Coral reefs are declining worldwide as a result of many anthropogenic disturbances. This trend is alarming because coral reefs are hotspots of marine biodiversity and considered the ‘rainforests of the sea. As in the rainforest, much of the diversity on a coral reef is cryptic, remaining hidden among the cracks and crevices of structural taxa. Although the cryptofauna make up the majority of a reef’s metazoan biodiversity, we know little about their basic ecology or how these communities respond to reef degradation. Emerging research shows that the species richness of the motile cryptofauna is higher among dead (framework) vs. live coral substrates and, surprisingly, increases within successively more eroded reef framework structures, ultimately reaching a maximum in dead coral rubble. Consequently, the paradigm that abundant live coral is the apex of reef diversity needs to be clarified. This provides guarded optimism amidst alarming reports of declines in live coral cover and the impending doom of coral reefs, as motile cryptic biodiversity should persist independent of live coral cover. Granted, the maintenance of this high species richness is contingent on the presence of reef rubble, which will eventually be lost due to physical, chemical, and biological erosion if not replenished by live coral calcification and mortality. The trophic potential of a reef, as inferred from the abundance of cryptic organisms, is highest on live coral. Among dead framework substrates, however, the density of cryptofauna reaches a peak at intermediate levels of degradation. In summary, the response of the motile cryptofauna, and thus a large fraction of the reef’s biodiversity, to reef degradation is more complex and nuanced than currently thought; such that species richness may be less sensitive than overall trophic function.
References
[1]
Jackson, J.B.C.; Kirby, M.X.; Berger, W.H.; Bjorndal, K.A.; Botsford, L.W.; Bourque, B.J.; Bradbury, R.H.; Cooke, R.; Erlandson, J.; Estes, J.A.; et al. Historical overfishing and the recent collapse of coastal ecosystems. Science 2001, 293, 629–638, doi:10.1126/science.1059199. 11474098
[2]
Pandolfi, J.M.; Bradbury, R.H.; Sala, E.; Hughes, T.P.; Bjorndal, K.A.; Cooke, R.G.; McArdle, D.; McClenachan, L.; Newman, M.J.H.; Paredes, G.; et al. Global trajectories of the long-term decline of coral reef ecosystems. Science 2003, 301, 955–958, doi:10.1126/science.1085706. 12920296
[3]
Hughes, T.P.; Baird, A.H.; Bellwood, D.R.; Card, M.; Connolly, S.R.; Folke, C.; Grosberg, R.; Hoegh-Guldberg, O.; Jackson, J.B.C.; Kleypas, J.A.; et al. Climate change, human impacts, and the resilience of coral reefs. Science 2003, 301, 929–933, doi:10.1126/science.1085046. 12920289
[4]
Connell, J.H. Diversity in tropical rain forests and coral reefs. Science 1978, 199, 1302–1310, doi:10.1126/science.199.4335.1302. 17840770
[5]
Reaka-Kudla, M.L. The global biodiversity of coral reefs. In Biodiversity II: Understanding and Protecting Our Biological Resources; Reaka-Kudla, M.L., Wilson, D.E., Wilson, E.O., Eds.; Joseph Henry Press: Washington, DC, USA, 1997; pp. 83–108.
[6]
Adrianov, A.V. Current problems in marine biodiversity studies. Russ. J. Mar. Biol. 2004, 30, S1–S16, doi:10.1007/s11179-005-0013-x.
[7]
Small, A.; Adey, W.; Spoon, D. Are current estimates of coral reef biodiversity too low? The view through the window of a microcosm. Atoll Res. Bull. 1998, 458, 1–20, doi:10.5479/si.00775630.458.1.
[8]
Reaka, M.L.; Rodgers, P.J.; Kudla, A.U. Patterns of biodiversity and endemism on Indo-West Pacific coral reefs. Proc. Natl. Acad. Sci. USA 2008, 105, 11474–11581, doi:10.1073/pnas.0802594105. 18695226
[9]
Roberts, C.M.; McClean, C.J.; Veron, J.E.N.; Hawkins, J.P.; Allen, G.R.; McAllister, D.E.; Mittermeier, C.G.; Schueler, F.W.; Spalding, M.; Wells, F.; et al. Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 2002, 295, 1280–1284, doi:10.1126/science.1067728. 11847338
[10]
Munday, P.L. Habitat loss, resource specialization, and extinction on coral reefs. Glob. Change Biol. 2004, 10, 1642–1647, doi:10.1111/j.1365-2486.2004.00839.x.
[11]
Carpenter, K.E.; Abrar, M.; Aeby, G.; Aronson, R.B.; Banks, S.; Bruckner, A.; Chiriboga, A.; Cortés, J.; Delbeek, J.C.; DeVantier, L.; et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 2008, 321, 560–563, doi:10.1126/science.1159196. 18653892
[12]
Glynn, P.W. In tandem reef coral and cryptic metazoan declines and extinctions. Bull. Mar. Sci. 2011, 87, 1–28, doi:10.5343/bms.2010.1004.
[13]
Wilson, E.O. The Diversity of Life; W. W. Norton and Company: New York, NY, USA, 1992.
[14]
Carlton, J.T.; Geller, J.B.; Reaka-Kudla, M.L.; Norse, E.A. Historical extinctions in the sea. Ann. Rev. Ecol. Syst. 1999, 30, 515–538, doi:10.1146/annurev.ecolsys.30.1.515.
[15]
Baker, A.C.; Glynn, P.W.; Riegl, B. Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast Shelf Sci. 2008, 80, 435–471, doi:10.1016/j.ecss.2008.09.003.
[16]
Wilkinson, C. Status of Coral Reefs of the World: 2000; Australian Institute of Marine Science: Townsville, Australia, 2000.
[17]
Maynard, J.A.; Baird, A.H.; Pratchett, M.S. Revisiting the Cassandra syndrome; the changing climate of coral reef research. Coral Reefs 2008, 27, 745–749, doi:10.1007/s00338-008-0432-1.
[18]
Enochs, I.C.; Toth, L.T.; Brandtneris, V.W.; Afflerbach, J.C.; Manzello, D.P. Environmental determinants of motile cryptofauna on an eastern Pacific coral reef. Mar. Ecol. Prog. Ser. 2011, 438, 105–118, doi:10.3354/meps09259.
[19]
Ginsburg, R.N. Geological and biological roles of cavities in coral reefs. In Perspectives on Coral Reefs; Barnes, D.J., Ed.; Australian Institute of Marine Science: Townsville, Australia, 1983; pp. 148–153.
[20]
Richter, C.; Wunsch, M.; Rasheed, M.; K?tter, I.; Badran, M.I. Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 2001, 413, 726–730, doi:10.1038/35099547. 11607030
[21]
Caley, M.J.; Buckley, K.A.; Jones, G.P. Separating ecological effects of habitat fragmentation, degradation, and loss on coral commensals. Ecology 2001, 82, 3435–3448.
[22]
Enochs, I.C.; Hockensmith, G. Effects of coral mortality on the community composition of cryptic metazoans associated with Pocillopora damicornis. In Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, FL, USA, 7–11 July 2008; pp. 1368–1372.
[23]
Coker, D.J.; Pratchett, M.S.; Munday, P.L. Coral bleaching and habitat degradation increase susceptibility to predation for coral-dwelling fishes. Behav. Ecol. 2009, 20, 1204–1210, doi:10.1093/beheco/arp113.
[24]
Enochs, I.C.; Manzello, D.P. Species richness of motile coral reef cryptofauna across a gradient of framework erosion in Pacific Panamá. Coral Reefs 2012. in press.
[25]
Enochs, I.C. Motile cryptofauna associated with live and dead coral substrates: Implications for coral mortality and framework erosion. Mar. Biol. 2012. in press.
[26]
Lang, J.C.; Chornesky, E.A. Competition between scleractinian reef corals: A review of mechanisms and effects. In Ecosystems of the World: Coral Reefs; Dubinsky, Z., Ed.; Elsevier Press: Amsterdam, The Netherlands, 1990; pp. 209–252.
[27]
Moran, D.P.; Reaka, M.L. Bioerosion and availability of shelter for benthic reef organisms. Mar. Ecol. Prog. Ser. 1988, 44, 249–263, doi:10.3354/meps044249.
[28]
Jackson, J.B.C. Distribution and ecology of clonal and aclonal benthic invertebrates. In Population Biology and Evolution of Clonal Organisms; Jackson, J.B.C., Buss, L.W., Cook, R.E., Eds.; Yale University Press: New Haven, CT, USA, 1985; pp. 297–355.
[29]
Bailey-Brock, J.; Brock, R.; Kam, A.; Fukunaga, A.; Akiyama, H. Anthropogenic disturbances on shallow cryptofaunal communities in a marine life conservation district on Oahu, Hawai’i. Int. Rev. Hydrobiol. 2007, 92, 291–300, doi:10.1002/iroh.200610958.
[30]
Patton, W.K. Community structure among the animals inhabiting the coral Pocillopora damicornis at Heron Island, Australia. In Symbiosis in the Sea; Vernberg, W., Ed.; University of South Carolina Press: Columbia, SC, USA, 1974; pp. 219–243.
[31]
Stimson, J. Stimulation of fat-body production in the polyps of the coral Pocillopora damicornis by the presence of mutualistic crabs of the genus Trapezia. Mar. Biol. 1990, 106, 211–218, doi:10.1007/BF01314802.
[32]
Rotjan, R.D.; Lewis, S.M. Impact of coral predators on tropical reefs. Mar. Ecol. Prog. Ser. 2008, 367, 73–91, doi:10.3354/meps07531.
[33]
Alvarez-Filip, L.; Dulvy, N.K.; Gill, J.A.; C?té, I.M.; Watkinson, A.R. Flattening of Caribbean coral reefs: Region-wide declines in architectural complexity. Proc. Roy. Soc. Lond. B 2009, 276, 3019–3025, doi:10.1098/rspb.2009.0339.
[34]
Manzello, D.P. Reef development and resilience to acute (El Ni?o Warming) and chronic (high-CO2) disturbances in the eastern tropical Pacific: A real-world climate change model. In Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, FL, USA, 7–11 July 2008; pp. 1299–1304.
[35]
Reaka-Kudla, M.L.; Feingold, J.S.; Glynn, P.W. Experimental studies of rapid bioerosion of coral reefs in the Galápagos Islands. Coral Reefs 1996, 15, 101–107.
[36]
Wilson, S.K.; Dolman, A.M.; Cheal, A.J.; Emslie, M.J.; Pratchett, M.S.; Sweatman, H.P.A. Maintenance of fish diversity on disturbed coral reefs. Coral Reefs 2009, 28, 3–14, doi:10.1007/s00338-008-0431-2.
[37]
Graham, N.A.J.; Wilson, S.K.; Jennings, S.; Polunin, N.V.C.; Robinson, J.; Bijoux, J.P.; Daw, T.M. Lag effects in the impacts of mass coral bleaching on coral reef fish, fisheries, and ecosystems. Conserv. Biol. 2007, 21, 1291–1300, doi:10.1111/j.1523-1739.2007.00754.x.
[38]
Graham, N.A.J.; Wilson, S.K.; Pratchett, M.S.; Polunin, N.V.C.; Spalding, M.D. Coral mortality versus structural collapse as drivers of corallivorous butterflyfish decline. Biodiver. Conserv. 2009, 18, 3325–3336, doi:10.1007/s10531-009-9633-3.
[39]
Peyrot-Clausade, M. Motile cryptofauna of Tuléar reef flats. Mar. Biol. 1980, 59, 43–47, doi:10.1007/BF00396981.
[40]
Veron, J.E.N. Corals of the World; Australian Institute of Marine Science: Townsville, Australia, 2000.
[41]
Coles, S.L. Species diversity of decapods associated with living and dead reef coral Pocillopora meandrina. Mar. Ecol. Prog. Ser. 1980, 2, 281–291, doi:10.3354/meps002281.
[42]
Shirayama, Y.; Horikoshi, M. A new method of classifying the growth form of corals and its application to a field survey of coral-associated animals in Kabira Cove, Ishigaki Island. J. Oceanogr. Soc. Jpn. 1982, 28, 193–207, doi:10.1007/BF02111102.
[43]
Kirsteuer, E. Quantitative and qualitative aspects of the Nemertean Fauna in tropical coral reefs. In Proceedings of the 1st International Symposium Coral Reefs, Mandapam Camp, India, 12–16 January 1969; pp. 363–371.
[44]
Preston, N.P.; Doherty, P.J. Cross-shelf patterns in the community structure of coral-dwelling Crustacea in the central region of the Great Barrier Reef. I. Agile shrimps. Mar. Ecol. Prog. Ser. 1990, 66, 47–61, doi:10.3354/meps066047.
Grigg, R.W.; Maragos, J.E. Recolonization of hermatypic corals on submerged lava flows in Hawaii. Ecology 1974, 55, 387–395, doi:10.2307/1935226.
[47]
Siitonen, J. Forest management, coarse woody debris and saproxylic organisms: Fennoscandian boreal forests as an example. Ecol. Bull. 2001, 49, 11–41.
[48]
Schiegg, K. Saproxylic insect diversity of beech: Limbs are richer than trunks. For. Ecol. Manag. 2001, 149, 295–304, doi:10.1016/S0378-1127(00)00563-6.
[49]
Nordén, B.; Ryberg, M.; G?tberg, F.; Olausson, B. Relative importance of coarse and fine woody debris for the diversity of wood-inhabiting fungi in temperate broadleaf forests. Biol. Cons. 2004, 117, 1–10, doi:10.1016/S0006-3207(03)00235-0.
[50]
Nilsson, S.G.; Hedin, J.; Niklasson, M. Biodiversity and its assessment in boreal and nemoral forests. Scand. J. For. Res.Suppl. 2001, 3, 10–26.
Peyrot-Clausade, M.; Hutchings, P.; Richard, G. Temporal variations of macroborers in massive Porites lobata on Moorea, French Polynesia. Coral Reefs 1992, 11, 161–166, doi:10.1007/BF00255471.