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Coral Reefs

, Volume 31, Issue 3, pp 653–661 | Cite as

Species richness of motile cryptofauna across a gradient of reef framework erosion

  • I. C. EnochsEmail author
  • D. P. Manzello
Report

Abstract

Coral reef ecosystems contain exceptionally high concentrations of marine biodiversity, potentially encompassing millions of species. Similar to tropical rainforests and their insects, the majority of reef animal species are small and cryptic, living in the cracks and crevices of structural taxa (trees and corals). Although the cryptofauna make up the majority of a reef’s metazoan biodiversity, we know little about their basic ecology. We sampled motile cryptofaunal communities from both live corals and dead carbonate reef framework across a gradient of increasing erosion on a reef in Pacific Panamá. A total of 289 Operational Taxonomic Units (OTUs) from six phyla were identified. We used species-accumulation models fitted to individual- and sample-based rarefaction curves, as well as seven nonparametric richness estimators to estimate species richness among the different framework types. All procedures predicted the same trends in species richness across the differing framework types. Estimated species richness was higher in dead framework (261–370 OTUs) than in live coral substrates (112–219 OTUs). Surprisingly, richness increased as framework structure was eroded: coral rubble contained the greatest number of species (227–320 OTUs) and the lowest estimated richness of 47–115 OTUs was found in the zone where the reef framework had the greatest vertical relief. This contradicts the paradigm that abundant live coral indicates the apex of reef diversity.

Keywords

Reef framework structure Biodiversity Rarefaction Rubble Eastern tropical Pacific 

Notes

Acknowledgments

We gratefully acknowledge the knowledge and advice of P. Glynn, the field support of V. Brandtneris and L. Toth, the identifications of A. Anker, A. Baeza, R. Brusca, Y. Camacho Garcia, G. Coan, J. Garcia-Gomez, G. Hendler, R. Lemaitre, H. Lessios, J. Llopiz, G. Paulay, L. Harris, A. Schulze, E. Schwabe, J. Thomas, and P. Valentich-Scott, as well as the laboratory assistance of J. Afflerbach, I. Chambers, A. Goodson, A. Gracie, D. Graham, A. Jung, J. Kelly, N. Kraft, L. O’Neill, A. Mallozzi, A. Pflaumer, and S. Thompson. A. Bakun, P. Glynn, C. Langdon, D. Lirman, and B. Riegl provided manuscript advice. Financial support for this project was provided by the American Museum of Natural History Lerner-Gray Fund and a National Science Foundation grant to Peter W. Glynn, #OCE-0526361. Collection of specimens was approved by the Autoridad Nacional del Ambiente (ANAM). Two anonymous reviewers and topic editor H. Sweatman greatly improved the manuscript. M. Reaka deserves special acknowledgement for helping us understand the myriad of factors responsible for our findings.

Supplementary material

338_2012_886_MOESM1_ESM.eps (2.7 mb)
Supplementary material 1 (EPS 2770 kb)
338_2012_886_MOESM2_ESM.doc (20 kb)
Supplementary material 2 (DOC 22 kb)

References

  1. Abele L, Patton WK (1976) The size of coral heads and the community biology of associated decapod crustaceans. J Biogeogr 3:35–47CrossRefGoogle Scholar
  2. Bailey-Brock JH, Brock RE, Kam A, Fukunaga A, Akiyama A (2007) Anthropogenic disturbance on shallow cryptofaunal communities in a marine life conservation district on Oahu, Hawai’i. Int Rev Hydrobiol 92:291–300CrossRefGoogle Scholar
  3. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  4. Bakus GJ (1966) Some relationships of fishes to benthic organisms on coral reefs. Nature 210:280–284CrossRefGoogle Scholar
  5. Beyer HL (2004) Hawth’s Analysis Tools for ArcGIS. Available at http://www.spatialecology.com/htools
  6. Brander KM, McLeod AAQR, Humphreys WF (1971) Comparison of species diversity and ecology of reef-living invertebrates on Aldabra atoll and at Watamu, Kenya. Symp Zool Soc Lond 28:391–431Google Scholar
  7. Bruce AJ (1976) Shrimps and prawns of coral reefs, with special reference to commensalism. In: Jones OA, Endean R (eds) Biology and geology of coral reefs. Academic Press, New York, pp 37–94Google Scholar
  8. Caley MJ, Buckley KA, Jones G (2001) Separating ecological effects of habitat fragmentation, degradation, and loss on coral commensals. Ecology 82:3435–3448CrossRefGoogle Scholar
  9. Choi DR, Ginsburg RN (1983) Distribution of coelobites (cavity-dwellers) in coral rubble across the Florida Reef Tract. Coral Reefs 2:165–172CrossRefGoogle Scholar
  10. Coles SL (1980) Species diversity of decapods associated with living and dead reef coral Pocillopora meandrina. Mar Ecol Prog Ser 2:281–291CrossRefGoogle Scholar
  11. Colwell RK (2009) EstimateS: Statistical estimation of species richness and shared species from samples. Version 8.2. http://purl.oclc.org/estimates
  12. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310PubMedCrossRefGoogle Scholar
  13. Depczynski M, Bellwood DR (2003) The role of cryptobenthic reef fishes in coral reef trophodynamics. Mar Ecol Prog Ser 256:183–191CrossRefGoogle Scholar
  14. Enochs IC, Hockensmith G (2009) Effects of coral mortality on the community composition of cryptic metazoans associated with Pocillopora damicornis. Proc 11th Int Coral Reef Symp 26:1368–1372Google Scholar
  15. Enochs IC, Toth LT, Brandtneris VW, Afflerbach JC, Manello DP (2011) Environmental determinants of motile cryptofauna on an eastern Pacific coral reef. Mar Ecol Prog Ser 438:105–118CrossRefGoogle Scholar
  16. Glynn PW (1973) Acanthaster: Effect on coral reef growth in Panamá. Science 180:504–506PubMedCrossRefGoogle Scholar
  17. Glynn PW (1980) Defense by symbiotic Crustacea of host corals elicited by chemical cues from predator. Oecologia 47:287–290CrossRefGoogle Scholar
  18. Glynn PW (1983) Increased survivorship in corals harboring crustacean symbionts. Mar Biol Lett 4:105–111Google Scholar
  19. Glynn PW (1990) Coral mortality and disturbance to coral reefs in the eastern tropical Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Nino-Southern Oscillation. Elsevier, Amsterdam, pp 55–126CrossRefGoogle Scholar
  20. Glynn PW (1997) Bioerosion and coral reef growth: a dynamic balance. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 68–98CrossRefGoogle Scholar
  21. Glynn PW (2006) Fish utilization of simulated coral reef frameworks versus eroded rubble substrates off Panama, eastern Pacific. Proc 10th Int Coral Reef Symp 1:250–256Google Scholar
  22. Glynn PW, Maté JM (1997) Field guide to the Pacific coral reefs of Panamá. Proc 8th Int Coral Reef Symp 1:145–166Google Scholar
  23. Glynn PW, Maté JM, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panamá and Ecuador during the 1997–1998 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982-1983 event. Bull Mar Sci 69:79–109Google Scholar
  24. Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347CrossRefGoogle Scholar
  25. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162PubMedCrossRefGoogle Scholar
  26. Holdridge LR, Grenke WC, Hatheway WH, Liang T, Tosi JA (1971) Forest environments in tropical life zones. Pergamon Press, OxfordGoogle Scholar
  27. Hutchings PA (1981) Polychaete recruitment onto dead coral substrates at Lizard Island, Great Barrier Reef, Australia. Bull Mar Sci 31:410–423Google Scholar
  28. Idjadi JA, Edmunds PJ (2006) Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar Ecol Prog Ser 319:117–127CrossRefGoogle Scholar
  29. Jackson JBC, Winston JE (1982) Ecology of cryptic coral reef communities. I. Distribution and abundance of major groups of encrusting organisms. J Exp Mar Biol Ecol 57:135–147CrossRefGoogle Scholar
  30. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638PubMedCrossRefGoogle Scholar
  31. Kirsteuer E (1969) Quantitative and qualitative aspects of the nemertean fauna in tropical coral reefs. Proc 1st Int Symp Coral Reefs 1:363-371Google Scholar
  32. Klumpp DW, McKinnon AD, Mundy CN (1988) Motile cryptofauna of a coral reef: abundance, distribution and trophic potential. Mar Ecol Prog Ser 45:95–108CrossRefGoogle Scholar
  33. Knudsen JW (1967) Trapezia and Tetralia (Decapoda, Brachyura, Xanthidae) as obligate ectoparasites of pocilloporid and acroporid corals. Pac Sci 21:51–57Google Scholar
  34. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comp Geosci 32:1259–1269CrossRefGoogle Scholar
  35. Kohn AJ (1983) Microhabitat factors affecting abundance and diversity of Conus on coral reefs. Oecologia 60:293–301CrossRefGoogle Scholar
  36. Kohn AJ, Leviten PJ (1976) Effect of habitat complexity on population density and species richness in tropical intertidal predatory gastropod assemblages. Oecologia 25:119–210CrossRefGoogle Scholar
  37. Lang JC, Chornesky EA (1990) Competition between scleractinian reef corals: a review of mechanisms and effects. In: Dubinsky Z (ed) Coral reefs, Ecosystems of the world, vol 25. Elsevier, Amsterdam, pp 209–252Google Scholar
  38. Lewis JB, Snelgrove PVR (1990) Corallum morphology and composition of crustracean cryptofauna of the hermatypic coral Madracis mirabilis. Mar Biol 106:267–272CrossRefGoogle Scholar
  39. Manzello DP, Kleypas JA, Budd DA, Eakin CM, Glynn PW, Langdon C (2008) Poorly cemented coral reefs of the eastern tropical Pacific: possible insights into reef development in a high-CO2 world. Proc Natl Acad Sci USA 105:10450–10455PubMedCrossRefGoogle Scholar
  40. McClanahan TR (1990) Kenyan coral reef-associated gastropod assemblages: distribution and diversity patterns. Coral Reefs 9:63–74CrossRefGoogle Scholar
  41. McCloskey LR (1970) The dynamics of the community associated with a marine scleractinian coral. Int Rev Gesamten Hydrobiol Hydrogr 55:13–81CrossRefGoogle Scholar
  42. Monod J (1950) La technique de culture continue, théorie et applications. Ann Inst Pasteur 79:390–410Google Scholar
  43. Moran DP, Reaka ML (1988) Bioerosion and availability of shelter for benthic reef organisms. Mar Ecol Prog Ser 44:249–263CrossRefGoogle Scholar
  44. Moran DP, Reaka ML (1991) Effects of disturbance: disruption and enhancement of coral reef cryptofaunal populations by hurricanes. Coral Reefs 9:215–224CrossRefGoogle Scholar
  45. Palumbi SR, Jackson JBC (1982) Ecology of cryptic coral reef communities. II. Recovery from small disturbance events by encrusting bryozoa: the influence of “host” species and lesion size. J Exp Mar Biol Ecol 64:103–115CrossRefGoogle Scholar
  46. Patton WK (1974) Community structure among the animals inhabiting the coral Pocillopora damicornis at Heron Island, Australia. In: Vernberg W (ed) Symbiosis in the sea. Univ South Carolina Press, Columbia, pp 219–243Google Scholar
  47. Patton WK (1994) Distribution and ecology of animals associated with branching corals (Acropora spp.) from the Great Barrier Reef, Australia. Bull Mar Sci 55:193–211Google Scholar
  48. Peyrot-Clausade M (1974) Ecological study of coral reef cryptobiotic communities: an analysis of the polychaete cryptofauna. Proc 2nd Int Coral Reef Symp 1:269–284Google Scholar
  49. Peyrot-Clausade M (1977) Settlement of an artificial biota by coral reef cryptofauna.. Proc 3rd Int Coral Reef Symp 1:101–103Google Scholar
  50. Peyrot-Clausade M (1980) Motile cryptofauna of Tuléar reef flats. Mar Biol 59:43–47CrossRefGoogle Scholar
  51. Peyrot-Clausade M (1981) Motile cryptofauna of Tuléar Great Reef outer slope: Brachyura and Anomura distributions. Proc 4th Int Coral Reef Symp 2:745–754Google Scholar
  52. Preston NP, Doherty PJ (1994) Cross-shelf patterns in the community structure of coral-dwelling Crustacea in the central region of the Great Barrier Reef. II. Cryptofauna. Mar Ecol Prog Ser 104:27–38CrossRefGoogle Scholar
  53. Ratkowsky DA (1983) Nonlinear regression modeling: a unified practical approach. Marcel Dekker, New YorkGoogle Scholar
  54. Ratkowsky DA (1990) Handbook of nonlinear regression models. Marcel Dekker, New YorkGoogle Scholar
  55. Reaka ML (1985) Interactions between fishes and motile benthic invertebrates on reefs: the significance of motility vs. defensive adaptations. Proc 5th Int Coral Reef Congr, Tahiti 5:439–444Google Scholar
  56. Reaka-Kudla ML (1997) The global biodiversity of coral reefs. In: Reaka-Kudla ML, Wilson DE, Wilson EO (eds) Biodiversity II: Understanding and protecting our biological resources. Joseph Henry Press, Washington DC, pp 83–108Google Scholar
  57. Richter C, Wunsch M, Rasheed M, Kötter I, Badran MI (2001) Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature 413:726–730PubMedCrossRefGoogle Scholar
  58. 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 295:1280–1284PubMedCrossRefGoogle Scholar
  59. Rotjan RD, Lewis SM (2008) Impact of coral predators on tropical reefs. Mar Ecol Prog Ser 367:73–91CrossRefGoogle Scholar
  60. Scheffers SR, Nieuwland G, Bak RPM, van Duyl FC (2004) Removal of bacteria and nutrient dynamics within the coral reef framework of Curaçao (Netherlands Antilles). Coral Reefs 23:413–422CrossRefGoogle Scholar
  61. Takada Y, Abe O, Shibuno T (2007) Colonization patterns of mobile cryptic animals into interstices of coral rubble. Mar Ecol Prog Ser 343:35–44CrossRefGoogle Scholar
  62. Takada Y, Abe O, Shibuno T (2008) Cryptic assemblages in coral-rubble interstices along a terrestrial-sediment gradient. Coral Reefs 27:665–675CrossRefGoogle Scholar
  63. Tews J, Brose U, Grimm V, Tielborger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92CrossRefGoogle Scholar
  64. Tjørve E (2003) Shapes and functions of species-area curves: a review of possible models. J Biogeogr 30:827–835CrossRefGoogle Scholar
  65. Valles H, Kramer DL, Hunte W (2006) A standard unit for monitoring recruitment of fishes to coral reef rubble. J Exp Mar Biol Ecol 336:171–183CrossRefGoogle Scholar
  66. van Duyl FC, Scheffers SR, Thomas FIM, Driscoll M (2006) The effect of water exchange on bacterioplankton depletion and inorganic nutrient dynamics in coral reef cavities. Coral Reefs 25:23–36CrossRefGoogle Scholar
  67. Vivien ML (1973) Contribution a la connaissance de l’éthologie alimentaire de l’ichtyofaune du platier interne des récifs coralliens de Tuléar (Madagascar). Tethys Suppl 5:221–308Google Scholar
  68. Vytopil E, Willis BL (2001) Epifaunal community structure in Acropora spp. (Scleractinia) on the Great Barrier Reef: implications of coral morphology and habitat complexity. Coral Reefs 20:281–288CrossRefGoogle Scholar
  69. Weibull W (1951) A statistical distribution function of wide applicability. J Appl Math 18:293–296Google Scholar
  70. Wulff JL, Buss LW (1979) Do sponges help hold coral reefs together? Nature 281:474–475CrossRefGoogle Scholar
  71. Zimmerman TL, Martin JW (2004) Artificial reef matrix structures (ARMS): an inexpensive and effective method for collecting coral reef-associated invertebrates. Gulf Caribb Res 16:59–64Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  2. 2.Atlantic Oceanographic and Meteorological Laboratories (AOML)National Oceanographic and Atmospheric Administration (NOAA)MiamiUSA

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