Skip to main content
SpringerLink
Log in

Characteristics of the infestation of Seriatopora corals by the coral gall crab Hapalocarcinus marsupialis Stimpson, 1859 on the great reef of toliara, Madagascar

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

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 discuss 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 sexually 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 difficulties to define the symbiotic status of a symbiont if one considers inflexible the three categories of symbiosis commonly defined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Castro P (1976) Brachyuran crabs symbiotic with scleractinian corals: a review of their biology. Micronesica 12(1):99–110

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hines AH (1986) Larval patterns in the life histories of brachyuran crabs (crustacea, decapoda, brachyura). Bull Mar Sci 39(2):444–466

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kropp RK (1986) Feeding biology and mouthpart morphology of three species of coral gall -crabs (decapoda: cryptochiridae). J Crustacean Biol 6:377–384

    Article  Google Scholar 

  • Kropp RK (1990) Revision of the genera of gall crabs (crustacea: cryptochiridae) occurring in the Pacific Ocean. Pac Sci 44(4):417–448

    Google Scholar 

  • Marshall SM, Orr AP (1960) Feeding and nutrition. In: Waterman TH (ed) The physiology of crustacea. Academic Press, New York, pp. 227–258

    Google Scholar 

  • McCain JC, Coles SL (1979) A new species of crab (brachyura, hapalocarcinidae) inhabiting pocilloporid corals in Hawaii. Crustaceana 36:81–89

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Orians GH, Wittenberger JF (1991) Spatial and temporal scales in habitat selection. Amer Nat 137:S29–S49

    Article  Google Scholar 

  • Parmentier E, Michel L (2013) Boundary lines in symbiosis forms. Symbiosis 60:1–5

    Article  Google Scholar 

  • Patton WK (1966) Decapod crustacea commensal with Queensland branching corals. Crustaceana 10:271–295

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rasband WS (1997) ImageJ. U. S, National Institutes of Health, Bethesda, Maryland, USA

    Google Scholar 

  • 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

    Google Scholar 

  • Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Van der Meij SET (2012) Host preference, colour patterns and distribution records of Pseudocryptochirus viridis hiro, 1938 (decapoda, cryptochiridae). Crustaceana 85(7):769–777

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Van der Meij SET, Hoeksema BW (2013) Distribution of gall crabs inhabiting mushroom corals on semporna reefs, Malaysia. Mar Biodiv 43:53–59

    Article  Google Scholar 

  • Van der Meij SET, Schubart CD (2014) Monophyly and phylogenetic origin of the gall crab family cryptochiridae (decapoda: brachyura). Invertebr Syst 28:491–500

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Veron JEN, Pichon M (1976) Scleractinia of Eastern Australia part 1. families thamnasteriidae, astrocoeniidae, pocilloporidae. Aust Inst Mar Sci Monogr Ser 1:1–86

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgments

LT thanks the “Académie de Recherche et d’Enseignement Supérieur Wallonie-Bruxelles - Commission de la Coopération au Développement” (named “Commission Universitaire pour le Développement” at the time of the study) for funding the scientific mission to Madagascar. G.C. thanks the “Académie Royale de Belgique” for the Agathon De Potter grant. This work is a contribution of the Laboratory of Biology of Marine Organisms and Biomimetics (University of Mons, Belgium) and the Polyaquaculture Research Unit (IH.SM, Toliara, Madagascar).

Author information

Authors and Affiliations

  1. Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, Pentagone 2B, University of Mons, 7000, Mons, Belgium

    Lucas Terrana, Guillaume Caulier & Igor Eeckhaut

  2. Polyaquaculture Research Unit, IH.SM, University of Toliara, 601, Toliara, Madagascar

    Gildas Todinanahary & Igor Eeckhaut

  3. Laboratory of Oceanology, MARE Centre, University of Liège, Liège, Belgium

    Gilles Lepoint

Authors
  1. Lucas Terrana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guillaume Caulier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gildas Todinanahary
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gilles Lepoint
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Igor Eeckhaut
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucas Terrana.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Terrana, L., Caulier, G., Todinanahary, G. et al. Characteristics of the infestation of Seriatopora corals by the coral gall crab Hapalocarcinus marsupialis Stimpson, 1859 on the great reef of toliara, Madagascar. Symbiosis 69, 113–122 (2016). https://doi.org/10.1007/s13199-016-0391-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-016-0391-1

Keywords

Search

Navigation