Abstract
Coral bleaching and related reef degradation have caused significant declines in the abundance of reef-associated fishes. Most attention on the effects of bleaching has focused on corals, but bleaching is also prevalent in other cnidarians, including sea anemones. The consequences of anemone bleaching are unknown, and the demographic effects of bleaching on associated fish recruitment, survival, and reproduction are poorly understood. We examined the effect of habitat degradation including host anemone bleaching on fish abundance, egg production, and recruitment of the panda anemonefish (Amphiprion polymnus) near Port Moresby, Papua New Guinea. Following a high-temperature anomaly in shallow waters of the region, most shallow anemones to a depth of 6 m (approximately 35% of all the anemones in this area) were severely bleached. Anemone mortality was low but bleached anemones underwent a ~34% reduction in body size. Total numbers of A. polymnus were not affected by bleaching and reduction in shelter area. While egg production of females living in bleached anemones was reduced by ~38% in 2009 compared to 2008, egg production of females on unbleached anemones did not differ significantly between years. Total recruitment in 2009 was much lower than in 2008. However, we found no evidence of recruiting larvae avoiding bleached anemones at settlement suggesting that other factors or different chemical cues were more important in determining recruitment than habitat quality. These results provide the first field evidence of detrimental effects of climate-induced bleaching and habitat degradation on reproduction and recruitment of anemonefish.
References
Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42
Adjeroud M, Augustin D, Galzin R, Salvat B (2002) Natural disturbances and interannual variability of coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997. Mar Ecol Prog Ser 237:121–131
Allen GR (1972) Anemonefishes: their classification and biology. TFH Publications, Neptune City, NJ
Arvedlund M, Nielsen LE (1996) Do the anemonefish Amphiprion ocellaris (Pisces: Pomacentridae) imprint themselves to their host sea anemone Heteractis magnifica (Anthozoa: Actinidae)? Ethology 102:197–211
Arvedlund M, McCormick MI, Fautin DG, Bildsoe M (1999) Host recognition and possible imprinting in the anemonefish Amphiprion melanopus (Pisces: Pomacentridae). Mar Ecol Prog Ser 188:207–218
Beldade R, Holbrook S, Schmitt R, Planes S, Bernardi G (2009) Isolation and characterization of eight polymorphic microsatellite markers from the orange-fin anemonefish, Amphiprion chrysopterus. Conserv Genet Res 1:333–335
Bellwood DR, Hoey AS, Ackerman JL, Depczynski M (2006) Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Global Change Biol 12:1587–1594
Bonin MC, Munday PL, McCormick MI, Srinivasan M, Jones GP (2009) Coral-dwelling fishes resistant to bleaching but not to mortality of host corals. Mar Ecol-Prog Ser 394:215–222
Booth DJ (1992) Larval settlement patterns and preferences by domino damselfish, Dascyllus albisella Gill. J Exp Mar Biol Ecol 155:85–104
Booth DJ, Bereta GA (2002) Changes in a fish assemblage after a coral bleaching event. Mar Ecol Prog Ser 245:205–212
Buston PM (2003a) Forcible eviction and prevention of recruitment in the clown anemonefish. Behav Ecol 14:576–582
Buston PM (2003b) Mortality is associated with social rank in the clown anemonefish (Amphiprion percula). Mar Biol 143:811–815
Buston PM, García MB (2007) An extraordinary life span estimate for the clown anemonefish Amphiprion percula. J Fish Biol 70:1710–1719
Buston PM, Bogdanowicz SM, Wong A, Harrison RG (2007) Are clownfish groups composed of close relatives? An analysis of microsatellite DNA variation in Amphiprion percula. Mol Ecol 16:3671–3678
Coker DJ, Pratchett MS, Munday PL (2009) Coral bleaching and habitat degradation increase susceptibility to predation for coral-dwelling fishes. Behav Ecol 20:1204–1210
Cole AJ, Pratchett MS, Jones GP (2009) Effects of coral bleaching on the feeding response of two species of coral-feeding fish. J Exp Mar Biol Ecol 373:11–15
Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS, Srinivasan M, Syms C, Thorrold SR (2008) Coral reef fish smell leaves to find island homes. Proc R Soc B 275:2831–2839
Donelson JM, McCormick MI, Munday PL (2008) Parental condition affects early life-history of a coral reef fish. J Exp Mar Biol Ecol 360:109–116
Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc Nat Acad Sci USA 104:5483–5488
Elliott JK, Elliott JM, Mariscal RN (1995) Host selection, location, and association behaviors of anemonefishes in field settlement experiments. Mar Biol 122:377–389
Emslie MJ, Cheal AJ, Sweatman H, Delean S (2008) Recovery from disturbance of coral and reef fish communities on the Great Barrier Reef, Australia. Mar Ecol-Prog Ser 371:177–190
Fautin DC, Allen GR (1992) Field guide to anemonefishes and their host sea anemones. Western Australia Museum, Perth
Feary DA, Almany GR, Jones GP, McCormick MI (2007) Coral degradation and structure of tropical reef fish communities. Mar Ecol Prog Ser 333:243–248
Gagliano M, McCormick MI (2007) Maternal condition influences phenotypic selection on offspring. J Anim Ecol 76:174–182
Garpe KC, Yahya SAS, Lindahl U, Ohman MC (2006) Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Mar Ecol-Prog Ser 315:237–247
Gerber S, Chabrier P, Kremer A (2003) FAMOZ: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol Ecol Notes 3:479–481
Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17
Green BS, McCormick MI (2005a) O2 replenishment to fish nests: males adjust brood care to ambient conditions and brood development. Behav Ecol 16:389–397
Green BS, McCormick MI (2005b) Maternal and paternal effects determine size, growth and performance in larvae of a tropical reef fish. Mar Ecol Prog Ser 289:263–272
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933
Jones GP, McCormick MI, Srinivasan M, Eagle JV (2004) Coral decline threatens fish biodiversity in marine reserves. Proc Nat Acad Sci USA 101:8251–8253
Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318
Jones AM, Gardner S, Sinclair W (2008) Losing ‘Nemo’: bleaching and collection appear to reduce inshore populations of anemonefishes. J Fish Biol 73:753–761
Jones GP, Almany G, Russ G, Sale P, Steneck R, van Oppen M, Willis B (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325
Kaufman LS (1983) Effects of Hurricane Allen on reef fish assemblages near Discovery Bay, Jamaica. Coral Reefs 2:43–47
Kokita T, Nakazono A (2001) Rapid response of an obligately corallivorous filefish Oxymonacanthus longirostris (Monacanthidae) to a mass coral bleaching event. Coral Reefs 20:155–158
Lecchini D, Shima J, Banaigs B, Galzin R (2005) Larval sensory abilities and mechanisms of habitat selection of a coral reef fish during settlement. Oecologia 143:326–334
Lindahl U, Öhman MC, Schelten CK (2001) The 1997/1998 mass mortality of corals: effects on fish communities on a Tanzanian coral reef. Mar Pollut Bull 42:127–131
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163
McClanahan TR, Weil E, Cortes J, Baird AH, Ateweberhan M (2009) Consequences of coral bleaching for sessile reef organisms. In: van Oppen MJH, Lough JM (eds) Ecological studies. Springer-Verlag, Berlin, pp 121–138
McCormick MI (2009) Behaviourally mediated phenotypic selection in a disturbed coral reef environment. Plos One 4:e7096
Moyer JT, Steene RC (1979) Nesting behavior of the anemonefish Amphiprion polymnus. Jpn J Ichthyol 26:209–214
Munday P, Leis J, Lough J, Paris C, Kingsford M, Berumen M, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–395
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 301:955–958
Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Pratchett MS, Wilson SK, Berumen ML, McCormick MI (2004) Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23:352–356
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 Annu Rev 46:251–296
Quenouille B, Bouchenak-Khelladi Y, Hervet C, Planes S (2004) Eleven microsatellite loci for the saddleback clownfish Amphiprion polymnus. Mol Ecol Notes 4:291–293
R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna
Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S (2009) Estimating connectivity in marine populations: an empirical evaluation of assignment tests and parentage analysis under different gene flow scenarios. Mol Ecol 18:1765–1776
Simpson SD, Meekan M, Montgomery J, McCauley R, Jeffs A (2005) Homeward sound. Science 308:221
Simpson SD, Meekan MG, Jeffs A, Montgomery JC, McCauley RD (2008) Settlement-stage coral reef fish prefer the higher-frequency invertebrate-generated audible component of reef noise. Anim Behav 75:1861–1868
Sweatman HPA (1988) Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues. J Exp Mar Biol Ecol 124:163–174
Thresher RE, Colin PL, Bell L (1989) Planktonic duration, distribution and population structure of Western and Central Pacific Damselfishes (Pomacentridae). Copeia 1989:420–434
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256
Acknowledgments
We are grateful to Chris McKelliget, Vanessa Messmer, Juan David Arango, and Motupore Island Research Centre staff for assistance in the field. Special thanks to Steve Neale for deployment of temperature loggers and to Ray Berkelmans and Alex Hendry for access to the AIMS temperature database. Funding has been provided by the ARC Centre of Excellence for Coral Reef Studies, the National Science Foundation (OCE 0424688), the Coral Reef Initiatives for the Pacific (CRISP), the TOTAL Foundation, Populations Fractionees et Insulares (PPF EPHE), and the Connectivity Working Group of the global University of Queensland—World Bank—Global Environmental Facility project, Coral Reef Target Research and Capacity Building for Management for financial support. Special thanks to Motupore Island Research Centre, Dik Knight, and Loloata Island resort for logistic support and three anonymous reviewers for helpful comments in a previous version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Environment Editor Prof. Rob van Woesik
Rights and permissions
About this article
Cite this article
Saenz-Agudelo, P., Jones, G.P., Thorrold, S.R. et al. Detrimental effects of host anemone bleaching on anemonefish populations. Coral Reefs 30, 497–506 (2011). https://doi.org/10.1007/s00338-010-0716-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-010-0716-0