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Coral Reefs

, Volume 37, Issue 3, pp 827–840 | Cite as

Variation in coral-associated cryptofaunal communities across spatial scales and environmental gradients

  • Chelsie W. W. Counsell
  • Megan J. Donahue
  • Kyle F. Edwards
  • Erik C. Franklin
  • Mark A. Hixon
Report

Abstract

Most of the diversity on coral reefs is in the cryptofauna, the hidden organisms that inhabit the interstitial spaces of corals and other habitat-forming benthos. However, little is known about the patterns and drivers of diversity in cryptofauna. We investigated how the cryptofaunal community associated with the branching coral Pocillopora meandrina varies across spatial scales and environmental gradients. We performed nondestructive visual surveys of the cryptofaunal community on 751 P. meandrina colonies around the island of O‘ahu (30–73 colonies per site, 3–6 sites per region, five regions). We identified 91 species, including 48 fishes and 43 invertebrates. Most of these species were observed rarely, with only 19 species occurring on greater than 5% of surveyed colonies. Variation in community abundance and species richness was greatest at the scale of the coral colony and lowest at the site scale. Abundance and species richness increased with increasing colony size and maximum wave height, and decreased with increasing surface chlorophyll-a. In an analysis of species-specific responses, colony size, wave height, and chlorophyll-a were significant drivers of occurrence. Depth and percent live coral tissue were also identified as important correlates for community composition with distinct responses across taxa. Analyzing species-specific responses to environmental gradients documented a unique pattern for the guard crab Trapezia intermedia, which had a higher probability of occurring on smaller colonies (in contrast to 18 other common taxa). The results of a principal coordinates analysis on community composition and a co-occurrence analysis further supported T. intermedia as having a unique distribution across colonies, even in comparison with four other Trapezia species. Overall, these patterns emphasize the importance of host coral characteristics (i.e., colony size and percent live tissue) and physical characteristics of the surrounding habitat (i.e., wave energy, chlorophyll-a, and depth) in structuring cryptofaunal communities and characterize species-specific responses to environmental gradients.

Keywords

Community ecology Cryptofauna Hawaiian Islands Pocillopora meandrina Environmental gradients Spatial scales 

Notes

Acknowledgements

C Counsell, M Donahue, E Franklin, and M Hixon developed the design for this study. M Donahue, the Hawai‘i Institute of Marine Biology, and the UH Department of Biology provided equipment for field surveys. J Jones and J Kuwabara supported this project with boat and dive safety support. Dive assistants included J Caldwell, IR Caldwell, R Coleman, C Couch, M Donahue, E Franklin, N Gutlay, M Hixon, C Jerolmon, K Lubarsky, A Moran, E Nalley, M Ross, N Silbiger, T Wester, and J Zill. C Counsell organized and conducted the surveys, managed the database, and with M Donahue’s guidance analyzed the data and wrote the manuscript. K Edwards assisted in developing and interpreting the species-specific community analysis. All authors reviewed the manuscript. C Counsell’s participation in this study was supported by a National Science Foundation Graduate Research Fellowship (Grant No. 2012103208). Additional funding support was provided by M Donahue and the Castle Foundation (Grant 3846, M Hixon PI). This is HIMB contribution no. 1731 and SOEST contribution no. 10409.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

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Supplementary material 1 (PDF 5 kb)
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Supplementary material 2 (PDF 33 kb)
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Supplementary material 3 (PDF 96 kb)
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Supplementary material 5 (PDF 17 kb)
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Supplementary material 6 (DOCX 70 kb)

References

  1. Abele LG (1976) Comparative species richness in fluctuating and constant environments: coral-associated decapod crustaceans. Science 192:461–463CrossRefPubMedGoogle Scholar
  2. Abele LG, Patton WK (1976) The size of coral heads and the community biology of associated decapod crustaceans. J Biogeogr 3:35–47CrossRefGoogle Scholar
  3. Anderson DR (2008) Model based inference in the life sciences: A primer on evidence. Fort Collins, Springer ScienceCrossRefGoogle Scholar
  4. Almany GR (2003) Priority effects in coral reef fish communities. Ecology 84:1920–1935CrossRefGoogle Scholar
  5. Arrhenius O (1921) Species and area. J Ecol 9:95–99CrossRefGoogle Scholar
  6. Austin AD, Austin SA, Sale PF (1980) Community structure of the fauna associated with the coral Pocillopora damicornis (L.) on the Great Barrier Reef. Aust J Mar Freshw Res 31:163–174CrossRefGoogle Scholar
  7. Barry CK (1965) Ecological study of the decapod crustaceans commensal with the branching coral Pocillopora meandrina var. Nobilis Verrill. MS thesis, Univ HawaiiGoogle Scholar
  8. Bartoń K (2016) MuMIn: Multi-model inference. R Packag version 1156Google Scholar
  9. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  10. Black R, Prince J (1983) Fauna associated with the coral Pocillopora damicornis at the southern limit of its distribution in Western Australia. J Biogeogr 10:135–152CrossRefGoogle Scholar
  11. Britayev TA, Spiridonov VA, Deart YV, El-Sherbiny M (2017) Biodiversity of the community associated with Pocillopora verrucosa (Scleractinia: Pocilloporidae) in the Red Sea. Mar Biodivers 47:1093–1109CrossRefGoogle Scholar
  12. Chase JM, Leibold MA (2002) Spatial scale dictates the productivity-biodiversity relationship. Nature 416:427–430CrossRefPubMedGoogle Scholar
  13. Chase TJ, Pratchett MS, Walker SPW, Hoogenboom MO (2014) Small-scale environmental variation influences whether coral-dwelling fish promote or impede coral growth. Oecologia 176:1009–1022CrossRefPubMedGoogle Scholar
  14. Coles SL (1980) Species diversity of decapods associated with living and dead reef coral Pocillopora meandrina. Mar Ecol Prog Ser 2:281–291CrossRefGoogle Scholar
  15. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310CrossRefPubMedGoogle Scholar
  16. Cornell HV, Karlson RH (2000) Coral species richness: ecological versus biogeographical influences. Coral Reefs 19:37–49CrossRefGoogle Scholar
  17. Darling ES, Graham NAJ, Januchowski-Hartley FA, Nash KL, Pratchett MS, Wilson SK (2017) Relationships between structural complexity, coral traits, and reef fish assemblages. Coral Reefs 36:1–15CrossRefGoogle Scholar
  18. Depczynski M, Bellwood D (2005) Wave energy and spatial variability in community structure of small cryptic coral reef fishes. Mar Ecol Prog Ser 303:283–293CrossRefGoogle Scholar
  19. Dollar SJ (1982) Wave stress and coral community structure in Hawaii. Coral Reefs 1:71–81CrossRefGoogle Scholar
  20. Enochs IC (2012) Motile cryptofauna associated with live and dead coral substrates: Implications for coral mortality and framework erosion. Mar Biol 159:709–722CrossRefGoogle Scholar
  21. Enochs IC, Hockensmith G (2008) 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
  22. Enochs IC, Manzello DP (2012) Responses of cryptofaunal species richness and trophic potential to coral reef habitat degradation. Diversity 4:94–104CrossRefGoogle Scholar
  23. Fletcher CH, Bochicchio C, Conger CL, Engels MS, Feirstein EJ, Frazer N, Glenn CR, Grigg RW, Grossman EE, Harney JN, Isoun E, Murray-Wallace CV, Rooney JJ, Rubin KH, Sherman CE, Vitousek S (2008) Geology of Hawaii reefs. In: Riegl B, Dodge R (eds) Coral reefs of the USA. Springer, New York, NY, pp 435–487CrossRefGoogle Scholar
  24. Franklin EC, Jokiel PL, Donahue MJ (2013) Predictive modeling of coral distribution and abundance in the Hawaiian Islands. Mar Ecol Prog Ser 481:121–132CrossRefGoogle Scholar
  25. Gochfeld DJ (2009) Territorial damselfishes facilitate survival of corals by providing an associational defense against predators. Mar Ecol Prog Ser 398:137–148CrossRefGoogle Scholar
  26. Goldshmid R, Holzman R, Weihs D, Genin A (2004) Aeration of corals by sleep-swimming fish. Limnol Oceanogr 49:1832–1839CrossRefGoogle Scholar
  27. Gotelli NJ, Abele LG (1983) Community patterns of coral-associated decapods. Mar Ecol Prog Ser 13:131–139CrossRefGoogle Scholar
  28. Gove JM, Williams GJ, McManus MA, Clark SJ, Ehses JS, Wedding LM (2015) Coral reef benthic regimes exhibit non-linear threshold responses to natural physical drivers. Mar Ecol Prog Ser 522:33–48CrossRefGoogle Scholar
  29. Gratwicke B, Speight MR (2005) The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J Fish Biol 66:650–667CrossRefGoogle Scholar
  30. Griffith DM, Veech JA, Marsh CJ (2016) cooccur: Probabilistic species co-occurrence analysis in R. J Stat Softw 69:1–17CrossRefGoogle Scholar
  31. Head CEI, Bonsall MB, Koldewey H, Pratchett MS, Speight M, Rogers AD (2015) High prevalence of obligate coral-dwelling decapods on dead corals in the Chagos Archipelago, central Indian Ocean. Coral Reefs 34:905–915CrossRefGoogle Scholar
  32. Holbrook SJ, Brooks AJ, Schmitt RJ, Stewart HL (2008) Effects of sheltering fish on growth of their host corals. Mar Biol 155:521–530CrossRefGoogle Scholar
  33. Holbrook SJ, Schmitt RJ, Brooks AJ (2011) Indirect effects of species interactions on habitat provisioning. Oecologia 166:739–749CrossRefPubMedPubMedCentralGoogle Scholar
  34. Huber ME, Coles SL (1986) Resource utilization and competition among the five Hawaiian species of Trapezia Crustacea, Brachyura. Mar Ecol Prog Ser 1:21–31CrossRefGoogle Scholar
  35. Jankowski MW, Gardiner NR, Jones GP (2015) Depth and reef profile: Effects on the distribution and abundance of coral reef fishes. Environ Biol Fishes 98:1373–1386CrossRefGoogle Scholar
  36. Jokiel PL (1991) Jokiel’s Illustrated Scientific Guide To Kane’Ohe Bay, OahuGoogle Scholar
  37. Kane CN, Brooks AJ, Holbrook SJ, Schmitt RJ (2009) The role of microhabitat preference and social organization in determining the spatial distribution of a coral reef fish. Environ Biol Fishes 84:1–10CrossRefGoogle Scholar
  38. 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
  39. Leray M, Béraud M, Anker A, Chancerelle Y, Mills SC (2012) Acanthaster planci outbreak: Decline in coral health, coral size structure modification and consequences for obligate decapod assemblages. PLoS One 7:1–10CrossRefGoogle Scholar
  40. Leray M, Meyer CP, Mills SC (2015) Metabarcoding dietary analysis of coral dwelling predatory fish demonstrates the minor contribution of coral mutualists to their highly partitioned, generalist diet. PeerJ 3:e1047CrossRefPubMedPubMedCentralGoogle Scholar
  41. López-Pérez A, Granja-Fernández R, Benítez-Villalobos F, Jiménez-Antonio O (2017) Pocillopora damicornis-associated echinoderm fauna: Richness and community structure across the southern Mexican Pacific. Mar Biodivers 47:481–490CrossRefGoogle Scholar
  42. McKeon CS, Moore JM (2014) Species and size diversity in protective services offered by coral guard-crabs. PeerJ 2:e574CrossRefPubMedPubMedCentralGoogle Scholar
  43. McKeon CS, Stier AC, McIlroy SE, Bolker BM (2012) Multiple defender effects: Synergistic coral defense by mutualist crustaceans. Oecologia 169:1095–1103CrossRefPubMedGoogle Scholar
  44. Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB, Willig MR, Dodson SI, Gough L (2001) What is the observed relationship between species richness and productivity? Ecology 82:2381–2396CrossRefGoogle Scholar
  45. de Nunes JACC, Sampaio CLS, Barros F (2013) How wave exposure, group size and habitat complexity influence foraging and population densities in fishes of the genus Halichoeres (Perciformes: Labridae) on tropical rocky shores. Mar Biol 160:2383–2394CrossRefGoogle Scholar
  46. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R Packag version 24-2Google Scholar
  47. Plaisance L, Caley MJ, Brainard RE, Knowlton N (2011) The diversity of coral reefs: What are we missing? PLoS One 6:1–7CrossRefGoogle Scholar
  48. Plaisance L, Knowlton AN, Paulay AG, Meyer AC (2009) Reef-associated crustacean fauna: biodiversity estimates using semi-quantitative sampling and DNA barcoding. Coral Reefs 28:977–986CrossRefGoogle Scholar
  49. Pratchett MS (2001) Influence of coral symbionts on feeding preferences of crown-of-thorns starfish Acanthaster planci in the western pacific. Mar Ecol Prog Ser 214:111–119CrossRefGoogle Scholar
  50. Preston EM (1971) Niche overlap and competition among five sympatric congeneric species of xanthid crabs. PhD thesis, Univ HawaiiGoogle Scholar
  51. Preston NP, Doherty PJ (1990) 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 66:47–61CrossRefGoogle Scholar
  52. Randall JE (1967) Food habits of reef fishes of the West Indies. Stud Trop Ocean 5:665–847Google Scholar
  53. Rasher DB, Hoey AS, Hay ME (2013) Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology 94:1347–1358CrossRefPubMedPubMedCentralGoogle Scholar
  54. Reaka-Kudla ML (1997) The global biodiversity of coral reefs: a comparison with rainforests. In: Reaka-Kudla ML, Wilson DE, Wilson EO (eds) Biodiversity II: Understanding and protecting our natural resources. National Academy Press, Washington, DC, pp 83–108Google Scholar
  55. Rouzé H, Lecellier G, Mills SC, Planes S, Berteaux-Lecellier V, Stewart H (2014) Juvenile Trapezia spp. crabs can increase juvenile host coral survival by protection from predation. Mar Ecol Prog Ser 515:151–159CrossRefGoogle Scholar
  56. Schmitt RJ, Holbrook SJ, Brooks AJ, Lape JCP, Schmitt J, Brooks J, Lape P (2009) Intraguild predation in a structured habitat: distinguishing multiple-predator effects from competitor effects. Ecology 90:2434–2443CrossRefPubMedGoogle Scholar
  57. Sgarbi L, Melo A (2017) You don’t belong here: explaining the excess of rare species in terms of habitat, space and time. Oikos 127:497–506CrossRefGoogle Scholar
  58. Shulman MJ, Ogden JC, Ebersole JP, McFarland WN, Miller SL, Wolf NG (1983) Priority effects in the recruitment of juvenile coral reef fishes. Ecology 64:1508–1513CrossRefGoogle Scholar
  59. Sin TM, Lee AC (2000) Host specialisation in trapeziid crabs: Consequences for rarity at local scales. Proc 9th Int Coral Reef Symp 23–27Google Scholar
  60. Smallhorn-West PF, Bridge TCL, Munday PL, Jones GP (2017) Depth distribution and abundance of a coral-associated reef fish: roles of recruitment and post-recruitment processes. Coral Reefs 36:157–166CrossRefGoogle Scholar
  61. Stella JS, Jones GP, Pratchett MS (2010) Variation in the structure of epifaunal invertebrate assemblages among coral hosts. Coral Reefs 29:957–973CrossRefGoogle Scholar
  62. Stella JS, Munday PL, Jones GP (2011) Effects of coral bleaching on the obligate coral-dwelling crab Trapezia cymodoce. Coral Reefs 30:719–727CrossRefGoogle Scholar
  63. Stewart HL, Holbrook SJ, Schmitt RJ, Brooks AJ (2006) Symbiotic crabs maintain coral health by clearing sediments. Coral Reefs 25:609–615CrossRefGoogle Scholar
  64. Stewart HL, Price NN, Holbrook SJ, Schmitt RJ, Brooks AJ (2013) Determinants of the onset and strength of mutualistic interactions between branching corals and associate crabs. Mar Ecol Prog Ser 493:155–163CrossRefGoogle Scholar
  65. Stier AC, Geange SW, Hanson KM, Bolker BM (2013) Predator density and timing of arrival affect reef fish community assembly. Ecology 94:1057–1068CrossRefPubMedGoogle Scholar
  66. Stier AC, Gil MA, McKeon CS, Lemer S, Leray M, Mills SC, Osenberg CW (2012) Housekeeping mutualisms: Do more symbionts facilitate host performance? PLoS One 7:2–7CrossRefGoogle Scholar
  67. Stier AC, Leray M (2014) Predators alter community organization of coral reef cryptofauna and reduce abundance of coral mutualists. Coral Reefs 33:181–191CrossRefGoogle Scholar
  68. Stier AC, McKeon CS, Osenberg CW, Shima JS (2010) Guard crabs alleviate deleterious effects of vermetid snails on a branching coral. Coral Reefs 29:1019–1022CrossRefGoogle Scholar
  69. Veech JA (2013) A probabilistic model for analysing species co-occurrence. Glob Ecol Biogeogr 22:252–260CrossRefGoogle Scholar
  70. 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

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Ocean and Earth Science Technology, Hawai‘i Institute of Marine BiologyUniversity of Hawai‘i at MānoaKāne‘oheUSA
  2. 2.Department of OceanographyUniversity of Hawai‘i at MānoaHonoluluUSA
  3. 3.Department of BiologyUniversity of Hawai‘i at MānoaHonoluluUSA

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