Characteristics of the infestation of Seriatopora corals by the coral gall crab Hapalocarcinus marsupialis Stimpson, 1859 on the great reef of toliara, Madagascar
[en] This study describes the association between the
obligatory symbiont coral gall crab
Hapalocarcinus
marsupialis
and its stony coral hosts
Seriatopora sp
.within
the Great Reef of Toliara in Madagascar and attempts to dis-
cuss their symbiotic status through comparison with previous
studies. These corals are inhabited by crabs living in galls that
can be categorised in four distinct morphological stages,
where the first one corresponds to a small bud and the last
one represents a completely closed gall surrounding the crab
inside. Within the reef, 563 colonies of
Seriatopora
species
were observed by scuba-diving at ten different stations:
37.8 % of them were infested by
H. marsupialis
, with a total
of 763 galls, and with a majority of stage 4 galls. Galls are
monopolised by females that can have different morphologies.
Females store the sperm in two spermathecae and are fertilised
when their morphology and size are similar to males and the
gall is not closed. Histological observations coupled with
scanning electronic microscopy analyses show that closed
galls are made of an external living tissue, a mid skeletal layer
and an internal living tissue. The internal living tissue includes
polyps similar to the external tissue, some of them being sex-
ually mature. Nitrogen and carbon isotopic signatures
confirmed that these crabs are filter-feeders and do not feed
on their host. This association perfectly highlights the difficul-
ties to define the symbiotic status of a symbiont if one con-
siders inflexible the three categories of symbiosis commonly
defined.
Research center :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Terrana, Lucas; Université de Mons - UMONS > Biologie Marine et Biomimétisme
Caulier, Guillaume; Université de Mons - UMONS > Biologie Marine et Biomimétisme
Todinanahary, Gildas; Institut d'Halieutique et de Sciences Marine de Tuléar (Madagascar) > Unité de Polyaquaculture
Lepoint, Gilles ; Université de Liège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Eeckhaut, Igor; Université de Mons - UMONS > Laboratoire de Biologie Marine et de Biomimétisme
Language :
English
Title :
Characteristics of the infestation of Seriatopora corals by the coral gall crab Hapalocarcinus marsupialis Stimpson, 1859 on the great reef of toliara, Madagascar
Abele LG (1984) Biogeography, colonization and experimental community structure of coral associated crustaceans. In: Strong Jr DR, Simberloff D, Abele LG, Thistle AB (eds) Ecological communities: conceptual issues and the evidence. Princeton University Press, Princeton, NJ, pp. 123–137
Abelson A, Galil BS, Loya Y (1991) Skeletal modifications in stony corals caused by indwelling crabs: hydrodynamical advantages for crab feeding. Symbiosis 10:233–248
Badaro MFS, Neves E, Castro P, Johnsson R (2012) Description of a new genus of cryptochiridae (decapoda: brachyura) associated with Siderastrea (anthozoa: scleractinia) with notes on feeding habits. Sci Mar 76(3):517–526
Becker C (2010) European pea crabs – taxonomy, morphology, and host-ecology (crustacea: brachyura: pinnotheridae) (dissertation). Goethe-University, Frankfurt/Main, Germany, 180 p
Carricart-Ganivet JP, Carrera-Parra LF, Quan-Young LI, García-Madrigal MS (2004) Ecological note on Troglocarcinus corallicola (brachyura: cryptochiridae) living in symbiosis with Manicina areolata (cnidaria: scleractinia) in the Mexican Caribbean. Coral Reefs 23:215–217
Castro P (1976) Brachyuran crabs symbiotic with scleractinian corals: a review of their biology. Micronesica 12(1):99–110
Caulier G, Lepoint G, Van Nedervelde F, Eeckhaut I (2014) The diet of the harlequin crab Lissocarcinus orbicularis, an obligate symbiont of sea cucumbers (holothuroids) belonging to the genera Thelenota, Bohadschia and Holothuria. Symbiosis 62:91–99
Davie P (2015) Cryptochiridae Paul'son, 1875. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=106753 on 2015–09-fv09
Helmuth BST, Timmerman BEH, Sebens KP (1997) Interplay of host morphology and symbiont microhabitat in coral aggregations. Mar Biol 130:1–10
Henderson JR (1906) XXXI.—On a new species of coral-infesting crab taken by the RIMS ‘Investigator’at the Andaman Islands. J Nat Hist 18:105, 211–219
Hines AH (1982) Allometric constraints and variables of reproductive effort in brachyuran crabs. Mar Biol 69:309–320
Hines AH (1986) Larval patterns in the life histories of brachyuran crabs (crustacea, decapoda, brachyura). Bull Mar Sci 39(2):444–466
Hines AH, Lipcius RN, Haddon AM (1987) Population dynamics and habitat partitioning by size, sex, and molt stage of blue crabs Callinectes sapidus in a subestuary of Central Chesapeake Bay. Mar Ecol Prog Ser 36:55–64
Jamieson BGM, Tudge CC (2000) Crustacea – Decapoda. In: Jamieson BGM (ed) In ‘Reproductive Biology of Invertebrates. Volume IX, Part C. Progress in Male Gamete Ultrastructure and Phylogeny’. Wiley, Chichester, UK, pp. 1–95
Johnsson R, Neves E, Franco GMO, da Silveira FL (2006) The association of two gall crabs (brachyura: cryptochiridae) with the reef-building coral Siderastrea stellata verrill, 1868. Hydrobiologia 559:379–384
Keshavmurthy S, Yang S-Y, Alamaru A et al (2013) DNA barcoding reveals the coral “laboratory-rat”, Stylophora pistillata encompasses multiple identities. Scientific Reports, Vol. 3, Number 1520
Kinne O (1980) Diseases of marine animals, I., general aspects, protozoa to gastropoda. Wiley, Chichester
Kotb MMA, Hartnoll RG (2002) Aspects of the growth and reproduction of the coral gall crab Hapalocarcinus marsupialis. J Crustacean Biol 22(3):558–566
Kropp RK (1986) Feeding biology and mouthpart morphology of three species of coral gall -crabs (decapoda: cryptochiridae). J Crustacean Biol 6:377–384
Kropp RK (1990) Revision of the genera of gall crabs (crustacea: cryptochiridae) occurring in the Pacific Ocean. Pac Sci 44(4):417–448
Marshall SM, Orr AP (1960) Feeding and nutrition. In: Waterman TH (ed) The physiology of crustacea. Academic Press, New York, pp. 227–258
McCain JC, Coles SL (1979) A new species of crab (brachyura, hapalocarcinidae) inhabiting pocilloporid corals in Hawaii. Crustaceana 36:81–89
Mohammed TAA, Yassien MH (2013) Assemblages of two gall crabs within coral species Northern Red Sea, Egypt. Asian J Sci Res 6(1):98–106
Mokady O, Loya Y, Lazar B (1998) Ammonium contribution from boring bivalves to their coral hosts - a mutualistic symbiosis? Mar Ecol Prog Ser 169:295–301
Nogueira MM, Menezes NM, Johnsson R, Neves E (2014) The adverse effects of cryptochirid crabs (decapoda: brachyura) on Siderastrea stellate verril, 1868 (anthozoa: scleractinia): causes and consequences of cavity establishment. Cah Biol Mar 55:155–162
Orians GH, Wittenberger JF (1991) Spatial and temporal scales in habitat selection. Amer Nat 137:S29–S49
Parmentier E, Michel L (2013) Boundary lines in symbiosis forms. Symbiosis 60:1–5
Patton WK (1974) Community structure among the animals inhabiting the coral Pocillopora damicornis at Heron Island, Australia. In: Vernberg, W.B. (Ed.), Symbiosis in the Sea. University of South Carolina Press, pp. 219–243
Patton WK (1976) Animal associates of living reef corals. Biology and Geology of Coral Reefs 3:1–37
Pichon M (1978) Recherches sur les peuplements à dominance d’anthozoaires dans les récifs coralliens de Tuléar (Madagascar). Atoll Res Bull 222:477
Pinzon JH, Sampayo E, Cox E, et al. (2013) Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among indo-Pacific cauliflower corals (pocillopora, scleractinia). J Biogeogr 40:1595–1608
Potts FA (1915) Hapalocarcinus, the gall-forming crab, with some notes on the related genus Cryploehirus. Papers from the Department of Marine Biology of the Carnegie Institution of Washington, 8:33–69
Pulliam HR, Danielson BJ (1991) Sources, sinks, and habitat selection: a landscape perspective on population dynamics. Amer Nat 137:S50–S66
Rasband WS (1997) ImageJ. U. S, National Institutes of Health, Bethesda, Maryland, USA
Reed JK, Gore RH, Scotto LE, Wilson KA (1982) Community composition, structure, areal and trophic relationships of decapods associated with shallow- and deepwater Oculina varicosa reef corals. Bull Mar Sci 32:761–786
Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91
Simon-Blecher N, Achituv Y (1997) Relationship between the coral pit crab Cryptochirus corallioidytes Heller and its host coral. J Exp Mar Biol Ecol 215:93–102
Simon-Blecher N, Chemedanov A, Eden N, Achituv Y (1999) Pit structure and trophic relationship of the coral pit crab Cryptochirus coralliodytes. Mar Biol 134:711–717
Stefani F, Benzoni F, Yang S-Y, et al. (2011) Comparison of morphological and genetic analyses reveals cryptic divergence and morphological plasticity in stylophora (cnidaria, scleractinia). Coral Reefs 30:1033–1049
Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011) Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanogr Mar Biol 49:43–104
Stimpson W (1859) Hapalocarcinus marsupialis, a remarkable new form of brachyurous crustacean on the coral reefs of Hawaii. Proc Boston Soc Nat Hist 6:412–413
Van der Meij SET (2012) Host preference, colour patterns and distribution records of Pseudocryptochirus viridis hiro, 1938 (decapoda, cryptochiridae). Crustaceana 85(7):769–777
Van der Meij SET (2014) Host species, range extensions, and an observation of the mating system of Atlantic shallow-water gall crabs (decapoda: cryptochiridae). Bull Mar Sci 90:1001–1010
Van der Meij SET (2015) Host relations and DNA reveal a cryptic gall crab species (crustacea: decapoda: cryptochiridae) associated with mushroom corals (scleractinia: fungiidae). Contrib Zool 84(1):39–57
Van der Meij SET, Hoeksema BW (2013) Distribution of gall crabs inhabiting mushroom corals on semporna reefs, Malaysia. Mar Biodiv 43:53–59
Van der Meij SET, Schubart CD (2014) Monophyly and phylogenetic origin of the gall crab family cryptochiridae (decapoda: brachyura). Invertebr Syst 28:491–500
Vehof J, Van der Meij SET, Türkay M, Becker C (2014) Female reproductive morphology of coral-inhabiting gall crabs (crustacea: decapoda: brachyura: cryptochiridae). Acta Zool-Stockholm 97(1):117–126
Veron JEN, Pichon M (1976) Scleractinia of Eastern Australia part 1. families thamnasteriidae, astrocoeniidae, pocilloporidae. Aust Inst Mar Sci Monogr Ser 1:1–86
Vytopil E, Willis BL (2011) Epifaunal community structure in Acropora spp (scleractinia) on the great barrier reef: implications of coral morphology and habitat complexity. Coral Reefs 20:281–288
Warner GF (1977) The biology of crabs. Van Nostrand Reinhold Co, New York, 202 pp
Warner PA, van Oppen MJH, Willis BL (2015) Unexpected cryptic species diversity in the widespread coral Seriatopora hystrix masks spatial-genetic patterns of connectivity. Mol Ecol 24:2993–3008
Wei TP, Chen HC, Lee YC, Tsai ML, Hwang JS, Peng SH, Chiu YW (2013) Gall polymorphism of coral-inhabiting crabs (Decapoda, Cryptochiridae): A perspective. J Mar Sci Tech-Japan 21(Suppl.):304–307
Wetzer R, Martin JW, Boyce SL (2009) Evolutionary origin of the gall crabs (family cryptochiridae) based on 16S rDNA sequence data. decapod crustacean phylogenetics. Crustacean Issues 18:475–490
