Coral Reefs

, Volume 33, Issue 2, pp 289–302 | Cite as

Long-lived groupers require structurally stable reefs in the face of repeated climate change disturbances

  • R. Karkarey
  • N. Kelkar
  • A. Savio Lobo
  • T. Alcoverro
  • R. Arthur
Report

Abstract

Benthic recovery from climate-related disturbances does not always warrant a commensurate functional recovery for reef-associated fish communities. Here, we examine the distribution of benthic groupers (family Serranidae) in coral reef communities from the Lakshadweep archipelago (Arabian Sea) in response to structural complexity and long-term habitat stability. These coral reefs that have been subject to two major El Niño Southern Oscillation-related coral bleaching events in the last decades (1998 and 2010). First, we employ a long-term (12-yr) benthic-monitoring dataset to track habitat structural stability at twelve reef sites in the archipelago. Structural stability of reefs was strongly driven by exposure to monsoon storms and depth, which made deeper and more sheltered reefs on the eastern aspect more stable than the more exposed (western) and shallower reefs. We surveyed groupers (species richness, abundance, biomass) in 60 sites across the entire archipelago, representing both exposures and depths. Sites were selected along a gradient of structural complexity from very low to high. Grouper biomass appeared to vary with habitat stability with significant differences between depth and exposure; sheltered deep reefs had a higher grouper biomass than either sheltered shallow or exposed (deep and shallow) reefs. Species richness and abundance showed similar (though not significant) trends. More interestingly, average grouper biomass increased exponentially with structural complexity, but only at the sheltered deep (high stability) sites, despite the availability of recovered structure at exposed deep and shallow sites (lower-stability sites). This trend was especially pronounced for long-lived groupers (life span >10 yrs). These results suggest that long-lived groupers may prefer temporally stable reefs, independent of the local availability of habitat structure. In reefs subject to repeated disturbances, the presence of structurally stable reefs may be critical as refuges for functionally important, long-lived species like groupers.

Keywords

Coral reefs Structural change Habitat stability Natural refugia Groupers 

Supplementary material

338_2013_1117_MOESM1_ESM.doc (104 kb)
Supplementary material 1 (DOC 104 kb)

References

  1. Almany GR (2004a) Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106:275–285CrossRefGoogle Scholar
  2. Almany GR (2004b) Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141:105–113PubMedCrossRefGoogle Scholar
  3. Arthur R (2000) Coral bleaching and mortality in three Indian reef regions during an El Niño southern oscillation event. Curr Sci (Bangalore) 79:1723–1729Google Scholar
  4. Arthur R, Done TJ, Marsh H (2005) Benthic recovery four years after an El-Nino-induced coral mass mortality in the Lakshadweep atolls. Curr Sci (Bangalore) 89:694–699Google Scholar
  5. Arthur R, Done TJ, Marsh H, Harriott V (2006) Local processes strongly influence postbleaching benthic recovery in the Lakshadweep Atolls. Coral Reefs 25:427–440CrossRefGoogle Scholar
  6. Auster, PJ (2005) Predatory behavior of piscivorous reef fishes varies with changes in landscape attributes and social context: integrating natural history observations in a conceptual model. In: Diving for Science 2005, Proceedings of the American Academy of Underwater Sciences, Connecticut Sea Grant, Groton, pp 115–127Google Scholar
  7. Bates D, Maechler M, Bolker B (2012) Linear mixed-effects models using S4 classes. R Package version 0.99-0Google Scholar
  8. Bellwood DR, Baird AH, Depczynski M, González-Cabello A, Hoey AS (2012) Coral recovery may not herald the return of fishes on damaged coral reefs. Oecologia 170:567–573PubMedCrossRefGoogle Scholar
  9. 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 25:647–653CrossRefGoogle Scholar
  10. Beukers-Stewart BD, Jones GP (2004) The influence of prey abundance on the feeding ecology of two piscivorous species of coral reef fish. J Exp Mar Biol Ecol 299:155–184CrossRefGoogle Scholar
  11. Bohnsack JA (1982) Effects of piscivorous predator removal on coral reef fish community structure. In: Cailliet GM, Simenstad CA (eds) Gutshop ‘81: Fish food habits studies. Washington Sea Grant Publication, Seattle, Washington, pp 258–267Google Scholar
  12. Bolker B, Skaug H, Magnusson A, Nielsen A (2012) Generalized Linear Mixed Models using AD Model Builder. R package version 0.6.5Google Scholar
  13. Cabanban AS, Myers R, Yeeting B, Pollard D, Kulbicki M, Fennessy S (2008) Cephalopholis sexmaculata. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1 www.iucnredlist.org. Downloaded on 18 September 2012
  14. Caley MJ, John JST (1996) Refuge availability structures assemblages of tropical reef fishes. J Anim Ecol 65:414–428CrossRefGoogle Scholar
  15. Chiappone M, Sluka R, Sullivan KS (2000) Groupers (Pisces: Serranidae) in fished and protected areas of the Florida Keys, Bahamas and northern Caribbean. Mar Ecol Prog Ser 198:261–272CrossRefGoogle Scholar
  16. Chollett I, Mumby PJ (2012) Predicting the distribution of Montastraea reefs using wave exposure. Coral Reefs 31:493–503CrossRefGoogle Scholar
  17. Crawley MJ (2007) The R book. John Wiley & Sons, Ltd. Chichester: West Sussex PO19 8SQ, EnglandGoogle Scholar
  18. Done T (1999) Coral community adaptability to environmental change at the scales of regions, reefs and reef zones. Am Zool 39:66–79Google Scholar
  19. Dulvy NK, Freckelton RP, Polunin NVC (2004a) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416CrossRefGoogle Scholar
  20. Dulvy NK, Polunin NVC, Mill AC, Graham NAJ (2004b) Size structural change in lightly exploited coral reef fish communities: evidence for weak indirect effects. Can J Fish Aquat Sci 61:466–475CrossRefGoogle Scholar
  21. Feary D, Almany GR, McCormick MI, Jones GP (2007) Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153:727–737PubMedCrossRefGoogle Scholar
  22. Floeter SR, Krohling W, Gasparini JL, Ferreira CEL, Zalmon IR (2007) Reef fish community structure on coastal islands of the southeastern Brazil: the influence of exposure and benthic cover. Environ Biol Fish 78:147–160CrossRefGoogle Scholar
  23. Friedlander AM, Parrish JD (1998) Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J Exp Mar Biol Ecol 224:1–30CrossRefGoogle Scholar
  24. Froese R, Pauly D (eds) (2012) FishBase. World Wide Web electronic publication. www.fishbase.org, version (08/2012)
  25. Fulton EA (2011) Interesting times: winners, losers and system shifts under climate change around Australia. ICES J Mar Sci 68:1329–1342CrossRefGoogle Scholar
  26. 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 315:237–247CrossRefGoogle Scholar
  27. Goeden GB (1989) Intensive fishing and a “keystone” predator species: Ingredients for community instability. Biol Conserv 22:273–281CrossRefGoogle Scholar
  28. Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326CrossRefGoogle Scholar
  29. Graham NAJ, Nash KL, Kool JT (2011) Coral reef dynamics in a changing world. Coral Reefs 30:283–294CrossRefGoogle Scholar
  30. Grandcourt E (2005) Demographic characteristics of selected epinepheline groupers (family: Serranidae; subfamily: Epinephelinae) from Aldabra Atoll, Seychelles. Atoll Res Bull 593:200–216Google Scholar
  31. Gust N (2002) Scarid biomass on the northern Great Barrier Reef: the influence of exposure, depth and substrata. Environ Biol Fish 64:353–366CrossRefGoogle Scholar
  32. Halford A, Cheal AJ, Ryan D, Williams DMCB (2004) Resilience to large-scale disturbance in coral and fish assemblages on the Great Barrier Reef. Ecology 85:1892–1905CrossRefGoogle Scholar
  33. Harmelin JG, Harmelin-Vivien M (1999) A review on habitat, diet and growth of the dusky grouper Epinephelus marginatus (Lowe, 1834). Mar Life 9:11–20Google Scholar
  34. Heithaus MR, Alejandro F, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210PubMedCrossRefGoogle Scholar
  35. Hixon MA, Beets JP (1993) Predation, prey refuges and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101CrossRefGoogle Scholar
  36. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  37. Hornell J (1910) Report on the results of a fishery cruise along the Malabar Coast and the Laccadive Islands in 1908. Madras Fisheries Bulletin 4:71–126Google Scholar
  38. James PSBR, Pillai CSG, Pillai PP, Livingston P, Mohan M (1986) Marine fisheries research in Lakshadweep - a historical resume. Mar Fish Inf Serv 68:7–9Google Scholar
  39. Jones S, Kumaran M (1959) The fishing industry of Minicoy Island with special reference to the tuna fishery. Indian J Fish 6:30–57Google Scholar
  40. Kerry JT, Bellwood DR (2012) The effect of coral morphology on shelter selection by coral reef fishes. Coral Reefs 31:415–424CrossRefGoogle Scholar
  41. Lieske E, Myers R (2002) Coral reef fishes: Indo-Pacific and Caribbean. Princeton Pocket Guides, Princeton University PressGoogle Scholar
  42. Lindberg WJ, Frazer TK, Portier KM, Vose F, Loftin J, Murie DJ, Mason DM, Nagy B, Hart MK (2006) Density-dependent habitat selection and performance by a large mobile reef fish. Ecol Appl 16:731–746PubMedCrossRefGoogle Scholar
  43. Liu M, Choat JH (2008) Cephalopholis argus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. www.iucnredlist.org. Downloaded on 18 September 2012
  44. Luckhurst BE, Luckhurst K (1978) Analysis of influence of substrate variables on coral-reef fish communities. Mar Biol 49:317–323CrossRefGoogle Scholar
  45. MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42:594–598CrossRefGoogle Scholar
  46. Madin JS, Connolly SR (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480PubMedCrossRefGoogle Scholar
  47. McClanahan TR (2011) Coral reef fish communities in management systems with unregulated fishing and small fisheries closures compared with lightly fished reefs–Maldives vs. Kenya. Aquat Conserv: Mar Freshw Ecosyst 21:186–198CrossRefGoogle Scholar
  48. McClanahan TR, Ateweberhan M, Graham NAJ, Wilson SK, Sebastian CR, Guillaume MMM, Bruggemann JH (2007) Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Mar Ecol Prog Ser 337:1–13CrossRefGoogle Scholar
  49. Myers AR, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283PubMedCrossRefGoogle Scholar
  50. Newton K, Côté IM, Pilling GM, Jennings S, Dulvy NK (2007) Current and future sustainability of island coral reef fisheries. Curr Biol 17:655–658PubMedCrossRefGoogle Scholar
  51. Obura DO, Grimsdith G (2009) Resilience assessment of coral reefs-Assessment protocol for coral reefs, focusing on coral bleaching and thermal stress. IUCN working group on Climate Change and Coral Reefs. IUCN, Gland, SwitzerlandGoogle Scholar
  52. Paine RT, Tegner MJ, Johnson EA (1998) Compounded perturbations yield ecological surprises. Ecosystems 1:535–545CrossRefGoogle Scholar
  53. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–959PubMedCrossRefGoogle Scholar
  54. Pears RJ, Choat HJ, Mapstone BD, Begg GA (2006) Demography of a large grouper, Epinephelus fuscoguttatus from Australia’s Great Barrier Reef: implications for fishery management. Mar Ecol Prog Ser 307:259–272CrossRefGoogle Scholar
  55. Pillai PP, Kumaran M, Pillai CSG, Mohan M, Gopakumar G, Livingston P, Srinath M (1986) Exploited and potential resources of live-bait fishes of Lakshadweep. Mar Fish Inf Serv 68:25–32Google Scholar
  56. Pinheiro J, Bates D, DebRoy S, Sarkar D and the R Development Core Team (2012) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-104Google Scholar
  57. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
  58. Russ GR, Alcala AC (1998) Natural fishing experiments in marine reserves 1983-1993: roles of life history and fishing intensity in family responses. Coral Reefs 17:399–416CrossRefGoogle Scholar
  59. Sabetian A (2003) The association of physical and environmental factors with abundance and distribution patterns of groupers around Kolombangara Island, Solomon Islands. Environ Biol Fish 68:93–99CrossRefGoogle Scholar
  60. Sadovy de Mitcheson Y, Craig MT, Bertoncini AA, Carpenter KE, Cheung WWL, Choat JH, Cornish AS, Fennessy ST, Ferreira BP, Heemstra PC, Liu M, Myers RF, Pollard DA, Rhodes KL, Rocha LA, Russell BC, Samoilys MA, Sanciangco J (2012) Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish Fish 14:1–18Google Scholar
  61. Samoilys MA (1997) Movement in a large predatory fish: coral trout, Plectropomus leopardus (Pisces: Serranidae), on Heron Reef, Australia. Coral Reefs 16:151–158CrossRefGoogle Scholar
  62. Sano M (2000) Stability of reef fish assemblages: responses to coral recovery after catastrophic predation by Acanthaster planci. Mar Ecol Prog Ser 198:121–130CrossRefGoogle Scholar
  63. Sattar SA, Najeeb A, Afzal MS, Islam F, Wood E (2011) Review of the Maldivian grouper fishery and export industry. Darwin Research Project, Marine Research Centre/Marine Conservation Society, UK, p 36Google Scholar
  64. Shanker D, Vinayachandran PN, Unnikrishnan AS, Shetye AR (2001) The monsoon currents in the north Indian Ocean. Prog Oceanogr 52:63–119CrossRefGoogle Scholar
  65. Sheppard CRC, Harris A, Sheppard ALS (2008) Archipelago-wide coral recovery patterns since 1998 in the Chagos Archipelago, central Indian Ocean. Mar Ecol Prog Ser 362:109–117CrossRefGoogle Scholar
  66. Shibuno T, Nakamura Y, Horinouchi M, Sano M (2008) Habitat use patterns of fishes across the mangrove-seagrass-coral reef seascape at Ishigaki Atoll, southern Japan. Ichthyol Res 55:218–237CrossRefGoogle Scholar
  67. Shpigel M, Fishelson L (1989) Food habits and prey selection of three species of groupers from the genus Cephalopholis (Serranidae: Teleostei). Environ Biol Fish 24:67–73CrossRefGoogle Scholar
  68. Siddiquie HN (1980) The ages of the storm beaches of the Lakshadweep (Laccadives). Mar Geol 38:11–20CrossRefGoogle Scholar
  69. Sluka RD (2000) Grouper and napoleon wrasse ecology in Laamu atoll, republic of Maldives: part 1. Habitat, behavior, and movement patterns. Atoll Res Bull 491:1–26CrossRefGoogle Scholar
  70. Sluka R, Reichenbach N (1996) The density and diversity of groupers at two sites in the Republic of Maldives. Atoll Res Bull 438:1–16Google Scholar
  71. Southwood TRE (1977) Habitat, the templet for ecological strategies? J Anim Ecol 46:337–365CrossRefGoogle Scholar
  72. Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. Univ of California Press, pp 215–217Google Scholar
  73. Syms C (1995) Multi-scale analysis of habitat association in a guild of blennioid fishes. Mar Ecol Prog Ser 125:31–43CrossRefGoogle Scholar
  74. Syms C, Jones GP (2000) Disturbance, habitat structure, and the dynamics of a coral-reef fish community. Ecology 81:2714–2729CrossRefGoogle Scholar
  75. Tamelander J, Hoon V (2008) The artisanal reef fishery on Agatti Island, Union Territory of Lakshadweep, India. In: Obura D, Tamelander J and Linden O (eds) Ten years after bleaching–facing the consequences of climate change in the Indian Ocean. CORDIO Status Report 2008. CORDIO (Coastal Oceans Research and Development, Indian Ocean)/Sida-SAREC, MombasaGoogle Scholar
  76. Unsworth RKF, Powell A, Hukom F, Smith DJ (2007) The ecology of Indo-Pacific grouper (Serranidae) species and the effects of a small scale no take area on grouper assemblage, abundance and size frequency distribution. Mar Biol 152:243–254CrossRefGoogle Scholar
  77. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  78. West JM, Salm RV (2003) Resistance and resilience to coral bleaching: Implications for coral reef conservation and management. Conserv Biol 17:956–967CrossRefGoogle Scholar
  79. 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? Global Change Biol 12:2220–2234CrossRefGoogle Scholar
  80. 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. Global Change Biol 14:2796–2809CrossRefGoogle Scholar
  81. Zeileis A, Kleiber C, Jackman S (2008) Regression Models for Count Data in R. Journal of Statistical Software, 27(8). URL http://www.jstatsoft.org/v27/i08/
  82. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, NYCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • R. Karkarey
    • 1
  • N. Kelkar
    • 1
  • A. Savio Lobo
    • 1
  • T. Alcoverro
    • 1
    • 2
  • R. Arthur
    • 1
  1. 1.Nature Conservation FoundationMysoreIndia
  2. 2.Department of Marine EcologyCentre d’Estudis Avançats de Blanes (CEAB, CSIC)BlanesSpain

Personalised recommendations