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Behavioural Differences Between Breeding and Nonbreeding Pairs of Protandry Monogamous False Clown Anemonefish Amphiprion Ocellaris

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Behavioural Differences Between Breeding and Nonbreeding Pairs of Protandry Monogamous False Clown Anemonefish Amphiprion Ocellaris Journal of Fisheries eISSN 2311-3111 [Early View version] pISSN 2311-729X Peer Reviewed | Open Access | Online First Original Article Behavioural differences between breeding and nonbreeding pairs of protandry monogamous false clown anemonefish Amphiprion ocellaris Eri Iwata1,2,3 Tasuku Yoshida1 Tetsuya Abe1 Kou Takahata1 Koji Masuda4 1 Department of Science and Technology, Iwaki Meisei University, 5-5-1 Chuoudai, Ihino, Iwaki, Fukushima 970-8551, Japan 2 Faculty of Veterinary Medicine, Okayama University of Science, 1-3, Ikoinooka, Imabari City, Ehime, 794-8555, Japan 3 Institute of Osaka Marine Research, 19-34, Shimodachou, Nishi Ku, Sakai City, Osaka, 593-8329, Japan 4 Department of Human and Animal-Plant Relationships, Tokyo University of Agriculture, 1737 Funako, Atsugi, Kanagawa 243-0034, Japan Correspondence Eri Iwata; Faculty of Veterinary Medicine, Okayama University of Science, 1-3, Ikoinooka, Imabari City, Ehime, 794-8555, Japan [email protected] Manuscript history Received 20 December 2019 | Revised 12 May 2020 | Accepted 18 May 2020 | Published online 25 May 2020 Citation Iwata E, Yoshida T, Abe T, Takahata K, Masuda K (2020) Behavioural differences between breeding and nonbreeding pairs of protandry monogamous false clown anemonefish Amphiprion ocellaris. Journal of Fisheries. http://journal.bdfish.org/index.php/fisheries/article/view/JFish20179 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. Keywords: Anemonefish; Amphiprion ocellaris; ornamental fish; social behaviour; breeding; sexual maturation 1 | INTRODUCTION Amphiprion (including A. ocellaris), live symbiotically with The false clown anemonefish Amphiprion ocellaris was sea anemones in the wild and have small home ranges one of the top ten most traded fish species between 1997 (Hattori 1994; Moyer 1980), hence they can adjust quite and 2002 (Wabnitz et al. 2003). Anemonefishes, genus well to small aquarium tanks (Fautin and Allen 1994a). In BdFISH Publication | journal.bdfish.org | © Creative Commons BY-NC-SA 4.0 License 1 Behavioral differences in Amphiprion ocellaris J Fish [Early View Version]; Iwata et al. fact, on the “Aquarium suitability index” of the famous in temperate waters, without passing through the func- marine aquarium guide, A. ocellaris was rated “4” or tional male stage (Hattori and Yanagisawa 1991a). In cap- “generally durable and hardy, with most individuals ac- tivity, when two immature anemonefish with ambisexual climatizing to the home aquarium” (Michael 2001). gonads are raised together, the two differentiate directly into a male and a female and form a breeding pair (Gold- More than 90% of the freshwater ornamental fish are stein 1989; Wilkerson 2003). bred in captivity; in contrast, most marine ornamental aquaculture remains comparatively problematic (Monti- In the captive breeding of A. ocellaris, pair formation is cini 2010). The Pomacentridae family, including the genus developed by forming a social unit consisting of five to six Amphiprion, accounts for about half of the catch, with the individuals and choosing the dominant and second- green damselfish Chromis vividis and A. ocellaris being the ranked individual (Madhu et al. 2006; Rohini Krishna et al. most marketable (Monticini 2010). Actually, several stud- 2015), which requires great care and time. Moreover, not ies reported that A. ocellaris densities, total body length all formed pairs spawn, some pairs remain bonded with- and group size became small (Maddupa et al. 2014) and out spawning even though the pairs are raised under the genetic diversity of A. ocellaris is reduced (Maddupa et al. same conditions. Our previous study indicated that some 2018). pairs of A. ocellaris did not exhibit sex differentiation after 450 days of pairing, with one pair pairing for 3 years In an online survey of marine aquarium hobbyists in 2009, without spawning (Iwata et al. 2010a). This phenomenon 76% of respondents revealed that they would preferen- appears to be counter-adaptative, as social groups of tially purchase cultured animals, while a further 21% said anemonefish normally form randomly to breed. this would depend on the price difference (Murray and Watson 2014). Amphiprion ocellaris breed under captive In the wild, the dominant female and second-ranked male conditions relatively easily compared with other marine form a breeding pair, and females lay their eggs on a bare fish (Wilkerson 2003) and are successfully produced by rock adjacent to the host sea anemone (Fautin and Allen several hatcheries. However, captive-bred A. ocellaris 1994b; Wilkerson 2003). Hatching occurs 6 to 8 days after cost more to purchase than wild-caught individuals, re- the eggs are laid. Larvae are planktonic but settle at the sulting in more than 600,000 wild-caught A. ocellaris be- bottom of the sea after 8 to 12 days (Wellington and Vic- ing imported into the US between 2008 and 2011 (Rhyne tor 1989) to find a suitable host sea anemone (Fautin and et al. 2017). Furthermore, A. ocellaris broodstocks are Allen 1994b). In a study on saddleback anemonefish, Am- produced from breeding pairs collected in the wild rather phiprion polymnus, many offspring settled remarkably than an F1 generation (Abol-Munafi et al. 2011), possibly close to home, but none returned to the same anemone because breeding pair formation relies on the complex as their parents, suggesting that direct kin relationships social structure of this species and so may be difficult to between individuals in a sea anemone are rare (Jones et achieve under captive conditions. Therefore, a more effi- al. 2005; Buston et al. 2007). Thus, the social groups of cient breeding technique is needed to protect A. ocellaris anemonefish form randomly, and which individuals con- in the wild. tribute to breeding in each group is determined only by their social rank. Furthermore, this protandrous breeding In the anemonefishes, the genus Amphiprion, is protan- strategy indicates that breeding individuals are replacea- drous fish that possess the ability to change sex in re- ble, and studies have shown that members of anemone- sponse to social cues (Fricke and Fricke 1977; Moyer and fish social groups remain relatively stable for years in a Nakazono 1978). In the wild, anemonefishes form social wild population (Moyer 1986). Hence, if the reproductive groups consisting of a monogamous breeding pair and pair of a social group does not spawn, the entire group several subadult nonbreeders or juveniles. Females are might lose the chance to reproduce for years, which the largest and dominant members of these social groups, would decrease their breeding success. displaying frequent dominant behaviour toward subordi- nate group members. The second-ranked individuals be- In this study, we evaluated the differences between come males, displaying less aggression, and others re- breeding and nonbreeding pairs of false clown anemone- main as nonreproductive individuals, displaying little ag- fish A. ocellaris under captive conditions, considering be- gression (Fricke and Fricke 1977; Iwata et al. 2008; Iwata havioural traits, physical parameters, plasma steroid con- and Manbo 2013). If a female disappears from the social centrations, and gonadal histology to seek solutions for unit, the male changes sex into a female and the largest the problem of breeding pair formation in captivity. It is of the nonbreeders becomes a functional male (Fricke well known among oceanarium keepers that if an individ- and Fricke 1977; Moyer and Nakazono 1978). However, ual from a nonbreeding pair of anemonefish is replaced under certain conditions immature anemonefishes with another, the newly-formed pair will occasionally start to ambisexual gonads will differentiate directly into males or breed (E. Iwata, personal observation). To confirm that females. For instance, nonbreeding Clark’s anemonefish, the replacement of individuals induces spawning, a re- Amphiprion clarkii, can directly differentiate into females placement test was also conducted. BdFISH Publication | journal.bdfish.org | © Creative Commons BY-NC-SA 4.0 License 2 Behavioral differences in Amphiprion ocellaris J Fish [Early View Version]; Iwata et al. 2 | METHODOLOGY of anemonefish shown
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