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Anemonefish musical chairs and the plight of the two-band anemonefish, Amphiprion bicinctus

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Abstract

Anemonefishes’ obligatory mutualism with sea anemones dictates their occurrence in marine habitats. We examined whether the spatial distribution, number, and size of the host anemones Heteractis crispa and Entacmaea quadricolor affected the settlement, habitat usage, and survival of the two-band anemonefish, Amphiprion bicinctus. In a 200 × 50 m study site off the coast of Israel in the Gulf of Eilat, we followed the fish and anemone populations initially in 13 censuses from October 1996 to August 1997 and follow-up censuses from 1998 to 2015. Based on size, anemonefish were categorized as adults, juveniles, or settlers. Settlers tended to cluster together but displayed significantly dispersed distributions in relation to adult individual fish and breeding pairs. Adult and juvenile anemonefish associated more with, and exhibited higher survival in, E. quadricolor. Settlers primarily inhabited H. crispa, with similar survival rates in the two anemone species. H. crispa was less occupied compared to E. quadricolor, but 95 % of the 233 anemones hosted fish during at least one census. From 1997 to 2015, anemone and anemonefish numbers plummeted by 86 % and 74 %, respectively. In 2015, all 27 remaining anemones were occupied, with most E. quadricolor inhabited by adults. The anemones left at the study site, on average, hosted more fish per anemone than those in the original population. This saturated habitat could hinder new anemonefish individuals from settling. These results indicate that if the anemone population does not recover, the anemonefish could face local extinction.

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References

  • Allen G (1972) Anemonefishes: their classification and biology. TFH Publications, Neptune City

    Google Scholar 

  • Ben-Tzvi O, Kiflawi M, Polak O, Abelson A (2009) The effect of adult aggression on habitat selection by settlers of two coral-dwelling damselfishes. PLoS One 4:e5511. doi:10.1371/journal.pone.0005511

    Article  PubMed  PubMed Central  Google Scholar 

  • Brolund TM, Tychsen A, Nielsen LE, Arvedlund M (2004) An assemblage of the host anemone Heteractis magnifica in the northern Red Sea, and distribution of the resident anemonefish. J Mar Biol Assoc UK 84:671–674. doi:10.1017/S0025315404009737h

    Article  Google Scholar 

  • Buston PM (2003) Forcible eviction and prevention of recruitment in the clown anemonefish. Behav Ecol 14:576–582. doi:10.1093/beheco/arg036

    Article  Google Scholar 

  • Buston PM (2004) Does the presence of non-breeders enhance the fitness of breeders? An experimental analysis in the clown anemonefish Amphiprion percula. Behav Ecol Sociobiol 57:23–31. doi:10.1007/s00265-004-0833-2

    Article  Google Scholar 

  • Cardini U, van Hoytema N, Al-Rshaidat MMD, Schuhmacher H, Wild C, Naumann MS (2015) 37 years later: revisiting a Red Sea long-term monitoring site. Coral Reefs 34:1111. doi:10.1007/s00338-015-1321-z

  • Chadwick NE, Arvedlund M (2005) Abundance of giant sea anemones and patterns of association with anemonefish in the northern Red Sea. J Mar Biol Assoc UK 85:1287–1292. doi:10.1017/S0025315405012440

    Article  Google Scholar 

  • Day J (2008) The need and practice of monitoring, evaluating and adapting marine planning and management—lessons from the great barrier reef. Mar Policy 32:823–831. doi:10.1016/j.marpol.2008.03.023

    Article  Google Scholar 

  • Dirnwöber M, Herler J (2007) Microhabitat specialisation and ecological consequences for coral gobies of the genus Gobiodon in the Gulf of Aqaba, northern Red Sea. Mar Ecol Prog Ser 342:265–275. doi:10.3354/meps342265

    Article  Google Scholar 

  • Dunn DF (1981) The clownfish sea anemones: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Trans Am Philos Soc 71:3–115. doi:10.2307/1006382

    Article  Google Scholar 

  • Elliott JK, Mariscal RN (2001) Coexistence of nine anemonefish species: differential host and habitat utilization, size and recruitment. Mar Biol 138:23–36. doi:10.1007/s002270000441

    Article  Google Scholar 

  • Elliott JK, Elliott JM, Mariscal RN (1995) Host selection, location and association behaviors of anemonefishes in field settlement experiments. Mar Biol 122:377–389. doi:10.1007/BF00350870

    Article  Google Scholar 

  • Fautin DG (1991) The anemonefish symbiosis: what is known and what is not. Symbiosis 10:23–46

    Google Scholar 

  • Fautin DG (1992) Anemonefish recruitment: the roles of order and chance. Symbiosis 14:143–160

    Google Scholar 

  • Fautin DG, Allen GR (1997) Field guide to anemonefishes and their host sea anemones, Revised edn. Western Australian Museum, Perth, Australia

    Google Scholar 

  • Fishelson L (1964) Observations on the biology and behaviour of Red Sea coral fishes. Bull Sea Fish Res Stn Haifa 37:11–26

  • Fishelson L (1970) Littoral fauna of the Red Sea: the population of non-scleractinian anthozoans of shallow waters of the Red Sea (Eilat). Mar Biol 6:106–116. doi:10.1007/BF00347239

  • Fishelson L (1995) Elat (Gulf of Aqaba) littoral: life on the red line of biodegradation. Isr J Zool 41:43–55. doi:10.1080/00212210.1995.10688777

  • Fishelson L, Popper D, Avidor A (1974) Biosociology and ecology of pomacentrid fishes around the Sinai peninsula (northern Red Sea). J Fish Biol 6:119–133. doi:10.1111/j.1095-8649.1974.tb04532.x

  • Fricke HW (1974) Eco-ethology of the anemone fish Amphiprion bicinctus (field studies in the Red Sea). Z Tierpsychol 36:429–512

  • Fricke HW (1979) Mating system, resource defence and sex change in the anemonefish Amphiprion akallopisos. Z Tierpsychol 50:313–326. doi:10.1111/j.1439-0310.1979.tb01034.x

    Article  Google Scholar 

  • Friedlander AM, Beets J (2008) Temporal trends in reef fish assemblages inside Virgin Islands National Park and around St. John, US Virgin islands, 1988–2006. NOAA Technical Memorandum NOS NCCOS 70. NOAA/National Centers for Coastal Ocean Science, Silver Spring, MD, p. 60

    Google Scholar 

  • Frisch AJ, Rizzari JR, Munkres KP, Hobbs J-PA (2016) Anemonefish depletion reduces survival, growth, reproduction and fishery productivity of mutualistic anemone–anemonefish colonies. Coral Reefs 35:375–386. doi:10.1007/s00338-016-1401-8

    Article  Google Scholar 

  • Godwin J, Fautin DG (1992) Defense of host actinians by anemonefishes. Copeia 1992:902–908. doi:10.2307/1446171

    Article  Google Scholar 

  • Hattori A (1991) Socially controlled growth and size-dependent sex change in the anemonefish Amphiprion frenatus in Okinawa, Japan. Jpn J Ichthyol 38:165–177. doi:10.1007/BF02905541

  • Hattori A (2002) Small and large anemonefishes can coexist using the same patchy resources on a coral reef, before habitat destruction. J Anim Ecol 71:824–831. doi:10.1046/j.1365-2656.2002.00649.x

    Article  Google Scholar 

  • Hattori A (2005) High mobility of the protandrous anemonefish Amphiprion frenatus: nonrandom pair formation in limited shelter space. Ichthyol Res 52:57–63. doi:10.1007/s10228-004-0253-3

    Article  Google Scholar 

  • Hobbs JP, Frisch AJ, Ford BM, Thums M, Saenz-Agudelo P, Furby KA, Berumen ML (2013) Taxonomic, spatial and temporal patterns of bleaching in anemones inhabited by anemonefishes. PLoS One 8:e70966. doi:10.1371/journal.pone.0070966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. doi:10.1126/science.1152509

    Article  CAS  PubMed  Google Scholar 

  • Holbrook SJ, Schmitt RJ (2005) Growth, reproduction and survival of a tropical sea anemone (Actiniaria): benefits of hosting anemonefish. Coral Reefs 24:67–73. doi:10.1007/s00338-004-0432-8

    Article  Google Scholar 

  • Huebner LK, Dailey B, Titus BM, Khalaf M, Chadwick NE (2012) Host preference and habitat segregation among Red Sea anemonefish: effects of sea anemone traits and fish life stages. Mar Ecol Prog Ser 464:1–15. doi:10.3354/meps09964

    Article  Google Scholar 

  • 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. doi:10.1111/j.1095-8649.2008.01969.x

    Article  Google Scholar 

  • Lönnstedt OM, Frisch AJ (2014) Habitat bleaching disrupts threat responses and persistence in anemonefish. Mar Ecol Prog Ser 517:265–270. doi:10.3354/meps11031

    Article  Google Scholar 

  • Loya Y (1975) Possible effects of water pollution on the community structure of Red Sea corals. Mar Biol 29:177–185. doi:10.1007/BF00388987

    Article  Google Scholar 

  • Madduppa HH, Timm J, Kochzius M (2014a) Interspecific, spatial and temporal variability of self-recruitment in anemonefishes. PLoS One 9:e90648. doi:10.1371/journal.pone.0090648

    Article  PubMed  PubMed Central  Google Scholar 

  • Madduppa HH, von Juterzenka K, Syakir M, Kochzius M (2014b) Socio-economy of marine ornamental fishery and its impact on the population structure of the clown anemonefish Amphiprion ocellaris and its host anemones in Spermonde archipelago, Indonesia. Ocean Coastal Manage 100:41–50. doi:10.1016/j.ocecoaman.2014.07.013

  • Maroz A, Fishelson L (1997) Juvenile production of Amphiprion bicinctus (Pomacentridae, Teleostei) and rehabilitation of impoverished habitats. Mar Ecol Prog Ser 151:295–297. doi:10.3354/meps151295

    Article  Google Scholar 

  • McVay MJ (2015) Population dynamics of clownfish sea anemones: patterns of decline, symbiosis with anemonefish, and management for sustainability. Auburn University, Thesis

    Google Scholar 

  • Mitchell JS, Dill LM (2005) Why is group size correlated with the size of the host sea anemone in the false clown anemonefish? Can J Zool 83:372–376. doi:10.1139/z05-014

    Article  Google Scholar 

  • Moyer JT (1980) Influence of temperate waters on the behavior of the tropical anemonefish Amphiprion clarkii at Miyake-jima, Japan. Bull Mar Sci 30:261–272

    Google Scholar 

  • Moyer JT, Sawyers CE (1973) Territorial behavior of the anemonefish Amphiprion xanthurus with notes on the life history. Jpn J Ichthyol 20:85–93

  • Munday PL, Jones GP, Pratchett MS, Williams AJ (2008) Climate change and the future for coral reef fishes. Fish Fish 9:261–285. doi:10.1111/j.1467-2979.2008.00281.x

    Article  Google Scholar 

  • Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Doving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci U S A 106:1848–1852. doi:10.1073/pnas.0809996106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfister RP, Goulet D (1999) Nonintrusive video technique for in situ sizing of coral reef fishes. Copeia 1999:789–793. doi:10.2307/1447616

    Article  Google Scholar 

  • Pinsky ML, Palumbi SR, Andréfouët S, Purkis SJ (2012) Open and closed seascapes: where does habitat patchiness create populations with high fractions of self-recruitment? Ecol Appl 22:1257-1267. doi:10.1890/11-1240.1

  • Planes S, Jones GP, Thorrold SR (2009) Larval dispersal connects fish populations in a network of marine protected areas. Proc Natl Acad Sci U S A 106:5693–5697. doi:10.1073/pnas.0808007106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porat D, Chadwick-Furman NE (2004) Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival. Hydrobiologia 530:513–520. doi:10.1007/s10750-004-2688-y

    Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Richardson DL (1999) Correlates of environmental variables with patterns in the distribution and abundance of two anemonefishes (Pomacentridae: Amphiprion) on an eastern Australian sub-tropical reef system. Environ Biol Fish 55:255–263. doi:10.1023/A:1007596330476

    Article  Google Scholar 

  • Rinkevich B (2005) What do we know about Eilat (Red Sea) reef degradation? A critical examination of the published literature. J Exp Mar Biol Ecol 327:183–200. doi:10.1016/j.jembe.2005.06.014

    Article  Google Scholar 

  • Ross RM (1978a) Territorial behavior and ecology of the anemonefish Amphiprion melanopus on Guam. Z Tierpsychol 46:71–83. doi:10.1111/j.1439-0310.1978.tb01439.x

    Google Scholar 

  • Ross RM (1978b) Reproductive behavior of the anemonefish Amphiprion melanopus on Guam. Copeia 1978:103–107. doi:10.2307/1443829

    Article  Google Scholar 

  • Sato M, Honda K, Bolisay KO, Nakamura Y, Fortes MD, Nakaoka M (2014) Factors affecting the local abundance of two anemonefishes (Amphiprion frenatus and A. perideraion) around a semi-closed bay in Puerto Galera, the Philippines. Hydrobiologia 733:63–69. doi:10.1007/s10750-013-1758-4

    Article  Google Scholar 

  • Scott A, Baird AH (2015) Trying to find Nemo: low abundance of sea anemones and anemonefishes on central and southern mid-shelf reefs in the Great Barrier Reef. Mar Biodivers 45:327–331. doi:10.1007/s12526-014-0245-0

    Article  Google Scholar 

  • Shuman CS, Hodgson G, Ambrose RF (2005) Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines. Coral Reefs 24:564–573. doi:10.1007/s00338-005-0027-z

    Article  Google Scholar 

  • Srinivasan M, Jones GP, Caley MJ (1999) Experimental evaluation of the roles of habitat selection and interspecific competition in determining patterns of host use by two anemonefishes. Mar Ecol Prog Ser 186:283–292. doi:10.3354/meps186283

    Article  Google Scholar 

  • Zakai D, Chadwick-Furman NE (2002) Impacts of intensive recreational diving on reef corals at Eilat, northern Red Sea. Biol Conserv 105:179–187. doi:10.1016/S0006-3207(01)00181-1

    Article  Google Scholar 

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Acknowledgments

We are indebted to Y. Loya, M. Fine and the faculty and staff of the Interuniversity Institute for Marine Sciences in Eilat for their assistance. We thank R. Pfister, A. Dwileski and A. Mazeroll for field assistance, M. McCauley, K.P. Shirur and anonymous reviewers for their comments, J. Hoeksema for statistical advice, A. Woolsey for ArcGIS assistance, and the Club Hotel Eilat for logistical support. Funding was provided by Sigma Xi, the McRight Fellowship, and the University of Mississippi Graduate School, Graduate Student Council, and Biology Department to JH and the National Science Foundation under Grant No. IOS 0747205 to TLG. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

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  1. Department of Biology, University of Mississippi, University, MS, 38677, USA

    Jacob Howell, Tamar L. Goulet & Denis Goulet

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  1. Jacob Howell
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  2. Tamar L. Goulet
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  3. Denis Goulet
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Correspondence to Denis Goulet.

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Howell, J., Goulet, T.L. & Goulet, D. Anemonefish musical chairs and the plight of the two-band anemonefish, Amphiprion bicinctus . Environ Biol Fish 99, 873–886 (2016). https://doi.org/10.1007/s10641-016-0530-9

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