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Biodiversity and distribution of epibiontic communities on
Caridina ensifera (Crustacea, Decapoda, Atyidae) from Lake
Poso: comparison with another ancient lake system of
Sulawesi (Indonesia)
Gregorio Fernandez-Leborans1 and Kristina von Rintelen2
1Department of Zoology, Faculty of
Biology, Pnta 9, Complutense University,
28040 Madrid, Spain; 2Museum fur
Naturkunde, Humboldt-Universitat Berlin,
Invalidenstrasse 43, D-10115 Berlin,
Germany
Keywords:
Caridina ensifera, epibiontic communities,
distribution, colonization patterns, Lake
Poso, lakes of the Malili system,
comparison, Sulawesi
Accepted for publication:
27 November 2008
Abstract
Fernandez-Leborans, G. and von Rintelen, K. 2010. Biodiversity and
distribution of epibiontic communities on Caridina ensifera (Crustacea,
Decapoda, Atyidae) from Lake Poso: comparison with another ancient lake
system of Sulawesi (Indonesia). — Acta Zoologica (Stockholm) 91: 163–175
The epibiont communities of the shrimp Caridina ensifera, endemic to Lake
Poso (Sulawesi, Indonesia), were analysed. Most of the epibiont species were
ciliated protozoa belonging to three suctorian genera (Acineta, Podophrya and
Spelaeophrya), three peritrich genera (Zoothamnium, Vorticella and Cothurnia),
and a haptorid genus (Amphileptus). There was also a rotifer epibiont of the
genus Embata. Epibionts were identified to species level. There were 14 to 1114
epibionts per shrimp. The distribution of the epibiont species on the surface of
the basibiont was recorded, calculating the number on the different colonized
individuals of C. ensifera. The most abundant species, Zoothamnium intermedium
and Acineta sulawesiensis, were also the most widely distributed. There was a
significant difference between the spatial distributions of the different epibiont
species. The analysis of the number of the epibiont species throughout the
anteroposterior axis of the shrimp showed a gradient from the anterior to the
posterior end of the body. Data from Lake Poso were compared with those of
the Malili lake system (Sulawesi), obtained from its endemic shrimp, Caridina
lanceolata. Lake Poso had the highest mean diversity, while Lake Mahalona
showed the highest maximum diversity. All lakes were correlated with respect to
the mean number of epibionts on the anatomical units of the shrimp, which
showed a similar general distribution. The distributions of the different epibiont
species were compared between the lakes. The possible adaptations of the
epibionts as well as the colonization patterns were discussed. From the statistical
results and the analysis of the distributions, we propose that in these
communities epibiont species have a pattern of colonization in which they follow
a behaviour as a whole; each species has a differential distribution, with the
species occupying the available substratum with the particular requirements of
each functional group, but there is a trend towards maintaining an equilibrium
among species and groups, compensating for diversity and number of
individuals. In all lakes there was an epibiont distribution model comprising the
maintenance of an anteroposterior axis gradient, which was supported by the
fluctuation in diversity and number of individuals of the different functional
groups of epibiont species. The functional role of the different groups of species
seems to tend towards sustainability with little global variation among the lakes.
Gregorio Fernandez-Leborans, Department of Zoology, Faculty of Biology, Pnta 9,
Complutense University, 28040 Madrid, Spain. E-mail: [email protected]
Acta Zoologica (Stockholm) 91: 163–175 (April 2010) doi: 10.1111/j.1463-6395.2009.00395.x
� 2009 The Authors
Journal compilation � 2009 The Royal Swedish Academy of Sciences 163
Introduction
During the last three decades a number of articles have
focused on epibiosis related to Crustacea (Dawson 1957;
Eldred 1962; Maldonado and Uriz 1992; Gili et al. 1993;
Morado and Small 1995; Dick et al. 1998; Key et al. 1999;
Fernandez-Leborans and Tato-Porto 2000a,b). Epibiosis is
an association between two organisms: the epibiont and the
basibiont. The term ‘epibiont’ includes organisms that, during
the sessile phase of their life cycle, are attached to the surface
of a living substratum, while the basibiont lodges the epibiont
(Wahl 1989; Wahl et al. 1997).
Despite the fact that the presence of epibionts (previously
referred to as commensals, epizoics, symbionts) on crusta-
ceans has long been known, it is only recently that a new
perspective has been brought to their study. This has not
only involved a noticeable increase of newly described taxa,
but has also highlighted the fact that epibiotic relationships
are important in many biological fields: physiological, eco-
logical, evolutionary and those related to conservation and
biodiversity.
A number of protozoan ciliate species have been described
as epibionts on crustaceans, and unique aspects of the bio-
logy and ecology of their basibiont crustacean taxa can be
explained by epibiosis (Bottom and Ropes 1988; Abello et al.
1990; Abello and Macpherson 1992). Crustacean groups
such as cladocerans, copepods, cirripeds, isopods, amphi-
pods and decapods, include species that have been found as
basibionts for protozoan and invertebrate epibionts (Ross
1983). Protozoan epibionts are representative of the follow-
ing groups: apostomatids, chonotrichids, suctorians, peri-
trichs and heterotrichs (Corliss 1979; Lynn and Small
2000). The invertebrate epibionts include forms that belong
to a number of different phyla (including Porifera, Cnidaria,
Platyhelminthes, Nemertea, Rotifera, Nematoda, Polychaeta,
Cirripedia, Decapoda, Gastropoda, Bivalvia, Phoronida,
Bryozoa and Ascidiacea).
On the Indonesian island of Sulawesi (the former Celebes)
two lake systems (the Malili lake system and Lake Poso;
Fig. 1) are important areas of aquatic biodiversity and har-
bour several endemic species flocks, for example shrimps
(Schenkel 1902; Woltereck 1937a,b; Chace 1997; Zitzler and
Cai 2006), molluscs (Korniushin and Glaubrecht 2003;
Rintelen and Glaubrecht 2004, 2006; Rintelen et al. 2004)
or fish (Parenti and Soeroto 2004; Herder et al. 2006). The
two lake systems are not connected but provide similar
environmental conditions for their respective faunas. The
freshwater shrimp Caridina ensifera (Crustacea, Decapoda,
Atyidae) is part of an endemic species flock of currently three
lacustrine and one riverine species described from Lake Poso
(Schenkel 1902; Chace 1997). It is abundant in the lake and
often collected by local fishermen (K. von Rintelen, personal
field observation).
The epibiont communities on C. ensifera were analysed for
their biological and taxonomical characteristics as well as
their distribution on the surface of the shrimp. These epi-
biont communities were compared with those of another
shrimp Caridina lanceolata, which is endemic to the Malili
lake system (Fernandez-Leborans et al. 2006). The aim of
this work is to contribute to the description and explanation
of the relationships and patterns of distribution of the
protozoan epibiont communities on the respective endemic
shrimp species in the two lake systems. Detailed data and
results of this study are described below.
Materials and Methods
Specimens of C. ensifera were collected from the south shore
of Lake Poso, Central Sulawesi, Indonesia, in March 2004
(Fig. 1). Samples were fixed in 95% ethanol and then trans-
ferred to 75% ethanol for light microscopy. In the laboratory,
shrimps were dissected and each anatomical unit was
observed under a stereoscopic microscope.
For scanning electron microscopy (SEM) of the epibionts,
shrimp specimens fixed in 95% ethanol were dehydrated in
100% ethanol for 30 min. Afterwards, they were critical-point
dried with a BAL-TEC CPD 030, mounted on aluminium
specimen stubs with standard adhesive pads and coated with
gold–palladium using a Polaron SC7640 Sputter Coater.
Pictures were taken on an LEO 1450VP SEM (software:
32 V02.03) at 10 kV.
Epibionts on the surface of the shrimp were observed and
counted on each anatomical unit under stereoscopic and
light microscopes. Number of colonial species was indicated
as number of zooids. To identify the protozoan epibionts,
they were isolated and treated using the Fernandez-Leborans
and Castro de Zaldumbide (1986) silver carbonate tech-
nique and with methyl green and neutral red. Permanent
slides were made for the stained ciliates. To identify the
rotifers, the trophi were analysed using the procedure
indicated by R.J. Shiel (University of Adelaide, Australia;
personal communication), treating isolated specimens,
in 10% glycerol/water solution, with 2.5% sodium
hypochlorite. Measurements of the epibionts were made with
an ocular micrometer. Light microscope images were
obtained using KS300 Zeiss IMAGE ANALYSIS software
and were used to identify the epibiont species. Statistical
analyses were performed using the STATGRAPHICS and SPSS
programs.
All epibionts examined are deposited in the Museum of
Natural History, Berlin, Germany (ZMB).
Results
The epibionts on C. ensifera included the following proto-
zoan ciliates: the suctorians Acineta sulawesiensis, Podophrya
maupasi and Spelaeophrya polypoides, the peritrichs Zootham-
nium intermedium, Vorticella globosa and Cothurnia compressa,
and the haptorid Amphileptus fusidens. In addition, there was
the rotifer Embata laticeps (Fig. 2).
Epibiosis on Caridina from Lake Poso • Fernandez-Leborans and von Rintelen Acta Zoologica (Stockholm) 91: 163–175 (April 2010)
� 2009 The Authors
164 Journal compilation � 2009 The Royal Swedish Academy of Sciences
Distribution of the epibionts
Of the infested shrimps, 25% were ovigerous females. The
number of epibionts per basibiont fluctuated between 14 and
1114 (mean 314.6). Only 0.45% of these epibionts were
rotifers, the ciliate protists comprised the highest proportion
of the mean number of epibionts (mean 313.19) (Table 1).
Among the ciliate epibionts, the highest number of individuals
were either Zoothamnium or Acineta, which represented
94.2% of the mean number of epıbionts (Acineta showed the
highest proportion, 59.94%). The other ciliates accounted for
5.33% of the mean number of epıbionts on the shrimp
(Table 1).
Antennulae, antennae, maxillipeds and uropods were the
anatomical units with the highest mean number of epıbionts.
The most abundant epibionts, Zoothamnium and Acineta,
were also the most widely distributed on the surface of the
shrimp. The rotifer, although rare, was also widely distributed
spatially on the basibionts (Table 2).
The statistical comparison between the spatial distributions
of the epibiont species on the body of C. ensifera indicated
a significant difference between the species (F, 11.05;
P £ 0.05). The principal component analysis performed
using the mean number of epibiont species on the anatomical
units of the shrimp showed, in the plot of the two first prin-
cipal components (Fig. 3), two clusters, one with Amphilep-
tus, Vorticella and Spelaeophrya, and another including
Zoothamnium, Acineta, Podophrya and Embata. This second
cluster integrated the epibiont species most widely distributed
on the basibiont, in contrast to the scarcely present species of
the other cluster. The ciliate Cothurnia appeared separately
from these clusters because of its presence on the posterior
end of the basibiont body in low numbers.
Hierarchical conglomerate analysis produced a dendro-
gram using the mean number of the different epibiont species
on the anatomical units of the shrimp. The units were
grouped in five clusters (Fig. 4). A cluster corresponded
to the antennulae, antennae and uropods (18.75% of the
Fig. 1—Geographical area of the study. —A. The Indo-Malaysian Archipelago. —B. Sulawesi. —C. Lake Poso. —D. Lakes of the Malili system.
Acta Zoologica (Stockholm) 91: 163–175 (April 2010) Fernandez-Leborans and von Rintelen • Epibiosis on Caridina from Lake Poso
� 2009 The Authors
Journal compilation � 2009 The Royal Swedish Academy of Sciences 165
anatomical units). These units had a high number of epi-
bionts (mean 15.80 epibionts per unit). The second cluster
included 46.88% of the anatomical units (rostrum, eyes,
second right pereiopod, third, fourth and fifth pereiopods,
fourth and fifth pleopods and telson); these units showed the
lowest number of epibionts (mean 2.87 epibionts per unit).
The third cluster comprised the rest of the pleopods (first,
second and third pleopods, 18.75% of the units) and had a
moderate number of epibionts (mean 8.27 per unit). In the
fourth cluster there were the first and left second pereiopods
Fig. 2—The epibiont species. —A. Acineta sulawesiensis (·1070). —B. Podophrya maupasi (·792). —C. Spelaeophrya polypoides (·280).
—D. Zoothamnium intermedium (·420). —E. Vorticella globosa (·710). —F. Cothurnia compressa (·820). —G. Amphileptus fusidens (·770).
—H. Embata laticeps (·200).
Epibiosis on Caridina from Lake Poso • Fernandez-Leborans and von Rintelen Acta Zoologica (Stockholm) 91: 163–175 (April 2010)
� 2009 The Authors
166 Journal compilation � 2009 The Royal Swedish Academy of Sciences
(9.38% of the units), with a mean of 9.26 epibionts per unit.
The fifth cluster corresponded to the maxillipeds (6.25%), the
units with the highest infestation (mean 49.6 epibionts per
unit).
Distribution along the anteroposterior axis of C. ensifera
Figure 5 shows the mean number of different epibiont
species and the total epibiont mean number along the antero-
posterior axis of the shrimp. Anatomical units were consid-
ered in five groups (rostrum, eyes, antennae and antennulae;
maxillipeds; pereiopods; pleopods; uropods and telson).
Zoothamnium was distributed mainly on the posterior half of
the body, especially on the pleopods where it represented
50.48% of the epibionts. It was also found attached to the
pereiopods (18.3%) and the maxillipeds (15.4%). In con-
trast, Acineta was more abundant on the anterior part of the
shrimp, and 73.90% of the epibionts were located on the
maxillipeds (43.2%), rostrum, antennae, antennulae and eyes.
Cothurnia and Vorticella presented a higher number of
epibionts towards the posterior end of the body, where they
represented 68.8% and 39% respectively, although Vorticella
showed a remarkable number of individuals on the pereio-
pods (35.3% of the epibionts). Spelaeophrya was more abun-
dant on the anterior part of the body (rostrum, antennae,
antennulae and eyes) (77.9%). Podophrya colonized mainly
the maxillipeds, and Amphileptus colonized the ends of the
body, while Embata colonized the anterior end, pereiopods
and pleopods. The epibiont community was distributed fol-
lowing a pattern in which the species occupied the places with
behaviour of an ensemble, each species showing a distinctive
distribution along the basibiont body. There was a significant
difference between the epibiont species considering the
mean number of epibionts on the different groups of
anatomical units (F, 5.98; P £ 0.05), and also considering the
Table 1 Length and width of the specimens of Caridina ensifera
analysed and distribution of the epibionts on the crustacean
Mean
Standard
deviation Minimum Maximum
Length of the shrimp (mm) 24.19 4.65 13.00 33.00
Width of the shrimp (mm) 3.90 0.78 2.00 5.00
Length of ovigerous female
shrimp (mm)
25.40 3.91 19.00 29.00
Width of ovigerous female
shrimp (mm)
4.60 0.55 4.00 5.00
Number of protozoa per shrimp 313.19 305.16 12.00 1110.00
Number of protozoa per
ovigerous female shrimp
662.20 266.05 429.00 1110.00
Number of rotifers per shrimp 1.43 1.75 0.00 6.00
Number of rotifers per
ovigerous female shrimp
3.40 2.30 1.00 6.00
Number of epibionts per shrimp 314.62 306.07 14.00 1114.00
Number of epibionts per
ovigerous shrimp
665.60 266.59 430.00 1114.00
n ¼ 40.
Fig. 4—Dendrogram of the hierarchical
cluster analysis (anatomical units)
performed using the mean numbers of
epibionts on the different anatomical units
of the shrimps analysed (metric distance:
City Block (Manhattan); method: Ward).
Fig. 3—Two first principal components of the principal component
analysis performed using the mean number of individuals of each
epibiont species on the anatomical unit of the different shrimps
analysed.
Acta Zoologica (Stockholm) 91: 163–175 (April 2010) Fernandez-Leborans and von Rintelen • Epibiosis on Caridina from Lake Poso
� 2009 The Authors
Journal compilation � 2009 The Royal Swedish Academy of Sciences 167
Table 2 Number of each genus of epibiont on the different anatomical units of Caridina ensifera
Anatomical unit Acineta Vorticella Podophrya Cothurnia Zoothamnium Spealophrya Amphileptus Emabata
Rostrum 3.05 ± 8.43 0.10 ± 0.44 – 0.05 ± 0.22 1.29 ± 5.89 – 0.10 ± 0.30 0.05 ± 0.22
(0–35) (0–2) (0–1) (0–27) (0–1) (0–1)
Left ocular orbit 0.10 0.44 0.05 ± 0.22 0.05 ± 0.22 – 0.52 ± 1.21 – – 0.05 ± 0.22
(0–2) (0–1) (0–1) (0–5) (0–1)
Right ocular orbit 0.29 ± 0.78 – – – 1.95 ± 5.06 – – –
(0–3) (0–22)
Left antennule 15.19 ± 19.78 0.10 ± 0.44 – 0.14 ± 0.48 1.43 ± 2.94 0.29 ± 0.90 0.14 ± 0.36 –
(0–68) (0–2) (0–2) (0–11) (0–4) (0–1)
Right antennule 13.86 ± 16.72 0.05 ± 0.22 – 0.29 ± 0.96 0.10 ± 0.44 – – –
(0–47) (0–1) (0–4) (0–2)
Left antenna 13.05 ± 18.80 – – 0.76 ± 1.41 2.14 ± 4.62 0.10 ± 0.30 0.05 ± 0.22 0.10 ± 0.30
(0–74) (0–5) (0–18) (0–1) (0–1) (0–1)
Right antenna 12.48 ± 17.07 – – 0.76 ± 2.30 2.10 ± 3.62 0.14 ± 0.65 0.14 ± 0.48 0.14 ± 0.48
(0–72) (0–9) (0–11) (0–3) (0–2) (0–2)
Left maxilliped 40.10 ± 44.51 – 0.86 ± 3.93 – 9.10 ± 16.86 – – 0.10 ± 0.44
(0–144) (0–18) (0–67) (0–2)
Right maxilliped 41.29 ± 54.08 – 0.33 ± 1.06 – 7.33 ± 13.19 – 0.10 ± 0.30 0.10 ± 0.44
(0–204) (0–4) (0–45) (0–1) (0–2)
Left first pereiopod 6.57 ± 12.43 – – – 5.81 ± 12.50 0.05 ± 0.22 0.05 ± 0.22 0.14 ± 0.36
(0–53) (0–48) (0–1) (0–1) (0–1)
Right first pereiopod 5.38 ± 11.01 – 0.24 ± 0.89 – 3.05 ± 5.30 – – –
(0–39) (0–4) (0–19)
Left second pereiopod 4.10 ± 5.74 – – – 2.52 ± 4.47 – – 0.05 ± 0.22
(0–21) (0–15) (0–1)
Right second pereiopod 2.14 ± 4.53 – 0.10 ± 0.44 – 2.57 ± 5.74 – – –
(0–19) (0–2) (0–20)
Left third pereiopod 1.95 ± 3.34 – – – 0.57 ± 1.36 – – 0.10 ± 0.44
(0–13) (0–6) (0–2)
Right third pereiopod 0.86 ± 2.41 – 0.05 ± 0.22 – 3.05 ± 7.33 – – 0.05 ± 0.22
(0–11) (0–1) (0–26) (0–1)
Left fourth pereiopod 1.62 ± 4.25 0.43 ± 1.96 – – 0.76 ± 1.95 – – –
(0–18) (0–9) (0–8)
Right fourth pereiopod 1.52 ± 2.80 0.05 ± 0.22 – – 0.62 ± 2.40 – – –
(0–10) (0–1) (0–11)
Left fifth pereiopod 0.38 ± 1.53 – – – 1.67 ± 3.90 – – –
(0–7) (0–15)
Right fifth pereiopod 0.38 ± 1.53 – – – – – – –
(0–7)
Left first pleopod 0.57 ± 1.40 – – – 6.10 ± 13.92 0.05 ± 0.22 – 0.10 ± 0.44
(0–6) (0–53) (0–1) (0–2)
Right first pleopod 1.43 ± 2.60 – – 0.10 ± 0.44 7.62 ± 13.08 – 0.05 ± 0.22 –
(0–11) (0–2) (0–44) (0–1)
Left second pleopod 0.57 ± 1.36 – – 0.14 ± 0.48 7.48 ± 24.84 – 0.05 ± 0.22 –
(0–5) (0–2) (0–114) (0–1)
Right second pleopod 0.52 ± 1.63 – 0.33 ± 1.53 0.14 ± 0.48 9.62 ± 24.57 – – 0.10 ± 0.44
(0–7) (0–7) (0–2) (0–109) (0–2)
Left third pleopod 0.86 ± 1.90 – – 0.14 ± 0.48 5.90 ± 13.46 – – 0.05 ± 0.22
(0–8) (0–2) (0–58) (0–1)
Right third pleopod 0.33 ± 0.91 0.05 ± 0.22 – – 7.52 ± 15.74 – – 0.05 ± 0.22
(0–3) (0–1) (0–60) (0–1)
Left fourth pleopod 0.71 ± 0.71 – – – 3.48 ± 7.98 – – –
(0–7) (0–29)
Right fourth pleopod 0.48 ± 1.54 – – 0.19 ± 0.51 3.19 ± 8.63 – – 0.05 ± 0.22
(0–7) (0–2) (0–38) (0–1)
Left fifth pleopod 0.62 ± 1.83 – – 0.76 ± 2.30 0.67 ± 1.56 0.05 ± 0.22 – –
(0–8) (0–9) (0–6) (0–1)
Right fifth pleopod 0.10 ± 0.30 – 0.14 ± 0.65 – 2.33 ± 4.85 – 0.10 ± 0.30 0.10 ± 0.30
(0–1) (0–3) (0–17) (0–1) (0–1)
Telson 0.33 ± 1.11 0.29 ± 1.31 0.29 ± 1.31 – 2.62 ± 3.83 – 0.38 ± 1.75 –
(0–5) (0–6) (0–6) (0–12) (0–8)
Left uropod 8.14 ± 11.78 – – 5.33 ± 10.91 3.19 ± 5.14 – – 0.10 ± 0.30
(0–44) (0–33) (0–16) (0–1)
Right uropod 9.67 ± 16.37 0.24 ± 1.09 0.10 ± 0.44 2.33 ± 5.15 1.52 ± 5.02 – – 0.05 ± 0.22
(0–60) (0–5) (0–2) (0–21) (0–23) (0–1)
Data are given as mean ± standard deviation (minimum–maximum); n ¼ 40.
Epibiosis on Caridina from Lake Poso • Fernandez-Leborans and von Rintelen Acta Zoologica (Stockholm) 91: 163–175 (April 2010)
� 2009 The Authors
168 Journal compilation � 2009 The Royal Swedish Academy of Sciences
mean number of epibionts on the different anatomical units
separately (F, 5.07; P £ 0.05). The total number of epibionts
indicated that each zone on the anteroposterior axis of the
shrimp did not present a remarkable difference in coloniza-
tion; the areas fluctuated between 11.02% on the posterior
end and 31.67% on the maxillipeds. The anterior region
(rostrum, antennae, antennulae, eyes and maxillipeds) of the
basibiont represented 54.37% of the epibionts. Pereiopods,
pleopods, uropods and telson accounted for 45.63% of the
colonization.
Comparison of epibiont communities from Lake Poso and the
Malili lake system
The data for the epibiont communities on C. ensifera from
lake Poso were compared with those of C. lanceolata from
lakes of the Malili system (Fernandez-Leborans et al. 2006),
both being shrimp species endemic to their respective
lacustrine areas. The specimens of C. ensifera from Lake Poso
were larger and had more individual epibionts than the
C. lanceolata basibionts from the lakes of the Malili system
(Table 3). The most epibiont species were found in Lake
Poso, which had 80% of epibiont species. In the Malili system,
Lake Mahalona had the most (70%) epibiont species,
whereas Lake Towuti had the lowest (30% of the species).
However, if the sum of mean number of individuals of the
different epibiont species was considered, Lake Towuti was
the most important of the lakes of the Malili system, with
49.34% of the total numbers of individuals in the Malili
system. Lake Poso showed the highest mean number of
epibionts, accounting for 38.28% of the total number of the
four lakes. The different groups of species tended to maintain
populations in the diverse lakes. This was the case for the
peritrich ciliates. In Lake Towuti, the number of species of
peritrich ciliates was low, but this was compensated for by an
increase in the number of individuals. In contrast, Lake
Mahalona had a higher number of peritrich species, but
lower numbers of these ciliates (Table 3).
The mean number of epibionts on the five groups of
anatomical units along the anteroposterior axis of the shrimp
was considered. We found a significant difference between
the different lakes (F, 3.59; P £ 0.05), especially between
Lake Matano and Lake Poso (t ¼ )2.66; P £ 0.05) (Fig. 6).
However, there was a significant correlation between the
distributions in Lake Mahalona and Lake Poso, and between
the mean of all three lakes of the Malili system and Lake Poso
(0.90; P £ 0.05). The mean number of epibionts on the different
anatomical units in all lakes of the Malili system correlated
with that in Lake Poso (0.72–0.94; P £ 0.05) (Fig. 7).
Considering the distribution of the epibiont species on the
basibionts, there were similarities among all lakes: Acineta
predominated on the anterior part of the basibiont, whereas
Fig. 5—Distribution of each epibiont
species (mean number of individuals) and
total mean number of epibionts, along the
anteroposterior axis of Caridina ensifera.
Anatomical units are considered in five
groups.
Acta Zoologica (Stockholm) 91: 163–175 (April 2010) Fernandez-Leborans and von Rintelen • Epibiosis on Caridina from Lake Poso
� 2009 The Authors
Journal compilation � 2009 The Royal Swedish Academy of Sciences 169
Zoothamnium and Cothurnia tended to appear on the posterior
areas of the shrimp. These epibiont species were generally the
most abundant. For each anatomical unit and epibiont spe-
cies, the mean number of epibionts was calculated. The pat-
tern arising from these values with respect to all the colonized
anatomical units showed peculiarities in each lake, which are
illustrated by the different dendrograms from the
hierarchical cluster analysis (Fernandez-Leborans et al. 2006).
The epibionts in the three lakes of the Malili system showed a
similar colonization pattern with respect to the anteroposterior
axis of the shrimp. There were more individual epibionts on
the anterior areas of the body, especially on the maxilli-
peds, antennae and antennulae. The pleopods and uropods
are the second most colonized group of appendages, in
Table 3 Length and width of the basibionts and number of epibionts in the Malili system (Fernandez-Leborans et al. 2006) and Lake Poso
Malili system
Lake Towuti Lake Matano Lake Mahalona Lake Poso
Length of the shrimp (mm) 21.26 (14.00–27.00) 16.10 (11.00–21.00) 15.90 (11.00–19.70) 24.19 (13.00–33.00)
Width of the shrimp (mm) 2.96 (2.00–4.50) 2.65 (2.00–4.00) 3.12 (2.00–4.60) 3.90 (2.00–5.00)
Number of epibionts per shrimp 250.90 (27.00–971.00) 131.25 (6.00–670.00) 135.75 (2.00–523.00) 314.62 (14.00–1114.00)
Acineta sulawesiensis 193.08 (4.00–730.00) 11.75 (0.00–31.00) 94.80 (0.00–318.00) 188.62 (1.00–585.00)
Cothurnia compressa 16.43 (0.00–59.00) 14.55 (0.00–98.00) 1.35 (0.00–23.00) 11.14 (0.00–49.00)
Zoothamnium intermedium 40.75 (0.00–357.00) 51.25 (0.00–177.00) 2.45 (0.00–42.00) 107.81 (0.00–691.00)
Vorticella globosa 5.80 (0.00–96.00) 15.15 (0.00–141.00) 1.33 (0.00–22.00)
Opercularia coarctata 4.00 (0.00–30.00)
Epistylis coronata 48.65 (0.00–523.00) 5.90 (0.00–68.00)
Podophrya maupasi 1.30 (0.00–22.00) 2.48 (0.00–18.00)
Spelaeophrya polypoides 0.67 (0.00–4.00)
Amphileptus fusidens 1.14 (0.00–13.00)
Embata sp. 1.43 (0.00–6.00)
Fig. 6—Distribution of the epibionts (total
mean number of individuals) along the
anteroposterior axis of the shrimps in the
lakes of the Malili system and Lake Poso.
Anatomical units are considered in five
groups.
Epibiosis on Caridina from Lake Poso • Fernandez-Leborans and von Rintelen Acta Zoologica (Stockholm) 91: 163–175 (April 2010)
� 2009 The Authors
170 Journal compilation � 2009 The Royal Swedish Academy of Sciences
comparison with the pereiopods, which contained the fewest
epibionts (Fernandez-Leborans et al. 2006). In both lake
systems, the maxillipeds and the anterior part of the body
(rostrum, antennae,antennulae and eyes), contained the
main weight of colonization (54.36%), followed by the
pleopods and pereiopods. The posterior end of the body
showed the lowest colonization.
With respect to epibiont diversity, the Shannon–Wiener
coefficients were calculated for each colonized shrimp. The
highest mean value corresponded to Lake Poso (0.744229),
and Lake Mahalona presented the highest maximum value
(3.7553). There were no significant differences between the
lakes and also no significant correlations. However, Lake
Mahalona had values of standardized skewness and stan-
dardized kurtosis indicating significant departures from a
normal distribution, and this fact separated this lake from
the rest, being corroborated by the hierarchical cluster and
principal component analyses (Fig. 8). In Lake Mahalona
Fig. 7—Distribution of the epibionts (total
mean number of individuals) along the
anteroposterior axis of the shrimps in the
lakes of the Malili system and Lake Poso.
Anatomical units are considered individually
(shrimp images: above, Caridina ensifera;
below, Caridina lanceolata).
Acta Zoologica (Stockholm) 91: 163–175 (April 2010) Fernandez-Leborans and von Rintelen • Epibiosis on Caridina from Lake Poso
� 2009 The Authors
Journal compilation � 2009 The Royal Swedish Academy of Sciences 171
(excepting Acineta which was present on all shrimps ana-
lysed) the epibiont species appeared in a lower proportion
than in the other lakes, and 70% of epibiont species appeared
on 10–40% of shrimps.
A multivariate analysis of variance was performed consid-
ering the diversity and total number of epibionts, and the sex,
length and width of the shrimps. This showed that in Lake
Poso there was a significant relation between the species
diversity of the epibiont community and the length and width
of the shrimps. In contrast, sex did not significantly affect the
diversity. The number of individual epibionts was related to
length, width and sex of the host shrimps. In the Malili
system, number and diversity of epibionts was related to
length, width and sex of shrimps in Lake Towuti, whereas
in Lake Matano only the number of epibionts was related
to length, width and sex of shrimps, and in Lake Mahalona
there were no significant relationships. Lake Mahalona data
reflected the diversity values indicated above.
Taking into account the mean number of epibiont species
on the anatomical units of C. ensifera, there was a significant
correlation between all lakes. The correlation between Lake
Poso and the lakes of the Malili system was lowest for Lake
Matano (0.70; P £ 0.05), and highest for Lake Towuti (0.94;
P £ 0.05) (Lake Mahalona 0.89; P £ 0.05). This contrasts
with the facts that, considering the mean number of epi-
bionts on the different anatomical units of the shrimp, there
was a significant difference between the three lakes of the
Malili system (F, 6.23; P £ 0.05), and that the canonical pop-
ulation analysis performed using the number of epibionts on
each anatomical unit of all the analysed shrimps, showed a
significant difference between these three lakes (F, 3.34;
P £ 0.05) (Fernandez-Leborans et al. 2006). In the canoni-
cal correlation analysis using the sum of epibionts on each
anatomical unit of all the analysed shrimps, there was a
significant difference between all lakes, Lake Matano being
the most different from the other lakes. The centroid in
Lake Matano appeared clearly separated from those of the
other lakes.
Discussion
The protozoan epibiont species found had not been recorded
as epibionts on the shrimp C. ensifera, although other species
of the genera Acineta, Podophrya, Zoothamnium, Vorticella and
Cothurnia had previously been observed as epibionts on
other crustaceans (Morado and Small 1995; Fernandez-
Leborans and Tato-Porto 2000a,b; Fernandez-Leborans
2001). The ciliate species found have been observed as epi-
bionts on another shrimp C. lanceolata (Fernandez-Leborans
et al. 2006). The suctorian species Spelaeophrya polypoides
was found on Caridina sp. in Chungking (China) (Nie and
Lu 1945), on Palaemonetes antennarius and Atyaephrya des-
maresti (Europa), and on Xiphocaridina (Africa and Asia)
(Daday 1910; Nozawa 1938; Hadzi 1940). Species similar to
Spelaeophrya polypoides and Spelaeophrya troglocaridis have
been described from the cave shrimp Troglocaris schmidti
(Stammer 1935; Matjasic 1956; Matthes et al. 1988). Species
of Amphileptus have never been found as epibionts on crusta-
ceans, although they are not typical sessile ciliates and there-
fore should be considered as ciliates of the fauna associated
with C. ensifera. A number of rotifer species have been
described as epibionts on crustaceans, e.g. Brachionus rubens
on the cladoceran Moina brachiata (Settele and Thalhofer
2003). Other rotifers are epizoic on diverse freshwater crus-
tacea, such as Daphnia, Asellus, Gammarus (May 1989), or
decapods (Austropotamobius, Astacus, Potamon, Chasmagnathus)
(Hauer 1926; Carlin 1939; Wulfert 1957; Hauer 1959; Mane-
Garzon and Montero 1973; Fontaneto et al. 2004).
The epibiont species observed are similar to others found
as epibionts or as free-living ciliates. However, in several
cases, they exhibit peculiar characteristics, which may con-
stitute adaptations to the epibiont life. For example, Acineta
sulawesiensis has a lorica as a free anterior part over the body
enveloping the tentacles, possibly protecting them from
damage caused by the movement of the basibiont. Other
ciliates, such as Cothurnia, are protected by a lorica completely
surrounding the body, and have a noticeably short stalk,
which allows the ciliate to settle close to the surface of the
basibiont. Something similar occurs in Podophrya, which has
a very short stalk, in contrast to free-living species. Zootham-
nium has a broad stalk, which is noticeably wider on
C. lanceolata; this width is not only a protection for the stalk,
but also for the colony (Fernandez-Leborans et al. 2006).
Spelaeophrya exhibits the most evident adaptation to the
epibiont life. Although it lacks a conspicuous lorica, the body
is flattened, and in the posterior area the body can be folded,
resting next to the surface of the antennae where these suc-
torians are most abundant. In several individuals, the macro-
nucleus was considerably flattened, and their anterior
appeared widened, probably as the result of the adoption
of a squashed shape by the ciliate to reduce friction at the
Fig. 8—Two first components of the principal component analysis
performed using the diversity values (Shannon–Wiener coefficients),
of the epibiont communities in the lakes of the Malili system and
Lake Poso.
Epibiosis on Caridina from Lake Poso • Fernandez-Leborans and von Rintelen Acta Zoologica (Stockholm) 91: 163–175 (April 2010)
� 2009 The Authors
172 Journal compilation � 2009 The Royal Swedish Academy of Sciences
linkage with the surface of the appendages of the
shrimp. These ciliates were only found as epibionts on
crustaceans.
The spatial distribution of epibiont species on the
C. ensifera exoskeleton followed a gradient from the anterior
to the posterior end of the body, with the maximum coloni-
zation on the anterior parts of the body, without a significant
difference between the left and right appendages. This phe-
nomenon was also observed in the epibiont communities of
C. lanceolata and could be correlated to the behaviour of the
shrimp (Fernandez-Leborans et al. 2006). Like C. lanceolata
in the Malili lake system C. ensifera is abundant and widely
distributed in Lake Poso and often found in pelagic swarms
(K. von Rintelen, personal field observation). Its rapid and
characteristic feeding behaviour, as described for Caridina in
general (Fryer 1960), along with its mobility bring mainly
the anterior parts (i.e. the feeding appendages) of the shrimp
into contact with different kinds of soft and hard substrates
(rocks, wood, sand, macrophytes), which was also observed
in C. lanceolata from the Malili lakes (Fernandez-Leborans
et al. 2006). In addition, the physical characteristics of the
surfaces and their morphology were important for coloniza-
tion. The surfaces of the antennulae and antennae provided
substrata for the settlement of epibionts, and the movement of
these appendages facilitates their colonization. Other units
with high number of epibionts, for example the maxillipeds,
showed three characteristics as a possible explanation for
their remarkable epibiosis: the widely available surface, the
protected location of these appendages, and the frequent
presence of nutrient particles linked to their function. Other
morphological sites with high levels of epibiosis were the
uropods, possibly because they have a wide exposed surface,
and their position in the body places them close to the
important passage of organic material from the digestion and
movement of the shrimp.
Many sessile organisms depend upon the characteristics of
the living subtratum to which they adhere (Gili et al. 1993)
and, therefore, the structure, dynamics, physiology and eco-
logy of the basibiont can be reflected in the colonization
pattern of the epibiont species, and in the development
of epibiont communities. Understanding epibiosis may
contribute to understanding the biology of the basibiont.
The number and distribution of epibionts on the different
anatomical units of the basibiont can indicate terminal
moulting, seasonal differences of moult pattern between the
two sexes, asynchronic moulting between populations in
different geographical areas, burying and feeding behaviours,
etc. (Bottom and Ropes 1988; Abello et al. 1990; Abello
and Macpherson 1992; Gili et al. 1993; Fernandez-Leborans
et al. 1997).
Lake Poso had the highest number and diversity of epibi-
ont species, mainly ciliate protozoans, whereas the frequency
of other epibionts was less than 1%. The data showed that
different epibiont species had distinctive spatial distributions
on the basibiont. This fact was reflected in the differential
presence of epibiont species on the anatomical units of the
shrimp, and it was also defined by the pattern of distribution
along the anteroposterior axis of the basibiont, which dif-
fered significantly between epibiont species. However, the
community seems to behave en masse, which can be verified
by the patterns of colonization. We hypothesize that the
species tend to occupy the available substratumthat has the
particular requirements of each functional group, but with
a trend towards maintaining an equilibrium among species
and groups, compensating through diversity and number of
individuals.
All lakes correlated with respect to the mean numbers of
epibiont species on the anatomical units of the shrimp,
although the three lakes of the Malili lake system differed
significantly. Taking into account the number of individual
epibionts on the anatomical units of the shrimps, all lakes
differed significantly, especially Lake Matano. With regard to
the spatial distribution of epibionts along the anteroposterior
axis of the shrimp we found similarities between the Malili
lakes in general and Lake Poso, but a significant difference
between Lake Matano and Lake Poso.
In summary, it can be concluded that all the lakes showed a
similar general pattern of epibiont spatial distribution on the
hosts, with some peculiar characteristics that separated the
lakes of the Malili system from Lake Poso. In the Malili
system the lakes Mahalona and Matano showed irregular
spatial distribution and diversity patterns. This may be
related to the ecological characteristics of these lakes. Lakes
of the Malili system are partially isolated, and are located in
a string from Lake Matano to Lake Towuti. Deforestation
and consequent eutrophication may affect the epibiont
communities in these lakes. In all the lakes there was a
colonization pattern comprising the maintenance of
a anteroposterior gradient, which was sustained by the
fluctuation in diversity and number of individuals of the
different functional groups of epibiont species. From the data of
diversity and proportions of number of species and individuals,
it can be deduced that the functional role of the different
groups of species seems to tend towards sustainability with
little global variation in the diverse lakes. This is the case of
the peritrich ciliates; in Lake Towuti, the number of species
was low, but this was compensated by an increase in the
number of individuals. In contrast, Lake Mahalona had
more peritrich species, but fewer individuals. The basibiont
represents a dynamic environment on which the epibiont
community species acquire a colonization pattern. The
species were located following a particular strategy, and this
was proved by the results: the species followed a tendency
correlated to the different lakes. Independent of the species
present and in all cases, each species was established as fitting
the same general distribution.
The protozoan ciliate epibionts probably do not harm the
basibiont. Within the epibiont community there are diverse
trophic links and, therefore, as occurs in free environments,
there is an energy feedback (microbial loop or other relations)
Acta Zoologica (Stockholm) 91: 163–175 (April 2010) Fernandez-Leborans and von Rintelen • Epibiosis on Caridina from Lake Poso
� 2009 The Authors
Journal compilation � 2009 The Royal Swedish Academy of Sciences 173
and several species can feed on other protozoa in the epi-
biotic community or on other organisms belonging to the
community associated with the host (that have free movement
around the basibiont), such as suctorians feeding on other
ciliates. Peritrich ciliates could depend on the nutrients
arising from the activities of the shrimp. Protozoa of lake
environments are considered as a major link in the limnetic
food web and they have key functions in energy flow and cycling
in freshwater ecosystems. Protozoa are a very important link
in the transfer of energy to the higher trophic levels and they
are a common nutrient for crustaceans and fish larvae
(Porter et al. 1985). The changes in the community structure
of protozoa may significantly affect other components of the
aquatic food web, and consequently may influence the distri-
bution and abundance of both lower and higher organisms
(Beaver and Crisman 1989; Carrick and Fahnenstiel 1992;
Cairns and McCormick 1993). Ciliates have important
ecological significance in free environments, especially in
benthic areas, where they show high growth rates and trophic
diversity (Patterson et al. 1989; Fenchel 1990; Fernandez-
Leborans and Fernandez-Fernandez 2002). Although on a
small scale, these conditions could be transferred to an
epibiotic community, which could reflect the biodiversity in
the environment (Fernandez-Leborans and Gabilondo 2006).
Lake Poso and the Malili lakes are isolated from each other
and harbour both a very distinctive fauna and a high number
of endemic taxa living under similar ecological conditions.
The various epibiontic communities found on C. ensifera and
on C. lanceolata (and on other Caridina species from the Malili
lakes; compare Fernandez-Leborans et al. 2006) in the
respective lake systems not only represent tendencies regard-
ing the colonization pattern and distribution of different
epibionts on their host, but also enhance our knowledge of
the lakes’ exceptional fauna. Human impacts (e.g. deforesta-
tion around the lakes or introduction of alien species) are a
permanent threat to the basibiont shrimps and could harm
the epibionts as well. The protection of both lake systems and
their unique communities should be a conservation goal.
Acknowledgements
We thank Matthias Glaubrecht and Thomas von Rintelen
(Museum of Natural History, Berlin, Germany) for collect-
ing the material from Lake Poso. We are further grateful to
Daisy Wowor and Ristiyanti Marwoto (Museum Zoologicum
Bogoriense, Bogor, Indonesia) for their logistical support in
Indonesia and to P.T. Inco in Soroako. LIPI (Indonesian
Institute of Sciences) provided research permits.
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Acta Zoologica (Stockholm) 91: 163–175 (April 2010) Fernandez-Leborans and von Rintelen • Epibiosis on Caridina from Lake Poso
� 2009 The Authors
Journal compilation � 2009 The Royal Swedish Academy of Sciences 175