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Marine Biology

, 165:138 | Cite as

Depth patterns in microhabitat versatility and selectivity in coral reef damselfishes

  • Chancey MacDonald
  • Mele I. Tauati
  • Geoffrey P. Jones
Original paper

Abstract

Increasing disturbances on coral reefs threaten fish species with close microhabitat associations in shallow waters, but deep reefs may provide refuge habitats. Assessing this potential requires a comprehensive understanding of how versatility in microhabitat use, preference, and selectivity interact with changes in habitat composition along depth gradients. We examined six damselfish species categorized by versatility of shallow-water microhabitat association (‘complex-coral-specialists’, ‘coral-associates’, and ‘generalists’), along a depth gradient from 10 to 30 m in Kimbe Bay, Papua New Guinea, and tested four important hypotheses. (1) We examined associations with hard-coral and complex-coral microhabitats. Hard-coral association declined with depth more among generalists than coral-associates but complex-coral microhabitat association declined for all species except one complex-coral-specialist. (2) We studied whether microhabitat selectivity declines with depth. Unexpectedly, selectivity increased with depth among both generalist and specialist species. (3) Within species, we tested for positive relationships between fish abundance and preferred microhabitat availability at each depth. However, relationships were stochastic across depths for all but one complex-coral-specialist. (4) Finally, we tested for positive relationships between the number of microhabitats selected by a species and the species’ abundance at each depth, finding that species’ abundances were not consistently related to microhabitat versatility. Our results suggest that several species currently utilize deep coral microhabitats (≤ 30 m), including specialists that strongly associate with vulnerable coral habitats in shallow water. Considerable microhabitat plasticity occurred along the gradient, even amidst stable preferences, and versatile species were not habitat limited, though restricted versatility may limit refuge potential for some species.

Notes

Acknowledgements

We thank Phillip Smith for field assistance and M. Bonin for theoretical and analytical advice, and J. Eurich and T. Rüger for helpful comments. M. Ikanga thanks her family for their support, patience and encouragement. Mahonia Na Dari—Guardians of the Sea and Walindi Plantation Resort provided valuable logistical support.

Compliance with ethical standards

Funding

This study was funded by a Grant to G. P. Jones from the Australian Research Council.

Conflict of interest

C. MacDonald declares that he has no conflict of interest. M. Ikanga declares that she has no conflict of interest. G. P. Jones declares that he has no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. Adjeroud M, Pratchett MS, Kospartov MC, Lejeusne C, Penin L (2007) Small-scale variability in the size structure of scleractinian corals around Moorea, French Polynesia: patterns across depths and locations. Hydrobiologia 589:117–126CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  3. Bean K, Jones GP, Caley MJ (2002) Relationships among distribution, abundance and microhabitat specialisation in a guild of coral reef triggerfish (family Balistidae). Mar Ecol Prog Ser 233:263–272CrossRefGoogle Scholar
  4. Berkström C, Jones GP, McCormick MI, Srinivasan M (2012) Ecological versatility and its importance for the distribution and abundance of coral reef wrasses. Mar Ecol Prog Ser 461:151–163CrossRefGoogle Scholar
  5. Bongaerts P, Ridgway T, Sampayo E, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327CrossRefGoogle Scholar
  6. Bongaerts P, Frade PR, Ogier JJ, Hay KB, Van Bleijswijk J, Englebert N, Vermeij MJ, Bak RP, Visser PM, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evol Biol 13:205CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bonin MC (2012) Specializing on vulnerable habitat: Acropora selectivity among damselfish recruits and the risk of bleaching-induced habitat loss. Coral Reefs 31:287–297CrossRefGoogle Scholar
  8. Bonin MC, Srinivasan M, Almany GR, Jones GP (2009) Interactive effects of interspecific competition and microhabitat on early post-settlement survival in a coral reef fish. Coral Reefs 28:265–274CrossRefGoogle Scholar
  9. Boström-Einarsson L, Bonin MC, Munday PL, Jones GP (2013) Strong intraspecific competition and habitat selectivity influence abundance of a coral-dwelling damselfish. J Exp Mar Biol Ecol 448:85–92CrossRefGoogle Scholar
  10. Bridge TC, Hughes TP, Guinotte JM, Bongaerts P (2013) Call to protect all coral reefs. Nat Clim Change 3:528–530CrossRefGoogle Scholar
  11. Bridge TCL, Luiz OJ, Coleman RR, Kane CN, Kosaki RK (2016) Ecological and morphological traits predict depth-generalist fishes on coral reefs. Proc R Soc B Biol Sci 283:2332–2336CrossRefGoogle Scholar
  12. Brokovich E, Einbinder S, Shashar N, Kiflawi M, Kark S (2008) Descending to the twilight-zone: changes in coral reef fish assemblages along a depth gradient down to 65 m. Mar Ecol Prog Ser 371:253–262CrossRefGoogle Scholar
  13. Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279CrossRefGoogle Scholar
  14. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, DeVantier L (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 32:560–563CrossRefGoogle Scholar
  15. Coker DJ, Pratchett MS, Munday PL (2012) Influence of coral bleaching, coral mortality and conspecific aggression on movement and distribution of coral-dwelling fish. J Exp Mar Biol Ecol 414:62–68CrossRefGoogle Scholar
  16. Coker DJ, Wilson SK, Pratchett MS (2014) Importance of live coral habitat for reef fishes. Rev Fish Biol Fish 24:89–126CrossRefGoogle Scholar
  17. Connolly SR, Bellwood DR, Hughes TP (2003) Indo-Pacific biodiversity of coral reefs: deviations from a mid-domain model. Ecology 84:2178–2190CrossRefGoogle Scholar
  18. Danilowicz BS (1996) Choice of coral species by naive and field-caught damselfish. Copeia 1996:735–739CrossRefGoogle Scholar
  19. Dollar SJ, Tribble GW (1993) Recurrent storm disturbance and recovery: a long-term study of coral communities in Hawaii. Coral Reefs 12:223–233CrossRefGoogle Scholar
  20. Eckert GJ (1985) Settlement of coral reef fishes to different natural substrata and at different depths. In: Proc 5th int coral reef congr Tahiti vol 5, pp 385–390Google Scholar
  21. Eurich JG, McCormick MI, Jones GP (2018) Habitat selection and aggression as determinants of fine-scale partitioning of coral reef zones in a guild of territorial damselfishes. Mar Ecol Prog Ser 587:201–215CrossRefGoogle Scholar
  22. Feary DA (2007) The influence of resource specialization on the response of reef fish to coral disturbance. Mar Biol 153:153–161CrossRefGoogle Scholar
  23. Feary DA, Almany GR, McCormick MI, Jones GP (2007) Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153(3):727–737CrossRefPubMedGoogle Scholar
  24. Feary DA, McCormick MI, Jones GP (2009) Growth of reef fishes in response to live coral cover. J Exp Mar Biol Ecol 373:45–49CrossRefGoogle Scholar
  25. Friedlander AM, Parrish JD (1998) Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J Exp Mar Biol Ecol 224:1–30CrossRefGoogle Scholar
  26. Fulton CJ, Bellwood DR (2005) Wave-induced water motion and the functional implications for coral reef fish assemblages. Limnol Oceanogr 50:255–264CrossRefGoogle Scholar
  27. Garcia-Sais JR (2010) Reef habitats and associated sessile-benthic and fish assemblages across a euphotic–mesophotic depth gradient in Isla Desecheo, Puerto Rico. Coral Reefs 29:277–288CrossRefGoogle Scholar
  28. Gardiner NM, Jones GP (2005) Habitat specialisation and overlap in a guild of coral reef cardinalfishes (Apogonidae). Mar Ecol Prog Ser 305:163–175CrossRefGoogle Scholar
  29. Garpe KC, Yahya SA, Lindahl U, Öhman MC (2006) Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Mar Ecol Prog Ser 315:237–247CrossRefGoogle Scholar
  30. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Change Biol 2:495–509CrossRefGoogle Scholar
  31. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Nat Acad Sci 103:8425–8429CrossRefPubMedGoogle Scholar
  32. Graham NA, Chabanet P, Evans RD, Jennings S (2011) Extinction vulnerability of coral reef fishes. Ecol Lett 14:341–348CrossRefPubMedPubMedCentralGoogle Scholar
  33. Green A (1996) Spatial, temporal and ontogenetic patterns of habitat use by coral reef fishes (Family Labridae). Mar Ecol Prog Ser 133:1–11CrossRefGoogle Scholar
  34. Hoey J, McCormick MI, Hoey AS (2007) Influence of depth on sex-specific energy allocation patterns in a tropical reef fish. Coral Reefs 26:603–613CrossRefGoogle Scholar
  35. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson J, Kleypas J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedGoogle Scholar
  36. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin MC, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo C, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefPubMedGoogle Scholar
  37. Jankowski MW, Graham NAJ, Jones GP (2015) The effects of depth on diversity, species distributions and habitat specialisation in coral reef fishes. Mar Ecol Prog Ser 540:203–215CrossRefGoogle Scholar
  38. Jones GP (1987) Competitive interactions among adults and juveniles in a coral reef fish. Ecology 68:1534–1547CrossRefGoogle Scholar
  39. Jones GP, Caley MJ, Munday PL (2002) Rarity in coral reef fish communities. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, p 81CrossRefGoogle Scholar
  40. Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101:8251CrossRefPubMedGoogle Scholar
  41. Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci 98:5419–5425CrossRefPubMedGoogle Scholar
  42. 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
  43. Lara EN, González EA (1998) The relationship between reef fish community structure and environmental variables in the southern Mexican Caribbean. J Fish Biol 53:209–221CrossRefGoogle Scholar
  44. Lecchini D, Galzin R (2005) Spatial repartition and ontogenetic shifts in habitat use by coral reef fishes (Moorea, French Polynesia). Mar Biol 147:47–58CrossRefGoogle Scholar
  45. Lesser MP, Slattery M (2011) Phase shift to algal dominated communities at mesophotic depths associated with lionfish (Pterois volitans) invasion on a Bahamian coral reef. Biol Invasions 13:1855–1868CrossRefGoogle Scholar
  46. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8CrossRefGoogle Scholar
  47. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali Y, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  48. MacDonald C, Bridge TC, Jones GP (2016) Depth, bay position and habitat structure as determinants of coral reef fish distributions: are deep reefs a potential refuge? Mar Ecol Prog Ser 561:217–231CrossRefGoogle Scholar
  49. MacNally RC (1995) Ecological versatility and community ecology. In: Cambridge Studies in Ecology, Cambridge University Press.  https://doi.org/10.1017/CBO9780511565427
  50. Madin JS, Connolly SR (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480CrossRefPubMedGoogle Scholar
  51. Manly B, McDonald L, Thomas D, McDonald T, Erickson W (2002) Resource selection by animals: statistical analysis and design for field studies. Kluwer, NordrechtGoogle Scholar
  52. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163CrossRefGoogle Scholar
  53. McClanahan TR, Baird AH, Marshall PA, Toscano MA (2004) Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar Pollut Bull 48:327–335CrossRefPubMedGoogle Scholar
  54. Menza C, Kendall M, Hile S (2008) The deeper we go the less we know. Rev Biol Trop 56(Sup 1):11–24Google Scholar
  55. Munday P (2002) Does habitat availability determine geographical-scale abundances of coral-dwelling fishes? Coral Reefs 21:105–116CrossRefGoogle Scholar
  56. Munday PL (2004) Habitat loss, resource specialization, and extinction on coral reefs. Glob Change Biol 10:1642–1647CrossRefGoogle Scholar
  57. Munday PL, Jones GP, Caley MJ (1997) Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar Ecol Prog Ser 152:227–239CrossRefGoogle Scholar
  58. Noonan SHC, Jones GP, Pratchett MS (2012) Coral size, health and structural complexity: effects on the ecology of a coral reef damselfish. Mar Ecol Prog Ser 456:127–137CrossRefGoogle Scholar
  59. Öhman MC, Munday PL, Jones GP, Caley MJ (1998) Settlement strategies and distribution patterns of coral-reef fishes. J Exp Mar Biol 225:219–238CrossRefGoogle Scholar
  60. Pereira PH, Munday PL (2016) Coral colony size and structure as determinants of habitat use and fitness of coral-dwelling fishes. Mar Ecol Prog Ser 553:163–172CrossRefGoogle Scholar
  61. Pereira PH, Munday PL, Jones GP (2015) Competitive mechanisms change with ontogeny in coral-dwelling gobies. Ecology 96:3090–3101CrossRefPubMedGoogle Scholar
  62. Pratchett MS, Munday P, Wilson SK, Graham NA, Cinner JE, Bellwood DR, Jones GP, Polunin NV, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes - ecological and economic consequences. Oceanogr Mar Biol Annu Rev 46:251–296Google Scholar
  63. Pratchett MS, Coker DJ, Jones GP, Munday PL (2012) Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss. Ecol Evol 2:2168–2180CrossRefPubMedPubMedCentralGoogle Scholar
  64. Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. University of Hawaii Press, HonoluluGoogle Scholar
  65. Riegl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. Int J Earth Sci 92:520–531CrossRefGoogle Scholar
  66. Roberts TE, Moloney JM, Sweatman HPA, Bridge TCL (2015) Benthic community composition on submerged reefs in the central Great Barrier Reef. Coral Reefs 34:569–580CrossRefGoogle Scholar
  67. Rooney J, Donham E, Montgomery A, Spalding H, Parrish F, Boland R, Fenner D, Gove J, Vetter O (2010) Mesophotic coral ecosystems in the Hawaiian Archipelago. Coral Reefs 29:361–367CrossRefGoogle Scholar
  68. Shima JS (2001) Recruitment of a coral reef fish: roles of settlement, habitat, and postsettlement losses. Ecology 82:2190–2199CrossRefGoogle Scholar
  69. Shulman MJ (1984) Resource limitation and recruitment patterns in a coral reef fish assemblage. J Exp Mar Biol Ecol 74:85–109CrossRefGoogle Scholar
  70. Smallhorn-West PF, Bridge TCL, Munday PL, Jones JP (2017) Depth distribution and abundance of a coral-associated reef fish: roles of recruitment and post-recruitment processes. Coral Reefs 36:157–166CrossRefGoogle Scholar
  71. Souza AT, Ilarri MI, Rosa IL (2011) Habitat use, feeding and territorial behavior of a Brazilian endemic damselfish Stegastes rocasensis (Actinopterygii: Pomacentridae). Environ Biol Fish 91:133–144CrossRefGoogle Scholar
  72. Srinivasan M (2003) Depth distributions of coral reef fishes: the influence of microhabitat structure, settlement, and post-settlement processes. Oecologica 137:76–84CrossRefGoogle Scholar
  73. Tilot V, Leujak W, Ormond R, Ashworth J, Mabrouk A (2008) Monitoring of South Sinai coral reefs: influence of natural and anthropogenic factors. Aquat Conserv Mar Freshw Ecosyst 18:1109–1126CrossRefGoogle Scholar
  74. Wilkinson E (2002) Status of coral reefs of the world. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  75. Wilson SK, Graham NA, Pratchett MS, Jones GP, Polunin NV (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob Change Biol 12:2220–2234CrossRefGoogle Scholar
  76. Wilson SK, Burgess SC, Cheal AJ, Emslie M, Fisher R, Miller I, Polunin NV, Sweatman H (2008) Habitat utilization by coral reef fish: implications for specialists vs. generalists in a changing environment. J Anim Ecol 77:220–228CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Marine Biology and Aquaculture Science, College of Science and EngineeringJames Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia

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