Changes in reef fish assemblages following multiple bleaching events in the world’s warmest sea (Kish Island, the Persian Gulf)

Abstract

Climate change affects the ecology of reef fish through changing their habitat, community and their feeding and territorial behavior. The corals and their associated reef fish in the Persian Gulf as the world’s warmest sea suffer from the increasing frequency and severity of mass bleaching events. Yet, the effects of climate-induced coral bleaching events on reef fish in this sea are poorly understood. Using a time series fish count data, this study evaluated the response of reef fish to multiple severe coral bleaching events in Kish Island located in the central Persian Gulf. The results showed a decline in species richness and diversity of reef fish after bleaching events which reduced mean coral cover by 85% following the 2007 bleaching event and by 95% following the 2017 bleaching event. Besides a drop in the number of fish species, the total density, and density of trophic groups changed as the results of coral loss. The variation in density of different trophic groups indicated an overall increase in the abundance of benthic invertebrate feeders (21.2–136.3%), omnivores (32.4–163.4%) and plankton feeders (218.5–488%). In contrast, the abundance of coral polyp feeders (−6.9 to −50%) and piscivores (−4.9 to −38.9%) significantly decreased after bleaching events. The density of herbivorous fish significantly increased by 97.1% after the bleaching event in 2007 and decreased by 10.5% after the bleaching event in 2017. In the present study, we demonstrated how the impact of the multiple bleaching events on associated reef fish assemblages sustained for about 6 years after the disturbance. These results have significant implications for our understanding of the response of reef fish to global warming and highlight the growing concern about the future of coral reef ecosystems and their associated reef fish in the region as the warmest sea in the world.

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References

  1. Aburto-Oropeza O, Ezcurra E, Moxley J, Sánchez-Rodríguez A, Mascareñas-Osorio I, Sánchez-Ortiz C, Erisman B, Ricketts T (2015) A framework to assess the health of rocky reefs linking geomorphology, community assemblage, and fish biomass. Ecol Indic 52:353–361

    Google Scholar 

  2. Almany GR (2004) Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106:275–284

    Google 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 80:435–471

    Google Scholar 

  4. Bellwood D, Hoey A, Hughes T (2012) Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proc Biol Sci 279:1621–1629

    PubMed  Google Scholar 

  5. Bellwood DR, Hoey AS, Ackerman JL, Depczynski M (2006) Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Glob Chang Biol 12:1587–1594

    Google Scholar 

  6. Berumen ML, Pratchett MS (2006) Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647–653

    Google Scholar 

  7. Bongaerts P, Riginos C, Brunner R, Englebert N, Smith S, Hoegh-Guldberg O (2017) Deep reefs are not universal refuges: reseeding potential varies among coral species. Sci Adv 3:e1602373

    PubMed  PubMed Central  Google Scholar 

  8. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327

    Google Scholar 

  9. Buchanan JR, Krupp F, Burt JA, Feary DA, Ralph GM, Carpenter KE (2016) Living on the edge: Vulnerability of coral-dependent fishes in the Gulf. Mar Pollut Bull 105:480–488

    CAS  PubMed  Google Scholar 

  10. Burt J, Bartholomew A, Usseglio P (2008) Recovery of corals a decade after a bleaching event in Dubai, United Arab Emirates. Mar Biol 154:27–36

    Google Scholar 

  11. Burt JA, Bartholomew A, Bauman A, Sale P (2009) Coral recruitment and early benthic community development on common materials used in the construction of artificial reefs. J Exp Mar Biol Ecol 373:72–78

    Google Scholar 

  12. Burt JA, Feary DA, Bauman AG, Usseglio P, Cavalcante GH, Sale PF (2011) Biogeographic patterns of reef fish community structure in the northeastern Arabian Peninsula. ICES J Mar Sci 68:1875–1883

    Google Scholar 

  13. Burt JA, Feary DA, Cavalcante G, Bauman AG, Usseglio P (2013) Urban breakwaters as reef fish habitat in the Persian Gulf. Mar Pollut Bull 72:342–350

    CAS  PubMed  Google Scholar 

  14. Burt JA, Paparella F, Al-Mansoori N, Al-Mansoori A, Al-Jailani H (2019) Causes and consequences of the 2017 coral bleaching event in the southern Persian/Arabian Gulf. Coral Reefs 38:567–589

    Google Scholar 

  15. Cheal AJ, Wilson SK, Emslie MJ, Dolman AM, Sweatman H (2008) Responses of reef fish communities to coral declines on the Great Barrier Reef. Mar Ecol Prog Ser 372:211–223

    Google Scholar 

  16. Clarke KR, Gorley RN (2006) PRIMER V6: user manual-tutorial: Plymouth Marine Laboratory

  17. Coles SL, Tarr BA (1990) Reef fish assemblages in the western Arabian Gulf: a geographically isolated population in an extreme environment. Bull Mar Sci 47:696–720

    Google Scholar 

  18. Coles SL (2003) Coral species diversity and environmental factors in the Arabian Gulf and the Gulf of Oman: a comparison to the Indo-Pacific region. Atoll Res Bull 507:1–19

    Google Scholar 

  19. D’Agostino D, Burt JA, Reader T, Vaughan GO, Chapman BB, Santinelli V, Cavalcante GH, Feary DA (2019) The influence of thermal extremes on coral reef fish behaviour in the Arabian/Persian Gulf. Coral Reefs

  20. de Bakker DM, van Duyl FC, Bak RPM, Nugues MM, Nieuwland G, Meesters EH (2017) 40 Years of benthic community change on the Caribbean reefs of Curaçao and Bonaire: the rise of slimy cyanobacterial mats. Coral Reefs 36:355–367

    Google Scholar 

  21. Dominici-Arosemena A, Wolff M (2006) Reef fish community structure in the Tropical Eastern Pacific (Panamá): living on a relatively stable rocky reef environment. Helgol Mar Res 60:287–305

    Google Scholar 

  22. Downing N (1985) Coral reef communities in an extreme environment: The Northwest Arabian Gulf. Proc 5th Int Coral Reef Congr 6: 343-348

  23. Edwards CB, Friedlander AM, Green AG, Hardt MJ, Sala E, Sweatman HP, Smith JE (2014) Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proc Biol Sci 281:20131835

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Endean R, Stablum W (1973) The apparent extent of recovery of reefs of Australia’s Great Barrier Reef devastated by the crown-of-thorns starfish. Atoll Res Bull 168:1–26

    Google Scholar 

  25. English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources. Australian Institute of Marine Science, Australia

    Google Scholar 

  26. Fatemi SMR, Shokri MR (2001) Iranian coral reefs status with particular reference to Kish Island, Persian Gulf. Inte Coral Reef Initiative (ICRI) Regional Workshop for the Indian Ocean, Maputo, Mozambique

  27. Feary DA, Burt JA, Cavalcante GH, Bauman AG (2012) Extreme physical factors and the structure of Gulf fish and reef communities. In: Riegl BM, Purkis SJ (eds) Coral reefs of the Gulf: adaptation to climatic extremes. Coral reefs of the world. 3: 163-170

  28. Floeter SR, Ferreira CEL, Dominici-Arosemena A, Zalmon IR (2004) Latitudinal gradients in Atlantic reef fish communities: trophic structure and spatial use patterns. J Fish Biol 64:1680–1699

    Google Scholar 

  29. Foster K, Foster G, Al-Cibahy A, Al-Harthi S, Purkis SJ, Riegl B (2012) Environmental setting and temporal trends in southeastern Gulf coral communities. In: Riegl B, Purkis S (eds) Coral reefs of the Gulf: Adaptation to climatic extremes. Coral reefs of the world 3: 51-70

  30. Frade PR, Bongaerts P, Englebert N, Rogers A, Gonzalez-Rivero M, Hoegh-Guldberg O (2018) Deep reefs of the Great Barrier Reef offer limited thermal refuge during mass coral bleaching. Nat Commun 9:3447

    PubMed  PubMed Central  Google Scholar 

  31. Garpe KC, Yahya SAS, Lindahl U, Öhman MC (2006) Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Mar Ecol Prog Ser 315:237–247

    Google Scholar 

  32. George JD, John DM (1999) High sea temperatures along the coast of Abu Dhabi (UAE), Arabian Gulf—their impact upon corals and macroalgae. Reef Encounter 25:21–23

    Google Scholar 

  33. George JD, John DM (2000) The coral reefs of Abu Dhabi, United Arab Emirates: past, present and future. Second Arab Int Conf Exhibition Env Biot (Coastal Habitats), Abu Dhabi, UAE, 8–12 April 2000, p 39

  34. George JD, John DM (2002) Is it curtains for coral reefs in the southern Arabian Gulf? In: Brooks S, Spencer T, Teleki K, Taylor M (eds). Int Soc Reef Stud Eur Meeting, Cambridge, 4–7 September 2002, p 36

  35. Ghazilou A, Shokri MR, Gladstone W (2016) Coral reef fish assemblages along a disturbance gradient in the northern Persian Gulf: a seasonal perspective. Mar Pollut Bull 105:599–605

    CAS  PubMed  Google Scholar 

  36. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Nat Acad Se 103:8425–8429

    CAS  Google Scholar 

  37. Graham NAJ, Chabanet P, Evans RD, Jennings S, Letourneur Y, MacNeil MA, McClanahan TR, Ohman MC, Polunin NVC, Wilson SK (2011) Extinction vulnerability of coral reef fishes. Ecol Lett 14:341–348

    PubMed  PubMed Central  Google Scholar 

  38. Grandcourt E (2012) Reef fish and fisheries in the Gulf. In: Riegl B, Purkis S (eds) Coral reefs of the Gulf: adaptation to climatic extremes. Coral reefs of the world 3: 127–161

  39. Gratwicke B, Speight M (2005) The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J Fish Biol 66:650–667

    Google Scholar 

  40. Hodgson G, Hill J, Kiene W, Maun L, Mihaly J, Liebeler J, Shuman C, Torres R (2006) Reef Check instruction manual: a guide to Reef Check coral reef monitoring. Reef Check Foundation, Pacific Palisades, California, USA, p 95

    Google Scholar 

  41. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JJB, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    CAS  Google Scholar 

  42. 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 CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo CY, 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 543:373–377

    CAS  PubMed  Google Scholar 

  43. Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Natl Acad Sci USA 101:8251–8253

    CAS  PubMed  Google Scholar 

  44. Jones GP, Syms C (1998) Disturbance, habitat structure and the ecology of fishes on coral reefs. Aus J Ecol 23:287–297

    Google Scholar 

  45. Keith SA, Baird AH, Hobbs JPA, Woolsey ES, Hoey AS, Fadli N, Sanders NJ (2018) Synchronous behavioural shifts in reef fishes linked to mass coral bleaching. Nat Clim Change 8:986–991

    Google Scholar 

  46. Krupp F, Muller T (1994) The status of fish populations in the northern Arabian Gulf two years after the 1991 GulfWar oil spill. Courier Forsch.-Inst. Senckenberg 166:67–75

    Google Scholar 

  47. Lamy T, Galzin R, Kulbicki M, Lison de Loma T, Claudet J (2016) Three decades of recurrent declines and recoveries in corals belie ongoing change in fish assemblages. Coral Reefs 35:293–302

    Google Scholar 

  48. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J of J Exp Mar Bio Ecol 375:1–8

    Google Scholar 

  49. Lieske E, Myers R (1996) Collins Pocket Guide. Harper Collins Publishers, Coral reef fishes. Indo-Pacific & Caribbean including the Red Sea

    Google Scholar 

  50. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163

    Google Scholar 

  51. McCain JC, Tarr AB, Carpenter KE, Coles SL (1984) Marine ecology of Saudi Arabia: a survey of coral reefs and reef fishes in the northern area, Arabian Gulf, Saudia Arabia. Fauna of Saudi Arabia 6:102–126

    Google Scholar 

  52. Mouillot D, Graham NAJ, Villéger S, Manson NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177

    PubMed  Google Scholar 

  53. Møller PR, Provença P, Kielgast J (2012) Fishes. In: Islamic Qatar (ed) Bangsgaard P, Kristensen RM, Møller PR, Nymann H. Archaeology and Heritage Project, End of season Report Environmental Studies, pp 46–61

    Google Scholar 

  54. Munday PL (2004) Habitat loss, resource specialization, and extinction on coral reefs. Glob Chang Biol 10:1642–1647. https://doi.org/10.1111/j.1365-2486.2004.00839.x

    Article  Google Scholar 

  55. Munday P, Jones G, Pratchett M, Williams A (2008) Climate change and the future for coral reef fishes. Fish Fish 9:261–285

    Google Scholar 

  56. Paparella F, Xu C, Vaughan GO, Burt JA (2019) Coral bleaching in the Persian/Arabian Gulf is modulated by summer winds. Front Mar Sci 6:205

    Google Scholar 

  57. Pereira P, Macedo C, Nunes J, de Barros Fernandes, Marangoni L, Bianchini A (2018) Effects of depth on reef fish communities: insights of a “deep refuge hypothesis” from Southwestern Atlantic reefs. PLoS One 13:e0203072

    PubMed  PubMed Central  Google Scholar 

  58. Pratchett MS (2005) Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar Biol 148:373–382

    Google Scholar 

  59. Pratchett MS, Hoey AS, Wilson SK, Messmer V, Graham NA (2011) Changes in biodiversity and functioning of reef fish assemblages following coral bleaching and coral loss. Diversity 3:424–452

    Google Scholar 

  60. Pratchett MS, Hoey AS, Feary DA, Bauman AG, Burt JA, Riegl BM (2013) Functional composition of Chaetodon butterflyfishes at a peripheral and extreme coral reef location, the Persian Gulf. Mar Pollut Bull 72:333–341

    CAS  PubMed  Google Scholar 

  61. Pratchett MS, Munday PL, Wilson SK, Graham NAJ, Cinner JE, Bellwood DR, Jones GP, Polunin NVC, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes—Ecological and economic consequences. Oceanogr Mar Biol 46:251–296

    Google Scholar 

  62. Pratchett MS, Wilson SK, Baird AH (2006) Declines in the abundance of Chaetodon butterflyfishes following extensive coral depletion. J Fish Biol 69:1269–1280

    Google Scholar 

  63. Reynolds RM (1993) Physical oceanography of the Gulf, Straits of Hormuz, and the Gulf of Oman: results from the Mt.Mitchell Expedition. Mar Pollut Bull 27:35–59

    Google Scholar 

  64. Rezai H, Wilson S, Claereboudt M, Riegl B (2004) Coral reef status in ROPME Sea area. In: Wilkinson CR (ed) Status of coral reefs of the world. Australian Institute of Marine Science, Townsville, pp 155–170

    Google Scholar 

  65. Riegl B (2002) Effects of the 1996 and 1998 positive sea-surface temperature anomalies on corals, coral diseases and fish in the Arabian Gulf (Dubai, UAE). Mar Biol 140:29–40

    Google Scholar 

  66. Riegl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. Int J Earth Sci 92:520–531

    Google Scholar 

  67. Riegl B, Purkis S (2015) Coral population dynamics across consecutive mass mortality events. Glob Change Biol 21:3995–4005

    Google Scholar 

  68. Riegl B, Johnston M, Purkis S, Howells E, Burt J, Steiner SCC, Sheppard CRC, Bauman A (2018) Population collapse dynamics in Acropora downingi, an Arabian/Persian Gulf ecosystem-engineering coral, linked to rising temperature. Glob Change Biol 24:2447–2462

    Google Scholar 

  69. Rogers A, Blanchard J, Mumby P (2014) Vulnerability of coral reef fisheries to a loss of structural complexity. Curr Biol 24:1000–1005

    CAS  PubMed  Google Scholar 

  70. Russ GR, Leahy SM (2017) Rapid decline and decadal-scale recovery of corals and Chaetodon butterflyfish on Philippine coral reefs. Mar Biol 164:29

    Google Scholar 

  71. Samways MJ (2005) Breakdown of butterflyfish (Chaetodontidae) territories associated with the onset of a mass coral bleaching event. Aquat Conserv 15:S101–S107

    Google Scholar 

  72. Sano M, Shimizu M, Nose Y (1984) Changes in structure of coral reef fish communities by the destruction of hermatypic corals: observational and experimental views. Pac Sci 38:51–79

    Google Scholar 

  73. Sano M, Shimizu M, Nose Y (1987) Long-term effects of destruction of hermatypic corals by Acanthaster planci infestation on reef fish communities at Iriomote Island, Japan. Mar Ecol Prog Ser 37:191–199

    Google Scholar 

  74. Shallard and Associates (2003) Distribution and abundance of demersal fish stocks in the UAE. Technical Report 1. Fish Resource Assessment Survey Project of Abu Dhabi and UAE Waters, Bruce Shallard and Associates and Government of Abu Dhabi, p 211

  75. Sheppard C, Loughland R (2002) Coral mortality and recovery in response to increasing temperature in the southern Arabian Gulf. Aquat Ecosyst Health Manag 5:395–402

    Google Scholar 

  76. Shokri MR, Mohammadi M, Bargahi H (2019) Tourism carrying capacity assessment of diving sites in Kish Island. Free Trade Zone of Kish Island, Kish Island, Iran, p 245

    Google Scholar 

  77. Shokri MR, Fatemi SMR, Crosby MP (2005) The status of butterflyfishes (Chaetodontidae) in the northern Persian Gulf, I.R. Iran. Aquat Conserv 15:S91–S99

    Google Scholar 

  78. Shuail D, Wiedenmann J, D’Angelo C, Baird AH, Pratchett MS, Riegl B, Burt JA, Petrov P, Amos C (2016) Local bleaching thresholds established by remote sensing techniques vary among reefs with deviating bleaching patterns during the 2012 event in the Arabian/Persian Gulf. Mar Pollut Bull 105:654–659

    CAS  PubMed  Google Scholar 

  79. Smith G, Saleh M, Sangoor K (1987) The reef ichthyofauna of Bahrain (Arabian Gulf) with comments on its zoogeographic affinities. Arab Gulf J Scient Res Agri Biol Sci 5:127–146

    Google Scholar 

  80. Shraim R, Dieng MM, Vinu M, Vaughan G, McParland D, Idaghdour Y, Burt JA (2017) Environmental extremes are associated with dietary patterns in Arabian Gulf reef fishes. Front Mar Sci 4

  81. Vaughan GO, Al-Mansoori N, Burt JA (2019) The Arabian Gulf. In: Sheppard C (eds) World Seas: An environmental evaluation. Academic Press

  82. Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Polunin NVC (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob Chang Biol 12:2220–2234

    Google Scholar 

  83. Wilson SK, Fisher R, Pratchett MS, Graham NAJ, Dulvy NK, Turner RA, Cakacaka A, Polunin NVC, Rushton SP (2008) Exploitation and habitat degradation as agents of change within coral reef fish communities. Glob Chang Biol 14:2796–2809

    Google Scholar 

  84. Wilson SK, Dolman AM, Cheal AJ, Emslie MJ, Pratchett MS, Sweatman HPA (2009) Maintenance of fish diversity on disturbed coral reefs. Coral Reefs 28:3–14

    Google Scholar 

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Acknowledgments

The authors wish to thank Dr. H. Rezai for his scientific advice. We also thank Ms. Maryam Mohammadi and her colleagues at the Department of the Environment of Kish Free Zone Organization for their support.

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HRB conceived and designed the experiments; HRB and MRS performed the experiments; MRS analyzed the data; MRS wrote the paper; HRB, FK, and MRF commented on the drafts of the paper

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Correspondence to Hamid Reza Bargahi.

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Bargahi, H.R., Shokri, M.R., Kaymaram, F. et al. Changes in reef fish assemblages following multiple bleaching events in the world’s warmest sea (Kish Island, the Persian Gulf). Coral Reefs 39, 603–624 (2020). https://doi.org/10.1007/s00338-020-01945-3

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Keywords

  • Reef fish
  • Community composition
  • Coral bleaching
  • Habitat loss
  • Climate change