Skip to main content

Advertisement

SpringerLink
Log in

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

  • Empirical article
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ackerly D (2009) Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc Natl Acad Sci U S A 106:19699–19706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ackerman JL, Bellwood DR (2000) Reef fish assemblages: a re-evaluation using enclosed rotenone stations. Mar Ecol Prog Ser 206:227–237

    Article  Google Scholar 

  • 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 42:433–442

    Article  Google Scholar 

  • Ahmadia GN, Sheard LJ, Pezold FL, Smith DJ (2012b) Cryptobenthic fish assemblages across the coral reef–seagrass continuum in SE Sulawesi, Indonesia. Aquat Biol 16:125–135

    Article  Google Scholar 

  • Allen GR, Erdmann MV (2012) Reef fishes of the East Indies. University of Hawaii Press, Honolulu

    Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Anderson MJ, Santana-Garcon J (2015) Measures of precision for dissimilarity based multivariate analysis of ecological communities. Ecol Lett 18:66–73

    Article  PubMed  Google Scholar 

  • Bellwood DR, Hughes TP (2001) Regional-scale assembly rules and biodiversity of coral reefs. Science 292:1532–1535

    Article  CAS  PubMed  Google Scholar 

  • Bellwood D, Wainwright P, Fulton C, Hoey A (2002) Assembly rules and functional groups at global biogeographical scales. Funct Ecol 16:557–562

    Article  Google Scholar 

  • Bellwood D, Hughes T, Connolly S, Tanner J (2005) Environmental and geometric constraints on Indo-Pacific coral reef biodiversity. Ecol Lett 8:643–651

    Article  Google Scholar 

  • Belmaker J, Ziv Y, Shashar N (2009) Habitat patchiness and predation modify the distribution of a coral-dwelling damselfish. Mar Biol 156:447–454

    Article  Google Scholar 

  • 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:e1003537

    Article  Google Scholar 

  • Brandl SJ, Casey JM, Knowlton N, Duffy JE (2017) Marine dock pilings foster diverse, native cryptobenthic fish assemblages across bioregions. Ecol Evol 7:7069–7079

    Article  PubMed  PubMed Central  Google Scholar 

  • Briggs JC (2007) Marine longitudinal biodiversity: causes and conservation. Divers Distrib 13:544–555

    Article  Google Scholar 

  • Briggs JC (2009) Diversity, endemism and evolution in the Coral Triangle. J Biogeogr 36:2008–2010

    Article  Google Scholar 

  • 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 283:20160277

    Article  Google Scholar 

  • Clarke KR, Somerfield PJ, Warwick RM (2014) Change in marine communities: an approach to statistical analysis and interpretation, 3rd edn. PRIMER-E, Plymouth

    Google Scholar 

  • Connolly SR, Hughes TP, Bellwood DR, Karlson RH (2005) Community structure of corals and reef fishes at multiple scales. Science 309:1363–1365

    Article  CAS  PubMed  Google Scholar 

  • Cornell HV (1999) Unsaturation and regional influences on species richness in ecological communities: a review of the evidence. Ecoscience 6:303–315

    Article  Google Scholar 

  • 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 61:1–12

    Article  Google Scholar 

  • Cowman PF, Bellwood D (2013) This historical biogeography of coral reef fishes: global patterns of origination and dispersal. J Biogeogr 40:209–224

    Article  Google Scholar 

  • Depczynski M, Bellwood D (2004) Microhabitat utilisation patterns in cryptobenthic coral reef fish communities. Mar Biol 145:455–463

    Article  Google Scholar 

  • Depczynski M, Bellwood DR (2006) Extremes, plasticity, and invariance in vertebrate life history traits: insights from coral reef fishes. Ecology 87:3119–3127

    Article  PubMed  Google Scholar 

  • Depczynski M, Fulton CJ, Marnane MJ, Bellwood DR (2007) Life history patterns shape energy allocation among fishes on coral reefs. Oecologia 153:111–120

    Article  PubMed  Google Scholar 

  • 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 41:613–637

    Google Scholar 

  • Forrester GE, Finley RJ (2006) Parasitism and a shortage of refuges jointly mediate the strength of density dependence in a reef fish. Ecology 87:1110–1115

    Article  PubMed  Google Scholar 

  • Friedlander AM, Parrish JD (1998) Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J Exp Mar Bio Ecol 224:1–30

    Article  Google Scholar 

  • Glavicic I, Kovacic M (2016) A quantitative sampling method for assessment of deep cryptobenthic ichthyofauna using trimix diving. Acta Ichthyol Piscat Szczecin 46:43–47

    Article  Google Scholar 

  • Goatley CHR, Brandl SJ (2017) Cryptobenthic reef fishes. Curr Biol 27:R452–R453

    Article  CAS  PubMed  Google Scholar 

  • 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 544:271–280

    Article  Google Scholar 

  • González-Cabello A, Bellwood DR (2009) Local ecological impacts of regional biodiversity on reef fish assemblages. J Biogeogr 36:1129–1137

    Article  Google Scholar 

  • 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 66:650–667

    Article  Google Scholar 

  • Gratwicke B, Speight MR (2005b) Effects of habitat complexity on Caribbean marine fish assemblages. Mar Ecol Prog Ser 292:301–310

    Article  Google Scholar 

  • Gravel D, Canham CD, Beaudet M, Messier C (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecol Lett 9:399–409

    Article  PubMed  Google Scholar 

  • Greenfield DW, Tornabene L (2014) Eviota brahmi n. sp. from Papua New Guinea, with a redescription of Eviota nigriventris (Teleostei: Gobiidae). Zootaxa 3793:133–146

    Article  PubMed  Google Scholar 

  • 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 94:431–442

    Article  Google Scholar 

  • Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131

    Article  CAS  PubMed  Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Herler J (2007) Microhabitats and ecomorphology of coral and coral rock associated gobiid fish (Teleostei: Gobiidae) in the northern Red Sea. Mar Ecol 28:82–94

    Article  Google Scholar 

  • Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432

    Article  Google Scholar 

  • Hixon MA, Jones GP (2005) Competition, predation, and density-dependent mortality in demersal marine fishes. Ecology 86:2847–2859

    Article  Google Scholar 

  • 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 62:653–663

    Article  PubMed  Google Scholar 

  • Holbrook SJ, Brooks AJ, Schmitt RJ (2002) Predictability of fish assemblages on coral patch reefs. Mar Freshw Res 53:181–188

    Article  Google Scholar 

  • 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 260–276

    Chapter  Google Scholar 

  • Hubbell S (2001a) A unified theory of biodiversity and biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Hubbell S (2001b) The unified neutral theory of species abundance and diversity. Princeton University Press, Princeton

    Google Scholar 

  • Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol Lett 5:775–784

    Article  Google Scholar 

  • Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145–159

    Article  Google Scholar 

  • 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 221–238

    Chapter  Google Scholar 

  • Karlson RH, Cornell HV (1999) Integration of local and regional perspectives on the species richness of coral assemblages. Am Zool 39:104–112

    Article  Google Scholar 

  • 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 32:1259–1269

    Article  Google Scholar 

  • 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:e83178

    Article  PubMed  PubMed Central  Google Scholar 

  • Kraft NJ, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283

    Article  PubMed  Google Scholar 

  • Ladd HS (1960) Origin of the Pacific island molluscan fauna. Am J Sci 258:137–150

    Google Scholar 

  • Lefèvre CD, Bellwood DR (2015) Disturbance and recolonisation by small reef fishes: the role of local movement versus recruitment. Mar Ecol Prog Ser 537:205–215

    Article  Google Scholar 

  • 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 35:399–409

    Article  Google Scholar 

  • Levin SA, Paine RT (1974) Disturbance, patch formation, and community structure. Proc Natl Acad Sci U S A 71:2744–2747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003

    Article  PubMed  Google Scholar 

  • 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 295–308

    Google Scholar 

  • Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757

    Article  Google Scholar 

  • Mora C, Chittaro PM, Sale PF, Kritzer JP, Ludsin SA (2003) Patterns and processes in reef fish diversity. Nature 421:933–936

    Article  CAS  PubMed  Google Scholar 

  • Munday PL (2000) Interactions between habitat use and patterns of abundance in coral-dwelling fishes of the genus Gobiodon. Environ Biol Fishes 58:355–369

    Article  Google Scholar 

  • Munday PL (2004) Habitat loss, resource specialization, and extinction on coral reefs. Glob Chang Biol 10:1642–1647

    Article  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  CAS  PubMed  Google Scholar 

  • Paine R (1974) Intertidal community structure. Oecologia 15:93–120

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • 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 344:1016–1019

    Article  CAS  PubMed  Google Scholar 

  • Pereira PHC, Munday PL, Jones GP (2015) Settlement of coral-dwelling gobies. Bull Ecol Soc Am 96:654–658

    Article  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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 321:654–657

    Article  CAS  PubMed  Google Scholar 

  • Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171

    Article  CAS  PubMed  Google Scholar 

  • Ricklefs RE (2006) Global variation in the diversification rate of passerine birds. Ecology 87:2468–2478

    Article  PubMed  Google Scholar 

  • Ricklefs RE (2008) Disintegration of the ecological community: American Society of Naturalists Sewall Wright award winner address. Am Nat 172:741–750

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Latham RE (1992) Intercontinental correlation of geographical ranges suggests stasis in ecological traits of relict genera of temperate perennial herbs. Am Nat 139:1305–1321

    Article  Google Scholar 

  • Roberts CM, Ormond RF (1987) Habitat complexity and coral reef fish diversity and abundance on Red Sea fringing reefs. Mar Ecol Prog Ser 41:1–8

    Article  CAS  Google Scholar 

  • Robertson DR (1996) Interspecific competition controls abundance and habitat use of territorial Caribbean damselfishes. Ecology 77:885–899

    Article  Google Scholar 

  • Roughgarden J (1974) Niche width: biogeographic patterns among Anolis lizard populations. Am Nat 108:429–442

    Article  Google Scholar 

  • Sale PF (1977) Maintenance of high diversity in coral reef fish communities. Am Nat 111:337–359

    Article  Google Scholar 

  • Sale PF (1980) Assemblages of fish on patch reefs—predictable or unpredictable? Environ Biol Fishes 5:243–249

    Article  Google Scholar 

  • Sutton M (1985) Patterns of spacing in a coral reef fish in two habitats on the Great Barrier Reef. Anim Behav 33:1332–1337

    Article  Google Scholar 

  • 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 66:391–400

    Article  PubMed  Google Scholar 

  • 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 82:200–210

    Article  PubMed  Google Scholar 

  • 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 88:1811–1834

    Article  CAS  PubMed  Google Scholar 

  • 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 250:97–115

    Article  CAS  PubMed  Google Scholar 

  • Webb CO, Losos JB, Agrawal AA (2006) Integrating phylogenies into community ecology. Ecology 87:S1–S2

    Article  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Webster MS, Hixon MA (2000) Mechanisms and individual consequences of intraspecific competition in a coral-reef fish. Mar Ecol Prog Ser 196:187–194

    Article  Google Scholar 

  • Wiens JA (1976) Population responses to patchy environments. Annu Rev Ecol Syst 7:81–120

    Article  Google Scholar 

  • Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397

    Article  Google Scholar 

  • 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 106:19729–19736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiens JJ, Harrison R (2004) Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58:193–197

    Article  PubMed  Google Scholar 

  • 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 13:1310–1324

    Article  PubMed  Google Scholar 

  • Willis TJ, Anderson MJ (2003) Structure of cryptic reef fish assemblages: relationships with habitat characteristics and predator density. Mar Ecol Prog Ser 257:209–221

    Article  Google Scholar 

  • 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 101:15664–15669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Oceans Conservation, World Wildlife Fund, 1250 24th St. NW, Washington, DC, 20037, USA

    Gabby N. Ahmadia

  2. College of Science and Engineering, Texas A&M University-Corpus Christi, 6300 Ocean Drive, Corpus Christi, TX, 78412-5806, USA

    Gabby N. Ahmadia, Luke Tornabene & Frank L. Pezold

  3. School of Aquatic and Fishery Sciences, University of Washington, 1122 NE Boat Street, Seattle, WA, 98105, USA

    Luke Tornabene

  4. Burke Museum of Natural History and Culture, 17th Avenue NE and NE 45th Street, Seattle, WA, 98105, USA

    Luke Tornabene

  5. Coral Reef Research Unit, School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK

    David J. Smith

Authors
  1. Gabby N. Ahmadia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luke Tornabene
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David J. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Frank L. Pezold
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabby N. Ahmadia.

Additional information

Topic Editor Dr. Michael Berumen

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmadia, G.N., Tornabene, L., Smith, D.J. et al. The relative importance of regional, local, and evolutionary factors structuring cryptobenthic coral-reef assemblages. Coral Reefs 37, 279–293 (2018). https://doi.org/10.1007/s00338-018-1657-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-018-1657-2

Keywords

Search

Navigation