Environmental Biology of Fishes

, Volume 102, Issue 1, pp 41–54 | Cite as

Low density populations of anemonefish with low replenishment rates on a reef edge with anthropogenic impacts

  • Kina HayashiEmail author
  • Katsunori Tachihara
  • James Davis Reimer


The population dynamics of anemonefish are expected to have unique patterns because of the symbiotic relationship with host anemones. Recent anthropogenic impacts may affect the abundance of anemones, which may also affect population dynamics of anemonefish. However, long-term field studies and demographic data on reproduction, immigration, and mortality rates are deficient. Here, we investigated the dynamics of anemonefish for 3 years on the reef edge with anthropogenic impacts of Okinawa-jima Island, southern Japan. During the study period, six species of host anemone were used as spawning grounds by four species of anemonefish, and as nurseries by six species of immature anemonefish. The density of breeding pairs was low (0.21–1.46 /ha), which may have been restricted by the abundance of host anemones. Survival rates were different among species; from 0.21 to 1.00 over 3 years. Ten cases of dissolution of breeding pairs were observed during the 3 years, and only five pairs were replenished. Through the study period, 215 individuals of six species of immature fish immigrated into the study site, and this number was skewed due to higher numbers of Amphiprion clarkii (77.7%). Demographic patterns differed among species, and requirements for conservation will therefore be different among species on the reef edges of Okinawa-jima Island under anthropogenic impact.


Amphiprion Host anemone Immigration Population dynamics Survival rate Okinawa 



We thank MISE and Tachihara laboratory members (University of the Ryukyus) who gave advice and helped with field work during this study. We also thank Okinawa Prefectural Archives for sharing historical aerial photographs. Two anonymous reviewers greatly improved an earlier version of this manuscript.

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

All authors declare that they have no conflict of interest.


  1. Aldenhoven JM (1986) Local variation in mortality rates and life expectancy estimates of the coral reef fish Centropyge bicolor (Pisces: Pomacanthidae). Mar Biol 92:237–244CrossRefGoogle Scholar
  2. Bowen BW, Rocha LA, Toonen RJ, Karl SA (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366CrossRefGoogle Scholar
  3. Buston PM (2003) Mortality is associated with social rank in the clown anemonefish (Amphiprion percula). Mar Biol 143:811–815CrossRefGoogle Scholar
  4. Buston PM, García MB (2007) An extraordinary life span estimate for the clown anemonefish Amphiprion percula. J Fish Biol 70:1710–1719CrossRefGoogle Scholar
  5. Dunn DF (1981) The clownfish sea anemones: Stichodactylidae (Coelenterata: Actiniaria) and other sea anemones symbiotic with pomacentrid fishes. Trans Am Philos Soc 71:1–115CrossRefGoogle Scholar
  6. Eckert GJ (1987) Estimates of adult and juvenile mortality for labrid fishes at one tree reef, great barrier reef. Mar Biol 95:161–171CrossRefGoogle Scholar
  7. Elliott JK, Mariscal RN (2001) Coexistence of nine anemonefish species: differential host and habitat utilization, size and recruitment. Mar Biol 138:23–36CrossRefGoogle Scholar
  8. Fautin DG (1991) The anemonefish symbiosis: what is known and what is not. Symbiosis 10:23–46Google Scholar
  9. Fautin DG (1992) Anemonefish recruitment: the roles of order and chance. Symbiosis 14:143–160Google Scholar
  10. Fautin DG, Allen GR (1992) Field guide to anemonefishes and their host sea anemones. Western Australian Museum, PerthGoogle Scholar
  11. Fricke H, Fricke S (1977) Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266:830–832CrossRefGoogle Scholar
  12. Frisch AJ, Hobbs JPA (2009) Rapid assessment of anemone and anemonefish populations at the Keppel Islands [electronic resource]: a report to the Great Barrier Reef Marine Park Authority. James Cook University, AustraliaGoogle Scholar
  13. Fujii H (2001) The present status of tidal flats on the Okinawa Island. Japanese J Benthology 56:29–31CrossRefGoogle Scholar
  14. Geospatial Information Authority of Japan (2018) 10 Jan 2018
  15. Graham NAJ, Chong-Seng KM, Huchery C, Hartley FAJ, Nash KL (2014) Coral reef community composition in the context of disturbance history on the great barrier reef, Australia. PLoS ONE 9(7):e101204CrossRefGoogle Scholar
  16. Hattori A (1991) Socially controlled growth and size-dependent sex change in the anemonefish Amphiprion frenatus in Okinawa, Japan. Jpn J Ichthyol 38:165–177Google Scholar
  17. Hattori A (2002) Small and large anemonefishes can coexist using the same patchy resources on a coral reef, before habitat destruction. J Anim Ecol 71:824–831CrossRefGoogle Scholar
  18. Hattori A, Yanagisawa Y (1991) Life-history pathways in relation to gonadal sex differentiation in the anemonefish, Amphiprion clarkii, in temperate waters of Japan. Environ Biol Fish 31:139–155CrossRefGoogle Scholar
  19. Hayashi K, Tachihara K, Reimer JD (2018) Patterns of coexistence of six anemonefish species around subtropical Okinawa-jima Island, Japan. Coral Reefs 37:1027–1038Google Scholar
  20. Hirose Y (1985) Habitat, distribution and abundance of coral reef sea-anemones (Actiniidae and Stichodactylidae) in Sesoko Island, Okinawa, with notes of expansion and contraction behavior. Galaxea 4:113–127Google Scholar
  21. Hirose Y (1995) Pattern of pair formation in protandrous anemonefishes, Amphiprion clarkii, A. frenatus and A. perideraion, on coral reefs of Okinawa, Japan. Environ Biol Fish 43:153–161CrossRefGoogle Scholar
  22. Hobbs JPA, 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:e70966CrossRefGoogle Scholar
  23. Holbrook SJ, Schmitt RJ, Messmer V, Brooks AJ, Srinivasan M, Munday PL, Jones GP (2015) Reef fishes in biodiversity hotspots are at greatest risk from loss of coral species. PLoS ONE 10(5):e0124054CrossRefGoogle Scholar
  24. Holtswarth JN, San Jose SB, Montes J, Humberto R, Morley JW, Pinsky ML (2017) The reproductive seasonality and fecundity of yellowtail clownfish (Amphiprion clarkii) in the Philippines. Bull Mar Sci 93:997–1007CrossRefGoogle Scholar
  25. Iwata E, Nagai Y, Hyoudou M, Sasaki H (2008) Social environment and sex differentiation in the false clown anemonefish, Amphiprion ocellaris. Zool Sci 25:123–128CrossRefGoogle Scholar
  26. Jones GP (1990) The importance of recruitment to the dynamics of a coral reef fish population. Ecology 71:1691–1698CrossRefGoogle Scholar
  27. Masuda H, Amaoka K, Arage C, Uyeno T, Yoshino T (1984) The fishes of the Japanese archipelago. Tokai University Press, TokyoGoogle Scholar
  28. Moyer JT (1976) Geological variation and social dominance in Japanese populations of the anemonefish Amphiprion clarkii. Jpn J Ichthyol 23:12–22Google Scholar
  29. Moyer JT (1986) Longevity of the anemonefish Amphiprion clarkii at Miyake-jima, Japan with notes on four other species. Copeia 1:135–139CrossRefGoogle Scholar
  30. Moyer JT, Nakazono A (1978) Protandrous hermaphroditism in six species of the anemonefish genus Amphiprion in Japan. Jap J Ichthyol 25:101–106Google Scholar
  31. Munro JJ, Williams DD (1985) Assessment and management of coral reef fisheries: biological, environmental and socio-economic aspects. In: Proceedings of the 5th international coral reef congress. Tahiti, vol 4, pp 544–580Google Scholar
  32. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  33. Nelson JS, Chou LM, Phang VPE (1998) Inter-habitat migration of the anemonefish Amphiprion ocellaris. Asian J Trop Biol 3:19–31Google Scholar
  34. Ochi H (1989) Mating behavior and sex change of the anemonefish Amphiprion clarkii in the temperate waters of southern Japan. Environ Biol Fish 26:257–275CrossRefGoogle Scholar
  35. Ono S, Reimer JD, Nozawa Y, Tsukahara J (2010) Long-term changes of infra-littoral zone zooxanthellate cnidarians in the Taisho lava field, Sakurajima, Kagoshima, Japan. Galaxea JCRS 12:15–22CrossRefGoogle Scholar
  36. Pinsky ML, Montes HR, Palumbi SR (2010) Using isolation by distance and effective density to estimate dispersal scales in anemonefish. Evolution 64:2688–2700CrossRefGoogle Scholar
  37. Reimer JD, Yang SY, White KN, Asami R, Fujita K, Hongo C, Ito S, Kawamura I, Maeda B, Mizuyama M, Obuchi M, Sakamaki T, Tachihara K, Tamura M, Tanahara A, Yamaguchi A, Kodama HJ (2015) Effects of causeway construction on environment and biota of subtropical tidal flats in Okinawa, Japan. Mar Pollut Bull 94:153–167CrossRefGoogle Scholar
  38. Sale PF (1978) Coexistence of coral reef fishes—a lottery for living space. Environ Biol Fish 3:85–102CrossRefGoogle Scholar
  39. Salles OC, Maynard JA, Joannides M, Barbu CM, Saenz-Agudelo P, Almany GR, Berumen ML, Thorrold SR, Jones GP, Planes S (2015) Coral reef fish populations can persist without immigration. Proc R Soc B 282:20151311CrossRefGoogle Scholar
  40. Scott A, Malcolm HA, Damiano C, Richardson DL (2011) Long-term increases in abundance of anemonefish and their host sea anemones in an Australian marine protected area. Mar Freshw Res 62:187–196CrossRefGoogle Scholar
  41. 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 24:564–573CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Graduate School of Engineering and ScienceUniversity of the RyukyusOkinawaJapan
  2. 2.Tropical Biosphere Research CenterUniversity of the RyukyusOkinawaJapan

Personalised recommendations