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.
References
Almany GR (2004a) Does increased habitat complexity reduce predation and competition in coral reef fish assemblages? Oikos 106:275–285
Almany GR (2004b) Differential effects of habitat complexity, predators and competitors on abundance of juvenile and adult coral reef fishes. Oecologia 141:105–113
Arthur R (2000) Coral bleaching and mortality in three Indian reef regions during an El Niño southern oscillation event. Curr Sci (Bangalore) 79:1723–1729
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) 89:694–699
Arthur R, Done TJ, Marsh H, Harriott V (2006) Local processes strongly influence postbleaching benthic recovery in the Lakshadweep Atolls. Coral Reefs 25:427–440
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 115–127
Bates D, Maechler M, Bolker B (2012) Linear mixed-effects models using S4 classes. R Package version 0.99-0
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 170:567–573
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
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 299:155–184
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 258–267
Bolker B, Skaug H, Magnusson A, Nielsen A (2012) Generalized Linear Mixed Models using AD Model Builder. R package version 0.6.5
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
Caley MJ, John JST (1996) Refuge availability structures assemblages of tropical reef fishes. J Anim Ecol 65:414–428
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 198:261–272
Chollett I, Mumby PJ (2012) Predicting the distribution of Montastraea reefs using wave exposure. Coral Reefs 31:493–503
Crawley MJ (2007) The R book. John Wiley & Sons, Ltd. Chichester: West Sussex PO19 8SQ, England
Done T (1999) Coral community adaptability to environmental change at the scales of regions, reefs and reef zones. Am Zool 39:66–79
Dulvy NK, Freckelton RP, Polunin NVC (2004a) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416
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 61:466–475
Feary D, Almany GR, McCormick MI, Jones GP (2007) Habitat choice, recruitment and the response of coral reef fishes to coral degradation. Oecologia 153:727–737
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 78:147–160
Friedlander AM, Parrish JD (1998) Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J Exp Mar Biol Ecol 224:1–30
Froese R, Pauly D (eds) (2012) FishBase. World Wide Web electronic publication. www.fishbase.org, version (08/2012)
Fulton EA (2011) Interesting times: winners, losers and system shifts under climate change around Australia. ICES J Mar Sci 68:1329–1342
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
Goeden GB (1989) Intensive fishing and a “keystone” predator species: Ingredients for community instability. Biol Conserv 22:273–281
Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326
Graham NAJ, Nash KL, Kool JT (2011) Coral reef dynamics in a changing world. Coral Reefs 30:283–294
Grandcourt E (2005) Demographic characteristics of selected epinepheline groupers (family: Serranidae; subfamily: Epinephelinae) from Aldabra Atoll, Seychelles. Atoll Res Bull 593:200–216
Gust N (2002) Scarid biomass on the northern Great Barrier Reef: the influence of exposure, depth and substrata. Environ Biol Fish 64:353–366
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 85:1892–1905
Harmelin JG, Harmelin-Vivien M (1999) A review on habitat, diet and growth of the dusky grouper Epinephelus marginatus (Lowe, 1834). Mar Life 9:11–20
Heithaus MR, Alejandro F, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210
Hixon MA, Beets JP (1993) Predation, prey refuges and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101
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 318:1737–1742
Hornell J (1910) Report on the results of a fishery cruise along the Malabar Coast and the Laccadive Islands in 1908. Madras Fisheries Bulletin 4:71–126
James PSBR, Pillai CSG, Pillai PP, Livingston P, Mohan M (1986) Marine fisheries research in Lakshadweep - a historical resume. Mar Fish Inf Serv 68:7–9
Jones S, Kumaran M (1959) The fishing industry of Minicoy Island with special reference to the tuna fishery. Indian J Fish 6:30–57
Kerry JT, Bellwood DR (2012) The effect of coral morphology on shelter selection by coral reef fishes. Coral Reefs 31:415–424
Lieske E, Myers R (2002) Coral reef fishes: Indo-Pacific and Caribbean. Princeton Pocket Guides, Princeton University Press
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 16:731–746
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
Luckhurst BE, Luckhurst K (1978) Analysis of influence of substrate variables on coral-reef fish communities. Mar Biol 49:317–323
MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42:594–598
Madin JS, Connolly SR (2006) Ecological consequences of major hydrodynamic disturbances on coral reefs. Nature 444:477–480
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 21:186–198
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 337:1–13
Myers AR, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283
Newton K, Côté IM, Pilling GM, Jennings S, Dulvy NK (2007) Current and future sustainability of island coral reef fisheries. Curr Biol 17:655–658
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, Switzerland
Paine RT, Tegner MJ, Johnson EA (1998) Compounded perturbations yield ecological surprises. Ecosystems 1:535–545
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 301:955–959
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 307:259–272
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 68:25–32
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 3.1-104
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/
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 17:399–416
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 68:93–99
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 14:1–18
Samoilys MA (1997) Movement in a large predatory fish: coral trout, Plectropomus leopardus (Pisces: Serranidae), on Heron Reef, Australia. Coral Reefs 16:151–158
Sano M (2000) Stability of reef fish assemblages: responses to coral recovery after catastrophic predation by Acanthaster planci. Mar Ecol Prog Ser 198:121–130
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 36
Shanker D, Vinayachandran PN, Unnikrishnan AS, Shetye AR (2001) The monsoon currents in the north Indian Ocean. Prog Oceanogr 52:63–119
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 362:109–117
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 55:218–237
Shpigel M, Fishelson L (1989) Food habits and prey selection of three species of groupers from the genus Cephalopholis (Serranidae: Teleostei). Environ Biol Fish 24:67–73
Siddiquie HN (1980) The ages of the storm beaches of the Lakshadweep (Laccadives). Mar Geol 38:11–20
Sluka RD (2000) Grouper and napoleon wrasse ecology in Laamu atoll, republic of Maldives: part 1. Habitat, behavior, and movement patterns. Atoll Res Bull 491:1–26
Sluka R, Reichenbach N (1996) The density and diversity of groupers at two sites in the Republic of Maldives. Atoll Res Bull 438:1–16
Southwood TRE (1977) Habitat, the templet for ecological strategies? J Anim Ecol 46:337–365
Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. Univ of California Press, pp 215–217
Syms C (1995) Multi-scale analysis of habitat association in a guild of blennioid fishes. Mar Ecol Prog Ser 125:31–43
Syms C, Jones GP (2000) Disturbance, habitat structure, and the dynamics of a coral-reef fish community. Ecology 81:2714–2729
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, Mombasa
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 152:243–254
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
West JM, Salm RV (2003) Resistance and resilience to coral bleaching: Implications for coral reef conservation and management. Conserv Biol 17:956–967
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 12:2220–2234
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 14:2796–2809
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/
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York, NY
Acknowledgments
We would like to thank the Lakshadweep Administration, Department of Environment and Forests, Department of Fisheries and the Department of Science and Technology for permits and logistic support. In addition, we thank Lacadives, Department of tourism (SPORTS) and supporters in the Lakshadweep: J. Hisham, Idris B., and Ibrahim M.K. For support and critical feedback, we thank Dr. K. Shanker, M.D. Madhusudan and Dr. Howells. We would also like to thank two anonymous reviewers, the editor and T.R. Shankar Raman for their critical inputs to improving the MS. This study was conducted with funding and in-kind support from Rufford Small Grants Foundation, National Geographic and Idea Wild.
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Karkarey, R., Kelkar, N., Lobo, A.S. et al. Long-lived groupers require structurally stable reefs in the face of repeated climate change disturbances. Coral Reefs 33, 289–302 (2014). https://doi.org/10.1007/s00338-013-1117-y
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DOI: https://doi.org/10.1007/s00338-013-1117-y