular neurochaeta of the middle bundle. G. Curved, spinous chaeta of the lower bundle.
Scale bar: A = 1 mm; B, C = 0.2 mm; D, E, F, G = 0.05 mm.
Eupanthalis kinbergi McIntosh, 1876
(Figs. 3, 7A,B)
Eupanthalis kinbergi McIntosh, 1876: 404, pl. 72,
figs. 12-15; Pettibone 1989: 24, figs. 11b-j, 12 [in
part]; Barnich & Fiege 2003: 97, fig. 50;
Martínez, Palmero, Brito & Núñez 2007: 3, fig.1.
Eupanthalis glabra Ben-Eliahu & Fiege,
1994: 149, figs. 2-5.
Material examined: Madeira, station 16/21,
32º38'07''N - 16º50'00''W, 75 m depth, medium
and fine sand, 1 specimen, 6 mm length, 1 mm
width. Canary islands: Lanzarote, station 438,
dredge 29º04'72''N - 13º45'94''W, 42 m depth,
medium sand, 1 specimen, 23 mm length, 3 mm
width. Fuerteventura, station 37, starting
28º08'50''N - 14º33'60''W, 146 m depth, ending:
28º08'98''N - 14º34'38''W, 157 m depth, organic
53
sand, 1 specimen, 50 mm length, 4 mm width.
Description: Body long, flattened dorsoventrally,
pale pink translucent colouration, with an
irregular white band in each chaetiger before
fixation, darker in the prostomium. Prostomium
oval and slightly bilobed, with two pairs of sessile
eyes, anterior pair larger than posterior pair. A
pair of lateral antennae smooth and tapering on
anterior part of prostomium, shorter than palps.
Median antenna absent. Very long palps tapering
and smooth. Tentaculophores paired, achaetous
with a pair of smooth tentacular cirri each; a
small nuchal lobe (Fig. 3A). Parapodia
subbiramous from chaetiger 2 (Fig. 3B, C). Elytra
delicate and translucent, with lateral pouches
bigger from chaetiger 24. Dorsal and ventral cirri
short, smooth and tapering. Second chaetiger with
ventral cirri longer (buccal cirri) than the
following. Notopodia reduced and achaetous,
with spinning gland from chaetiger 9. Neuropodia
with aciculum and neurochaetae distributed in
three bundles. Upper bundle with two kinds of
chaetae: long and slender distally spinous chaetae
(Fig. 3F) and capillary, short, distinctly spiked
chaetae Middle bundle consisting of acicular
chaetae with subdistal hair and with a long distal
arista (Figs. 3D, 7A, 7B). Lower bundle with
curved, spinous chaetae, long and slender, with
well-developed spines, getting stronger basally.
Tube soft consisting of mucus with sand and
debris attached to a fibrous framework.
Distribution: Atlantic Ocean and Mediterranean
and Red Sea.
Eupolyodontes gulo (Grube, 1855)
(Figs. 4, 7D,F)
Polyodontes gulo Grube, 1855: 83, pl. 3, fig. 2.
Eupolyodontes gulo, Fiege & Barnich 1998: 83,
figs. 1-3; Barnich & Fiege 2003: 99, fig. 51.
Eupolyodontes cornishii, Pettibone 1989: 36, figs.
20-22; Ben-Eliahu & Fiege 1994: 155, figs. 7, 8
a-c.
Eupolyodontes mitsukurii, Pettibone 1989: 51;
Nishi 1996: 31, figs. 1-5.
Material examined: Tenerife (Canary islands),
54
28º20'16''N -16º21'30''W, 72 m depth, associated
with deep coral community of Dendrophyllia
ramea, 1 fragment, 80 mm length, 30 mm width.
Description: Body long, dorsoventrally flattened
and brown pigmented after fixation. Only median
fragment with 33 chaetigers studied. All
parapodia
subbiramous,
elytrigerous
and
cirrigerous (Fig. 4A-B). Elytra large, delicate and
translucent, with lateral pouches and arborescent
branched veins. Dorsal and ventral cirri smooth
and tapering, shorter than chaetigerous lobe.
Notopodia reduced and achaetous, with a number
of dorsal and lateral digitiform branchial papillae
and conspicuous spinning gland. Upper bundle of
neurosetae with double brush-shaped, long and
slender neurochaetae (pseudopenicillate; Fig. 4C)
and short spiked chaetae. Middle bundle with
smooth acicular chaetae, with few hairs
subdistally (Figs. 4D, 7D). Lower bundle with
numerous curved, spinous chaetae (Figs. 4E, 7F).
Discussion: The chaetal and parapodial characters
agree with the description of Pettibone (1989) of
Eupolyodontes cornishii Buchanan, 1894, a junior
synonym of E. gulo, and of Barnich & Fiege
(2003). The species is characterized by knob-like
or digitiform parapodial branchiae from segment
9, and pseudopenicillate neurochaetae in the
upper bundle.
Distribution: East Atlantic, Mediterranean Sea,
Red Sea, New Caledonia and Japan.
Panthalis oerstedi Kinberg, 1856
(Fig. 5)
Panthalis oerstedi Kinberg, 1856: 387; Kinberg
1858: 25, pl. 7, fig. 34a-h, pl. 10, fig. 60; Fauvel
1923: 98, fig. 38; Pettibone 1989: 53, figs. 32-34;
Ben-Eliahu & Fiege 1994: 156, figs. 8f, 9a-c;
Chambers & Muir 1997: 138, fig. 43; Barnich &
Fiege 2003: 101, fig. 52.
Material examined: Cap Breton (Cantabric Sea),
start: 43º35'42''N - 1º57'00''W, 994 m depth,
ending: 43º37'00''N - 1º57'60''W, 976 m depth,
2 specimens, 56 mm length and 32 mm length, 19
mm and 9 mm width.
Fig. 3. Eupanthalis kinbergi. A. Anterior end, dorsal view. B. Mid-body cirrigerous parapodium. C. Mid-body
elytrigerous parapodium. D. Acicular aristate neurochaeta of the middle bundle. E. Curved, spinous
neurochaeta of the lower bundle. F. Distally spinous neurochaeta of the upper bundle, frontal and lateral view.
Scale bar: A = 1 mm; B, C = 0.2 mm.; D, E = 0.05 mm; F: 0.1 mm.
55
Fig. 4. Eupolyodontes gulo. A. Mid-body cirrigerous parapodium. B. Mid-body elytrigerous
parapodium. C. Double brush-shaped (pseudopenicilliate) neurochaeta of the upper bundle. D. Acicular
neurochaeta of the middle bundle. E. Curved, spinous neurochaeta of the lower bundle. Scale bar: A,
B = 0.156 mm; C = 0.062 mm; D = 0.122 mm; E = 0.031 mm.
56
Fig. 5. Panthalis oerstedi. A. Anterior end, dorsal view. B. Mid-body elytrigerous parapodium.
C. Mid-body cirrigerous parapodium. D. Brush-shaped (penicillate) neurochaeta of the upper bundle.
E. Spiked capillary neurochaeta of the upper bundle. F. Acicular aristate neurochaeta of the middle
bundle. G. Curved spinous neurochaeta of the lower bundle. Scale bar: A = 1 mm; B, C = 0.2 mm;
D-G = 0.05 mm.
57
Description: Prostomium bilobed, with a pair of
well-developed
ommatophores
without
pigmentation. Lateral antennae smooth and
tapering ventral to ommatophores. Median
antenna present, near posterior margin of
prostomium, shorter than lateral antennae. Palps
smooth, tapering, extending far beyond
ommatophores. Tentaculophores papillate on
inner side, paired each with capillary notochaetae
and a pair of smooth, short tentacular cirri (Fig.
5A). Anteriormost parapodia biramous, becoming
subbiramous posteriorly, elytrigerous and
cirrigerous (Fig. 5B, C). Elytra delicate and
translucent, with lateral pouches. Dorsal and
ventral cirri smooth and tapering, not reaching tip
of neurochaetae. Median and posterior notopodia
reduced and achaetous, with spinning gland from
chaetiger 9. Neuropodia with well-developed
aciculum and three bundles of neurochaetae.
Upper bundle with long, penicillate chaetae
(brush-shaped) (Fig. 5D) and spiked capillary
chaetae, shorter than the former (Fig. 5E). Middle
bundle with smooth acicular chaetae, hairy
subdistally, and with long apical arista (Fig. 5F).
Lower bundle with numerous curved, spinous
chaetae (Fig. 5G).
Distribution: North East Atlantic Ocean and
Mediterranean Sea.
Polyodontes maxillosus (Ranzani, 1817)
(Figs. 6, 7C, E)
Phyllodoce maxillosa Ranzani, 1817: 105, pl. 4.
Polyodontes maxillosus, Pettibone 1989: 101,
figs. 70-72; Ben-Eliahu & Fiege 1994: 157, figs.
8d, 9d; Barnich & Fiege 2003: 103 fig. 53.
Material examined: Tenerife, 28º25'9''N 16º32'20''W, 8-10 m depth, fine sand, 1 specimen,
30 mm length, 9 mm width.
Description: Body long, flattened dorsoventrally,
yellow coloured, darker dorsally before fixation.
Prostomium bilobed, with a pair of welldeveloped, darkly pigmented ommatophores.
Lateral antennae smooth and tapering, shorter
than palps, ventral to ommatophores. Median
antenna inserted near middle of prostomium, with
distinct ceratophore. Palps long, tapering and
smooth. Tentaculophores with papillae on dorsal
and inner sides, paired, each with capillary
58
notochaetae and a pair of short tentacular cirri
(Fig. 6A). Parapodia biramous on first segments
and subbiramous posteriorly (Fig. 6B, C). Elytra
delicate, translucent and with lateral pouches.
Dorsal and ventral cirri short, smooth and
tapering. From chaetiger 9 notopodia reduced and
achaetous, with spinning gland. Neuropodia with
well-developed aciculum and neurochaetae in
three bundles. Upper bundle with short, spiked
chaetae (Fig. 6G), and dense group of long and
slender, distally spinous chaetae (Fig. 6D).
Middle bundle with smooth acicular chaetae,
sometimes with aristate tip (Figs. 6F, H; 7C).
Lower bundle of curved, spinous chaetae (Figs.
6E, 7E).
Distribution: North East Atlantic Ocean, Western
and Eastern Mediterranean Sea, including the
Adriatic and the Aegean Sea, Red Sea.
ACKNOWLEDGEMENTS
We are grateful to Dr. Ruth Barnich of the
Senckenberg museum, Frankfurt and an
anonymous reviewer for their valuable help and
suggestions for the revision of the manuscript.
Our sincere thanks to the R/V TALIARTE crew
who helped us during the Fuerteventura
Expedition’97, and especially to J. Barquín, in
charge of the coordination of the campaign. We
are indebted to O. Monterroso, R. Riera and M.
Rodríguez for sampling and helping in the
Lanzarote ecocartographical project, and we
thank especially C. Durán and R. Acuña (Centro
de Investigaciones Submarinas, CIS), for their
help during this expedition. We are most grateful
to the R/V CÔTE D’AQUITAINE crew who kindly
helped in the sampling during Cape Breton
Expedition. We thank F. Aguirrezabalaga
(Sociedad Cultural INSUB, San Sebastián) who
lent us the specimens collected during this
expedition and A. Domingos-Abreu (Museum of
Funchal, Madeira) who lent us the type of
Euarche cristata. Finally, we thank the Fauna
Ibérica II Expedition crew for their help during
the campaign and the Museo Nacional de
Ciencias Naturales de Madrid, which kindly lent
us their material. This study was supported by the
project Fauna Ibérica VIII, number CGL200404680-C10-02.
Fig. 6. Polyodontes maxillosus. A. Anterior end, dorsal view. B. Mid-body elytrigerous
parapodium. C. Mid-body cirrigerous parapodium. D. Distally spinous neurochaetae of upper
bundle. E. Curved, spinous neurochaeta of lower bundle. F. Simple, acicular neurochaeta of middle
bundle. G. Spiked neurochaeta of upper bundle. H. Aristate, acicular neurochaeta of middle bundle.
Scale bar: A = 1 mm; B-C = 0.75 mm; D, E, F, H = 0.1 mm; G = 0.05 mm.
59
Fig. 7. Scanning Electronic Microscope image. A, B. Eupanthalis kinbergi, acicular
neurochaeta, detail of the tip and arista. C. Polyodontes maxillosus, acicular neurochaeta,
detail of the tip. D. Eupolyodontes gulo, acicular neurochaeta, detail of the tip. E.
Polyodontes maxillosus, curved, spinous neurochaetae of the lower bundle. F.
Eupolyodontes gulo, curved, spinous neurochaetae, detail. Scale: A = 2,500 x; B = 1,000 x;
C = 850 x; D = 350 x; E = 170 x; F = 700 x.
60
KEY TO THE IBERIAN AND MACARONESIAN ACOETIDAE
1.
With a pair of large ommatophores………………………………………………………2
-
Without ommatophores………………………………………………….……………….4
2
Ommatophores darkly pigmented………………………...…...……..….…….…………3
-
Ommatophores not pigmented..…………………………….... Panthalis oerstedi (pp. 57)
3
Double brush-shaped, pseudopenicillate neurochaetae present
.……..…………………………………….…………..….…..Eupolyodontes gulo (pp. 56)
-
Pseudopenicillate neurochaeta absent……………….......Polyodontes maxillosus (pp. 59)
4
Prostomium with cristate posterior margin………….....… Euarche cristata n.sp. (pp. 53)
-
Prostomium with smooth posterior margin.………….………………..……………...…5
5
Prostomium with three antennae.....................……….……….….Euarche tubifex (pp. 51)
-
Prostomium with two antennae………......………………....Eupanthalis kinbergi (pp. 55)
-
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Mexico (1877-78), and in the Caribbean Sea (187879) in the U.S. Coast Survey Steamer "Blake".
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Harvard College 15.
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errantes. Faune de France 5: 1-488 pp.
Fiege, D. & R. Barnich 1998. Redescription of
Eupolyodontes gulo (Grube, 1855) and partial
revision of the genus Eupolyodontes Buchanan,
1894 (Polychaeta: Acoetidae). Ophelia 48 (2): 8392.
Grube, E. 1855. Beschreibungen neuer oder weniger
bekannter Anneliden. Archiv für Naturgeschichte
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Annelids; in German]
Hutchings, P.A. 2000. Family Acoetidae. Pp. 112-115
in: Beesley, P.L., Ross, G.J.B. & Glasby, C.J.
(Eds). Polychaetes and Allied: The Southern
Synthesis. Fauna of Australia. Vol. 4A Polychaeta,
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Myzostomida, Pogonophora, Echiura, Sipuncula.
CSIRO Publishing: Melbourne xii, 465 pp.
Imajima, M. 1997. Polychaetous Annelids from Sagami
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Families Polynoidae and Acoetidae. Nacional
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Oscar den Förstes befallning utgifna af Kungliga
Svenska Vetenskaps Akademien, Zoologi 2: 9-32.
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Martínez, A., A.M. Palmero, M.C. Brito & J. Núñez
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62
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Accepted 3 November 2008.
Crustaceans associated with Cnidaria, Bivalvia,
Echinoidea and Pisces at São Tomé and Príncipe islands
PETER WIRTZ & CEDRIC D’UDEKEM D’ACOZ
Wirtz, P. & C. d’Udekem d’Acoz 2008. Crustaceans associated with Cnidaria,
Bivalvia, Echinoidea and Pisces at São Tomé and Príncipe islands. Arquipélago.
Life and Marine Sciences 25: 63-69.
Symbiotic crustaceans were searched for at sea anemones (Actiniaria), encrusting
anemones (Zoantharia), horny coral (Gorgonaria), black coral (Antipatharia), bivalves
(Bivalvia), and sea urchins (Echinoidea) at São Tomé and Príncipe Islands (Gulf of Guinea,
eastern central Atlantic). Sixteen species of crustaceans were found in association with
these invertebrate hosts; eleven of them were new records for the area and two species,
belonging to the genera Hippolyte and Heteromysis, were new for science. The thalassinid
Axiopsis serratifrons was occasionally associated with an undescribed species of gobiid
fish.
Key words: Decapoda, eastern central Atlantic, Mysidacea, symbiosis
Peter Wirtz (e-mail: peterwirtz2004@yahoo.com), Centro de Ciências do Mar,
Universidade do Algarve, Campus de Gambelas, PT-8005-139 Faro, Portugal; Cédric
d´Udekem d´Acoz (cedric.dudekem@naturalsciences.be), Department of Invertebrates,
Royal Belgian Institute of Natural Sciences, Rue Vautier 29, BE-1000 Brussels.
INTRODUCTION
Caridean shrimps are common associates of
invertebrates such as sea anemones, black coral,
horny coral, bivalves, and sea urchins in tropical
and subtropical waters (e.g. Criales 1984;
Gherardi 1991; Fransen 1994a; Spotte et al. 1995;
Goh et al. 1999; Baeza 2008). A survey of black
coral at Madeira, the Azores, the Canary islands,
and the Cape Verde islands resulted in the
discovery of new species of caridean shrimps
(Wirtz & d’Udekem d´Acoz 2001). The sea
anemone Telmatactis cricoides harbours 19
different species of crustaceans at Madeira Island
(Wirtz 1997; Wittmann 2008). Large bivalves
frequently contain shrimps of the genus Pontonia
(Fransen 1994b, in review) and a survey of
bivalves at the Cape Verde islands revealed
Pontonia species new for the area and new for
science (Wirtz & d’Udekem d´Acoz 2001). The
presence of crustaceans associated with
invertebrate hosts could therefore also be
expected for the islands of São Tomé and
Príncipe (Gulf of Guinea, eastern central Atlantic)
and such associations were searched for during
three expeditions in August 2002, FebruaryMarch 2004, and February 2006.
MATERIAL AND METHODS
Observations were made while SCUBA diving in
the area of Bom Bom islet on the north coast of
Príncipe Island, and around São Tomé Island in a
depth range of 0 – 60 m. The geographic
locations of the sampling sites were as follows:
A) Príncipe Island: Bom Bom islet 01º41'N 07º24'E; Pedra da Galé 01º43'N - 07º22'E;
Mosteiros 01º41'N - 07º28'E.
B) São Tomé Island: Ilhéus Cabra 00º25.226'N –
06º42.000'E; Kia 00º25.237'N – 06º41.698'E;
63
Lagoa Azul 00º24.377'N – 06º36.602'E;
Diogo Vaz 00º18.891'N – 06º29.358'E;
Santana Islet 00º14.554'N – 06º45.601'E;
Sete Pedras 00º02.505'N – 06º37.543'E;
Rolas islet 00º00.208'N – 06º31.436'E.
Crustaceans were collected with a small handheld aquarium net. Some of the species were
photographed in situ. Most specimens are now
deposited in the collections of Royal Belgian
Institute of Natural Sciences, Brussels under the
registration number I.G. 31097. Thor amboinensis
and Rapipontonia platalea are in the Nationaal
Natuurhistorisch Museum at Leiden, Netherlands,
under the numbers RMNH D 50697 and RMNH
D 50047/50048. See d’Udekem d´Acoz (2007)
for specimen data of the two Hippolyte species.
searched for associated crustaceans; none were
encountered.
RESULTS
ASSOCIACIONS WITH GORGONARIA
ASSOCIATIONS WITH ACTINIARIA
Telmatactis cricoides (Duchassaing, 1850)
This large sea anemone was occasionally
encountered at São Tomé and Príncipe, from 0.5
to 46 m depth. The association of the shrimp Thor
amboinensis (De Man, 1888) with Telmatactis
cricoides at Príncipe has already been recorded
by Wirtz (2004), who also noted the presence of
the cleaner shrimp Lysmata grabhami (Gordon,
1935) at Príncipe. These two shrimp species,
which live on both sides of the Atlantic, were
encountered in association with T. cricoides not
only at Príncipe Island but also at São Tomé
Island. Colour photos of both species associated
with Telmatactis cricoides (at Madeira Island) are
given by Wirtz & Debelius (2003).
A ball shaped dense aggregation of at least 30
individuals of an undescribed species of
Heteromysis (Crustacea, Mysidacea) hovered
directly over the oral disk of a T. cricoides at 46
meters depth, at Diogo Vaz. Specimens were sent
to K. Wittmann, who will describe the species.
Actinostella flosculifera (Lesueur, 1817)
The sea anemone Actinostella flosculifera is
common at São Tomé and Príncipe from tide
pools down to at least 25 m depth (Wirtz 2003). It
forms warty disks of up to 10 cm diameter. About
20 individuals of this sea anemone were visually
64
ASSOCIATIONS WITH ZOANTHARIA
Palythoa
caribaeorum
Duchassaing
de
Fonbressin & Michelotti, 1860
The zoanthid Palythoa caribaeorum forms large
dense mats in the intertidal and down to at least
15 m depth. The small crab Platypodiella picta
(A. Milne-Edwards, 1869) was common in
pockets formed by zoanthid mats at low tide level
at Bom Bom islet, Príncipe. The species has been
recorded in association with various zoanthid
species, from the Gulf of Guinea to Madeira
Island (d’Udekem d’Acoz 1999; Araújo & Freitas
2003).
Horny coral are plentiful at São Tomé and
Príncipe at places exposed to moderate currents.
Small red, blue, yellow and white gorgonians in
about five to 15 m depth were not collected and
could therefore not be identified. Below the
thermocline, at about 30 m depth (in February
2004), large gorgonians of many different colours
formed veritable forests. Branches of some of the
large gorgonians from which decapods were
collected were preserved together with the
crustaceans and sent to an expert for
identification (see Acknowledgements). Large red
and blue gorgonians growing below 10 m depth
turned out to be Muriceopsis tuberculata (Esper,
1792) and large orange to yellow gorgonians
below 10 m depth belong to the genus
Leptogorgia and probably to the species L. gaini
(Stiasny, 1940).
From unidentified small blue and white
gorgonians in 14 m depth at Rolas islet, the two
shrimp species Rapipontonia platalea (Holthuis,
1951) and Latreutes cf parvulus (Stimpson, 1866)
were collected. Rapipontonia platalea was also
collected from unidentified large gorgonians at
Rolas islet in 26 m depth and from unidentified
large gorgonians in 21 m depth at Sete Pedras and
in 45 m depth at Pedra da Galé.
From Leptogorgia in 10 m depth at Mosteiros
the shrimps Rapipontonia_platalea_and Pseudocoutierea wirtzi d’Udekem d’Acoz, 2001 were
collected, including ovigerous females of both
species (Figs. 1 and 2). Hippolyte longiallex
d'Udekem d’Acoz, 2007 were collected from
Muriceopsis tuberculata in 35 m depth at Pedra
da Galé, including ovigerous females.
One male and two ovigerous females of
Hippolyte longiallex were collected from
unidentified large gorgonians in 35 m depth at
Diogo Vaz, together with ovigerous females of
Hippolyte sp. group varians and one R. platalea.
Rapipontonia platalea is known from the Cape
Verde islands, from Guinea and from São Tomé
and Príncipe in the Eastern Atlantic and from
Tobago in the Western Atlantic (Wirtz 2003;
Hale & De Grave 2007). Wirtz & d’Udekem
d’Acoz (2001) noted that it lives in symbiosis
with black coral and gorgonians, while Hale &
De Grave (2007) found it on a hydroid encrusted
with a zoantharian. The Latreutes specimens
agree with the account of L. parvulus given by
Holthuis (1951) but their scaphocerites are
distinctly narrower. Latreutes parvulus is known
from the West Atlantic (North Carolina to Rio de
Janeiro) and from West Africa in “sponges
among shells, dead coral, hydroids, and on
seagrass flats” (Williams 1984); being reported
here from the Gulf of Guinea for the first time.
Wirtz & d’Udekem d’Acoz (2001) recorded
Pseudocoutierea wirtzi from Gorgonaria and
from the whip coral Stichopathes lutkeni Brook,
1889 at the Cape Verde islands; the known
distribution of this species is now extended to São
Tomé and Príncipe. The two Hippolyte species
were undescribed at the time of capture and have
since been described by d’Udekem d´Acoz
(2007).
ASSOCIATIONS WITH ANTIPATHARIA
Stichopathes lutkeni Brook, 1889
Six whip coral were searched visually and by
sliding their length between fingers at Rolas islet
in 25 m depth and about 20 more whip coral were
searched in the same way at Pedra da Galé and at
Diogo Vaz in about 30 m depth; no associated
decapods were encountered.
Species similar to Tanacetipathes spinescens
(Gray) var. minor Brook, 1889
In 45 m depth at Pedra da Galé bushes of a black
coral resembling Tanacetipathes spinescens
(Gray) var. minor Brook, 1889 were common.
Two juveniles of Hippolyte sp. group varians
were collected from two bushes of this
antipatharian; they are described by d’Udekem
d’Acoz (2007).
Antipathes gracilis Gray, 1860
In 45 m depth at Pedra da Galé and in 45 m depth
at Diogo Vaz, small bushes of this densely
branched greenish black coral (resembling a
hydrozoan at first sight) were encountered.
At Pedra da Galé, the following shrimp species
were collected from this antipatharian:
Periclimenes wirtzi d’Udekem d'Acoz, 1996
(many
specimens);
Periclimenes
group
amethysteus (two specimens, one damaged; with
this limited material and without information on
colour pattern they cannot be determined to the
species level); Rapipontonia platalea (one
specimen); Pontoniinae n. det. (1 specimen,
anterior legs missing), Balssia gasti (Balss, 1921)
(two specimens), Eualus cranchii (Leach, 1817)
(1 ovigerous female).
At Diogo Vaz, the shrimps Periclimenes wirtzi
and an unidentified Pontoniinae (perhaps a
juvenile Palaemonella atlantica) were collected
from the same antipatharian species.
Periclimenes wirtzi has previously been
reported from black coral at the Azores, Madeira,
the Canary islands, and the Cape Verde islands
(Wirtz & d’Udekem d’Acoz 2001); a colour
photo of this species is given in Wirtz & Debelius
(2003). Balssia gasti is known as an associate of
various anthozoans and sponges in the western
Mediterranean Sea and in the eastern Atlantic
from the Azores to Guinea (Wirtz & d’Udekem
d’Acoz 2001); several colour photos of this
species are given in Wirtz & Debelius (2003).
Eualus cranchii is a free-living species known
from Norway to West Africa and here reported
from the Gulf of Guinea for the first time.
ASSOCIATIONS WITH BIVALVIA
Spondylus sp.
Three large Spondylus (the common species at
São Tomé Island, presumably Spondylus
senegalensis Schreibers, 1793) were opened in a
65
depth range of 20 to 25 m at Rolas islet and a
further eleven Spondylus at Lagoa Azul, between
5 __and __15_ _m __depth. __None _of __them
contained symbiotic shrimps.
2007). The goby is currently being described by
Schliewen and Kovačić.
DISCUSSION
Pseudochama sp.
Three bivalves of the family Chamidae, probably
the species Pseudochama radians (Lamarck,
1819), were opened at Lagoa Azul and a further
six at Rolas islet and at Kia. None of them
contained symbiotic shrimps.
Pinna rudis Linné, 1758
More than 20 Pinna rudis were visually checked
(by looking into the gap between the valves of the
living mussel) while SCUBA diving at a depth
range of 5 – 20 m at Príncipe and São Tomé
Islands. At least one, usually two, Pontonia
pinnophylax (Otto, 1821) were seen in every one
of them. Ten Pinna rudis were opened at Lagoa
Azul and either a male-female pair (8 cases) or a
single female (two cases) of Pontonia
pinnophylax were found in each of them. The
species, which is common in the Eastern Atlantic
and the Mediterranean, apparently was not yet
recorded from São Tomé and Príncipe (Fransen
2002). A colour photo of a pair of Pontonia
pinnophylax from the Azores was published in
Wirtz & Debelius (2003).
Ostrea sp.
Thirteen animals of a common, large, white,
intertidal oyster were opened at Rolas islet. No
crustaceans were found in them.
ASSOCIATIONS WITH ECHINOIDEA
As noted previously (Wirtz 2004), the shrimp
Tuleariocaris neglecta Chace, 1969 was found on
the sea urchin Diadema antillarum Philippi, 1845
at Bom Bom islet, Príncipe, in 10 m depth.
ASSOCIATIONS WITH PISCES
The thalassinid Axiopsis serratifrons (A. MilneEdwards, 1873) builds tunnels on coarse bottoms
from 10 m depth down to at least 30 m depth at
São Tomé and Príncipe. Near Bom Bom islet and
near Diogo Vaz, some of these tunnels were also
inhabited by an undescribed gobiid fish of the
genus Didogobius (Wirtz 2005; Wirtz et al.
66
Two undescribed species and eleven species not
yet recorded in the Gulf of Guinea were found in
this survey of symbiotic crustaceans.
Associations with sea anemones were
previously reported from three species of the
mysid genus Heteromysis from the (sub)tropical
W. Atlantic: the Caribbean H. actiniae Clarke,
1955 appears to be an obligatory commensal of
the anemone Bartholomea annulata (Sueur,
1817), whereas H. bermudensis G. O. Sars, 1885
and H. mayana Brattegard, 1970 show facultative
associations with anemone species (references in
Wittmann 2008). Heteromysis wirtzi appears to
be an obligate associate of the sea anemone
Telmatactis cricoides at Madeira Island (Wirtz
1997, Wittmann 2008); in contrast to the
Heteromysis species that is associated with the
same sea anemone at São Tomé Island, it never
hovers over the oral disk of the anemone; instead,
it circles around the trunk of the sea anemone.
In the Cape Verde islands, bivalves of the
genera Spondylus and Pseudochama contain
symbiotic shrimps of the genus Pontonia (Wirtz
& d’Udekem d’Acoz 2001; Fransen 2002) and
the crab Nepinnotheres viridis Manning, 1993 can
be found in Pseudochama radians (Wirtz
unpublished). It therefore comes as a surprise that
no symbiotic decapods were found in these
bivalve species at São Tomé and Príncipe islands.
Periclimenes wirtzi has now been found from
the Azores to the equator, always on Antipathella
and Antipathes species; it appears to be a
specialist for bushy black coral.
As pointed out previously, it appears to be the
size and density of the host species that
determines the social structure of the symbiont
(Dellinger et al. 1997; Thiel & Baeza 2001; Wirtz
& d’Udekem d´Acoz 2001; Thiel et al. 2003).
Very small hosts harbour single animals, as is the
case of Pontonia species in Pseudochama and in
Spondylus. Larger but defendable hosts are often
occupied by a pair of associates (e.g. Knowlton
1980; Dellinger et al. 1997; Baeza 2008), whereas
Fig. 1. Rapipontonia platalea on Leptogorgia, at Mosteiros, Príncipe Island.
Fig. 2. Pseudocoutierea wirtzi on Leptogorgia, at Mosteiros, Príncipe Island.
67
the same species may live in groups of several
adult and juvenile animals on still larger
organisms (Dellinger et al. 1997; Wirtz &
d’Udekem d´Acoz 2001).
ACKNOWLEDGEMENTS
The first author is very grateful to his travel- and
diving-companion Karl Wittmann (who also
carried a large part of the financial cost of the
expedition to Príncipe) for all his help and his
friendship. The National Geographic Society
sponsored the 2006 expedition to São Tomé
(grant number 7937-05 to Sergio Floeter). The
Centro de Ciências do Mar (CCMAR) partially
financed three trips by the first author to São
Tomé and to Príncipe. The Direcção das Pescas
of the Republic of São Tomé and Príncipe gave
research and collection permits. Angus Gascoigne
was of great help on São Tomé Island. Manfred
Grasshoff of the Senckenberg Institute in
Frankfurt, Germany, identified the gorgonians.
Dennis Opresco commented on photos of the
Antipatharia. Jean Louis Testori and his crew of
Clube Maxell made SCUBA dives at São Tomé
Island possible. Many thanks also to Jannie and
Cecilia Fourie, the managers of Bom Bom Resort,
and their staff for their kindness and support.
Peter Dworschak of the Natural History Museum
at Vienna identified Axiopsis serratifrons; Ulrich
Schliewen and Marcelo Kovačić commented on
the identity of the goby species. Sammy De
Grave and Ivan Marin commented on an early
draft of the manuscript. Many thanks to all of
them!
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São Tomé and Príncipe islands, Gulf of Guinea
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Accepted 2 July 2008.
69
The Gulf of Guinea goby‐shrimp symbiosis and a review
of goby‐thalassinidean associations
PETER WIRTZ
Wirtz, P. 2008. The Gulf of Guinea goby-shrimp symbiosis and a review of gobythalassinidean associations. Arquipélago. Life and Marine Sciences 25: 71-76.
An undescribed species of the family Gobiidae shares the burrows of the axiid shrimp
Axiopsis serratifrons at São Tomé and Príncipe (central eastern Atlantic). In contrast to
similar associations of gobiid fishes with alpheid shrimps in the Indo-Pacific and the
western Atlantic (where the goby serves as a sentinel for the crustacean and the shrimp
leaves the burrow only if the goby remains at the burrow entrance), the axiid appears to
completely ignore the goby, which rests near the opening of the burrow. Facultative and
obligatory associations of gobies with thalassinidean shrimps are reviewed.
Key words: Axiidae, convergent evolution, Gobiidae, São Tomé and Príncipe, symbiosis
Peter Wirtz (e-mail: peterwirtz2004@yahoo.com), Centro de Ciências do Mar,
Universidade do Algarve, Campus de Gambelas, PT-8005-139 Faro, Portugal.
INTRODUCTION
Almost 130 species of gobies (Pisces Gobiidae)
from 20 different genera live in symbiosis with
pistol shrimps of the genus Alpheus in the IndoPacific (reviews by Karplus 1987; Nelson [cited
2008]). In some goby genera, like Amblyeleotris
or Cryptocentrus for instance, all known species
are associated with pistol shrimps. More than 30
different Alpheus species live with these gobies
(A. Anker, pers. comm.). The shrimp constructs a
burrow in the sand or gravel and continuously
keeps it clean from sediment seeping in. The
goby uses this tunnel as a refuge and to sleep in it.
This association is advantageous for both
partners. The pistol shrimp uses the goby as an
early warning system. The shrimp leaves the
burrow only when the goby remains near the
entrance and uses one of its two antennae to
permanently maintain contact with the fish. If the
fish indicates danger by fluttering the caudal fin
or even by fleeing into the tunnel the shrimp
rapidly retreats. In the popular aquarium literature
in English and German, these goby species are
called "watchman gobies" (Wächtergrundeln).
Most Alpheus species with gobies as tenants live
in pairs. Frequently a single goby is seen with a
pistol shrimp but sometimes two gobies associate
with Alpheus shrimps. Many of these associations
are obligatory, that is goby and shrimp are always
encountered together, never alone. Some of these
gobies live exclusively with certain Alpheus
species, others can occupy the burrows of several
shrimp species. In the pistol shrimps as well,
some Alpheus species live only with a certain
goby, while others can be encountered with
several different goby species.
In the tropical western Atlantic, the gobies
Nes longus and Ctenogobius saepepallens live
with the pistol shrimp Alpheus floridanus,
occasionally also the gobies Gobionellus
stigmalophius and Bathygobius curacao (Karplus
1992; Randall et al. 2005). While Nes longus and
its shrimp show a relation similar to the IndoPacific symbioses described above, the relation
between Ctenogobius saepepallens and the
alpheid shrimp is much looser: the shrimp
emerges also when the goby is not present at the
burrow opening and there is no antennal contact
when the goby is present; neither does the goby
71
communicate danger with caudal fin fluttering.
No goby-alpheid associations have been reported
from the eastern Atlantic.
This work describes a new goby-shrimp
symbiosis at the islands of São Tomé and
Príncipe (Gulf of Guinea), in the eastern central
Atlantic. A preliminary popular account of this
association, containing colour photos, was given
by Wirtz (2005).
MATERIAL AND METHODS
Initial observations were made during four
SCUBA dives in the area of Bom Bom Islet,
north coast of Príncipe Island (01º41'N - 07º24'E)
in February 2004. Additional observations were
made during three SCUBA dives at the coasts of
São Tomé Island, namely Diogo Vaz (00°19'N 06°29'E) and Santana Islet (0°15'N - 06°46'E) in
February 2006. Observations on the behaviour of
the fish and shrimp were mostly done at Diogo
Vaz. As these were done at 24 m depth, and only
two dives were performed, the total time spent on
observation was approx. 30 minutes. The
remainder dives at São Tomé was spent
attempting to collect specimens.
Two specimens of the goby were captured (one
at Diogo Vaz and one at Santana islet) with the
help of rotenone. They are now deposited in the
collection of the Zoological Museum at Munich,
Germany (ZSM 34186, Diogo Vaz) and in the
collection of the Universidade Federal de Espírito
Santo, Vitória, Brasil (UFES 133, Santana islet).
Two specimens of the crustacean were caught
at Diogo Vaz in 24 m depth by shooting a
harpoon into the entrance of the cave when the
crustacean was outside. They are now in the
collection of the Natural History Museum at
Vienna, Austria (NHMW 21950).
RESULTS
SPECIMENS IDENTIFICATION
The crustacean and the goby both reach a length
of about 5 centimetres. The two specimens of the
goby that were captured have been examined by
U. Schliewen and M. Kovačić. These experts
72
regard it as an undescribed species of the family
Gobiidae and are planning to describe the species
in the genus Didogobius (pers. comm.). The
crustacean has been identified by Peter
Dworschak (pers. comm.) as Axiopsis serratifrons
(A. Milne Edwards, 1873), family Axiidae,
infraorder Thalassinidea – a species widespread
on both sides’ of the Atlantic, Indian, and Pacific
Oceans.
THE HABITAT
The approximately 40 burrows of Axiopsis
serratifrons observed at Príncipe and at São
Tomé were on sandy bottoms that contained
small stones, fragments of coral and shells, from
about 7 m downwards to 25 m. No burrows were
seen on pure sand. Some were seen on bottom
consisting of larger stones with small patches of
sandy areas between them. The burrow opening
of about 3 cm diameter is stabilized by pieces of
rubble or shell fragments. This corresponds to
descriptions by Dworschak & Ott (1993) and
Dworschak (2004) for A. serratifrons burrows in
the Caribbean.
THE RELATION BETWEEN THE FISH AND THE
CRUSTACEAN
A single goby and a single shrimp were observed
associated in all cases; no pairs of either the
shrimp or the goby were recorded but a second
animal might have been hidden in the burrow
(Dworschak & Ott 1993, record that Axiopsis
serratifrons usually lives in pairs). Like pistol
shrimps of the genus Alpheus, A. serratifrons
frequently came out of the tunnel, transporting
sediment, usually small stones. The crustaceans
observed walked as far as two to three body
lengths away from the burrow opening, dropped
the stone and re-entered the burrow. In contrast
to the Alpheus species, they did not maintain
contact to their fish partner with an antenna when
outside the burrow (see Fig. 1). Frequently the
shrimp came out of the burrow before the goby.
In two burrows observed for about 10 minutes
each, the shrimp several times appeared and reentered the burrow without any goby appearing:
no goby probably was associated with these two
shrimps. In contrast, no goby was seen without an
associated Axiopsis serratifrons.
Fig. 1. Above, the undescribed goby in front of an Axiopsis serratifrons burrow; the shrimp is visible at the
entrance. Below, the shrimp is carrying a stone out of the burrow; it does not maintain antennal contact with the
goby, which rests in the entrance of the burrow.
73
When a diver approached slowly, the goby did
not give any warning signals such as tail flicks
but at some point rapidly disappeared into the
burrow. The Axiopsis then also retreated, after the
goby. It was not clear if the retreat of the goby did
or did not cause the retreat of the shrimp.
DISCUSSION
Apparently a goby-shrimp association, similar to
that between gobies and pistol shrimps of the
genus Alpheus in the Indopacific and in the
western Atlantic, has evolved again and
completely independently in the eastern Atlantic.
The relation between the undescribed goby and
the axiid shrimp Axiopsis serratifrons at São
Tomé and Príncipe does not appear to be as tight
as that between Indopacific guardian gobies and
their pistol shrimps. Perhaps the goby has only
moved into a convenient hole in the ground and,
as it does not cause any damage to the axiid, is
tolerated but largely ignored by the crustacean.
The more evolved relation between most guardian
gobies and their pistol shrimps may have started
in such a way at some time in the past: in a
second step, the pistol shrimps then learned to
interpret and to exploit the behaviour of the goby
(Karplus 1987, 1992; Randall et al. 2005).
Axiopsis serratifrons is a circumtropical
species; it has never been observed with gobies in
other areas, even when resin casts of the burrow
were made (Dworschak & Ott 1993). The
undescribed goby has so far only been recorded at
São Tome and Príncipe islands but because of the
great similarity in their fish faunas (Wirtz et al.
2007; Floeter et al. 2008), it might well also occur
at the Cape Verde islands, where A. serratifrons
is known to live (Abed-Navandi 2000).
Several other associations of gobies with
thalassinidean shrimps have been reported from
other areas. In some of these, the goby appears to
co-occupy a thalassinidean burrow only for a
short term, in others it appears to permanently
live in the burrow as an adult.
The goby Clevlandia ios uses the _burrows _of
Calianassa affinis and Calianassa californiensis
and Upogebia pugettensis only briefly as a place
of refuge either from predators or during tidal
exposure (MacGinitie 1939; MacGinitie &
74
MacGinitie 1968; Hoffman 1981). The shrimps
were often observed chasing the gobies out of the
burrows (Hoffman 1981). The case of the goby
Lepidogobius lepidus occasionally encountered
with Upogebia pugettensis is quite similar:
gobies are in the burrows only occasionally and
the shrimps have been observed chasing the goby
out of the burrow (Grossman 1979; Hoffman
1981). Kinoshita (2002) records an individual of
the goby species Chaenogobius macrognathos
from 24 burrows of the thalassinidean Upogebia
major in Japan; as only a single association was
recorded, this could be an artefact and the
observation needs verification. The Japanese
gobies Gymnogobius cylindricus, G. uchidai, G.
scrobiculatus, and Eutaeniichthys gilli live on
mud flats and can be encountered in the burrows
of Upogebia major (Senou 2004; Suzuki et al.
2006) but no studies on these species are
available.
A single animal or a pair of the goby
Austrolethops wardi was encountered by Kneer
(2006) in three of five burrows of Neaxius
acanthus in Indonesia; the goby apparently does
not leave the burrow of the shrimp but does not
appear to have any obvious morphological
adaptations to its way of life, such as reduced eye
size (Kneer et al. in prep). MacGinitie (1939)
describes the biology of the blind goby
Typhlogobius californiensis, which lives in pairs,
deep in the burrow of pairs of Callianassa affinis
(now called Callianassa biffari Holthuis 1991,
Dworschak pers. comm.) in California; the blind
gobies do not leave the burrow of the crustacean.
Itani & Tanase (1996) recorded the blind goby
Luciogobius pallidus from the burrow of
Upogebia yokoyai in Japan, but only a single
goby was encountered in about 100 burrows
investigated, and the presence of a shrimp was
not checked (Itani, pers. comm.).
The occurrence of at least two species of blind
gobies in the burrows of thalassinideans suggests
an alternate evolutionary scenario to the one
described above: instead of developing into a
“watchman goby – shrimp symbiosis”, a goby –
thalassinidean association might develop in such
a way that the goby spends more and more time
inside the burrow of the shrimp, finally adapting
to this cave-like environment morphologically.
ACKNOWLEDGEMENTS
Peter Dworschak of the Natural History Museum
at Vienna identified the crustacean and sent
references, photocopies, and helpful comments.
Gyo Itani sent numerous Japanese references and
photocopies and provided summaries of them.
Arthur Anker sent information on alpheids
associated with gobies. The National Geographic
Society (grant to Sergio Floeter for an expedition
to São Tomé) and the Centro de Ciências do Mar
of the University of the Algarve partly financed
this study. My diving companion Karl Wittmann
also carried a large part of the cost of the trip to
Príncipe Island. Cecila and Jannie Fourie,
managers of the Bom Bom resort on Príncipe
Island, helped in many ways. Carlos Eduardo
Ferreira captured the gobies. Ulrich Schliewen
and Marcelo Kovačić commented on the identity
of the goby species. Many thanks to all of them!
REFERENCES
Abed-Navandi, D. 2000. Thalassinideans new to the
fauna of Bermuda and the Cape Verde Islands.
Annalen des Naturhistorischen Museums in Wien
102B: 291-299.
Dworschak, P.C. 2004. Biology of Mediterranean and
Caribbean Thalassinidea (Decapoda). Pp: 15-22 in:
Tamaki, A. (Ed). Proceedings of the Symposium on
"Ecology of large bioturbators in tidal flats and
shallow sublittoral sediments - from individual
behavior to their role as ecosystem engineers".
November 1-2, 2003, Nagasaki. Nagasaki
University. 118 pp.
Dworschak, P.C. & J. Ott 1993. Decapod burrows in
mangrove-channel and backreef environments at
the Atlantic Barrier Reef, Belize. Ichnos 2:
277-290.
Floeter, S.R., L.A. Rocha, D.R. Robertson, J.C.
Joyeux, W. Smith-Vaniz, P. Wirtz et al. 2008.
Atlantic reef fish biogeography and evolution.
Journal of Biogeography 35: 22-47.
Grossman, G.D. 1979. Symbiotic burrow-occupying
behaviour in the bay goby, Lepidogobius lepidus.
California Fish and Game 65: 122-124.
Hoffman, C.J. 1981. Associations between the goby
Clevelandia ios (Jordan and Gilbert) and the ghost
shrimp Callianassa califirniensis Dana in natural
and artificial burrows. Pacific Science 35: 211-216.
Itani, G. & H. Tanase 1996. A blind goby, Luciogobius
pallidus Regan, collected from a burrow of a mud
shrimp, Upogebia yokoyai Makarov. Nanki Sei
Butu 38(1): 53-54. [In Japanese].
Karplus, I. 1987. The association between gobiid fishes
and burrowing alpheid shrimps. Oceanography and
Marine Biology Annual Review 25: 507-562.
Karplus, I. 1992. Obligatory and facultative gobyshrimp partnerships in the western tropical
Atlantic. Symbiosis 12: 275-291.
Kinoshita, K. 2002. Burrow structure of the mud
shrimp Upogebia major (Decapoda: Thalassinidea:
Upogebiidae). Journal of Crustacean Biology
22(2): 474-480.
Kneer, D. 2006. The role of Neaxius acanthus
(Thalassinidea: Strahlaxiidae) and its burrows in a
tropical seagrass meadow, with some remarks on
Corallianassa
coutierei
(Thalassinidea:
Callianassidae). Diplomarbeit, Freie Universität
Berlin. 91 pp.
Kneer, D., H. Asmus, H. Ahnelt & J.A. Vonk (in prep)
Records of Austrolethops wardi (Teleostei:
Gobiidae) as an inhabitant of burrows of the
thalassinid shrimp Neaxius acanthus in tropical
seagrass beds of the Spermonde Archipelago,
Indonesia.
MacGinitie, G.E. 1939. The natural history of the blind
goby, Typhlogobius californiensis Steindachner.
American Midland Naturalist 21(2): 489-505.
MacGinitie, G.E. & N. MacGinitie 1968. Natural
history of marine animals. MacGraw-Hill, New
York. 523 pp.
Nelson, R. (Internet). The shrimp-goby chronicles;
(cited 17 June 2008). Available from:
www.explorebiodiversity.com/Hawaii/Shrimpgoby/general/index.htm.
Randall, J.E., P.S. Lobel & C.W. Kennedy 2005.
Comparative ecology of the gobies Nes longus and
Ctenogobius saepepallens, both symbiotic with the
snapping
shrimp
Alpheus
floridanus.
Environmental Biology of Fishes 74, 119-127.
Senou, H. (ed.) 2004. A photographic guide to the
gobioid fishes of Japan. Heibonsha, Tokyo. 534 pp.
[In Japanese]
Suzuki, T., H. Yoshigou, A. Nomoto, S. Yodo, J.
Nakashima & S. Matui 2006. Morphology, habitat
and distribution of the endangered goby,
Gymnogobius cylindricus (Perciformes, Gobiidae).
Bulletin of the biogeographic Socity of Japan 61:
125-134. [In Japanese]
Wirtz, P. 2005. Eine neue Grundel-Krebs-Symbiose
aus dem Ostatlantik. Die Aquarien- und TerrarienZeitschrift 08: 66-68. [A new shrimp-gobysymbiosis from the West Atlantic; in German;
translation
available
at:
http://explorebiodiversity.com/Hawaii/Shrimpgoby/general/Grun-
75
delKrebs.htm]
Wirtz, P, C.E.L. Ferreira, S.R. Floeter, R. Fricke, J.L.
Gasparini, T. Iwamoto et al. 2007. Coastal Fishes
of São Tomé and Príncipe islands, Gulf of Guinea
(Eastern Atlantic Ocean) – an update. Zootaxa
1523: 1-48.
Accepted 17 June 2008.
76
Effects of fish removal in the Furnas Lake, Azores
ANA BIO1, A. COUTO2, R. COSTA2, A. PRESTES2, N. VIEIRA1,3, A. VALENTE3,4 & J. AZEVEDO2
Bio, A., A. Couto, R. Costa, A. Prestes, N. Vieira, A. Valente & J. Azevedo 2008.
Effects of fish removal in the Furnas Lake, Azores. Arquipélago. Life and Marine
Sciences 25: 77-87.
The Furnas Lake is a small volcanic, monomitic and increasingly eutrophised water body.
Next to agricultural nutrient inputs, high densities of herbivorous fish are thought to
contribute to high levels of turbidity in the lake, through zooplankton consumption and
re-suspension of the nutrients accumulated in the sediment. According to the alternative
state hypothesis a shift from turbid to clear water conditions is favoured by reduction of
nutrient concentrations, increased light availability and reduction of planktivorous and
benthos-feeding fish stock. To improve water quality in the Furnas Lake, a substantial part
of the bottom-feeding fish population (62% of the estimated common carp population,
Cyprinus carpio, and 5% of the estimated roach population, Rutilus rutilus) was removed.
Effects of fish removal on turbidity and associated trophic state were analysed next to postmanipulation chlorophyll a concentration, zooplankton and macrophytes densities. Results
suggest that fish removal was not enough to change lake conditions towards a lasting clear
state dominated by macrophytes. Excessive nutrient load, in water and sediments, nutrient
input from the lake basin and fish recruitment causing enhanced zooplankton grazing are
appointed causes. Any further biomanipulation efforts should be associated to nutrient
reduction; and continued monitoring of water quality, fish stock, macrophytes and
zooplankton is needed.
Key words: range size, functional groups, herbivore, predator, resource availability model
1
Ana Bio (e-mail: anabio@ciimar.up.pt), CIMAR/CIIMAR, Centro Interdisciplinar de
Investigação Marinha, Universidade do Porto, Rua dos Bragas 289, PT-4050-125 Porto,
Portugal; 2Departamento de Biologia, Universidade dos Açores, PT-9501-801 Ponta
3
Delgada, Portugal; Departamento de Zoologia e Antropologia, Faculdade de Ciências,
4
Universidade do Porto, PT-4169-007 Porto, Portugal; Unidade de Investigação em
Eco-Etologia, ISPA, PT-1149-049 Lisbon, Portugal.
INTRODUCTION
Scheffer et al. (1993) suggested that turbidity in
shallow lakes is not a smooth function of their
nutrient status. Lakes are thought to have two
distinct equilibria between which they can
alternate: a clear state dominated by macrophytes
and a turbid state dominated by algae. Turbidity
hinders vegetation growth through reduced light
availability. Vegetation, in turn, lowers turbidity
reducing re-suspension of sediments and
protecting
(hiding)
phytoplankton-grazing
zooplankton
from
planktivorous
fish.
Furthermore, vegetation competes with algae for
nutrients. It was found that vegetation can
stabilize clear water conditions up to certain
nutrient loadings, but increasing nutrient loadings
favour algal growth, causing turbidity and a rapid
reduction in macrophytes. To invert that situation
and regain a vegetation-rich, clear-water state,
nutrients have to be drastically reduced, or light
availability increased (e.g. lowering the water
level). The switch to a clear state can also be
triggered by reducing the planktivorous fish stock
(Jeppesen et al. 2007b). Omnivorous, benthosfeeding fish like carps degrade water quality in
several ways (Crivelli 1983; Breukelaar et al.
1994; Beklioglu et al. 2003). They increase water
77
turbidity
consuming
zooplankton
and
macrophytes and revolving the sediment, resuspending sediment and accumulated nutrients
(increasing turbidity directly with suspended
solids and indirectly by
feeding on
phytoplankton). Studies investigating the
interaction
between
planktivorous
fish,
algal biomass and turbidity (Langeland 1990;
Meijer et al. 1994; Tátrai et al. 1997). There are,
however, few studies on biomanipulation applied
to warm lakes (Moss et al. 2004; Romo et al.
2004; Romo et al. 2005; Scasso et al. 2001;
Vázquez et al. 2004).
Lake Furnas is a small, shallow water body
located in an ancient volcanic
crater, on the island of São
Miguel, Azores. Agriculture and
fertilized pasture are common
activities in its basin, contributing
to the lake’s nutrient load and
causing an increasing eutrophication. In the recent past the
lake has been turbid and algal
blooms have been frequent (Santos
et al. 2005). The lake has a
protected
status
but
local
authorities
have
difficulties
controlling fertilization in the lake
drainage area, and consequent
nutrient input. In the mid-nineties,
bottom aeration was adopted in an
effort to improve water quality
increasing
dissolved
oxygen
concentrations near the bottom and
in the water column. Water
quality, however, did not improve,
as positive effects may have been
offset by the negative effects of
sediment
re-suspension
and
consequent nutrient release into
the water column (Azevedo et al.
2006). In the lake common carps
are abundant and predators scarce.
Considering the alternative state
hypothesis, and given that Lake
Furnas has shown relatively low
phosphorous concentrations in
recent years but high herbivorous
and benthos-feeding fish density,
biomanipulation was decided on,
Fig. 1. Batimetry of the Furnas Lake (isobaths at 0.5 m intervals) and
to provide an impulse for a switch
location of the sample sites A to D.
to clear-water conditions. The carp
Cyprinus carpio (L.) populations
zooplankton, phytoplankton and water chemistry were substantially reduced, removing more than
in Northern and central Europe, included several 60% of the estimated population, and lake
experiments of planktivorous fish removal, which evolution was monitored in terms of water quality
frequently resulted in significant decreases in parameters, macrophytes and zooplankton.
78
LAKE FURNAS
Lake Furnas is located at 37º45'30''N25º20'03''W, at an altitude of 281 m, with
maximum length, width and depth of 2025 m,
1600 m and 15 m, respectively, and average depth
of 6.9 m (Fig. 1). The island’s climate is marine
temperate, with an average temperature of
13.6 ºC; a dry season and a colder, wet season;
and a yearly average precipitation of 1874 mm.
The lake has a total area of 1.93 km2 and a
basin of 12.45 km2, occupied by forest (533 ha),
pasture (460 ha; mainly cattle) and agriculture
(5.7 ha). Basin land use, excessive fertilization
and soil slope (averaging 20%) contribute to soil
erosion and lake deterioration through sediment
and
nutrient
inputs
(Porteiro
2000).
DROTRH/INAG (2001) estimated potential
diffuse nutrient sources between 1996 and 1998
to reach 6.9 T per ha and yr of nitrogen, and
0.79 kg per ha and yr of phosphate; affluent
creeks were estimated to supply 29.8 T·yr–1 of N
and 1.44 T·yr–1 of P to the lake. These values
exceed the loads permissible for such a shallow
lake 10 and 7.5 times and critical loads for
eutrophication 5 and 4 times, for N and P
respectively (Santos et al. 2005; Harper 1992).
PRE-BIOMANIPULATION DATA
Records of water quality are available from 1994
onward. Between 1994 and 2004, there are
generally two to four observations per year of
total phosphorus, total nitrogen, dissolved oxygen
and pH (Fig. 2). The same applies for turbidity
(secchi depth), but with almost monthly
observations after July 2001 (Fig. 3).
In 2004, total phosphorous (TP) in the lake
water ranged from 24 to 76 µg·l–1, with an
12
300
TP sur
TP bot
8
200
4
100
DO sur
DO bot
10
3000
TN sur
TN bot
2500
5
4
3
2
1
0
9
8
7
6
0
5
_
4
5
4
3
2
1
0
9
8
7
6
5
4
0
pH sur
pH bot
9
2000
8
1500
2004
2003
2002
2001
2000
1999
1998
1997
1996
1994
2005
2004
2003
2002
2001
2000
1999
1998
1997
5
1996
0
1995
6
1994
500
1995
7
1000
??
Fig. 2 Pre-biomanipulation data for surface (sur) and bottom (bot) total phosphorous (TP, in µg⋅l-1), total
nitrogen (TN, in µg⋅l-1), dissolved oxygen (DO, in mg⋅l-1) and pH.
average of 45 µg·l–1; an improvement in
comparison to the mid-nineties, when surface TP
values of more than 300 µg·l–1 were recorded.
Total nitrogen (TN) shows an opposite trend,
increasing from about 700 µg·l–1 in the midnineties, towards an average of 1120 µg·l–1 in
2004. Between 1994 and 2004, Secchi disk
depths varied between 30 and 250 cm and the
lake’s trophic state was meso- to eutrophic, with
Secchi depth-based Index (TSI) values between
47 and 77. Algal blooms occurred regularly,
especially after heavy rainfalls. Conditions at the
79
0
90
80
60
50
40
2
TSI
Secchi depth (m)
70
1
30
20
10
3
2007
2006
2005
2004
2003
2002
2001
2000
1999
1998
1997
1996
1995
1994
0
Fig. 3 Secchi depth in left axis and grey line; and Secchi depth-based Carlson’s Trophic
State Index (TSI) values on right axis and black line; arrows mark fish removal periods.
nutrient depletion (typical of a stratified lake)
should cause phytoplankton decline.
Before biomanipulation, total dissolved solids
(TDS) and electrical conductivity (EC) were only
measured from January to July 2004, ranging
from 72 ppm to 82 ppm, with an average of
75.4 ppm, and from 143 µs to 165 µs, with an
average of 151.3 µs, respectively.
Fish population is dominated by benthosfeeding, omnivorous common carp and roach.
There are also three carnivorous species – pike,
zander and perch – considered to be of great
interest to sport fishing.
lake bottom were frequently anoxic in summer.
In 1995, bottom aeration was introduced to
increase dissolved oxygen (DO) and decrease
eutrophication. An aerator was placed near the
bottom (close to the sample point B of the present
study) and switched on during a few to 180 hours
per month, especially during the summers of 1995
to 1997 and almost during the whole years of
1999 and 2000 (Fig. 4). Aeration as applied in
this lake, is not strictly hypolimnetic as the flow
caused by ascending air bubbles drags sediments
and nutrients to the lake surface, causing vertical
mixing
and
favouring
phytoplankton
development, even in the summer periods when
Aeration (h)
200
150
100
50
2007
2006
2005
2004
2003
2002
2001
2000
1999
1998
1997
1996
1995
1994
0
Fig. 4 Monthly hypolimnetic aeration.
MATERIAL AND METHODS
BIOMANIPULATION
Prior to biomanipulation, in 2004, a mark and
recapture experiment estimated average common
carp (Cyprinus carpio) densities of 88 kg·ha-1,
with a 95% confidence interval from 50 to
80
186 kg·ha-1 (Azevedo et al. in press). Roach
(Rutilus rutilus) density was estimated to range
from 20 to 80 kg·ha-1 (unpublished data).
During April, May and June of 2005, about 10
tons of fish were captured with nets (80 mm mesh
size) and removed from the lake. These included
2805 carps, totalling 9204 kg – i.e. about 54% of
the estimated population – and 7069 roaches,
weighting 470 kg. During May and June of 2006,
452 carps, totalling 1384 kg (about 8% of the
original estimated population) were removed.
Less fish was captured in the second year,
because there was less bigger-sized fish available
and because of exceptionally low temperatures
for the season, causing carps to avoid lake
margins and, hence, capture.
WATER QUALITY ASSESSMENT
After biomanipulation, water samples were taken
approximately every two weeks, at 4 fixed
representative sample sites (A to D, Fig. 1). At
each site, Secchi disk depth was determined and 1
to 4 water samples taken at different depths.
Chlorophyll a concentrations were determined
filtering water through a 47 mm, 0.45 µm pore
size nitrocellulose filter and extracting the
pigments in an aqueous solution of acetone.
Chlorophyll a concentrations were subsequently
determined spectrophotometrically and resulting
absorbance measurements applied to a standard
equation.
Water
temperature,
electrical
conductivity (EC), total dissolved solids (TDS)
and pH were measured with a Hanna Combo pH
& EC HI 98129. In the deepest part of the lake a
series of 12 temperature and luminosity sensors
was placed, performing 6 measurements per hour,
at depths of 0.3 m, and 1 to 11 m with 1m
intervals.
ZOOPLANKTON AND MACROPHYTES
Next to water samples, plankton was collected at
the four sites, at the surface and near the bottom,
with bottom water depths averaging 5.6 m at site
A, 2.1 m at B, 11.6 m at C and 9.4 m at D.
Samples were collected using a Schindler trap,
preserved in a 5% formalin solution with 20 g·l-1
sucrose and divided into halves with a Folsom
plankton sample splitter in the lab. One half of
each sample was preserved for future analysis, the
other was lumped, mixing samples from sites A
to D into one surface and one bottom sample for
each sampling period. These were used to identify
zooplankton according to taxonomic groups
(cladocera, copepods, rotifers or others) and size
classes (0.5, 1.0, 1.5 and 2.0 mm). Main
macrophyte species were mapped in spring 2005
and 2006, through visual surveys on a 20 m ×
20 m grid (the lake was subdivided into
approximately 4750 squares). Macrophyte cover
was recorded according to 5 classes (no
macrophytes, 25%, 50%, 75% and 100% cover)
and total lake covering calculated.
DATA ANALYSIS
Carlson’s Trophic State Index (TSI) was
computed from Secchi disk depth measurements
using the equation (Carlson 1977):
TSI = 10x (6 – ln(secchi depth in m) / ln(2)).
Carlson's index uses a natural logarithm
transformation of Secchi disk values as a measure
of algal biomass on a scale from 0 to 110, where
each increase of ten units represents a doubling of
algal biomass. To assess possible correlations
between variables, cross-correlations were
computed for the time series, after confirming
data stationarity, and tested for significance.
Cross-correlations between aeration and turbidity
were calculated separately for the periods with
seasonal and monthly samples between 1994 and
2004. Post-biomanipulation data analysis was
based on monthly averages. Comparison of preand post-biomanipulation data was difficult given
the lack of comparable data (e.g. nutrient
concentrations were not measured after
biomanipulation, chlorophyll a, macrophytes and
zooplankton where not sampled before
biomanipulation); not enough data for time series
analysis; yet data with seasonal patterns and
autocorrelation that should not be compared by
simple statistical tests. Given these limitations it
was not possible to distinguish inter-annual
variation
from
temporal
trends
or
biomanipulation effects. All analyses were done
in R (R Dev. Core Team 2005).
RESULTS
WATER QUALITY
Considering July 2005 the first month after
biomanipulation, there is a marked decrease in
turbidity in the first summer after biomanipulation (Fig. 3), but, within one year,
turbidity approached pre-manipulation values.
81
82
200
95
190
90
180
85
170
05
05
05
5
05
05
06
06
06
06
06
06
06
06
06
6
06
06
07
07
TDS (ppm)
100
9
pH
8
6
Jul-05
Ago-05
Set-05
Out-05
Nov-05
Dez-05
Jan-06
Fev-06
Mar-06
Abr-06
Mai-06
Jun-06
Jul-06
Ago-06
Set-06
Out-06
Nov-06
Dez-06
Jan-07
Fev-07
7
Fig. 5. Above, monthly averages of surface total
dissolved solids (TDS), grey line; electrical
conductivity (EC), black line; below, pH monthly
averages.
surface or bottom dissolved oxygen levels (only
available for 1994 – 2004).
There was, however, a significant correlation
between precipitation and turbidity or trophic
state. Monthly average Secchi depth is negatively
and TSI is positively correlated to the
precipitation (Fig. 7). They are both significantly
correlated to the precipitation observed in the
same month (lag 0, correlation = −0.42 and 0.46,
for Secchi depth and TSI respectively) and to that
observed in the two months before (lag −1 with
correlations of −0.64 and 0.64; and lag −2 with
correlations of −0.45 and 0.46, respectively).
There is little spatial heterogeneity in water
quality within the lake, except for sample point B
which showed significantly higher turbidity in the
first summer after biomanipulation, frequent
peaks in chlorophyll a concentration and less
alkaline values when compared to the other sites.
ZOOPLANKTON AND MACROPHYTES
Zooplankton (Fig. 6) is dominated by rotifers
(especially in winter) and cladocera (especially in
spring and summer). Copepods and other
zooplankton taxa are less abundant. All groups
show a sharp decrease in numbers in the winter of
EC (µs)
Analogously, the TSI dropped from about 63 in
late spring to 47 in summer 2005, after the first
biomanipulation. In December 2005 the TSI rose
to 55 and in the winter of 2007 to 65.
Total dissolved solids and EC remain quite
similar, though slightly increasing, for the two
years (Fig. 5). Considering the few measurements
of TDS and EC taken in 2004, there is an increase
towards 2005 and 2006, though more historical
data would be needed for a sound comparison
between before and after biomanipulation values.
EC increased from an average of 151.3 µs before
to 184.4 µs after biomanipulation, and TDS, from
75.4 ppm to 92.0 ppm, respectively. Chlorophyll
a concentrations (Fig. 6) and pH also increased
from 2005 to 2006 (a variation similar to that
observed in previous years, Fig. 2).
Except for pH, all water parameters show
marked seasonal variation, with temperature
increasing in summer, chlorophyll a and turbidity
decreasing in summer, and TDS and EC
decreasing in spring. Lake Furnas shows
characteristics of a typical volcanic lake in
temperate regions. Depth-dependent temperature
measurements revealed that the Furnas lake is a
warm monomitic lake, with stratification between
April and September reaching a maximum
difference of 4.8 ºC between surface and bottom
water at 11 m depth. Chlorophyll a concentrations
appear to have a single peak in winter, instead of
a spring and an autumn peak (this should be
confirmed with long-term observations).
Several of the water quality parameters are
strongly correlated. Total dissolved solids and
electrical conductivity show significant positive
correlation (correlation of 0.978). Chlorophyll a
shows significant negative correlation with
temperature (–0.817).
No statistically significant correlation between
aeration and turbidity was found. Months with
intensive aeration tend to have high turbidity (all
months with ≥20 hours of aeration have ≤0.8m
secchi disk depths), but many months without
aeration have high turbidity too. After
biomanipulation only little aeration took place, in
comparison to the period before, and again no
statistically significant correlation was found
between aeration and turbidity. Cross-correlation
showed also no significant correlation between
140
Rotifers
120
Observed prec.
M ean prec.
TSI
2.0 mm
1.5 mm
100
300
1.0 mm
80
0.5 mm
70
60
20
120
7
6
6
6
6
6
6
6
6
6
6
6
6
5
5
5
5
5
Cladocera
100
80
60
200
60
100
50
0
40
40
60
Fev-07
Dez-06
Out-06
Jun-06
Fev-06
Abr-06
Ago-06
5
05
0
05
20
Dez-05
Copepods
Out-05
7
07
Jun-05
6
06
6
6
6
6
06
6
6
06
6
6
06
06
6
06
6
6
6
6
06
6
5
05
6
5
06
5
5
05
5
5
5
0
40
Ago-05
20
other
40
0.6
20
200
150
50
40
30
Jan-07
Nov-06
Sep-06
Jul-06
May-06
0
Mar-06
10
0
Jan-06
50
Nov-05
20
Sep-05
100
Fig. 6. Monthly average zooplankton densities (ind·l–1)
per taxonomic group and size class; total zooplankton
density (notice the different y-axis scale) is presented
with average monthly Chlorophyll a concentration
(line, right axis, in mg⋅l-1).
2006. Monthly average zooplankton numbers
follow monthly chlorophyll a concentrations in
the first year, but collapse in the second year, in
spite of increasing chlorophyll. In terms of
individual size, cladocera and copepods belong
predominantly to the 1.0 mm size class, whereas
rotifers (and other zooplankton) are smaller,
occupying mostly the 0.5 mm class.
Macrophyte growth was restricted to the lake
shore, covering about 3.7% of the lake surface in
the spring of 2005 and 5.4% in the spring of 2006.
The main species found were Egeria densa
(Planch.), Ceratophyllum demersum (L.) and
Potamogeton lucens (L.). The most abundant
Cross-correlation
7
6
6
6
6
6
6
2.0 mm
1.5 mm
1.0 mm
0.5 mm
CHL
zooplankton
250
6
6
6
6
6
6
5
5
5
5
5
5
0
Jul-05
Average zooplankton densities (ind·l–1)
5
0
TSI
Precipitation (mm))
40
0.4
0.2
0.0
-0.2
-0.4
-10
-5
0
Lag
5
10
Fig. 7. Above, observed and average monthly
precipitation (years 1961–1990), and Secchi depthbased Carlson’s Trophic State Index values (TSI);
below, cross-correlation between observed monthly
precipitation and TSI (CI for α = 0.05 are given by
dashed lines).
species Egeria densa and the least abundant
Ceratophyllum demersum about doubled their
estimated biomass from 2005 to 2006, while the
biomass of Potamogeton lucens remained
approximately unchanged.
DISCUSSION
Biomanipulation in the Furnas Lake did not yield
the wanted shift towards stable clear-water
conditions. Immediately after the first fish
removal campaign a marked decrease in turbidity
was observed. However, similar summer
83
decreases were observed in 2002 and 2003, and
within one year after fish removal turbidity
approached
pre-manipulation
values.
Analogously, the lake’s trophic state, which had
been mesotrophic to eutrophic in the recent past
improved visibly after the first biomanipulation
effort, reaching a TSI of less than 50. But this
phenomenon lasted only a few months and, by the
end of 2005, TSI values had climbed to eutrophic
conditions.
Contrary to the expected improvement in water
quality, there was an increase in chlorophyll a
concentrations, indicating increasing phytoplankton biomass, and a decrease in zooplankton
densities in the two years after biomanipulation.
Macrophyte biomass, however, increased,
probably due to the reduction of damage by adult
carps. But the macrophyte cover is still very
limited, and the gain in biomass after
biomanipulation is likely to be lost given the
increasing turbidity. While macrophyte growth is
limited by grazing and light availability
(turbidity), macrophyte fixation may also be
hampered by the steep slopes of the lake border
and by lake depth.
However the available data series are short and
the observed variations in water quality
macrophytes and zooplankton may reflect typical
inter-annual variability. To assess possible longterm results continued monitoring of fish stock,
macrophytes, zooplankton and water quality
(including nutrient concentrations) would be
necessary (monitoring stopped after February
2007, due to lack of funding).
Confirming
previous
observations,
the
deterioration of the trophic state is associated to
precipitation, showing the impact of run-off
nutrient input from the lake basin. No statistically
significant effect of aeration on turbidity could be
found in either pre- nor post-biomanipulation
data. Aeration showed also no positive effect on
dissolved oxygen concentrations (only available
for the pre-biomanipulation period). It is however
difficult to assess the true effect of aeration as it
was not continuously applied, but intensified in
the warmer seasons and suspended during winter.
Its application should therefore be reviewed,
testing its effects and testing alternative methods,
such as truly hypolimnetic aeration.
84
Given our results, there are several possible
reasons for the apparent failure to achieve a
lasting clear water state:
1) Fish removal may have been insufficient. Lake
restoration through biomanipulation has been
successfully applied in temperate regions
(Jeppesen et al. 2007a) but a number of
conditions must be met. For biomanipulation to
be successful, studies in the Netherlands suggest
that biomanipulation should involve drastic
planktivorous and benthivorous fish stock
reduction, removing >75% of the populations
(Meijer et al. 1999). A lake is considered to have
a good ecological status when fish stocks are
about 20 kg·ha-1 of benthivores and planktivores
each. Van de Bund & Van Donk (2002) show an
example where removing 50% of fish lead to
rapid recovery of pre-biomanipulation conditions.
In the Furnas Lake only about 60% of the
common carp and a small proportion of the roach
populations was removed. Furthermore, small
fish were not captures (80 mm net mesh-size).
2) Lake Furnas is sub-tropical. Only little is
known about the trophic dynamics and the role of
fishes in warm lakes. Jeppesen et al. (2005b,
2007a) present site studies suggesting that it is
more difficult to provoke and not least maintain a
trophic cascade effect by biomanipulation in
subtropical and tropical lakes than in temperate
lakes, for which the concept of biomanipulation
as a restoration tool was developed, with very
short-termed effects, even after massive
planktivorous fish-stock reduction. Biological
interactions differ, with often higher dominance
and abundance of small fish, more aggregation of
fish in vegetation, more fish cohorts per year,
higher proportions of omnivorous feeding by fish
and less piscivory in subtropical and tropical
lakes than in temperate lakes (Jeppesen et al.
2005b). Although lake Furnas behaves more like
a temperate than a sub-tropical system in terms of
dominance and abundance of small fish, the
recruitment of fish may have indeed been a
decisive factor in the biomanipulation outcome.
Adult fish removal is likely to have favoured the
development of juveniles, causing increas-ed
zooplankton consumption, decreased phytoplankton grazing, and consequently increased
turbidity (Scheffer et al. 1993). This could
explain the observed reduction in zooplankton in
the second year after biomanipulation.
Unfortunately, fish densities and size distributions
were not monitored after biomanipulation.
3) Nutrient levels may have been excessive. In
the years before biomanipulation, the Furnas
Lake had total phosphorous concentrations of
30 to 80 µg·l–1, apparently low enough to expect
biomanipulation to succeed (Meijer et al. 1999) –
however recent data is missing. But there are
studies suggesting that the influence of nutrient
loading on phytoplankton biomass is greater in
southern shallow lakes, indicating that nutrient
control may have to be a greater priority in these
systems than in more northern lakes (Romo et al.
2004, 2005; Moss et al. 2004). There are
examples of rapid switches to a turbid state after
P loadings increased to only 100 – 150 µg⋅l-1, and
of only short term increases in water transparency
in some warm shallow lakes after biomanipulation in combination with nutrient
reduction (Scasso et al. 2001; Beklioglu et al.
2003). Langeland (1990) argues that if the
external phosphorus load is mainly caused by
supply from non-point sources, which are
difficult to reduce, and the internal load is high,
the only realistic procedure is to manipulate the
fish stocks. The Furnas basin is classified as
protected water shed, and local authorities are
trying to enforce the strict rules that apply. But it
has proven very difficult to control nutrient input
into the lake. Furthermore, the sediments
constitute a nutrient pool, which may take
decades to diminish even if input could be
drastically diminished. A study of data from 2001
to 2003 (Rodrigues et al. 2004), confirms nutrient
accumulation in the sediments, revealing 873 mg
of total phosphorous per kilogram of surface
sediment, next to 20 g of aluminium and 18 g of
iron. It is estimated that about 90% of the
phosphorous mineralized by algae is stored in the
sediment in metal complexes, serving as a
phosphorous pool that can be re-dissolved and
made available to the phytoplankton, when
environmental conditions change. Sediments are
very mineralized (only 20% of organic matter in
dry weight) and display slightly acid, anaerobic
conditions (redox potential of -160 mV). Under
these conditions, biomanipulation may be
indispensable, though it remains a challenge to
managers to control the density of fish stocks in
biomanipulated systems over time. Another
nutrient that may be of importance is nitrogen.
González Sagrario et al. (2005) suggest that,
given moderate phosphorous concentrations,
nitrogen concentrations between 1000 and
2000 µg⋅l-1, as those observed in the Furnas Lake,
suppress macrophyte growth. Yet the lower total
nitrogen concentrations observed in the 90’s,
compared to the following decade, were
apparently (data are scarce for the 90’s) not
associated to a better trophic state.
4) Exceptionally rainy 2006 spring and winter
seasons may have further compromised
biomanipulation success, reducing water quality
through sediment and nutrient input from the
nutrient rich basin. Turbidity (and the TSI) in the
Furnas lake is known to oscillate, with peaks
generally following strong rainfalls (Santos et al.
2005); a relationship confirmed by our data. In
January 2007, after extreme rainfalls in December
(December precipitation doubled the normal
monthly average), the lake suffered the worst
algal bloom (mainly Microcystis aeruginosa)
recorded so far.
Recent studies suggest that a drastic reduction of
the external nutrient loading seems to be the best
way forward for restoring lakes (Jeppesen et al.
2005b), though appropriate nutrient thresholds are
not yet established for sub-tropical regions.
Studies in European and North American Lakes
(Anderson et al. 2005) showed that many
approached a new equilibrium of phosphorus (P)
and nitrogen (N) concentrations within 10 to 15
years and 0 to 5 years, respectively, after a major
reduction in loading. Phytoplankton biomass
decreased and a shift towards meso-oligotrophic
species dominance occurred. Worldwide studies
showed that fish respond surprisingly fast to the
loading reduction in lakes, with an increase in the
percentage of piscivores and decrease of total fish
biomass (Anderson et al. 2005; Jeppesen et al.
2005a). Local authorities now plan to improve
fertilization control in the basin of the Furnas
85
Lake and to create retention basins in affluent
creeks, to retain solids and nutrients and reduce
sediment accumulation and eutrophication in the
lake. Given the nutrient sediment pool and the
impact of non-algal light attenuation caused by
sediment re-suspension (Ibelings et al. 2007),
further biomanipulation may be necessary. But
according to the present study and lake subtropical characteristics, biomanipulation should
be combined with a significant reduction in
nutrient inputs and possibly applied repeatedly.
More data are needed for a better understanding
of the processes in the Furnas lake and more
studies are necessary for a better understanding of
warm lake systems in general; an understanding
that will become even more important as future
climate warming is expected to aggravate lake
eutrophication as a result of increasing water
residence times and decrease of vertical mixing,
as well as enhanced growth of phytoplankton
(Santos et al. 2004; Schindler 2006; Matzinger et
al. 2007; Jeppesen et al. 2007b).
ACKNOWLEDGEMENTS
This study was funded by the Direcção Regional
do Ordenamento do Território e dos Recursos
Hídricos (DROTRH), the Azorean governmental
agency for the management of water resources
and land use.
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Accepted 18 October 2008.
87
SHORT COMMUNICATION
New records of the giant ciliate Zoothamnium niveum
(Protozoa, Peritrichia)
PETER WIRTZ
Wirtz, P. 2008. New records of the giant ciliate Zoothamnium niveum (Protozoa,
Peritrichia). Arquipélago. Life and Marine Sciences 25: 89-91.
Peter Wirtz (e-mail: peterwirtz2004@yahoo.com), Centro de Ciências do Mar,
Universidade do Algarve, Campus de Gambelas, PT-8005-139 Faro, Portugal.
INTRODUCTION
RESULTS
Zoothamnium niveum (Hemprich & Ehrenberg,
1831) is a giant, colonial marine ciliate from
sulfide-rich habitats. It is covered with
chemoautotrophic sulfide-oxidizing bacteria that
give a snow-white appearance to the animal. The
feather-like colonies reach a size of up to 1.5 cm
(Bauer-Nebelsick et al. 1996; Ott et al. 1998;
Clamp & Williams 2006; Rinke et al. 2006,
2007). The species has been reported from rotting
plant material in shallow water in the Red Sea,
from Florida and the Caribbean, and from Corsica
Island (western Mediterranean Sea). It is here
reported from the eastern Atlantic, from the
eastern Mediterranean Sea and from an additional
site in the western Mediterranean Sea.
1) LANZAROTE ISLAND, CANARY ISLANDS,
EASTERN ATLANTIC
In front of Puerto del Carmen (28°55'05''N 13°39'36''W), on 20 April 1995, a large
aggregation of Zoothamnium niveum, consisting
of several hundred “feathers” was observed in
6 m depth. The aggregation grew on the three
sides of a rocky depression (Fig. 1). Some loose
plant material had aggregated in this depression
but no special attention was paid to it at that time.
MATERIAL AND METHODS
All observations were performed SCUBA diving
from shallow water down to 60 m depth. Animals
were photographed in situ, collected and
preserved in ethanol. Voucher specimens
collected at the Giglio site described below, were
deposited in the collection of the Bavarian State
collection of Zoology, Munich, Germany
(ZSM 20080136).
2) CYPRUS ISLAND, EASTERN MEDITERRANEAN
Zoothamnium niveum was encountered in a small
cave in 6.5 m depth near Cabo Greco, southeastern tip of Cyprus Island (34°57'45''N,
34°04'26''E), on 18 May 2002. The animals were
growing on the rock wall of the cave close to
cracks in the wall. No rotting plant material was
seen anywhere near them. Specimens were sent to
the university of Vienna, where the species
identification was confirmed (Ott, pers. comm.)
3) GIGLIO ISLAND, WESTERN MEDITERRANEAN
A rotting tree trunk was encountered on sandy
bottom in 30 m depth in the bay of Campese
(42°22'01''N - 10°53'33''E) on 26 September
2007. Zoothamnium niveum was growing on it,
close to the line where the wood touched the
89
sand. A sample attached to an empty Torpedo
tube sticking out from the wood was collected
and deposited in the Bavarian State collection of
Zoology in Munich, Germany. The water
temperature at this site was not measured but was
estimated to be no more than 19 degrees Celsius.
Fig. 1. Dense growth of Zoothamnium niveum at Lanzarote Island. Each of the feather-like structures is about
1 cm long.
DISCUSSION
At the Cyprus site, no rotting plant material was
in evidence. It appears possible that sulfidic water
seeped from the cracks of the cave wall where
Zoothamnium niveum was growing but rotting
plant material may have been present previously
and may have somehow been swept away
recently. The record in 30 m depth at the Giglio
site is the deepest record of the species, which
until now has been encountered in a depth range
of 0.3 to 14.9 m (Ott et al. 1998; Rinke et al.
2007). The water temperature at this site is also
the lowest recorded for Z. niveum growth.
As it is growing on short-lived substrates, the
species probably is an r-strategist that has widespread and frequent propagules. Colonization by
90
Zoothamnium occurs through a “swarmer
macrozooid” dispersal stage (Bauer-Nebelsick et
al. 1996). Ott et al. 1998 wrote “the high growth
rate, short life span and the extraordinary habitat
locating abilities of the swarmers (M. Bright, J.
Ott, unpubl. obs.) are consistent with the life style
of a pioneer in gap dynamics”. This, together with
the fact that the species has now been found at
sites in the western Atlantic, the eastern Atlantic,
the Mediterranean Sea, and the Red Sea, indicates
that the species is probably common throughout
(sub)tropical oceans of the world and has simply
been overlooked in other areas until now.
ACKNOWLEDGEMENTS
I am grateful to Renee and Dea van Leeuwen at
Puerto del Carmen, Lanzarote, and to Hubert
Böhm at Pernera, Cyprus, for their kind help. The
Centro de Ciências do Mar (CCMAR) financed
the trip to Cyprus Island.
REFERENCES
Bauer-Nebelsick, M., C.F. Bardele & J.A. Ott 1996.
Redescription of Zoothamnium niveum (Hemprich
&
Ehrenberg,
1831)
Ehrenberg,
1838
(Oligohymenophora, Peritrichida), a ciliate with
ectosymbiotic,
chemoautotrophic
bacteria.
European Journal of Protistology 32: 18–30.
Clamp, J.C. & Williams, D. 2006. A molecular
phylogenetic investigation of Zoothamnium
(Ciliophora Peritrichia, Sessilida). Journal of
Eukariotic Microbiology 53: 494–498.
Ott, J.A., M. Bright & F. Schiemer 1998. The ecology
of a novel symbiosis between a marine peritrich
ciliate and chemoautotrophic bacteria. P.S.Z.N.
Marine Ecology 19: 229–243.
Rinke, C., S. Schmitz-Esser, K. Stoecker, A.D.
Nussbaumer, D.A. Molnar, K. Vanura, M. Wagner,
M. Horn, J.A. Ott & M. Bright 2006. “Candidatus
Thiobios zoothamnicoli”, an ectosymbiotic
bacterium covering the giant marine ciliate
Zoothamnium niveum. Applied and Environmental
Microbiology 72: 2014–2021.
Rinke, C., R. Lee, S. Katz & M. Bright 2007. The
effects of sulphide on growth and behaviour of the
thiotrophic Zoothamnium niveum symbiosis.
Proceedings of the Royal Society B 274: 22592269.
Accepted 17 June 2007.
91
SHORT COMMUNICATION
First record of the mealy plum aphid Hyalopterus pruni
(Geoffroy), (Homoptera, Aphidoidea) in Madeira Island
FERNANDO A. ILHARCO & A. ONOFRE SOARES
Ilharco, F.A. & A.O. Soares 2008. First record of the mealy plum aphid
Hyalopterus pruni (Geoffroy), (Homoptera, Aphidoidea) in Madeira Island.
Arquipélago. Life and Marine Sciences 25: 93-94.
Fernando A. Ilharco, Departamento de Protecção de Plantas, Entomologia, Estação
Agronómica Nacional, PT-2784-505 Oeiras, Portugal; António Onofre Soares
(e-mail: onofre@uac.pt), CIRN, Departamento de Biologia, Universidade dos Açores, Rua
da Mãe de Deus, 13-A, PT-9501-801 Ponta Delgada, Portugal.
During a scientific expedition to Madeira Island
organized by the Department of Biology of the
University of the Azores, in September 1997, for
studying coccinellids associated with some
crops, the second author (A.O. Soares) collected
14 aphid samples, one of them containing the
mealy plum aphid, Hyalopterus pruni (Geoffroy,
1762), a species until then unknown in the
archipelago of Madeira and a potential threat to
some Prunus crops. The first author (F.A.
Ilharco) considers Hyalopterus amygdali
(Blanchard) a possible synonym of H. pruni. In
Macaronesia, H. pruni is already known in
Canary islands (Nafria et al. 1977), and van
Harten (1993) reported it from Cape Verde
islands. It is a cosmopolitan aphid species, with
Prunus trees as primary hosts and the
gramineous Arundo donax L. and Phragmites
australis (Cav.) Steudel (= P. communis Trin.) as
secondary hosts. In Madeira Island it was
collected on Arundo donax on 26 Setember 1997
in Santana, Fajã da Rocha-do-Barco. In
continental Portugal, H. pruni is a common
species, either on primary hosts or Arundo and
Phragmites. A large population was also seen on
cultivated bamboo (Ilharco, 1996).
On Prunus trees H. pruni lives in large
colonies on the underside of leaves, excreting
abundant honeydew. On secondary host plants
the aphid lives on the upper surface of leaves
(Fig. 1), frequently forming also large colonies.
The aphids are green on Prunus but green or red
on Arundo or Phragmites, with the body covered
by wax powder. They are not visited by ants.
Other aphid species collected by the second
author during this expedition to Madeira Island:
Acyrthosiphon pisum (Harris) – vagrant,
Seixal
Aphis fabae Scopoli - vagrant, Faial
Aphis gossypii Glover - on Hibiscus sp.,
Funchal
Aphis spiraecola Patch - vagrant, Faial
Brevicoryne brassicae (Linné) – on Brassica
oleraceae L., Santana
Cavariella theobaldi (Gillette & Bragg) – on
Salix sp., Camacha and Levada da Serra
Rhopalosiphum maidis (Fitch) - on Zea mays
L., Santo da Serra
93
Fig. 1. Hyalopterus pruni on Phragmites australis (by F.A. Ilharco)
Rhopalosiphum padi (Linné) - on Zea mays,
Santo da Serra and Curral das Freiras
Sitobion avenae (Fabricius) - vagrants, Porto
Moniz, Faial and Seixal
Uroleucon sonchi (Linné) - on Sonchus sp.,
Quinta Grande; vagrants, Seixal and Faial
REFERENCES
Harten, A. van 1993. The aphids (Homoptera:
Aphidoidea) of the Cape Verde Islands. Courier
Forschungsinstitut Senckenberg 159: 381-385.
Ilharco, F.A. 1996. 2º aditamento ao Catálogo dos
Afídeos de Portugal Continental (Homoptera,
Aphidoidea). Agronomia Lusitana 45(1-3): 5-66
(1991-95). [Second supplement to the Aphid
Catalogue of Continental Portugal; in Portuguese]
Nafria, J.M.N., Hernandez, A.C. & Durante, M.P.M
1977. Los pulgones (Hom. Aphidoidea) de las Islas
Canarias. Pp. 17-37 in: Nafria, J.M.N., M.P.M.
Durante & A.C. Hernandez (Eds). Estudios
afidológicos de las Islas Canarias y de la
Macaronesia. Excelentisimo Cabildo Insular de
Tenerife, Aula de Cultura, Salamanca. 91 pp. [The
aphids (Hom. Aphidoidea) of Canary Islands; in
Spanish]
Accepted 21 October 2008.
94
EDITORIAL NOTES
We acknowledge with gratitude the financial support given by Fundação para a Ciência e
Tecnologia (FCT), Lisboa and by IMAR, Centro do Instituto do Mar, at the University of the
Azores, which made it possible to publish this issue.
The Editor of Arquipélago - Life and Marine Sciences, sincerely thanks the scientist listed below,
who served as reviewers for the numbers 23A, 24 and Supplement 6:
23A:
Alexandra Marçal Correia, Portugal
Carlo Nike Bianchi, Italy
Cecília Sergio, Portugal
Filipe Porteiro, Azores, Portugal
Helena Isidro, Azores, Portugal
Jacob Gonzalez-Solis, Spain
Joël Bried, France
Ian Tittley, UK
Pablo Abaunza, Spain
Peter Boyle, UK
Poul Møller Pedersen, Denmark
Rosalina Gabriel, Azores, Portugal
Ruth Nielsen, Denmark
Supplement 6. Parasitology workshop:
Neil Campbell, UK
Paul Brickle, Falkland islands
24:
Alexander Arkhipin, Falkland Islands
Chad Jones USA
Dale Calder, Canada
Daphne Lee, New Zealand
Gary Williams, USA
Graham Pierce, UK
Jacob Gonzalez-Solis, Spain
Joël Bried, Azores, Portugal
Lawrence Lacey, USA
Leen van Ofwegen. Netherlands
M. Alexandra Bitner, Poland
Malcolm Clarke, Azores, Portugal
Mark Bolton, UK
Michael Kirby, USA
Michel Canard, France
Monica Silva, Azores, Portugal
Pedro Afonso, Azores, Portugal
Peter Schuckert, Switzerland
Rafael La Perna, Italy
Roger Williams, USA
Takashi Kamijo, Japan
Ted Pietch USA
95
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ISSN 0873-4704
ARQUIPÉLAGO - Life and Marine Sciences
No. 25 - 2008
CONTENTS:
PAGE
GASPAR, C., P.A.V. BORGES & K.J. GASTON
Diversity and distribution of arthropods in native forests of the Azores archipelago
1
BORGES, P.A.V.
Distribution and abundance of arthropod species in pasture communities of three Azorean islands
(Santa Maria, Terceira and Pico)
31
MONTIEL, R., V. VIEIRA, T. MARTINS, N. SIMÕES & M.L. OLIVEIRA
The speciation of Noctua atlantica (Lepidoptera, Noctuidae) occurred in the Azores as supported
by a molecular clock based on mitochondrial COI sequences
43
PALMERO, A.M., A. MARTÍNEZ, M.C. BRITO & J. NÚÑEZ
Acoetidae (Annelida, Polychaeta) from the Iberian Peninsula, Madeira and Canary islands,
with description of a new species
49
WIRTZ, P. & C. D’UDEKEM D’ACOZ
Crustaceans associated with Cnidaria, Bivalvia, Echinoidea and Pisces at São Tomé
and Príncipe islands
63
WIRTZ, P.
The Gulf of Guinea goby-shrimp symbiosis and a review of goby-thalassinidean associations
71
BIO, A., A. COUTO, R. COSTA, A. PRESTES, N. VIEIRA, A. VALENTE & J. AZEVEDO
Effects of fish removal in the Furnas Lake, Azores
77
SHORT COMMUNICATIONS:
WIRTZ , P.
New records of the giant ciliate Zoothamnium niveum (Protozoa, Peritrichia)
89
ILHARCO, F.A. & A. ONOFRE SOARES
First record of the mealy plum aphid Hyalopterus pruni (Geoffroy), (Homoptera, Aphidoidea)
in Madeira Island
93
EDITORIAL NOTES
95
Filipe Porteiro