Behavioural differences between breeding and nonbreeding pairs of protandry monogamous false clown anemonefish Amphiprion ocellaris

  • Eri Iwata Department of Science and Technology, Iwaki Meisei University, 5-5-1 Chuoudai, Ihino, Iwaki, Fukushima 970-8551, Japan; Faculty of Veterinary Medicine, Okayama University of Science, 1-3, Ikoinooka, Imabari City, Ehime, 794-8555, Japan; Institute of Osaka Marine Research, 19-34, Shimodachou, Nishi Ku, Sakai City, Osaka, 593-8329, Japan https://orcid.org/0000-0003-4178-7551
  • Tasuku Yoshida Department of Science and Technology, Iwaki Meisei University, 5-5-1 Chuoudai, Ihino, Iwaki, Fukushima 970-8551, Japan
  • Tetsuya Abe Department of Science and Technology, Iwaki Meisei University, 5-5-1 Chuoudai, Ihino, Iwaki, Fukushima 970-8551, Japan
  • Kou Takahara Department of Science and Technology, Iwaki Meisei University, 5-5-1 Chuoudai, Ihino, Iwaki, Fukushima 970-8551, Japan
  • Koji Masuda Department of Human and Animal-Plant Relationships, Tokyo University of Agriculture, 1737 Funako, Atsugi, Kanagawa 243-0034, Japan
Keywords: Anemonefish, Amphiprion ocellaris, ornamental fish, social behaviour, breeding, sexual maturation

Abstract

Anemonefishes are some of the most popular marine ornamental fishes. Due to the adverse impacts of commercial fishing on the wild populations of anemonefishes, a more suitable and efficient captive breeding programme must be promoted. In the wild, anemonefishes are protandrous sex-changing fish, but when two immature individuals with ambisexual gonads are raised together in captivity, the two differentiate directly into a male and a female, to form a breeding pair. However, not all the formed pairs spawn, explaining the great care required in captive breeding. This behaviour appears to be counter-adaptative, as anemonefish social groups form randomly in the wild, and such phenomenon would disturb their breeding success. This study evaluated the behavioural and physiological differences between breeding and nonbreeding pairs of false clown anemonefish Amphiprion ocellaris under captive conditions. Behavioural observations revealed that nonbreeding females monopolized the shelter provided, whereas breeding females allowed breeding males to use the shelter and the pair frequently stayed together in the shelter. Both nonbreeding and breeding females possessed mature ovarian tissue and similar level of plasma estradiol concentrations, but nonbreeding males had a smaller amount of testicular tissue and lower plasma 11-ketotestosterone levels compared to breeding males.

References

Abol-Munafi AB, Nozrazmi-Lokman NH, Asma NA, Sarmiza S, Abduh MY (2011) Histological study of gonad of the protandrous anemonefish (Amphiprion ocellaris). Journal of Animal and Veterinary Advances 10: 3031–3036.

Aday DD, Wahl DH, Philipp DP (2003) A mechanism for social inhibition of sexual maturation in bluegill. Journal of Fish Biology 62: 486–490.

Bushmann PJ, Burns JR (1994) Social control of male sexual maturation in the swordtail characin, Corynopoma riisei. Journal of Fish Biology 44: 263–272.

Buston PM (2003a) Forcible eviction and prevention of recruitment in the clown anemonefish. Behavioral Ecology 14: 576–582.

Buston PM (2003b) Social hierarchies: size and growth modification in clownfish. Nature 424: 145–146.

Buston PM (2004) Does the presence of non-breeders enhance the fitness of breeders? An experimental analysis in the clown anemonefish Amphiprion percula. Behavioral Ecology and Sociobiology 57: 23–31.

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. Molecular Ecology 16: 3671–3678.

Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influence. Aquaculture 208: 191–364.

Fautin DG, Allen GR (1994a) Aquarium care. In: Anemonefishes and their host sea anemones. Tetra Press, Melle, Germany. pp. 141–146.

Fautin DG, Allen GR (1994b) Life history of anemonefishes (Chapter 4). In: Anemonefishes and their host sea anemones. Tetra Press, Melle, Germany, pp. 125–132.

Fricke H, Fricke S (1977) Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266: 830–832.

Fricke HW (1979) Mating system, resource defence and sex change in the anemonefish Amphiprion akallopisos. Zeitschrift für Tierpsychologie 50: 313–326.

Godwin JR, Thomas P (1993) Sex change and steroid profiles in the protandrous anemonefish Amphiprion melanopus (Pomacentridae, Teleostei). General and Comparative Endocrinology 91: 144–157.

Goldstein R (1989) Breeding marine clownfish. Aquarium Fish Magazine 1: 32.

Guerrero-Estevez S, Moreno-Mendosa N (2010) Sexual determination and differentiation in teleost fish. Reviews in Fish Biology and Fisheries 20: 87–100.

Hattori A (1991) Socially controlled growth and size-dependent sex change in the anemonefish Amphiprion frenatus in Okinawa, Japan. Japanese Journal of Ichthyology 38: 165–177.

Hattori A (1994) Inter-group movement and mate acquisition tactics of protandrous anemonefish, Amphiprion clarkii, on a coral reef, Okinawa. Japan. Japanese Journal of Ichthyology 41: 159–165.

Hattori A, Yanagisawa Y (1991a) Life-history pathways in relation to gonadal sex differentiation in the anemonefish, Amphiprion clarkii, in temperate waters of Japan. Environmental Biology of Fishes 31: 139–155.

Hattori A, Yanagisawa Y (1991b) Sex change of the anemonefish Amphiprion clarkii in a habitat of high host density: a removal study. Japanese Journal of Ecology 41: 1–8.

Iwata E, Mambo J (2013) Territorial behavior reflects sexual status in groups of false clown anemonefish (Amphiprion ocellaris) under laboratory conditions. Acta Ethologia 16: 96–103.

Iwata E, Mikami K, Manbo J, Moriya-Ito K, Sasaki H (2012) Social interaction influences blood cortisol values and brain aromatase genes in the protandrous false clown anemonefish, Amphiprion ocellaris. Zoological Science 29: 849–855.

Iwata E, Nagai Y, Hyoudou M, Sasaki H (2008) Social environment and sex differentiation in false clown anemonefish, Amphiprion ocellaris. Zoological Science 25: 123–128.

Iwata E, Nagai Y, Sasaki H (2010a) Immunohistochemistry of brain arginine vasotocin and isotocin in false clown anemonefish Amphiprion ocellaris. Open Fish Science Journal 3: 147–153.

Iwata E, Nagai Y, Sasaki H (2010b) Social rank modulates brain arginine vasotocin immunoreactivity in false clown anemonefish (Amphiprion ocellaris). Fish physiology and Biochemistry 36: 337–345.

Iwata E, Suzuki N, Ohno S (2019) Influence of social stability on the sex determination process in false clown anemonefish (Amphiprion ocellaris). Marine and Freshwater Behavior and Physiology 52: 107–119.

Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Current Biology 15: 1314–1318.

Maddupa HS, Timm J, Kochzius M (2018) Reduced genetic diversity in the clown anemonefish Amphiprion ocellaris in exploited reefs of Spermonde Archipelago, Indonesia. Frontiers in Marine Science 5: 80.

Maddupa HS, von Juterzenka K, Syakir M, Kochzius M (2014) 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 Management 100: 41–50.

Madhu K, Madhu R, Krishnan L, Sasidharan CS, Venugopalan KM (2006) Spawning and larval rearing of Amphiprion ocellaris under captive condition. Marine Fisheries Information Service 188: 1–5.

Madhu R, Madhu K, Retheesh T (2012) Life history pathways in false clown Amphiprion ocellaris Cuvier, 1830: a journey from egg to adult under captive condition. Journal of the Marine Biological Association of India 54: 77–90.

Michael C (2001) Marine Fishes. 500+ essential-to-know aquarium species. TFH Publications, Neptune City, NJ.

Monticini P (2010) The ornamental fish trade. Production and commerce of ornamental fish: technical-managerial and legislative aspect. GLOBEFISH Research Programme, Vol. 102, FAO, Rome.

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

Moyer JT (1986) Longevity of the anemonefish Amphiprion clarkii at Miyake-Jima Japan with notes on four other species. Copeia 1986: 135–139.

Moyer JT, Nakazono A (1978) Protandrous hermaphroditism in six species of the anemoefish genus Amphiprion in Japan. Japanese Journal of Ichthyology 25: 101–106.

Moyer JT, Sawyers CE (1973) Territorial behavior of the anemonefish Amphiprion xanthurus with notes on the life history. Japanese Journal Ichthyology 20: 85–93.

Murray JM, Watson GJ (2014) A critical assessment of marine aquarist biodiversity data and commercial aquaculture: identifying gaps in culture initiatives to inform local fisheries managers. PLoS ONE 9: e105982.

Ochi H (1989a) Acquisition of breeding space by nonbreeders in the anemonefish Amphiprion clarkii in temperate waters of southern Japan. Ethology 83: 279–294.

Ochi H (1989b) Mating behavior and sex change of the anemonefish, Amphiprion clarkii, in the temperate waters of southern Japan. Environmental Biology of Fishes 26: 257–275.

Rhyne AL, Tlusty MF, Szczebak JT, Holmberg RJ (2017) Expanding our understanding of the trade in marine aquarium animals. PeerJ 5: e2949;

Rohini Krishna MV, Anil MK, Neethu Raj P (2015) Studies on growth and development of hatchery produced juveniles of Amphiprion clarkii (Bennett, 1830). The International Journal of Science & Technoledge 3: 150–155.

Ross RM (1978) Territorial behavior and ecology of the anemonefish Amphiprion melanopus on Guam. Zeitschrift für Tierpsychologie 46: 71–83.

Schmiege PFP, D’Aloia CC, Buston PM (2016) Anemonefish personalities influence the strength of mutualistic interactions with host sea anemones. Marine Biology 164: 24.

Wabnitz C, Taylor M, Green E, Razak T (2003) From ocean to aquarium: the global trade in marine ornamental species. UNEP World Conservation Monitoring Centre, Cambridge, UK.

Wellington GM, Victor BC (1989) Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomcentridae). Marine Biology 101: 557–567.

Wilkerson JD (2003) Breeding and rearing (Part III). In: Clownfishes: a guide to their captive care, breeding, and natural history. Microcosm Ltd., Charlotte, VT. pp. 129–223.

Wong MYL, Beasley AL, Douglass T, Whalan S, Scott A (2017) Some anemonefish lack personality: a comparative assessment of behavioral variation and repeatability in relation to environmental and social factors. Coral Reefs 36: 1307–1316.

Yanagisawa Y, Ochi H (1986) Step-fathering in the anemonefish Amphiprion clarkii: a removal study. Animal Behaviour 34: 1769–1780.

Published
2020-05-25
How to Cite
Iwata, E., Yoshida, T., Abe, T., Takahara, K., & Masuda, K. (2020). Behavioural differences between breeding and nonbreeding pairs of protandry monogamous false clown anemonefish Amphiprion ocellaris. Journal of Fisheries, 8(2), 808-816. https://doi.org/10.17017/j.fish.179