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The stony coral Agaricia tenuifolia Dana, 1848 as a new gall crab host (Decapoda: Cryptochiridae)

Abstract

Infrequently studied coral species are seldom mentioned as host organisms of associated fauna. Here we report on the stony coralAgaricia tenuifoliaDana, 1848 hosting a gall crab (Cryptochiridae) for the first time. This coral-dwelling crab was observed at the southern coast of Bonaire in the Dutch Caribbean. Based on the shape of the dwelling, and the host specificity of cryptochirids, the crab is tentatively identified asOpecarcinus hypostegus(Shaw & Hopkins, 1977).

Key words:
Associated organisms; Caribbean; Crustacea; host specificity; Scleractinia.

In the Caribbean, many stony corals are host to one or more associated organisms, including numerous crustacean species (Zlatarski and Martínez-Estalella, 1982Zlatarski, V.N. and Martínez-Estalella, N. 1982. Les Scléractiniaires de Cuba avec des données sur les organismes associés. Sofia, Editions l’Académie bulgare des Sciences, 472p.). About 30 scleractinian species are known to be inhabited by one of three coral gall crabs of the family Cryptochiridae (Kropp and Manning, 1987Kropp, R.K. and Manning, R.B. 1987. The Atlantic gall crabs, family Cryptochiridae (Crustacea: Decapoda: Brachyura). Smithsonian Contributions to Zoology, 462: 1-21.; van der Meij, 2014van der Meij, S.E.T. 2014. Host species, range extensions, and an observation of the mating system of Atlantic shallow-water gall crabs (Decapoda: Cryptochiridae). Bulletin of Marine Science, 90: 1001-1010.; Hoeksema et al., 2017Hoeksema, B.W.; van Beusekom, M; ten Hove, H.A.; Ivanenko, V.N.; van der Meij, S.E.T. and van Moorsel, G.W.N.M. 2017. Helioseris cucullata as a host coral at St. Eustatius, Dutch Caribbean. Marine Biodiversity, 47: 71-78.): Kroppcarcinus siderastreicola Badaro, Neves, Castro & Johnsson, 2012, Troglocarcinus corallicola Verrill, 1908, and Opecarcinus hypostegus (Shaw & Hopkins, 1977). The latter species is known to only inhabit corals belonging to the family Agariciidae; five Agaricia species (Agaricia agaricites (Linnaeus, 1758), Agaricia fragilis Dana, 1848, Agaricia grahamae Wells, 1973, Agaricia humilis Verrill, 1901, and Agaricia lamarcki H. Milne Edwards & Haime, 1851) as well as Helioseris cucullata (Ellis & Solander, 1786) host this gall crab. Earlier records of O. hypostegus inhabiting Siderastrea Blainville, 1830 corals are doubtful, and should likely be attributed to K. siderastreicola (Hoeksema et al., 2017).

On 18 November 2016, during a period of relatively low wave-action, a shore-dive was made in front of the lighthouse Willemstoren (12°01’39”N 68°14’12”W) at the southern coast of Bonaire (Dutch Caribbean). At this locality, corals were investigated for the presence of cryptochirid crabs. Photos were taken with a Nikon D7100 with 60 mm lens in a Hugyfot housing. Between 5 and 15 m depth, around the drop-off, many colonies of Agaricia tenuifolia Dana, 1848 were present. In one of these colonies a gall crab was encountered and photographically documented (Fig. 1). The identity of the gall crab was not confirmed by a collected specimen, but the shape of the dwelling strongly indicates the presence of O. hypostegus (compare Kropp and Manning, 1987Kropp, R.K. and Manning, R.B. 1987. The Atlantic gall crabs, family Cryptochiridae (Crustacea: Decapoda: Brachyura). Smithsonian Contributions to Zoology, 462: 1-21.: Fig. 10d, e). Moreover, no other cryptochirids are known to inhabit Agariciidae corals (van der Meij, 2014van der Meij, S.E.T. 2014. Host species, range extensions, and an observation of the mating system of Atlantic shallow-water gall crabs (Decapoda: Cryptochiridae). Bulletin of Marine Science, 90: 1001-1010.; Hoeksema et al., 2017Hoeksema, B.W.; van Beusekom, M; ten Hove, H.A.; Ivanenko, V.N.; van der Meij, S.E.T. and van Moorsel, G.W.N.M. 2017. Helioseris cucullata as a host coral at St. Eustatius, Dutch Caribbean. Marine Biodiversity, 47: 71-78.; van Tienderen and van der Meij, 2017van Tienderen, K.M. and van der Meij, S.E.T. 2017. Extreme mitochondrial variation in the Atlantic gall crabOpecarcinus hypostegus(Decapoda: Cryptochiridae) reveals adaptive genetic divergence overAgariciacoral hosts.Scientific Reports, 7: 39461.). A future effort to collect gall crabs from A. tenuifolia might be undertaken to confirm the crab’s identity. But even in the implausible case that the crab belongs to another cryptochirid species, this observation is relevant, as it is the first record of A. tenuifolia acting as a host to gall crabs. In the Agariciidae, only Agaricia undata (Ellis & Solander, 1786) and Leptoseris cailleti (Duchassaing & Michelotti, 1864) have not yet been found inhabited by gall crabs. As both species occur relatively deep (ca 20-80 m depth and 30-150 m depth, respectively) they are less likely to be encountered by divers (Aronson et al., 2008Aronson, R.; Bruckner, A.; Moore, J.; Precht, B. and Weil, E. 2008. Agaricia undata, Leptoseris cailleti. The IUCN Red List of Threatened Species 2008: e.T133100A3560174, e.T133686A3864752. ). In addition, L. cailleti is a rarely reported, uncommon coral species (Fenner, 2001Fenner, D. 2001. Biogeography of three Caribbean corals (Scleractinia) and the invasion of Tubastraea coccinea into the Gulf of Mexico. Bulletin of Marine Science, 69: 1175-1189.).

Figure 1
A gall crab, tentatively identified as Opecarcinus hypostegus, in its dwelling (inset) in the scleractinian coral Agaricia tenuifolia at Willemstoren, Bonaire.

Infrequently studied species such as A. tenuifolia are rarely mentioned in lists of host organisms (Nelson et al., 2016Nelson, H. R.; Kuempel, C.D. and Altieri, A.H. 2016. The resilience of reef invertebrate biodiversity to coral mortality. Ecosphere, 7: e01399.; Hoeksema et al., 2017Hoeksema, B.W.; van Beusekom, M; ten Hove, H.A.; Ivanenko, V.N.; van der Meij, S.E.T. and van Moorsel, G.W.N.M. 2017. Helioseris cucullata as a host coral at St. Eustatius, Dutch Caribbean. Marine Biodiversity, 47: 71-78.). Several non-mutually exclusive explanations exist for the lack of data on symbionts of A. tenuifolia. Two explanations are related to research: 1) The species is known to occur in turbulent water, not easily accessible for underwater research, and 2) Presence of A. tenuifolia is not always noticed in research due to its similarity to its congener A. agaricites. Experienced observers have expressed difficulties to discern between the species (van Duyl, 1985van Duyl, F.C. 1985. Atlas of the living reefs of Curaçao and Bonaire (Netherlands Antilles). Utrecht, Natuurwetenschappelijke studiekring voor Suriname en de Nederlandse Antillen, 117, 35 p. Available at http://www.dcbd.nl/document/atlas-living-reefs-curaçao-and-bonaire-netherlands-antilles
http://www.dcbd.nl/document/atlas-living...
). Colonies of A. tenuifolia form large box-like structures consisting almost exclusively of bifacial lobes. Agaricia agaricites grows bifacial lobes as well, especially in the shallow zone where A. tenuifolia may be abundant, but its lobes are thicker and the rims are less wavy than in A. tenuifolia. In addition, A. agaricites tends to form more horizontal unifacial plates. At Willemstoren (Bonaire), both species co-exist and the morphological difference is obvious.

Another explanation is related to the organisms themselves; the host may be less attractive for gall crabs. To find only one crab among many host colonies at this and other (see below) localities suggests a less favourable environment for gall crabs. In Bonaire, coral colonies of other Agaricia Lamarck, 1801 species, such as A. agaricites and A. lamarcki, often host many gall crabs, a situation similar to that of Curaçao (van Tienderen and van der Meij, 2016van Tienderen, K.M. and van der Meij, S.E.T. 2016. Occurrence patterns of coral-dwelling gall crabs (Cryptochiridae) over depth intervals in the Caribbean.PeerJ, 4: e1794.). Ongoing adaptive divergence of O. hypostegus over Agariciidae corals, a possible sign of further diversification in this species, was suggested to cause the observed differences in host occurrence (van Tienderen and van der Meij, 2016van Tienderen, K.M. and van der Meij, S.E.T. 2016. Occurrence patterns of coral-dwelling gall crabs (Cryptochiridae) over depth intervals in the Caribbean.PeerJ, 4: e1794.; 2017van Tienderen, K.M. and van der Meij, S.E.T. 2017. Extreme mitochondrial variation in the Atlantic gall crabOpecarcinus hypostegus(Decapoda: Cryptochiridae) reveals adaptive genetic divergence overAgariciacoral hosts.Scientific Reports, 7: 39461.).

Specific research on poorly investigated or rare species may result in new ecological data (Hoeksema et al., 2017Hoeksema, B.W.; van Beusekom, M; ten Hove, H.A.; Ivanenko, V.N.; van der Meij, S.E.T. and van Moorsel, G.W.N.M. 2017. Helioseris cucullata as a host coral at St. Eustatius, Dutch Caribbean. Marine Biodiversity, 47: 71-78.). Especially in the presently threatened coral reef environments, ecological relationships should be studied before it is impossible to do so. Also, the gathered knowledge may have important applications for coral reef conservation. Off Bonaire, the presence of A. tenuifolia has decreased dramatically. For example at Playa Bengé (12°17’27” 68°24’44”) in the Washington-Slagbaai National Park, only barren remnants remain of the grooves and spurs that carried an abundant cover of this coral in the late seventies and beginning of the eighties of the previous century (GvM pers. obs). Nevertheless, A. tenuifolia is still available for research at several locations along the eastern windward coast of Bonaire. Apart from Willemstoren, the species was also found at Mamparia Gutu (12°04’36” 68°13’49”) and in White Hole (12°05’39”N 68°13’41”W). During low-wind periods, waves and swell are reduced and offer appropriate research conditions to discover ecological relationships unknown from the better-studied leeward sides of Caribbean islands.

Acknowledgements

During underwater fieldwork at Bonaire GvM was accompanied by Micky Streefkerk. We thank two anonymous reviewers for their constructive comments.

References

  • Aronson, R.; Bruckner, A.; Moore, J.; Precht, B. and Weil, E. 2008. Agaricia undata, Leptoseris cailleti The IUCN Red List of Threatened Species 2008: e.T133100A3560174, e.T133686A3864752.
  • Fenner, D. 2001. Biogeography of three Caribbean corals (Scleractinia) and the invasion of Tubastraea coccinea into the Gulf of Mexico. Bulletin of Marine Science, 69: 1175-1189.
  • Hoeksema, B.W.; van Beusekom, M; ten Hove, H.A.; Ivanenko, V.N.; van der Meij, S.E.T. and van Moorsel, G.W.N.M. 2017. Helioseris cucullata as a host coral at St. Eustatius, Dutch Caribbean. Marine Biodiversity, 47: 71-78.
  • Kropp, R.K. and Manning, R.B. 1987. The Atlantic gall crabs, family Cryptochiridae (Crustacea: Decapoda: Brachyura). Smithsonian Contributions to Zoology, 462: 1-21.
  • Nelson, H. R.; Kuempel, C.D. and Altieri, A.H. 2016. The resilience of reef invertebrate biodiversity to coral mortality. Ecosphere, 7: e01399.
  • van der Meij, S.E.T. 2014. Host species, range extensions, and an observation of the mating system of Atlantic shallow-water gall crabs (Decapoda: Cryptochiridae). Bulletin of Marine Science, 90: 1001-1010.
  • van Duyl, F.C. 1985. Atlas of the living reefs of Curaçao and Bonaire (Netherlands Antilles). Utrecht, Natuurwetenschappelijke studiekring voor Suriname en de Nederlandse Antillen, 117, 35 p. Available at http://www.dcbd.nl/document/atlas-living-reefs-curaçao-and-bonaire-netherlands-antilles
    » http://www.dcbd.nl/document/atlas-living-reefs-curaçao-and-bonaire-netherlands-antilles
  • van Tienderen, K.M. and van der Meij, S.E.T. 2016. Occurrence patterns of coral-dwelling gall crabs (Cryptochiridae) over depth intervals in the Caribbean.PeerJ, 4: e1794.
  • van Tienderen, K.M. and van der Meij, S.E.T. 2017. Extreme mitochondrial variation in the Atlantic gall crabOpecarcinus hypostegus(Decapoda: Cryptochiridae) reveals adaptive genetic divergence overAgariciacoral hosts.Scientific Reports, 7: 39461.
  • Zlatarski, V.N. and Martínez-Estalella, N. 1982. Les Scléractiniaires de Cuba avec des données sur les organismes associés. Sofia, Editions l’Académie bulgare des Sciences, 472p.

Publication Dates

  • Publication in this collection
    2018

History

  • Received
    19 June 2017
  • Accepted
    20 Nov 2017
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com