Coral Reefs

, Volume 37, Issue 1, pp 279–293 | Cite as

The relative importance of regional, local, and evolutionary factors structuring cryptobenthic coral-reef assemblages

  • Gabby N. Ahmadia
  • Luke Tornabene
  • David J. Smith
  • Frank L. Pezold
Empirical article


Factors shaping coral-reef fish species assemblages can operate over a wide range of spatial scales (local versus regional) and across both proximate and evolutionary time. Niche theory and neutral theory provide frameworks for testing assumptions and generating insights about the importance of local versus regional processes. Niche theory postulates that species assemblages are an outcome of evolutionary processes at regional scales followed by local-scale interactions, whereas neutral theory presumes that species assemblages are formed by largely random processes drawing from regional species pools. Indo-Pacific cryptobenthic coral-reef fishes are highly evolved, ecologically diverse, temporally responsive, and situated on a natural longitudinal diversity gradient, making them an ideal group for testing predictions from niche and neutral theories and effects of regional and local processes on species assemblages. Using a combination of ecological metrics (fish density, diversity, assemblage composition) and evolutionary analyses (testing for phylogenetic niche conservatism), we demonstrate that the structure of cryptobenthic fish assemblages can be explained by a mixture of regional factors, such as the size of regional species pools and broad-scale barriers to gene flow/drivers of speciation, coupled with local-scale factors, such as the relative abundance of specific microhabitat types. Furthermore, species of cryptobenthic fishes have distinct microhabitat associations that drive significant differences in assemblage community structure between microhabitat types, and these distinct microhabitat associations are phylogenetically conserved over evolutionary timescales. The implied differential fitness of cryptobenthic fishes across varied microhabitats and the conserved nature of their ecology are consistent with predictions from niche theory. Neutral theory predictions may still hold true for early life-history stages, where stochastic factors may be more important in explaining recruitment. Overall, through integration of ecological and evolutionary techniques, and using multiple spatial scales, our study offers a unique perspective on factors determining coral-reef fish assemblages.


Neutral theory Niche theory Species assembly Phylogenetic niche conservatism Coral reefs Coral Triangle 



We thank Jocelyn Curtis-Quick, Dan Lazell, Iwan, Pippa Mansell, Laura Sheard, Conservation Society of Pohnpei, and Brian Lynch and students from the College of Micronesia for field assistance. We are grateful for the support of the staff at the Hoga Marine Research Center, Professor Jamal Jompa and the Universitas Hasanuddin, the Wakatobi Government, the Taman National Wakatobi, RISTEK, and the staff of the Gump Station in Moorea. Funding for field work was provided by Operation Wallacea, PADI Foundation Grant and AMNH Lerner-Gray Fund for Marine Research awarded to G.N.A. and by NSF OISE-0553910 to F.P.

Supplementary material

338_2018_1657_MOESM1_ESM.file (386 kb)
Supplementary material 1 (File 385 kb)
338_2018_1657_MOESM2_ESM.docx (13 kb)
Supplementary material 2 (DOCX 12 kb)
338_2018_1657_MOESM3_ESM.docx (253 kb)
Supplementary material 3 (DOCX 253 kb)


  1. Ackerly D (2009) Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc Natl Acad Sci U S A 106:19699–19706CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ackerman JL, Bellwood DR (2000) Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar Ecol Prog Ser 206:227–237CrossRefGoogle Scholar
  3. Ahmadia GN, Pezold FL, Smith DJ (2012a) Cryptobenthic fish biodiversity and microhabitat use in healthy and degraded coral reefs in SE Sulawesi, Indonesia. Marine Biodivers 42:433–442CrossRefGoogle Scholar
  4. Ahmadia GN, Sheard LJ, Pezold FL, Smith DJ (2012b) Cryptobenthic fish assemblages across the coral reef–seagrass continuum in SE Sulawesi, Indonesia. Aquat Biol 16:125–135CrossRefGoogle Scholar
  5. Allen GR, Erdmann MV (2012) Reef fishes of the East Indies. University of Hawaii Press, HonoluluGoogle Scholar
  6. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525CrossRefGoogle Scholar
  7. Anderson MJ, Santana-Garcon J (2015) Measures of precision for dissimilarity based multivariate analysis of ecological communities. Ecol Lett 18:66–73CrossRefPubMedGoogle Scholar
  8. Bellwood DR, Hughes TP (2001) Regional-scale assembly rules and biodiversity of coral reefs. Science 292:1532–1535CrossRefPubMedGoogle Scholar
  9. Bellwood D, Wainwright P, Fulton C, Hoey A (2002) Assembly rules and functional groups at global biogeographical scales. Funct Ecol 16:557–562CrossRefGoogle Scholar
  10. Bellwood D, Hughes T, Connolly S, Tanner J (2005) Environmental and geometric constraints on Indo-Pacific coral reef biodiversity. Ecol Lett 8:643–651CrossRefGoogle Scholar
  11. Belmaker J, Ziv Y, Shashar N (2009) Habitat patchiness and predation modify the distribution of a coral-dwelling damselfish. Mar Biol 156:447–454CrossRefGoogle Scholar
  12. Boukaert R, Heled J, Kuhnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefGoogle Scholar
  13. Brandl SJ, Casey JM, Knowlton N, Duffy JE (2017) Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions. Ecol Evol 7:7069–7079CrossRefPubMedPubMedCentralGoogle Scholar
  14. Briggs JC (2007) Marine longitudinal biodiversity: causes and conservation. Divers Distrib 13:544–555CrossRefGoogle Scholar
  15. Briggs JC (2009) Diversity, endemism and evolution in the Coral Triangle. J Biogeogr 36:2008–2010CrossRefGoogle Scholar
  16. Camp EF, Hobbs J-PA, De Brauwer M, Dumbrell AJ, Smith DJ (2016) Cohabitation promotes high diversity of clownfishes in the Coral Triangle. Proc R Soc Lond B Biol Sci 283:20160277CrossRefGoogle Scholar
  17. Clarke KR, Somerfield PJ, Warwick RM (2014) Change in marine communities: an approach to statistical analysis and interpretation, 3rd edn. PRIMER-E, PlymouthGoogle Scholar
  18. Connolly SR, Hughes TP, Bellwood DR, Karlson RH (2005) Community structure of corals and reef fishes at multiple scales. Science 309:1363–1365CrossRefPubMedGoogle Scholar
  19. Cornell HV (1999) Unsaturation and regional influences on species richness in ecological communities: a review of the evidence. Ecoscience 6:303–315CrossRefGoogle Scholar
  20. Cornell HV, Lawton JH (1992) Species interactions, local and regional processes, and limits to the richness of ecological communities: a theoretical perspective. J Anim Ecol 61:1–12CrossRefGoogle Scholar
  21. Cowman PF, Bellwood D (2013) This historical biogeography of coral reef fishes: global patterns of origination and dispersal. J Biogeogr 40:209–224CrossRefGoogle Scholar
  22. Depczynski M, Bellwood D (2004) Microhabitat utilisation patterns in cryptobenthic coral reef fish communities. Mar Biol 145:455–463CrossRefGoogle Scholar
  23. Depczynski M, Bellwood DR (2006) Extremes, plasticity, and invariance in vertebrate life history traits: insights from coral reef fishes. Ecology 87:3119–3127CrossRefPubMedGoogle Scholar
  24. Depczynski M, Fulton CJ, Marnane MJ, Bellwood DR (2007) Life history patterns shape energy allocation among fishes on coral reefs. Oecologia 153:111–120CrossRefPubMedGoogle Scholar
  25. Dominici-Arosemena A, Wolff M (2005) Reef fish community structure in Bocas del Toro (Caribbean, Panama): gradients in habitat complexity and exposure. Caribb J Sci 41:613–637Google Scholar
  26. Forrester GE, Finley RJ (2006) Parasitism and a shortage of refuges jointly mediate the strength of density dependence in a reef fish. Ecology 87:1110–1115CrossRefPubMedGoogle Scholar
  27. Friedlander AM, Parrish JD (1998) Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J Exp Mar Bio Ecol 224:1–30CrossRefGoogle Scholar
  28. Glavicic I, Kovacic M (2016) A quantitative sampling method for assessment of deep cryptobenthic ichthyofauna using trimix diving. Acta Ichthyol Piscat Szczecin 46:43–47CrossRefGoogle Scholar
  29. Goatley CHR, Brandl SJ (2017) Cryptobenthic reef fishes. Curr Biol 27:R452–R453CrossRefPubMedGoogle Scholar
  30. Goatley C, Gonzalez-Cabello A, Bellwood DR (2016) Reef-scale partitioning of cryptobenthic fish assemblages across the Great Barrier Reef, Australia. Mar Ecol Prog Ser 544:271–280CrossRefGoogle Scholar
  31. González-Cabello A, Bellwood DR (2009) Local ecological impacts of regional biodiversity on reef fish assemblages. J Biogeogr 36:1129–1137CrossRefGoogle Scholar
  32. Gratwicke B, Speight M (2005a) 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
  33. Gratwicke B, Speight MR (2005b) Effects of habitat complexity on Caribbean marine fish assemblages. Mar Ecol Prog Ser 292:301–310CrossRefGoogle Scholar
  34. Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 9:399–409CrossRefPubMedGoogle Scholar
  35. Greenfield DW, Tornabene L (2014) Eviota brahmi n. sp. from Papua New Guinea, with a redescription of Eviota nigriventris (Teleostei: Gobiidae). Zootaxa 3793:133–146CrossRefPubMedGoogle Scholar
  36. Harborne AR, Mumby PJ, Ferrari R (2012) The effectiveness of different meso-scale rugosity metrics for predicting intra-habitat variation in coral-reef fish assemblages. Environ Biol Fishes 94:431–442CrossRefGoogle Scholar
  37. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131CrossRefPubMedGoogle Scholar
  38. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  39. Herler J (2007) Microhabitats and ecomorphology of coral and coral rock associated gobiid fish (Teleostei: Gobiidae) in the northern Red Sea. Mar Ecol 28:82–94CrossRefGoogle Scholar
  40. Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432CrossRefGoogle Scholar
  41. Hixon MA, Jones GP (2005) Competition, predation, and density-dependent mortality in demersal marine fishes. Ecology 86:2847–2859CrossRefGoogle Scholar
  42. Hodge JR, Read CI, van Herwerden L, Bellwood DR (2012) The role of peripheral endemism in species diversification: evidence from the coral reef fish genus Anampses (Family: Labridae). Mol Phylogenet Evol 62:653–663CrossRefPubMedGoogle Scholar
  43. Holbrook SJ, Brooks AJ, Schmitt RJ (2002) Predictability of fish assemblages on coral patch reefs. Mar Freshw Res 53:181–188CrossRefGoogle Scholar
  44. Holt RD, Gaines MS (1993) The influence of regional processes on local communities: examples from an experimentally fragmented landscape. In: Levin SA, Powell TM, Steele JH (eds) Patch dynamics. Springer, Berlin, pp 260–276CrossRefGoogle Scholar
  45. Hubbell S (2001a) A unified theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  46. Hubbell S (2001b) The unified neutral theory of species abundance and diversity. Princeton University Press, PrincetonGoogle Scholar
  47. Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol Lett 5:775–784CrossRefGoogle Scholar
  48. Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145–159CrossRefGoogle Scholar
  49. Jones GP, McCormick MI (2002) Numerical and energetic processes in the ecology of coral reef fishes. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 221–238CrossRefGoogle Scholar
  50. Karlson RH, Cornell HV (1999) Integration of local and regional perspectives on the species richness of coral assemblages. Am Zool 39:104–112CrossRefGoogle Scholar
  51. 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. Comput Geosci 32:1259–1269CrossRefGoogle Scholar
  52. Komyakova V, Munday PL, Jones GP (2013) Relative importance of coral cover, habitat complexity and diversity in determining the structure of reef fish communities. PLoS One 8:e83178CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kraft NJ, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283CrossRefPubMedGoogle Scholar
  54. Ladd HS (1960) Origin of the Pacific island molluscan fauna. Am J Sci 258:137–150Google Scholar
  55. Lefèvre CD, Bellwood DR (2015) Disturbance and recolonisation by small reef fishes: the role of local movement versus recruitment. Mar Ecol Prog Ser 537:205–215CrossRefGoogle Scholar
  56. Lefèvre CD, Nash KL, González-Cabello A, Bellwood DR (2016) Consequences of extreme life history traits on population persistence: do short-lived gobies face demographic bottlenecks? Coral Reefs 35:399–409CrossRefGoogle Scholar
  57. Levin SA, Paine RT (1974) Disturbance, patch formation, and community structure. Proc Natl Acad Sci U S A 71:2744–2747CrossRefPubMedPubMedCentralGoogle Scholar
  58. Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003CrossRefPubMedGoogle Scholar
  59. McKenna MC (1973) Sweepstakes, filters, corridors, Noah’s Arks, and beached Viking funeral ships in palaeogeography. In: Tarling DH, Runcorn SK (eds) Implications of continental drift to the earth sciences, vol 1. Academic Press, London, pp 295–308Google Scholar
  60. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  61. Mora C, Chittaro PM, Sale PF, Kritzer JP, Ludsin SA (2003) Patterns and processes in reef fish diversity. Nature 421:933–936CrossRefPubMedGoogle Scholar
  62. Munday PL (2000) Interactions between habitat use and patterns of abundance in coral-dwelling fishes of the genus Gobiodon. Environ Biol Fishes 58:355–369CrossRefGoogle Scholar
  63. Munday PL (2004) Habitat loss, resource specialization, and extinction on coral reefs. Glob Chang Biol 10:1642–1647CrossRefGoogle Scholar
  64. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884CrossRefPubMedGoogle Scholar
  65. Paine R (1974) Intertidal community structure. Oecologia 15:93–120CrossRefPubMedGoogle Scholar
  66. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefPubMedGoogle Scholar
  67. Pellissier L, Leprieur F, Parravicini V, Cowman PF, Kulbicki M, Litsios G, Olsen SM, Wisz MS, Bellwood DR, Mouillot D (2014) Quaternary coral reef refugia preserved fish diversity. Science 344:1016–1019CrossRefPubMedGoogle Scholar
  68. Pereira PHC, Munday PL, Jones GP (2015) Settlement of coral-dwelling gobies. Bull Ecol Soc Am 96:654–658CrossRefGoogle Scholar
  69. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  70. Renema W, Bellwood D, Braga J, Bromfield K, Hall R, Johnson K, Lunt P, Meyer C, McMonagle L, Morley R (2008) Hopping hotspots: global shifts in marine biodiversity. Science 321:654–657CrossRefPubMedGoogle Scholar
  71. Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171CrossRefPubMedGoogle Scholar
  72. Ricklefs RE (2006) Global variation in the diversification rate of passerine birds. Ecology 87:2468–2478CrossRefPubMedGoogle Scholar
  73. Ricklefs RE (2008) Disintegration of the ecological community: American Society of Naturalists Sewall Wright award winner address. Am Nat 172:741–750CrossRefPubMedGoogle Scholar
  74. Ricklefs RE, Latham RE (1992) Intercontinental correlation of geographical ranges suggests stasis in ecological traits of relict genera of temperate perennial herbs. Am Nat 139:1305–1321CrossRefGoogle Scholar
  75. Roberts CM, Ormond RF (1987) Habitat complexity and coral reef fish diversity and abundance on Red Sea fringing reefs. Mar Ecol Prog Ser 41:1–8CrossRefGoogle Scholar
  76. Robertson DR (1996) Interspecific competition controls abundance and habitat use of territorial Caribbean damselfishes. Ecology 77:885–899CrossRefGoogle Scholar
  77. Roughgarden J (1974) Niche width: biogeographic patterns among Anolis lizard populations. Am Nat 108:429–442CrossRefGoogle Scholar
  78. Sale PF (1977) Maintenance of high diversity in coral reef fish communities. Am Nat 111:337–359CrossRefGoogle Scholar
  79. Sale PF (1980) Assemblages of fish on patch reefs—predictable or unpredictable? Environ Biol Fishes 5:243–249CrossRefGoogle Scholar
  80. Sutton M (1985) Patterns of spacing in a coral reef fish in two habitats on the Great Barrier Reef. Anim Behav 33:1332–1337CrossRefGoogle Scholar
  81. Tornabene L, Chen Y, Pezold F (2013) Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: Gobiidae: Eviota). Mol Phylogenet Evol 66:391–400CrossRefPubMedGoogle Scholar
  82. Tornabene L, Valdez S, Erdmann M, Pezold F (2015) Support for a ‘center of origin’ in the Coral Triangle: cryptic diversity, recent speciation, and local endemism in a diverse lineage of reef fishes (Gobiidae: Eviota). Mol Phylogenet Evol 82:200–210CrossRefPubMedGoogle Scholar
  83. Tornabene L, Valdez S, Erdmann MV, Pezold FL (2016) Multi-locus sequence data reveal a new species of coral reef goby (Teleostei: Gobiidae: Eviota), and evidence of Pliocene vicariance across the Coral Triangle. J Fish Biol 88:1811–1834CrossRefPubMedGoogle Scholar
  84. Underwood A, Chapman M, Connell S (2000) Observations in ecology: you can’t make progress on processes without understanding the patterns. J Exp Mar Bio Ecol 250:97–115CrossRefPubMedGoogle Scholar
  85. Webb CO, Losos JB, Agrawal AA (2006) Integrating phylogenies into community ecology. Ecology 87:S1–S2CrossRefGoogle Scholar
  86. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  87. Webster MS, Hixon MA (2000) Mechanisms and individual consequences of intraspecific competition in a coral-reef fish. Mar Ecol Prog Ser 196:187–194CrossRefGoogle Scholar
  88. Wiens JA (1976) Population responses to patchy environments. Annu Rev Ecol Syst 7:81–120CrossRefGoogle Scholar
  89. Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397CrossRefGoogle Scholar
  90. Wiens JA, Stralberg D, Jongsomjit D, Howell CA, Snyder MA (2009) Niches, models, and climate change: assessing the assumptions and uncertainties. Proc Natl Acad Sci U S A 106:19729–19736CrossRefPubMedPubMedCentralGoogle Scholar
  91. Wiens JJ, Harrison R (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58:193–197CrossRefPubMedGoogle Scholar
  92. Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, Damschen EI, Jonathan Davies T, Grytnes JA, Harrison SP (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecol Lett 13:1310–1324CrossRefPubMedGoogle Scholar
  93. Willis TJ, Anderson MJ (2003) Structure of cryptic reef fish assemblages: relationships with habitat characteristics and predator density. Mar Ecol Prog Ser 257:209–221CrossRefGoogle Scholar
  94. Witman JD, Etter RJ, Smith F (2004) The relationship between regional and local species diversity in marine benthic communities: a global perspective. Proc Natl Acad Sci U S A 101:15664–15669CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Gabby N. Ahmadia
    • 1
    • 2
  • Luke Tornabene
    • 2
    • 3
    • 4
  • David J. Smith
    • 5
  • Frank L. Pezold
    • 2
  1. 1.Oceans Conservation, World Wildlife FundWashingtonUSA
  2. 2.College of Science and EngineeringTexas A&M University-Corpus ChristiCorpus ChristiUSA
  3. 3.School of Aquatic and Fishery SciencesUniversity of WashingtonSeattleUSA
  4. 4.Burke Museum of Natural History and CultureSeattleUSA
  5. 5.Coral Reef Research Unit, School of Biological SciencesUniversity of EssexColchesterUK

Personalised recommendations