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Marine Biodiversity

, Volume 49, Issue 1, pp 11–23 | Cite as

Polyps fishing on a crab: novel association between Hydrichthella epigorgia (Hydrozoa, Ptilocodiidae) and Achaeus (Crustacea, Inachidae)

  • Joan J. Soto ÀngelEmail author
  • Luis Martell
  • Ferran Palero
Original Paper
First Online:

Abstract

Hydrozoans are a ubiquitous component of the marine benthos which may occur associated with a wide range of taxa. Some of these associations have been recently reviewed, while others remain mostly unexplored, such as the case of hydrozoans and brachyuran crabs. The present study describes a novel association between the ptilocodiid Hydrichthella epigorgia and spider crabs of the genus Achaeus. Three complementary approaches have been followed in order to determine the prevalence and specificity of this interaction: (1) in situ observations, (2) assessment of independent observations from image repositories, and (3) analyses of specimens kept in museum collections. The present contribution constitutes the first report of H. epigorgia in the Red Sea and the first evidence of a Ptilocodiidae epibiont on a crustacean. The prevalence obtained is the highest ever reported for a hydroid–crab association (96%), which suggests specific ecological interactions between both species. The Achaeus crabs are reported using H. epigorgia polyps as fishing rods to capture zooplankton, with pereiopods 2–3 acting as “fishing legs” and harboring a much larger amount of dactylozooids than other pereiopods. Different morphotypes are described for H. epigorgia in relation to the substrate used, and the validity of the representatives of the genus is discussed. Further experimental studies will clarify whether the Achaeus–H. epigorgia association may represent a novel case of mutualism in hydroid–crab epibiosis.

Keywords

Behavior Coral reef Decorator crab Epibiosis Red Sea Symbiosis 
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Notes

Acknowledgements

We are deeply indebted to Alex Mustard, Anne Frijsinger and Mat Vestjens, Borut Furlan, Cigdem Cooper, David Hall, Gustav Paulay (Florida Museum of Natural History, Gainesville), Herbert Meyrl, Ilan Ben Tov, Jamie Craggs, Ole Johan Brett, Pawel Borowka, Rafi Amar, Richard Aspinall and Steve Jones for kindly providing us with high-quality photographs of living specimens. Thanks are due also to two anonymous reviewers for their thorough revisions and useful suggestions. FP acknowledges the project CHALLENGEN (CTM2013-48163) of the Spanish Government and a post-doctoral contract funded by the Beatriu de Pinos Programme of the Generalitat de Catalunya.

Supplementary material

12526_2017_746_MOESM1_ESM.xlsx (24 kb)
ESM 1 Worldwide records of Hydrichthella epigorgia Stechow, 1909 (XLSX 24 kb)

References

  1. Abelló P, Villanueva R, Gili JM (1990) Epibiosis in deep-sea crab populations as indicator of biological and behavioural characteristics of the host. J Mar Biol Assoc UK 70:687–695CrossRefGoogle Scholar
  2. Aurivillius CWS (1888) Die maskirun der oxyrrhynchen dekapoden. Besondere anpassungen ihres korperbaues vermittelt. Eine biologisch-morphologische studie. K Sven Vetenskapsakademiens Handl 23:1–92Google Scholar
  3. Baba K, Noda H (1993) A rare collection of a small species of Gymnodoris (Nudibranchia: Polyceridae) held alive by the chelipeds of the crabs, Lybia hatagumoana (Brachyura: Xanthidae), from the bottom off Kanayama Bay, Kii, Japan. Venus 52:283–289Google Scholar
  4. Berke SK, Woodin SA (2008) Energetic costs, ontogenetic shifts and sexual dimorphism in spider crab decoration. Funct Ecol 22:1125–1133CrossRefGoogle Scholar
  5. Boero F, Bouillon J (2005) Cnidaria and Ctenophora. In: Rhode K (ed) Marine Parasitology. CSIRO, Collingwood, pp 177–182Google Scholar
  6. Bouillon J (1967) Révision de la famille des Ptilocodiidae avec la description d’un nouveau genre et d’une nouvelle espèce. Bull Acad R Belg 53:1106–1131Google Scholar
  7. Bouillon J (1978) Sur un nouveau genre et une nouvelle espèce de Ptilocodidae, Hydrichthelloides reticulata et la super-famille des Hydractinoidea (Hydroida-Athecata). Steenstrupia 5:53–67Google Scholar
  8. Cruz-Rivera E (2001) Generality and specificity in the feeding and decoration preferences of three Mediterranean crabs. J Exp Mar Biol Ecol 266:17–31CrossRefGoogle Scholar
  9. d’Udekem d’Acoz C (1999) Inventaire et distribution des crustacés décapodes de l’Atlantique nord-oriental, de la Méditerranée et des eaux continentales adjacentes au nord de 25°N. Patrim Nat 40:1–383Google Scholar
  10. De Grave S, Pentcheff ND, Ahyong ST et al (2009) A classification of living and fossil genera of decapod crustacea. Raffles Bull Zool Suppl Ser 21:1–109Google Scholar
  11. Di Camillo C, Bo M, Puce S et al (2008) The epibiontic assemblage of Geryon longipes (Crustacea: Decapoda: Geryonidae) from the Southern Adriatic Sea. Ital J Zool 75:29–35Google Scholar
  12. Duerden JE (1905) On the habits and reactions of crabs bearing actinians in their claws. Proc Zool Soc Lond 2:491–511Google Scholar
  13. Dvoretsky AG, Dvoretsky VG (2008) Epifauna associated with the northern stone crab Lithodes maia in the Barents Sea. Polar Biol 31:1149–1152CrossRefGoogle Scholar
  14. Edwards C (1972) The hydroids and the Medusae Podocoryne Areolata, P. Borealis and P. Carnea. J Mar Biol Assoc UK 52:97CrossRefGoogle Scholar
  15. Fernandez-Leborans G (2013) A review of cnidarian epibionts on marine crustacea. Oceanol Hydrobiol Stud 42:347–357CrossRefGoogle Scholar
  16. Gili JM, Hughes RG (1995) The ecology of marine benthic hydroids. Oceanogr Mar Biol Annu Rev 33:351–426Google Scholar
  17. Gili JM, Vervoort W, Pagés F (1989) Hydroids from the West African coast: Guinea Bissau, Namibia and South Africa. Sci Mar 53:67–112Google Scholar
  18. Gili JM, Abello P, Villanueva R (1993) Epibionts and intermoult duration in the crab Bathynectes piperitus. Mar Ecol Prog Ser 98:107–113CrossRefGoogle Scholar
  19. Goater TM, Goater CP, Esch GW (2014) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, CambridgeGoogle Scholar
  20. Griffin DJG (1968) Two new species of Achaeus (Crustacea, Decapoda, Majidae) from South Africa. Crustaceana 15:235–248CrossRefGoogle Scholar
  21. Griffin DJG, Tranter HA (1974) Spider crabs of the family majidae (Crustacea: Decapoda: Brachyura) from the red sea. Israel J Zool 23:162–198Google Scholar
  22. Griffin DJG, Tranter HA (1986) The Decapoda Brachyura of the Siboga expedition. Part VIII Majidae. Siboga-Expeditie Monogr 39:1–335Google Scholar
  23. Guinot D (1966) La faune carcinologique (Crustacea Brachyura) de l’Ocean Indien Occidental et de la Mer Rouge. Catalogue, Remarques Biogeographiques et Bibliographie. Mem Inst Fondam Afr Noire 77:238–352Google Scholar
  24. Guinot D, Wicksten MK (2015) Camouflage: carrying behaviour, decoration behaviour, and other modalities of concealment in Brachyura. In: Castro P, Davie PJF, Guinot D et al (eds) Decapoda: Brachyura (part 1), treatise on zoology–anatomy, taxonomy, biology, vol 9C-I. Brill, Leiden, pp 583–638Google Scholar
  25. Guinot D, Doumenc D, Chintiroglou C (1995) A review of the carrying behaviour in brachyuran crabs, with additional information on the symbioses with sea anemones. Raffles Bull Zool 43:377–416Google Scholar
  26. Hamond R (1957) Notes on the hydrozoa of the Norfolk coast. J Linn Soc Lond Zool 43:294–324CrossRefGoogle Scholar
  27. Hartnoll RG (1985) Growth, sexual maturity and reproductive output. In: Wenner AM (ed) Crustacean issues. 3. Factors in adult growth. Balkema, Rotterdam, pp 101–128Google Scholar
  28. Hirohito E (1988) Athecata. The hydroids of Sagami Bay. Biological laboratory imperial household, Tokyo, pp 1–179Google Scholar
  29. Hwang S-J, Song J-I (2013) Four new records of Dendronephthya species (Octocorallia: Alcyonacea: Nephtheidae) from Korea. Anim Syst Evol Divers 29:160–174CrossRefGoogle Scholar
  30. Karplus I, Fiedler GC, Ramcharan P (1998) The intraspecific fighting behavior of the Hawaiian boxer crab, Lybia edmondsoni - fighting with dangerous weapons? Symbiosis 24:287–301Google Scholar
  31. Lieske E, Myers R (2004) Coral reef guide: Red Sea. Harper Collins, LondonGoogle Scholar
  32. Mastrototaro F, Aguilar R, Chimienti G et al (2016) The rediscovery of Rosalinda incrustans (Cnidaria: hydrozoa) in the Mediterranean Sea. Ital J Zool 83:244–247CrossRefGoogle Scholar
  33. McGaw IJ (2006) Epibionts of sympatric species of cancer crabs in Barkley sound, British Columbia. J Crustac Biol 26:85–93CrossRefGoogle Scholar
  34. Miers EJ (1879) On the classification of the Maioid Crustacea or Oxyrhyncha, with a synopsis of the families, sub-families and genera. J Linn Soc Lond Zool 14:634–673CrossRefGoogle Scholar
  35. Millard NAH (1975) Monograph on the Hydroida of southern Africa. Ann S Afr Mus 68:1–513Google Scholar
  36. Mori M, Manconi R (1990) Macroepizoites associated with Paromola cuvieri (Risso, 1816) (Decapoda, Homolidae) of the Ligurian Sea. Crustaceana 58:124–129Google Scholar
  37. Ng PKL, Davie PJF, Guinot D, Davie PJF (2008) Systema Brachyurorum: part I. An annotated checklist of extant brachyuran crabs of the world. Raffles Bull Zool 17:1–286Google Scholar
  38. Pfeifer R, Berking S (1995) Control of formation of the two types of polyps in Thecocodium quadratum (Hydrozoa, Cnidaria). Int J Dev Biol 39:395–400Google Scholar
  39. Pica D, Bastari A, Vaga CF, et al (2017) Hydroid diversity of Eilat Bay with the description of a new Zanclea species. Mar Biol Res doi: 10.1080/17451000.2016.1236202
  40. Puce S, Calcinai B, Bavestrello G et al (2005) Hydrozoa (Cnidaria) symbiotic with Porifera: a review. Mar Ecol 26:73–81CrossRefGoogle Scholar
  41. Puce S, Bavestrello G, Di Camillo CG, Boero F (2007) Symbiotic relationships between hydroids and bryozoans. Symbiosis 44:137–143Google Scholar
  42. Puce S, Cerrano C, Di Camillo CG, Bavestrello G (2008a) Hydroidomedusae (Cnidaria: hydrozoa) symbiotic radiation. J Mar Biol Assoc UK 88:1715–1721CrossRefGoogle Scholar
  43. Puce S, Di Camillo CG, Bavestrello G et al (2008b) Hydroids symbiotic with octocorals from the Sulawesi Sea, Indonesia. J Mar Biol Assoc UK 88:1643–1654CrossRefGoogle Scholar
  44. Schnytzer Y, Giman Y, Karplus I, Achituv Y (2013) Bonsai anemones: growth suppression of sea anemones by their associated kleptoparasitic boxer crab. J Exp Mar Biol Ecol 448:265–270CrossRefGoogle Scholar
  45. Schnytzer Y, Giman Y, Karplus I, Achituv Y (2017) Boxer crabs induce asexual reproduction of their associated sea anemones by splitting and intraspecific theft. Peer J 5:e2954CrossRefGoogle Scholar
  46. Schuchert P (2010) The European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Capitata part 2. Rev Suisse Zool 117:337–555CrossRefGoogle Scholar
  47. Schuchert P (2017) World Hydrozoa database. http://www.marinespecies.org/hydrozoa. Accessed 20 Jan 2017
  48. Stachowicz JJ, Hay ME (1999) Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivores. Ecology 80:495–509CrossRefGoogle Scholar
  49. Stechow E (1909) Hydroidpolypen der japanischen Ostküste. I. Teil: Athecata und Plumularidae. Abh Math Klasse Kg Bayer Akad Wiss S1:1–111Google Scholar
  50. Stechow E (1926) Einige neue Hydroiden aus verschiedenen Meeres gebieten. Zool Anz 68:96–108Google Scholar
  51. Wicksten M (1993) A review and a model of decorating behavior in spider crabs (Decapoda, Brachyura, Majidae). Crustaceana 64:314–325CrossRefGoogle Scholar
  52. Woods C, Page M (1999) Sponge masking and related preferences in the spider crab Thacanophrys filholi (Brachyura: Majidae). Mar Freshw Res 50:135–143Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Laboratory of Marine Biology, Department of ZoologyUniversity of ValenciaBurjassotSpain
  2. 2.University Museum of Bergen, Natural History Collections, University of BergenBergenNorway
  3. 3.Centre d’Estudis Avançats de Blanes (CEAB-CSIC)BlanesSpain
  4. 4.INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia AgrobiotechSophia AntipolisFrance
  5. 5.Department of Life SciencesThe Natural History MuseumLondonUK

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