Abstract
Macro- and meiobenthos contribute substantially to the diversity of marine habitats and should account for a significant fraction of the diversity in coral reefs. The aims of the present study are to characterize macro- and meiobenthic communities in a Caribbean coral reef and to analyze the effects of habitat type on the α-, β-, and γ-diversity of free-living nematodes. Two reef sites with four habitat types each were selected: seagrass bed, bare sand, coral rubble, and algal turf. Habitats within sites were adjacent to each other and characterized by their physical architecture, hydrodynamic regime, and foundation species. The diversity of marine communities was high, with eight phyla represented in the macrobenthos and 18 phyla in the meiobenthos. The structure of macrobenthos was strongly associated with the habitat type. This relationship was weaker for meiobenthos, which is likely related to ecological drift, hydrodynamic regime, and macrobenthic influence. The nematode species richness was high at both studied scales: α-diversity ranged from 31 to 83 species per habitat and γ-diversity for the whole reef was 156 ± 4 species. The nematode assemblages consisted of few dominant and many rare species, which is typical of hyperdiverse faunas. The β-diversity was large in the reef with few shared species and the presence of distinctive nematode assemblages adapted to the physical architecture and food availability of each habitat. The results imply that the physical structure and heterogeneity of the coral reef habitats are important for maintaining the high diversity of small invertebrates, especially regarding the richness and turnover of nematode species.
Similar content being viewed by others
References
Alongi DM (1986) Population structure and trophic composition of the free-living nematodes inhabiting carbonate sands of Davies Reef, Great Barrier Reef, Australia. Austr J Mar Freshw Res 37:609–619
Alongi DDM (1989) The role of soft-bottom benthic communities in tropical mangrove and coral reef ecosystems. Crit Rev Aquat Sci 1:243–280
Anderson MJ, Gorley RN, Clarke RK (2008) Permanova+ for Primer: guide to software and statistical methods. PRIMER-E Ltd. Plymouth
Ansari ZA, Parulekar AH (1994) Meiobenthos in the sediments of seagrass meadows of Lakshadweep atolls, Arabian Sea. Vie Milieu 44:185–190
Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202
Armenteros M, Creagh B, González-Sansón G (2009) Distribution patterns of the meiofauna in coral reefs from the NW shelf of Cuba. Rev Invest Mar Univ Habana 30:37–43
Armenteros M, Ruiz-Abierno A, Sosa Y, Pérez-García JA (2012) Habitat heterogeneity effects on macro- and meiofauna (especially nematodes) in Punta Francés coral reef (SW Cuban Archipelago). Rev Invest Mar Univ Habana 32:50–61
Bertness MD, Bruno JF, Silliman BR, Stachowicz JJ (eds) (2014) Marine community ecology and conservation. Sinauer Associates, Sunderland
Boucher G (1997) Structure and biodiversity of nematode assemblages in the SW lagoon of New Caledonia. Coral Reefs 16:177–186
Boucher G, Clavier J (1990) Contribution of benthic biomass to overall metabolism in New Caledonia lagoon sediments. Mar Ecol Prog Ser 64:271–280
Bouchet VMP, Sauriau PG, Debenay JP, Mermillod-Blondin F, Schmidt S, Amiard JC, Dupas B (2009) Influence of the mode of macrofauna-mediated bioturbation on the vertical distribution of living benthic foraminifera: First insight from axial tomodensitometry. J Exp Mar Biol Ecol 371:20–33
Caballero-Aragón H, Alcolado PM, Rey-Villiers N, Perera-Valderrama S, González-Méndez J (2016) Coral communities condition in varying wave exposure: the gulf of Cazones, Cuba. Rev Biol Trop 64:95–109
Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorial. PRIMER-E Ltd., Plymouth
Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. Home page: http://purl.oclc.org/estimates
Curini-Galletti M, Artois T, Delogu V, De Smet WH, Fontaneto D, Jondelius U, Leasi F, Martínez A, Meyer-Wachsmuth I, Nilsson KS, Tongiorgi P, Worsaae K, Todaro MA (2012) Patterns of diversity in soft-bodied meiofauna: dispersal ability and body size matter. PLoS One 7:e33801
de Jesús-Navarrete A (2007) Nematodos de los arrecifes de Isla Mujeres y Banco Chinchorro, Quintana Roo, México. Rev Biol Mar Oceanogr 42:193–200
De Troch M, Raes M, Muthumbi A, Gheerardyn H, Vanreusel A (2008) Spatial diversity of nematode and copepod genera of the coral degradation zone along the Kenyan coast, including a test for the use of higher-taxon surrogacy. Afr J Mar Sci 30:25–33
Derycke S, Backeljau T, Moens T (2013) Dispersal and gene flow in free-living marine nematodes. Front Zool 10:1
Fontaneto D, Flot J-F, Tang CQ (2015) Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar Biodiv 45:433–451
Frouin P, Hutchings P (2001) Macrobenthic communities in a tropical lagoon (Tahiti, French Polynesia, central Pacific). Coral Reefs 19:277–285
Gamenick I, Giere O (1994) The microdistribution of coral sand meiofauna affected by water currents. Vie Milieu 44:93–100
Gerrodette T (2011) Inference without significance: measuring support for hypotheses rather than rejecting them. Mar Ecol 32:404–418
Gheerardyn H, de Troch M, Ndaro SGM, Raes M, Vincx M, Vanreusel A (2008) Community structure and microhabitat preferences of harpacticoid copepods in a tropical reef lagoon (Zanzibar Island, Tanzania). J Mar Biol Assoc UK 88:747–758
Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments. Springer, Berlin
Gittenberger A, Draisma SG, Arbi UY, Langenberg V, Erftemeijer PL, Tuti Y, Hoeksema BW (2015) Coral reef organisms as bioregion indicators off Halmahera, Moluccas, Indonesia. Aquat Conserv Mar Freshw Ecosyst 25:743–755
Gobin JF (2007) Free-living marine nematodes of hard bottom substrates in Trinidad and Tobago, West Indies. Bull Mar Sci 81:73–84
Gobin JF, Warwick RM (2006) Geographical variation in species diversity: a comparison of marine polychaetes and nematodes. J Exp Mar Biol Ecol 330:234–244
Gómez O, Ibarzábal DR, Silva A (1980) Evaluación cuantitativa de bentos en la región suroccidental de Cuba. Informe Científico-Técnico Instituto de Oceanología 149:1–25
Gray JS, Elliott M (2009) Ecology of marine sediments. Oxford University Press, Oxford
Guzmán HM, Obando VL, Cortés J (1987) Meiofauna associated with a Pacific coral reef in Costa Rica. Coral Reefs 6:107–112
Hall MO, Bell SS (1993) Meiofauna on the seagrass Thalassia testudinum: population characteristics of harpacticoid copepods and associations with algal epiphytes. Mar Biol 116:137–146
Hansen LA, Alongi DM, Moriarty DJW, Pollard PC (1987) The dynamics of benthic microbial communities at Davies Reef, central Great Barrier Reef. Coral Reefs 6:63–70
Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399–489
Hicks GRF, Coull BC (1983) The ecology of marine meiobenthic harpacticoid copepods. Oceanogr Mar Biol Annu Rev 21:67–175
Hull SL (1997) Seasonal changes in diversity and abundance of ostracods on four species of intertidal algae with differing structural complexity. Mar Ecol Prog Ser 161:71–182
Ibarzábal DR (1985) Distribución de los poliquetos bentónicos en el área de Punta del Este, Isla de la Juventud, Cuba. Rep Inv Inst Oceanol 33:3–31
Klumpp DW, McKinnon AD, Mundy CN (1988) Motile cryptofauna of a coral reef: abundance, distribution and trophic potential. Mar Ecol Prog Ser 45:95–108
Logan D, Townsend KA, Townsend K, Tibbetts IR (2008) Meiofauna sediment relations in leeward slope turf algae of Heron Island reef. Hydrobiologia 610:269–276
López-Cánovas CI, Lalana R (2001) Benthic meiofauna distribution at three coral reefs from SW of Cuba. Rev Invest Mar Univ Habana 22:199–204
Magurran AE, McGill BJ (2011) Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford
Nacorda HME, Yap HT (1996) Macroinfaunal biomass and energy flow in a shallow reef flat of the northwestern Philippines. Hydrobiologia 341:37–49
Nash KL, Graham NAJ, Jennings S, Wilson SK, Bellwood DR (2016) Herbivore cross-scale redundancy supports response diversity and promotes coral reef resilience. J Appl Ecol 53:646–655
Netchy K, Hallock P, Lunz KS, Daly KL (2016) Epibenthic mobile invertebrate diversity organized by coral habitat in Florida. Mar Biodivers 46:451–463
Netto SA, Attrill MJ, Warwick RM (1999a) The effect of a natural water-movement related disturbance on the structure of meiofauna and macrofauna communities in the intertidal sand flat of Rocas Atoll (NE, Brazil). J Sea Res 42:291–302
Netto SA, Warwick RM, Attrill MJ (1999b) Meiobenthic and macrobenthic community structure in carbonate sediments of Rocas Atoll (North-east, Brazil). Estuar Coast Shelf Sci 48:39–50
Ólafsson E (2003) Do macrofauna structure meiofauna assemblages in marine soft-bottoms? a review of experimental studies. Vie Milieu 53:249–265
Ott J, Bright M, Bulgheresi S (2004) Symbioses between marine nematodes and sulfur-oxidizing chemoautotrophic bacteria. Symbiosis 36:103–126
Pavlyuk ON, Trebukhova JA (2006) Meiobenthos in Nha Trang Bay of the South China Sea (Vietnam). Ocean Sci J 41:139–148
Pérez-García JA, Ruiz-Abierno A, Armenteros M (2015) Does morphology of host marine macroalgae drive the ecological structure of epiphytic meiofauna? J Mar Biol Oceanogr 4:1
Pfannkuche O, Thiel H (1988) Sample processing. In: Thiel H, Higgins RP (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 134–145
Raes M, De Troch M, Ndaro SGM, Muthumbi A, Guilini K, Vanreusel A (2007) The structuring role of microhabitat type in coral degradation zones: a case study with marine nematodes from Kenya and Zanzibar. Coral Reefs 26:113–126
Raes M, Decraemer W, Vanreusel A (2008) Walking with worms: coral-associated epifaunal nematodes. J Biogeogr 35:2207–2222
Riddle MJ (1988) Patterns in the distribution of macrofaunal communities in coral reef sediments on the central Great Barrier Reef. Mar Ecol Prog Ser 47:281–292
Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284
Semprucci F, Colantoni P, Baldelli G, Rocchi M, Balsamo M (2010) The distribution of meiofauna on back-reef sandy platforms in the Maldives (Indian Ocean). Mar Ecol 31:592–607
Semprucci F, Colantoni P, Sbrocca C, Baldelli G, Rocchi M, Balsamo M (2011) Meiofauna in sandy back-reef platforms differently exposed to the monsoons in the Maldives (Indian Ocean). J Mar Syst 87:208–215
Semprucci F, Colantoni P, Sbrocca C, Baldelli G, Balsamo M (2014) Spatial patterns of distribution of meiofaunal and nematode assemblages in the Huvadhoo lagoon (Maldives, Indian Ocean). J Mar Biol Assoc UK 94:1377–1385
Sharma J, Baguley J, Bluhm BA, Rowe G (2011) Do meio- and macrobenthic nematodes differ in community composition and body weight trends with depth? PLoS One 6:e14491
St. John J, Jones GP, Sale PF (1989) Distribution and abundance of soft-sediment meiofauna and a predatory goby in a coral reef lagoon. Coral Reefs 8:51–57
Tarjan AC (1980) An illustrated guide to the marine nematodes. Institute of Food and Agricultural Sciences. University of Florida
Vellend M (2010) Conceptual synthesis in community ecology. Quarter Rev Biol 85:183–206
Vincx M (1996) Meiofauna in marine and freshwater sediments. In: Hall GS (ed) Methods for the examination of organismal diversity in soils and sediments. CAB International, Wallingford, pp 187–195
Warwick RM, Platt HM, Somerfield PJ (1998) Free-living marine nematodes. Pt III. Monhysterids, vol 53. The Linnean Society of London and The Estuarine and Coastal Sciences Association, Shrewsbury
Whittaker RJ, Willis KJ, Field R (2001) Scale and species richness: towards a general, hierarchical theory of species diversity. J Biogeogr 28:453–470
WoRMS Editorial Board (2016) World Register of Marine Species. Available from http://www.marinespecies.org at VLIZ. Accessed 2016. doi:10.14284/170
Acknowledgments
We would like to thank Abel Valdivia and Jose Andrés Pérez for the revision and helpful discussions of an early version of the manuscript. We also thank the three anonymous referees for their valuable comments on an earlier draft of this paper. The field expeditions were funded in the framework of Operation Wallacea Cuba 2009 and 2010.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by B. W. Hoeksema
Rights and permissions
About this article
Cite this article
Ruiz-Abierno, A., Armenteros, M. Coral reef habitats strongly influence the diversity of macro- and meiobenthos in the Caribbean. Mar Biodiv 47, 101–111 (2017). https://doi.org/10.1007/s12526-016-0553-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-016-0553-7