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271
THE RAFFLES BULLETIN OF ZOOLOGY 2006
THE RAFFLES BULLETIN OF ZOOLOGY 2006 54(2): 271-276
Date of Publication: 31 Aug.2006
© National University of Singapore
CARIDINA SPONGICOLA, NEW SPECIES, A FRESHWATER SHRIMP
(CRUSTACEA: DECAPODA: ATYIDAE) FROM THE ANCIENT MALILI LAKE
SYSTEM OF SULAWESI, INDONESIA
Kristina Zitzler
Museum of Natural History, Humboldt University, Invalidenstrasse 43, 10115 Berlin, Germany
Email: Kristina.Zitzler@museum.hu-berlin.de
Yixiong Cai
Biodiversity Centre, National Parks Board, 1 Cluny Road, Singapore 259569, Republic of Singapore
Email: caiyixiong@yahoo.com
ABSTRACT. – The ancient Malili lake system of Sulawesi, Indonesia, harbours an endemic species flock of
atyid shrimps. Caridina spongicola, new species, is described from the outlet of Lake Towuti, the largest of
the five connected lakes. The new species differs from all other Caridina species by a combination of
morphological features and a unique colour pattern, and is unusual among atyid shrimps in being associated
with an undescribed species of freshwater sponge. The shrimps are most likely commensals: they appear to
feed on diatoms accumulating on or within the sponge, and do no harm the host. Caridina spongicola, new
species, is the second reported atyid shrimp that lives in symbiosis with another organism.
KEY WORDS. – Caridina, Malili lake system, Sulawesi, symbiosis, sponge-dweller, taxonomy.
INTRODUCTION
The Malili lake system of Sulawesi, Indonesia (Fig. 1A),
harbours an endemic species flock of currently 10 described
species of the atyid genus Caridina (Woltereck, 1937a, b;
Brooks, 1950; Chace, 1997). During intensive collecting from
2003 to 2005, an unidentified species was discovered in Lake
Towuti, the largest of the five connected Malili lakes in the
central highlands of Sulawesi. It shows an exceptional habitat
preference for a currently undescribed species of freshwater
sponge, which is endemic to a small area in the outlet bay of
Lake Towuti (Fig. 1A). This unusual association, together
with morphological characters and diagnostic colour pattern,
provide sufficient data for the description of a new species.
Type specimens are deposited in the Museum Zoologicum
Bogoriense, Bogor, Indonesia (MZB); Museum für
Naturkunde (Museum of Natural History), Berlin, Germany
(ZMB); and Zoological Reference Collection of the Raffles
Museum of Biodiversity Research, National University of
Singapore, Singapore (ZRC). The abbreviation cl is used for
the carapace length, measured from the postorbital to the
posterior margin of the carapace. All measurements and
qualitative characters are from 28 specimens, unless otherwise
indicated.
TAXONOMY
FAMILY ATYIDAE DE HAAN, 1849
Caridina H. Milne Edwards, 1837
Caridina spongicola, new species
(Figs. 1-3)
Material examined. – Holotype - ovigerous female (eggs without
eyes), cl 2.4 mm (MZB Cru 1559), Indonesia, Sulawesi Selatan,
Lake Towuti, west shore, outlet bay, west of Cape Tokaluku,
02°47.261'S 121°23.17'E, coll. T. von Rintelen & K. Zitzler, 29
Jul.2004.
Paratypes – 3 females; cl 2.0-2.4 mm; 2 ovigerous females, cl 2.4-
2.8 mm , same data as holotype; 5 males, cl 1.8-2.3 mm (MZB Cru
1560), same data as holotype. 2 ovigerous females (some SEM
material), cl 2.4 mm; 11 females (some SEM material), cl 1.9-2.6
mm (ZMB 29027), Indonesia, Sulawesi Selatan, Lake Towuti, west
shore, outlet bay, west of Cape Tokaluku, 02°47.32'S 121°23.38'E,
coll. T. von Rintelen & K. Zitzler, 21 Sep.2003; 4 males (some SEM
material), cl 1.9-2.1 mm (ZMB 29027), same data as previous
sample; 9 males, cl 2.1-2.4 mm, 12 females, cl 2.2-2.6 mm, 6
ovigerous females, cl 2.4-2.6 mm (ZRC 2006.0114) Indonesia,
Sulawesi Selatan, Lake Towuti, west shore, outlet bay, west of Cape
Tokaluku, 02°46.277'S 121°21.83'E, coll. Y. Cai, T. von Rintelen
& K. Zitzler, 3 Jan.2005.
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Zitzler & Cai: A new freshwater shrimp from Sulawesi
Fig. 1. A, Malili Lake system of Sulawesi: Caridina spongicola, new species, collecting sites in the outlet bay of Lake Towuti; B, rostrum
variation within a population of C. spongicola (ZMB 29027) (scale bar: 1 mm); C, Caridina spongicola in its natural habitat; D, colour
pattern of C. spongicola (ZMB).
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THE RAFFLES BULLETIN OF ZOOLOGY 2006
Fig. 2. Caridina spongicola, new species, paratype female (cl 2.1mm) (ZMB 29027), Lake Towuti, Sulawesi: A, cephalothorax and cephalic
appendages, lateral view; B, preanal carina; C, dactylus of third pereiopod; D, third pereiopod; E, telson; F, uropodal diaeresis; G, dactylus
of fifth pereiopod; H, fifth pereiopod; I, distal end of telson; J, first pereiopod, K, second pereiopod; L, SEM images of chela and carpus of
first and second pereiopods. Scale bars: A = 1 mm; B, D, H-M = 0.5 mm; C, F-G = 0.2 mm.
274
Zitzler & Cai: A new freshwater shrimp from Sulawesi
Fig. 3. Caridina spongicola, new species, paratype female (cl 2.6 mm) (ZMB 29027), Lake Towuti, Sulawesi. A, cephalothorax and cephalic
appendages; lateral view; B, mandible; C, maxillule; D, first maxilliped; E, third maxilliped; F, second maxilliped ; G, maxilla; H, male first
pleopod; paratype male (cl 1.9 mm) (ZMB 29027); I, male second pleopod; paratype male (cl 1.9 mm) (ZMB 29027). Scale bars: A = 1 mm;
B-G = 0.5 mm; H, I = 0.2 mm.
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THE RAFFLES BULLETIN OF ZOOLOGY 2006
Comparative material examined. – Caridina lingkonae Woltereck,
1937: 2 females, cl 3.5-3.8 mm, 3 ovigerous females (ZRC), Lake
Towuti, Watidi, 4 km east of Timampu, Sulawesi, Indonesia, coll.
M. Kottelat & A. Werner, 15 Mar.1989; 2 females, cl 2.8-4.0 mm,
ZRC, Lake Towuti, estuary of Sungei Batuopa, about 2 km south of
Timampu, Sulawesi, Indonesia, coll. M. Kottelat & A. Werner, 14
Mar.1989.
Description. – Rostrum straight and slender (Fig. 1B, 2A,
3A), anterior third slightly upturned, reaching to or slightly
beyond third segment of antennular peduncle, 0.9-1.0 times
as long as carapace, armed dorsally with 11-19 + 3-5 teeth,
posterior to orbital margin, armed ventrally with 4-10 teeth,
dorsal anterior teeth less densely spaced. Antennal spine
situated below inferior orbital angle. Pterygostomian angle
broadly rounded.
Eyes (Figs. 2A, 3A) well developed, anterior end reaching to
or beyond half length of basal segment of antennular
peduncle. Antennular peduncle 0.8-0.9 times as long as
carapace (n=10), second segment slightly shorter than basal
segment, about twice as long as third segment. Stylocerite
reaching well beyond half length of basal segment of
antennular peduncle, but not reaching end of basal segment.
Scaphocerite slender, 3.5-4.8 times as long as wide (n=7).
Sixth abdominal somite 0.5-0.7 times length of carapace, 1.5-
2.0 times as long as fifth somite (n=21), 0.7-1.0 times length
of telson. Telson (Figs. 2E, I) 2.8-4.1 times as long as wide
(n=13), distal margin rounded, without projection, with 3-4
pairs of spinules and 1 pair of dorsolateral spinules; distal
end with 4 pairs of spines, lateral pair distinctly longer than
intermediate pairs, median pair shortest. Preanal carina (Fig.
2B) rounded, without spine. Uropodal diaeresis (Fig. 2F) with
10-12 movable spinules (n=12).
Incisor process of mandible (Fig. 3B) ending in irregular teeth,
molar process truncated. Lower lacinia of maxillule (Fig. 3C)
broadly rounded, upper lacinia elongated, with a number of
distinct teeth on inner margin, palp slender. Upper endites of
maxilla (Fig. 3G) subdivided, palp elongate, scaphognathite
tapering posteriorly. Palp of first maxilliped (Fig. 3D)
truncate, ending in triangular shape. Podobranch of second
maxilliped (Fig. 3F) reduced to small lamina. Third
maxilliped (Fig. 3E) with ultimate segment slightly shorter
than penultimate segment.
Chela of first pereiopod (Fig. 2J) 0.5-0.9 mm, distinctly
stouter and shorter (mean length 0.6 mm) than chela of second
pereiopod (mean length 0.8 mm, n=26) (Fig. 2K), Carpus of
first pereiopod 0.4-0.8 mm, 0.7-1.3 times as long as chela,
Chela of second pereiopod 0.7-1.0 mm, Carpus of second
pereiopod distinctly longer than carpus of first pereiopod (0.9-
1.4 mm), 1.2-1.4 times as long as chela. Third pereiopod (Figs.
2C, D) terminating in one claw with 1-2 accessory spines on
flexor margin (n=7), fifth pereiopod (Figs. 2G, H) terminating
in one claw with 21-31 spinules on flexor margin (n=7).
Endopod of male first pleopod (Fig. 3H) without appendix
interna, appendix interna of male second pleopod (Fig. 3I)
not reaching end of appendix masculina.
Ovigerous females with 12-18 eggs (n=4 females); egg size
0.8-0.9 x 0.4-0.6 mm (n=53, eggs with and without eyes);
sex ratio females/males 2.1.
Distribution. – Caridina spongicola is endemic to Lake
Towuti within the Malili lake system.
Habitat. – During an extensive substrate specific sampling
in the Malili lake system in 2003 and 2004, Caridina
spongicola was found unexceptionally with a currently
undescribed freshwater sponge that, according to a
preliminary study, belongs to the common Spongillidae (C.
Eckert, pers. comm.) (Fig. 1 C). It grows in the outlet of Lake
Towuti at depths of 2-5 m. The shrimp either occurs on the
sponge or dwells inside its osculae.
Biology. – A preliminary gut content analysis was carried
out to investigate the shrimps’ diet. None of the six dissected
guts contained traces of poriferean spicules. The spicules are
presumably too big (0.2-0.3 mm; C. Eckert, pers. comm.) to
be consumed by the shrimps. On the other hand, a variety of
different diatoms, which possibly accumulate on or within
the sponge, were found in the guts. These findings suggest
that the shrimps do not feed on sponge’s tissue and thus do
not parasitize their hosts. Instead, they appear to be
commensals using the sponge’s cavities as shelter and the
inherent accumulation of diatoms as a food supply.
Colour pattern. – Carapace with three transversal dark brown
bands (Fig. 1C, D), first two usually joint at dorsal surface to
form a n-shaped band in lateral view; anterior part of
cephalothorax, antennular peduncle, bases of antennae and
posterior rostrum similarly pigmented, whereas anterior
rostrum, antennae and distal antennules mostly unpigmented;
first and second pereiopod white with light brown setae, other
pereiopods white with brown bands; abdomen with a
conspicuous white stripe expanding laterally along each side,
dorsally densely covered with dark brown bands except for
a white patch on third sternum, ventrally uniformly brown;
uropods with a characteristic brown band on distal endopod,
endopod and exopods with white-pigmented tips,
respectively; pleopods and telson colourless; eggs usually
dark brown. This colour pattern remains visible even if the
shrimps are under stress though the intensity of the colour
merely fades.
Etymology. – The name spongicola, the combination of two
Latin words, spongia, sponge, and cola, dweller, refers to
the unexceptional occurrence on sponges.
Remarks. – With respect to the shape of the rostrum, Caridina
spongicola is at first sight morphologically similar to C.
lingkonae, which was described from Lake Towuti
(Woltereck, 1937a), but can be distinguished by a lower
number of ventral teeth in C. spongicola (4-10 vs. 8-16 in C.
lingkonae), a shorter rostrum in C. linkgonae compared to
the length of the antennular peduncle (usually reaching
beyond vs. reaching to antennular peduncle in C. spongicola).
It differs further from C. lingkonae by the ratio of the sixth
abdominal segment to cl (0.5-0.7 vs. 0.81-0.97 in C.
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Zitzler & Cai: A new freshwater shrimp from Sulawesi
lingkonae) (Woltereck, 1937b), the stouter first two
pereiopods, and the number of accessory spines (1-2 vs. 7-8
in C. lingkonae) and spinules (21-31 vs. 48-52 in C.
lingkonae) on the dactylus of the third and fifth pereiopods,
respectively.
The rostrum of C. spongicola displays a high degree of
variation within the populations (Fig. 1B). However, certain
qualitative characters, i.e. the general shape or the
arrangement of the rostral teeth, are constant not only in C.
spongicola, but in all currently described Malili lakes species
(see Woltereck, 1937a; b; Zitzler, pers. observ.). When alive,
the atyid shrimps of the Malili Lake system may be easily
recognized by their distinctive, conspicuous and usually
species-specific live colour patterns (K. Zitzler, unpubl. data).
So far, C. spongicola is the only freshwater shrimp that
associates with sponges. Interestingly, in the East African
Lake Tanganyika, another atyid shrimp, Limnocaridina
iridinae, appears to be associated, presumably also
commensally, with a bivalve, Iridina sp. (Roth-Woltereck,
1958). The two associations may be even seen as a nice
example of ecological convergence between atyid shrimps
of the Great Rift lakes in eastern Africa and the Malili Lake
system in Sulawesi.
Compared to other Caridina species, C. spongicola is also
rather small (cl 1.8-2.8 mm). The medium egg size (0.8-0.9
x 0.4-0.6 mm) and small numbers of eggs (12-18) suggests
an abbreviated larval development, which is typical for
lacustrine species.
ACKNOWLEDGEMENTS
The first author would like to thank Hannelore Hoch and
Matthias Glaubrecht (Berlin) for their supervision and
financial support, respectively, in Berlin. Both authors thank
Arthur Anker (Panama) and Daisy Wowor (MZB) for their
suggestions to improve the manuscript, Peter K.L. Ng
(RMBR) for his general support, Ristiyanti Marwoto and
Daisy Wowor for their logistical support in Indonesia and
Singapore, and LIPI (Indonesian Institute of Sciences) for
research and collecting permits. P.T. INCO in Soroako,
Sulawesi, provided valuable logistic support during fieldwork.
Finally, many thanks to Thomas von Rintelen (Berlin) for
his immense help during field work in Indonesia and his
valuable comments on the manuscript, as well as Carsten
Eckert (Berlin), who answered our questions concerning the
fascinating sponge in Lake Towuti.
LITERATURE CITED
Brooks, J. L., 1950. Speciation in ancient lakes. Quarterly Review
of Biology, 25: 131-176.
Chace, F. A., 1997. The caridean shrimps (Crustacea: Decapoda)
of the Albatross Philippine Expedition, 1907-1910, Part 7:
Families Atyidae, Eugonatonotidae, Rhynchocinetidae,
Bathypalaemonellidae, Processidae, and Hippolytidae.
Smithsonian Contributions to Zoology, 587: 1-106.
Milne Edwards, H., 1837. Histoire naturelle des Crustacés,
Comprenant l’ Anatomie, la Physiologie et la Classification de
ces Animaux. Volume 2, Libraire Encyclopedique de Roret,
Paris. 532 pp.
Roth-Woltereck, E., 1958. Limnocaridina iridinae, n. sp. Eine
interessante Garnele aus dem Tanganjika-See (Decapoda
Atyidae). Zoologischer Anzeiger, 161: 188-192.
Woltereck, E., 1937a. Systematisch –variationsanalytische
Untersuchungen über die Rassen-und Artbildung bei
Süßwassergarnelen aus der Gattung Caridina (Decapoda,
Atyidae). Internationale Revue der gesamten Hydrobiologie und
Hydrographie, 34: 208-262.
Woltereck, E., 1937b. Zur Systematik und geographischen
Verbreitung der Caridinen. Internationale Revue der gesamten
Hydrobiologie und Hydrographie, 34: 294-330.
