Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-18T16:52:14.908Z Has data issue: false hasContentIssue false

Characterizing population structure of coral-associated fauna from mesophotic and shallow habitats in the Caribbean

Published online by Cambridge University Press:  29 June 2018

Alex J. Veglia
Affiliation:
Department of Marine Sciences, University of Puerto Rico at Mayagüez, PO Box 9000, Mayagüez, Puerto Rico 00681, USA
Nicholas M. Hammerman
Affiliation:
Department of Marine Sciences, University of Puerto Rico at Mayagüez, PO Box 9000, Mayagüez, Puerto Rico 00681, USA School of Biological Sciences, University of Queensland, Gehrmann Laboratories, Level 8, Research Road, St Lucia, QLD 4072, Australia
Carlos R. Rivera Rosaly
Affiliation:
Department of Marine Sciences, University of Puerto Rico at Mayagüez, PO Box 9000, Mayagüez, Puerto Rico 00681, USA
Matthew Q. Lucas
Affiliation:
Universidad Interamericana de Puerto Rico, Recinto de Arecibo, PO Box 4050, Arecibo, Puerto Rico 00614, USA
Alexandra Galindo Estronza
Affiliation:
Department of Marine Sciences, University of Puerto Rico at Mayagüez, PO Box 9000, Mayagüez, Puerto Rico 00681, USA
Paulo H. Corgosinho
Affiliation:
Universidade Estadual de montes Claros, Campus Universitário Professor Darcy Ribeiro, Avenida Dr Ruy Braga, S/N – CEP 39401-089, Montes Claros, MG, Brazil
Nikolaos V. Schizas*
Affiliation:
Department of Marine Sciences, University of Puerto Rico at Mayagüez, PO Box 9000, Mayagüez, Puerto Rico 00681, USA
*
Correspondence should be addressed to: Alex J. Veglia, Department of Marine Sciences, University of Puerto Rico at Mayagüez, PO Box 9000, Mayagüez, Puerto Rico 00681, USA email: [email protected]

Abstract

Symbiotic relationships are a common phenomenon among marine invertebrates, forming both obligatory and facultative dependencies with their host. Here, we investigate and compare the population structure of two crustacean species associated with both shallow and mesophotic ecosystems: an obligate symbiont barnacle (Ceratoconcha domingensis), of the coral Agaricia lamarcki and a meiobenthic, free-living harpacticoid copepod (Laophontella armata). Molecular analyses of the Cytochrome Oxidase Subunit I (COI) gene revealed no population structure between mesophotic and shallow barnacle populations within south-west Puerto Rico (ΦST = 0.0079, P = 0.33). The absence of population structure was expected due to the pelagic naupliar larvae of the barnacles and the connectivity patterns exhibited by the coral itself within the same region. Laophontella armata exhibited significant structure based on the mitochondrial COI gene between the mesophotic reef ecosystem of El Seco, Puerto Rico and mangrove sediments of Curaçao (ΦST = 0.2804, P = 0.0). The El Seco and Curaçao copepods shared three COI haplotypes despite the obligatory benthic development of harpacticoid copepods and the geographic distance between the two locations. Three other COI haplotypes from El Seco exhibited higher than expected (up to 7%) intra-species variability, potentially representing three new cryptic species of harpacticoid copepods or rare, deeply divergent lineages of L. armata. This result is evidence for the urgent need of a deeper investigation into the meiofauna diversity associated with mesophotic coral ecosystems (MCEs), arguably the most diverse metazoan component of MCEs.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally.

References

Appeldoorn, R.S., Hensley, D.A., Shapiro, D.Y., Kioroglou, S. and Sanderson, B.G. (1994) Egg dispersal in a Caribbean coral reef fish, Thalassoma bifasciatum. II. Dispersal off the reef platform. Bulletin of Marine Science 5, 271280.Google Scholar
Aronson, R., Bruckner, A., Moore, J., Precht, B. and Weil, E. (2008) Agaricia lamarcki. The IUCN red list of threatened species 2008, e. T132970A3515504. Gland and Cambridge: IUCN.Google Scholar
Ballantine, D.L. and Ruiz, H. (2010) Two new deep-water Peyssonnelia species, P. iridescens and P. gigaspora (Peyssonneliaceae, Rhodophyta), from Puerto Rico, Caribbean Sea. Phycologia 49, 537544.Google Scholar
Bandelt, H.J., Forster, P. and Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 1, 3748.Google Scholar
Blackall, L.L., Wilson, B. and van Oppen, M.J. (2015) Coral – the world's most diverse symbiotic ecosystem. Molecular Ecology 24, 53305347.Google Scholar
Bongaerts, P., Frade, P.R., Ogier, J.J., Hay, K.B., van Bleijswijk, J., Englebert, N., Vermeij, M.J., Bak, R.P., Visser, P.M. and Hoegh-Guldberg, O. (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evolutionary Biology 13, 205.Google Scholar
Bongaerts, P., Riginos, C., Brunner, R., Englebert, N., Smith, S.R. and Hoegh-Guldberg, O. (2017) Deep reefs are not universal refuges: reseeding potential varies among coral species. Marine Ecology 3, e1602373.Google Scholar
Buhl-Mortensen, L., Vanreusel, A., Gooday, A.J., Levin, L.A., Priede, I.G., Buhl-Mortensen, P., Gheerardyn, H., King, N.J. and Raes, M. (2010) Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Marine Ecology 31, 2150.Google Scholar
Burton, R.S. (1998) Intraspecific phylogeography across the Point Conception biogeographic boundary. Evolution 52, 734745.Google Scholar
Burton, R.S., Feldman, M.W. and Curtsinger, J.W. (1979) Population genetics of Tigriopus californicus. Copepoda: Harpacticoida. I. Population structure along the central California coast. Marine Ecology Progress Series 1, 2939.Google Scholar
Carpenter, K.E., Abrar, M., Aeby, G., Aronson, R.B., Banks, S., Bruckner, A., Chiriboga, A., Cortes, J., Delbeek, J.C., DeVantier, L., Edgar, G.J., Edwards, A.J., Fenner, D., Guzman, H.M., Hoeksema, B.W., Hodgson, G., Johan, O., Licuanan, W.Y., Veron, J.E.N., Wallace, C., Weil, E. and Wood, E. (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 25, 560563.Google Scholar
Chen, Y.Y., Lin, H.C. and Chan, B.K. (2012) Description of a new species of coral-inhabiting barnacle, Darwiniella angularis sp. n. (Cirripedia, Pyrgomatidae) from Taiwan. ZooKeys 214, 43Google Scholar
Cheng, Y.R., Mayfield, A.B., Meng, P.J., Dai, C.F. and Huys, R. (2016) Copepods associated with scleractinian corals: a worldwide checklist and a case study of their impact on the reef- building coral Pocillopora damicornis (Linnaeus, 1758) (Pocilloporidae). Zootaxa 4174, 291345.Google Scholar
Connor, R.C. (1995) The benefits of Mutualism: a conceptual framework. Biological Reviews 70, 427457.Google Scholar
Cowen, R.K. and Sponaugle, S. (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443466.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 8, 11641165.Google Scholar
Darwin, C. (1859) The origin of species. London: J. Murray.Google Scholar
Delrieu-Trottin, E., Mona, S., Maynard, J., Neglia, V., Veuille, M. and Planes, S. (2017) Population expansions dominate demographic histories of endemic and widespread Pacific reef fishes. Scientific Reports 7, 40519. doi: 10.1038/srep40519.Google Scholar
Denis, F., Ravallec, R., Pavillon, J.F. and Van Wormhoudt, A. (2009) Genetic differentiation of Atlantic populations of the intertidal copepod Tigriopus brevicornis. Scientia Marina 73, 579587.Google Scholar
Edmands, S. (2001) Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes. Molecular Ecology 10, 17431750.Google Scholar
Excoffier, L. and Lischer, H.E. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 3, 564567.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Gardner, T.A. (2003) Long-term region-wide declines in Caribbean corals. Science 301, 958960.Google Scholar
Geddes, D.C. (1968) Marine biological investigations in the Bahamas 3. Harpacticoid copepods belonging to the family Tetragonicipitidae Lang. Sarsia 32, 2138.Google Scholar
Glynn, P.W. and Enochs, I. (2011) Invertebrates and their roles in coral reef ecosystems. In Dubinsky, Z. and Stambler, N (eds) Coral reefs: an ecosystem in transition. Dordrecht: Springer, pp. 273325.Google Scholar
Gollner, S.H., Stuckas, H., Kihara, T.C., Laurent, S., Kodami, S., Martinez Arbizu, P. and Duperron, S. (2016) Mitochondrial DNA analyses indicate high diversity, expansive population growth and high genetic connectivity of vent copepods (Dirivultidae) across different oceans. PloS ONE 11, e0163776.Google Scholar
Gregg, C.S., Foltz, D.W. and Fleeger, J.W. (2010) Genetic diversity in a deep-sea harpacticoid copepod found near two oil-drilling sites in the Gulf of Mexico. Journal of Crustacean Biology 30, 651657.Google Scholar
Hammerman, N.M., Rivera-Vicens, R.E., Galaska, M.P., Weil, E., Alfaro, M., Appeldoorn, R.S. and Schizas, N.V. (2017) Population connectivity of the plating coral, Agaricia lamarcki from southwest Puerto Rico. Coral Reefs 37, 183. doi: 10.1007/s00338-017-1646-x.Google Scholar
Handschumacher, L., Steinarsdottir, M.B., Edmands, S. and Ingolfson, A. (2010) Phylogeography of the rock-pool copepod Tigriopus brevicornis (Harpacticoida) in the northern North Atlantic, and its relationship to other species of the genus. Marine Biology 157, 13571366.Google Scholar
Harvell, C.D., Altizer, S., Cattadori, I.M., Harrington, L. and Weil, E. (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90, 912920.Google Scholar
Hinderstein, L.M., Marr, J.C.A., Martinez, F.A., Dowgiallo, M.J., Puglise, K.A., Pyle, R.L., Zawada, D.G. and Appeldoorn, R.S. (2010) Theme section on mesophotic coral ecosystems: characterization, ecology, and management. Coral Reefs 29, 247251.Google Scholar
Holstein, D.M., Smith, T.B., Gyory, J. and Paris, C.B. (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Scientific Reports 5, 12407. doi: 10.1038/srep12407.Google Scholar
Humes, A.G. (1985) Cnidarians and copepods: a success story. Transactions of the American Microsocial Society 104, 313320.Google Scholar
Ivanenko, V.N. (1998) Laperocheres koorius, a new genus and species (Copepoda: Siphonostomatoida: Asterocheridae) associated with the sponge Amphimedon in Australia. Proceedings of the Biological Society of Washington 111, 263271.Google Scholar
Johannesson, K. (1988) The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic dispersal stage (L. littorea)? Marine Biology 88, 507513.Google Scholar
Kahng, S.E., Copus, J.M. and Wagner, D. (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Current Opinion in Environmental Sustainability 7, 7281.Google Scholar
Kahng, S.E., Copus, J.M. and Wagner, D. (2016) Mesophotic coral ecosystems. In Rossi, S., Bramanti, L., Gori, A. and Orejas, C. (eds) Marine Animal Forests. Cham: Springer. doi: 10.1007/978-3-319-17001-5_4-1.Google Scholar
Katoh, K. and Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 4, 772780.Google Scholar
Knowlton, N., Brainard, R.E., Fisher, R., Moews, M., Plaisance, L. and Caley, M.J. (2010) Coral reef biodiversity. In McIntyre, A.D. (ed.) Life in the World's Oceans: diversity distribution and abundance. Chichester: Wiley-Blackwell, pp. 6574.Google Scholar
Kramarsky-Winter, E., Harel, M., Siboni, N., Ben Dov, E., Brickner, I., Loya, Y. and Kushmaro, A. (2006) Identification of a protist–coral association and its possible ecological role. Marine Ecology Progress Series 317, 6773.Google Scholar
Leigh, J. W. and Bryant, D. (2015) popart: fullãfeature software for haplotype network construction. Methods in Ecology and Evolution 6, 11101116.Google Scholar
Librado, P. and Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 11, 14511452.Google Scholar
Liu, J.C.W., Hoeg, J.T. and Chan, B.K.K. (2017) How do coral barnacles start their life in their hosts? Biology Letters 12, 20160124.Google Scholar
Lucas, M.Q., Stat, M., Smith, M.C., Weil, E. and Schizas, N.V. (2016) Symbiodinium (internal transcribed spacer 2) diversity in the coral host Agaricia lamarcki (Cnidaria: Scleractinia) between shallow and mesophotic reefs in the Northern Caribbean (20–70 m). Marine Ecology 37, 10791087. doi: 10.1111/maec.12367.Google Scholar
Mokady, O., Loya, Y., Achituv, Y., Geffen, E., Graur, D., Rozenblatt, S. and Brickner, I (1999) Speciation vs phenotypic plasticity in coral inhabiting barnacles: Darwin's observations in an ecological context. Journal of Molecular Evolution 49, 367375.Google Scholar
Neigel, J., Domingo, A. and Stake, J. (2007) DNA barcoding as a tool for coral reef conservation. Coral Reefs 26, 487. doi: 10.1007/s00338-007-0248-4.Google Scholar
Nelson, H.R., Kuempel, C.D. and Altieri, A.H. (2016) The resilience of reef invertebrate biodiversity to coral mortality. Ecosphere 7, e01399.Google Scholar
Pešić, V., Chatterjee, T., Alfaro, M. and Schizas, N.V. (2014) A new species of Litarachna (Acari, Hydrachnidia, Pontarachnidae) from a Caribbean mesophotic coral ecosystem with notes on a littoral Litarachna sp. ZooKeys 425, 8997.Google Scholar
Plaisance, L., Caley, M.J., Brainard, R.E. and Knowlton, N. (2011) The diversity of coral reefs: what are we missing? PLoS ONE 10, e25026.Google Scholar
Plaisance, L., Knowlton, N., Paulay, G. and Meyer, C. (2009) Reef-associated crustacean fauna: biodiversity estimates using semi-quantitative sampling and DNA barcoding. Coral Reefs 28, 977986.Google Scholar
Pyle, R.L. and Kosaki, R.K. (2016) Prognathodes basabei, a new species of butterflyfish (Perciformes, Chaetodontidae) from the Hawaiian Archipelago. ZooKeys 614, 137152.Google Scholar
Raupach, M.J. and Radulovici, A.E. (2015) Looking back on a decade of barcoding crustaceans. Zookeys 539, 5381.Google Scholar
Rohwer, F., Seguritan, V., Azam, F. and Knowlton, N. (2002) Diversity and distribution of coral-associated bacteria. Marine Ecology Progress Series 243, 110.Google Scholar
Schizas, N.V., Coull, B.C., Chandler, G.T. and Quattro, J.M. (2002) Sympatry of distinct DNA lineages in a copepod inhabiting estuarine creeks in the southeastern USA. Marine Biology 140, 585594.Google Scholar
Schizas, N.V., Dahms, H.U., Kangtia, P., Corgosinho, P.H.C. and Galindo Estronza, A. (2015) A new species of Longipedia Claus, 1863 (Copepoda: Harpacticoida: Longipediidae) from Caribbean mesophotic reefs with remarks on the phylogenetic affinities of Polyarthra. Marine Biology Research 11, 789803.Google Scholar
Schizas, N.V., Street, G.T., Coull, B.C., Chandler, G.T. and Quattro, J.M. (1999) Molecular population structure of the marine benthic copepod Microarthridion littorale along the southeastern and Gulf coasts of the USA. Marine Biology 135, 399405.Google Scholar
Sekar, R., Mills, D.K., Remily, E.R., Voss, J.D. and Richardson, L.L. (2006) Microbial communities in the surface mucopolysaccharide layer and the black band microbial mat of black band-diseased Siderastrea siderea. Applied and Environmental Microbiology 72, 59635973.Google Scholar
Slattery, M., Lesser, M.P., Brazeau, D., Stokes, M.D. and Leichter, J.J. (2011) Connectivity and stability of mesophotic coral reefs. Journal of Experimental Marine Biology and Ecology 408, 3241.Google Scholar
Stella, J.S., Pratchett, M.S., Hutchings, P.A. and Jones, G.P. (2011) Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanography and Marine Biology – An Annual Review 49, 43104.Google Scholar
Stock, J.H. (1987) Copepoda Siphonostomatoida associated with West Indian hermatypic corals. 1: Associates of Scleractinia: Faviinae. Bulletin of Marine Science 40, 464483.Google Scholar
Stock, J.H. (1988) Copepods associated with reef corals: a comparison between the Atlantic and the Pacific. Hydrobiologia 167/168, 545547.Google Scholar
Swofford, D.L. (2001) PAUP: Phylogenetic analysis using parsimony (and other methods) 4.0.b5. doi: 10.1111/j.0014-3820. 2002.tb00191.x.Google Scholar
Tamura, K. and Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 3, 512526.Google Scholar
Toonen, R.J., Andrews, K.R., Baums, I.B., Bird, C.E., Concepcion, G.T., Daly-Engel, T.S., Eble, J.A., Faucci, A., Gaither, M.R., Iacchei, M., Puritz, J.B., Schultz, J.K., Skillings, D.J., Timmers, M.A. and Bowen, B.W. (2011) Defining boundaries for ecosystem-based management: a multispecies case study of marine connectivity across the Hawaiian Archipelago. Journal of Marine Biology 2011, 460173. doi: 10.1155/2011/460173.Google Scholar
Tsang, L.M., Chan, B.K.K., Shih, F.L., Chu, K.H. and Chen, C.A. (2009) Host-associated speciation in the coral barnacle Wanella milleporae (Cirripedia: Pyrogomatidae) inhabiting the Millepora coral. Molecular Ecology 18, 14631475.Google Scholar
Weir, B.S. and Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 13581370.Google Scholar
Willett, C. and Ladner, J. (2009) Investigations of fine-scale phylogeography in Tigriopus californicus reveal historical patterns of population divergence. BMC Evolutionary Biology 9, 139.Google Scholar
Willey, A. (1935) Harpacticoid Copepoda from Bermuda. Part II. Annals and Magazine of Natural History Series 10, 50100.Google Scholar
Young, P.S. and Christoffersen, M.L. (1984) Recent coral barnacles of the genus Ceratoconcha (Cirripedia: Pyrgomatidae) from Northeast Brazil. Bulletin of Marine Science 35, 239252.Google Scholar
Zitello, A.G., Whitall, D.R., Dieppa, A., Christensen, J.D., Monaco, M.E. and Rohmann, S.O. (2008) Characterizing Jobos Bay, Puerto Rico: a watershed modeling analysis and monitoring plan. NOAA Technical Memorandum NOS NCCOS 76, 81 pp.Google Scholar