biodiversityanddistributionofepibionticcommunitieson...

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)


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



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).




(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.




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.




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.




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.




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).




(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.




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)




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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