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Three way symbiosis between a goby, a shrimp, and a crab

Marine Biodiversity volume 46, pages 897–900 (2016)Cite this article

Abstract

A unique case of triple symbiosis between a goby, a pistol shrimp, and a porcellanid crab sharing the same burrow close to reef patches in Lembeh Strait, Indonesia, is described from direct observations for the first time. The burrow, typically occupied by shrimps and gobies, is shared with the porcellanid Enosteoides lobatus. In the goby–shrimp association, the fish inhabits the burrow, which is constructed and kept clean by the shrimp, and the fish warns the shrimp of potential dangers approaching their refuge. The porcellanid lives in the burrow and also benefits from living in a habitat where it could not survive without the two sentinel species. Because the limiting resource for the suspension-feeding porcellanid is protected space, this liaison is an adaptation by E. lobatus to a symbiotic life in a habitat that protects it from predation, and is optimal for filter feeding.

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References

  • Baba K (1960) The genera Gymnodoris and Nembrotha from Japan (Nudibranchia-Polyceridae). Publications of the Seto Marine Biological Laboratory 8:71--74

  • De Grave S, Anker A (2000) A new genus and new species of alpheid shrimp (Crustacea: Decapoda) from Papua New Guinea. Raffles Bull Zool 48:249–256

    Google Scholar 

  • De Man JG (1908) Diagnoses of new species of macrurous decapod Crustacea from the” Siboga-Expedition”. Notes Leyden Mus 30:98–112

    Google Scholar 

  • Dolorosa R, Werding B (2014) A new mangrove-inhabiting porcellanid crab of the genus Enosteoides (Crustacea: Decapoda: Anomura) from Puerto Princesa Bay, Palawan, the Philippines. Bull Mar Sci 90:865–872

    Article  Google Scholar 

  • Haig J (1960) The Porcellanidae (Crustacea Anomura) of the eastern Pacific. Allan Hancock Pacific Expeditions 24, pp 1–440

  • Hart JFL (1964) Shrimps of the genus Betaeus on the Pacific Coast of North America with descriptions of three new species. Proc U S Natl Mus 115:431–466

    Article  Google Scholar 

  • Herre AWCT (1936) Eleven new fishes from the Malay Peninsula. Bull Raffles Mus 12:5–16

    Google Scholar 

  • Hiller A, Kraus H, Almon M, Werding B (2006) The Petrolisthes galathinus complex: Species boundaries based on color pattern, morphology and molecules, and evolutionary interrelationships between this complex and other Porcellanidae (Crustacea: Decapoda: Anomura). Mol Phylogenet Evol 40:547–569

    CAS  Article  PubMed  Google Scholar 

  • Hiller A, Viviani CA, Werding B (2010) Hypercarcinisation: An evolutionary novelty in the commensal porcellanid Allopetrolisthes spinifrons (Crustacea: Decapoda: Porcellanidae). Nauplius 18:95–102

    Google Scholar 

  • Jensen GC (1986) Some observations of the alpheid shrimp Betaeus setosus Hart with its host, Pachycheles rudis Stimpson. Bull South Calif Acad Sci 85:180–18

    Google Scholar 

  • Johnson DS (1958) The Indo-West Pacific species of the genus Polyonyx (Crustacea, Decapoda, Porcellanidae). Ann Zool 11(8):95–119

    Google Scholar 

  • Karplus I (1979) The tactile communication between Cryptocentrus steinitzi (Pisces, Gobiidae) and Alpheus purpurilenticularis (Crustacea, Alpheidae). Z Tierpsychol 49:173–196

    Google Scholar 

  • Karplus I (1987) The association between gobiid fishes and burrowing alpheid shrimps. Oceanogr Mar Biol Annu Rev 25:507–562

    Google Scholar 

  • Karplus I (1992) Obligatory and facultative goby shrimp partnerships in the western tropical Atlantic. Symbiosis 12:275–291

    Google Scholar 

  • Karplus I (2014) Symbiosis in fishes: The biology of interspecific partnerships. Wiley Blackwell, Oxford, pp 1–449

    Book  Google Scholar 

  • Linnaeus C (1758) Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata. Laurentius Salvius, Holmiae ii, 824 pp

  • Longley WH, Hildebrand SF (1941) Systematic Catalogue of the Fishes of Tortugas, Florida. Carnegie Institute of Washington, Publication 535, 331 pp

  • Miya Y, Miyake S (1969) Description of Alpheus bellulus sp. nov. associated with gobies from Japan (Crustacea, Decapoda, Alpheidae). Publ Seto Mar Biol Lab 16:307–314

    Google Scholar 

  • Miyake S (1942) Studies on the decapod crustaceans of Micronsia. III. Porcellanidae. Palau Trop Biol Station Stud 2:329–379

    Google Scholar 

  • Nakasone Y, Miyake S (1968) A new species of Porcellana (Anomura: Porcellanidae) from the Palau Islands, with description of its related forms. Occasional Paper of Zoological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka, Japan 1: 165–171

  • Osawa M (2009) New records of three species of the genus Enosteoides Johnson, 1970 (Decapoda: Anomura: Porcellanidae) from Japan, with description of a new species. Bull Natl Mus Nat Sci Ser A Zool Supplement 3:157–166

    Google Scholar 

  • Osumi D, Yamasu T (2000) Feeding behavior and early development of Gymnodoris nigricolor Baba, 1960 (Mollusca: Nudibranchia) associated with the fins of marine gobies. Jpn J Benthol 55:9–14

    Article  Google Scholar 

  • Polunin NVC, Lubbock R (1977) Prawn-associated gobies (Teleostei: Gobiidae) from the Seychelles, western Indian Ocean: Systematics and ecology. J Zool 183:63–101

    Article  Google Scholar 

  • Randall JE, Lobel PS, Kennedy CW (2005) Comparative ecology of the gobies Nes longus and Ctenogobius saepepallens, both symbiotic with the snapping shrimp Alpheus floridanus. Environ Biol Fishes 74:119–127

    Article  Google Scholar 

  • Schmitt WL (1924) The macruran, anomuran and stomatopod Crustacea. Bijdragen tot de kennis der fauna von Curaçao. Resultaten eener reis van Dr. C. J. van der Horst, in 1920. Bijdragen tot de Dierkunde 23:61–81

    Google Scholar 

  • Schoppe S, Werding B (1995) The boreholes of the sea urchin genus Echinometra: (Echinodermata: Echinoidea: Echinometridae) as a microhabitat in tropical South America. Mar Ecol 17:181–186

    Article  Google Scholar 

  • Stimpson W (1858) Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republica Federata missa, Cadwaladaro Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Pars VII. Crustacea Anomura. Proc Acad Nat Sci Phila 1858:225–252

    Google Scholar 

  • Viviani CA (1969) Los Porcellanidae (Crustacea Anomura) chilenos: Distribución geográfica, y algunas observaciones biocenóticas sobre los porcelánidos en la bahía de Mehuín. Stud. Neotrop. Fauna Environ 6:40–56

    Google Scholar 

  • Viviani CA, Hiller A, Werding B (2010) Swarming in open space in the rocky intertidal: A new population-settlement strategy in the eastern Pacific porcellanid crab Allopetrolisthes punctatus (Decapoda, Anomura, Porcellanidae). Crustaceana 83:435–442

    Article  Google Scholar 

  • Werding B (1983) Kommensalische Porzellaniden aus der Karibik (Decapoda, Anomura). Crustaceana 45:1–14

    Article  Google Scholar 

  • Werding B (2001) Description of two new species of Polyonyx Stimpson, 1858 from the Indo-West Pacific, with a key to the species of the Polyonyx sinensis group (Crustacea: Decapoda: Porcellanidae). Proc Biol Soc Wash 114:109–119

    Google Scholar 

  • Werding B, Haig J (1982) The porcellanid crabs of the Isla Gorgona, Pacific coast of Colombia, with a description of Clastotoechus grogonensis sp. nov. (Crustacea: Anomura). Anales del Instituto de Investigaciones Marinas de Punta de Betín 12:57–70

    Google Scholar 

  • Werding B, Hiller A (2004) Description of a new species of Petrolisthes from the Western Pacific (Decapoda, Anomura, Porcellanidae). Crustaceana 77:257–264

    Article  Google Scholar 

  • Williams EH, Williams LB (1986) The first association of an adult mollusk (Nudibranch: Doridae) and a fish (Perciformes: Gobiidae). Venus 45:210–212

    Google Scholar 

  • Wirtz P (2008) The Gulf of Guinea goby-shrimp symbiosis and a review of goby-thalassinidean associations. Arquipélago. Life Mar Sci 25:71–76

    Google Scholar 

Download references

Acknowledgments

NAD-Lembeh, Indonesia, graciously provided to B.C extensive logistic help. H.A. Lessios (STRI) critically read an earlier draft of this mansucript. I. Karplus (Agricultural Research Organization - ARO, Volcani Center, Israel) reviewed this manuscript and kindly helped with identification of fish species. A. Anker (Universidade Federal do Ceará, Brazil) helped identifying the alpheid species. L. Corbari (Muséum National d'Histoire Naturelle, Paris, France) provided us with porcellanid material. We thank the editor and reviewers for their contributions to improve this manuscript. This study was supported by a Smithsonian grant to A.H.

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Authors and Affiliations

  1. Institut für Allgemenie und Spezielle Zoologie, Justus-Liebig Universität Giessen, Heinrich-Buff-Ring 26-32, 35392, Giessen, Germany

    Bernd Werding

  2. Department of Ecology and Environmental Sciences, Umea University, SE 901 87, Umea, Sweden

    Bent Christensen

  3. Smithsonian Tropical Research Institute, Apartado 0843-03092, Panama, Republic of Panama

    Alexandra Hiller

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  1. Bernd Werding
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  2. Bent Christensen
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  3. Alexandra Hiller
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Correspondence to Alexandra Hiller.

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Communicated by R. Thiel

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Werding, B., Christensen, B. & Hiller, A. Three way symbiosis between a goby, a shrimp, and a crab. Mar Biodiv 46, 897–900 (2016). https://doi.org/10.1007/s12526-016-0453-x

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  • DOI: https://doi.org/10.1007/s12526-016-0453-x

Keywords

  • Goby–shrimp association
  • Gobiidae
  • Alpheidae
  • Porcellanidae
  • Symbiosis
  • Indo-West Pacific