Орган обоняния у анемоновых рыб рода Amphiprion (Amphiprioninae, Pomacentridae)

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Abstract

Изучена морфология органа обоняния у пяти видов анемоновых рыб рода Amphiprion: A. polymnus, A. clarkii, A. frenatus, A. perideraion и A. ocellaris. У всех рыб имеется одна ноздря, обонятельная розетка стреловидного типа, отсутствует вторичная складчатость на обонятельных складках, имеется два вентиляционных мешка (этмоидальный и более крупный лакримальный). Розетка располагается на медиальной (A. clarkii и A. perideraion) или вентромедиальной (A. polymnus, A. frenatus, A. ocellaris) стороне обонятельной полости, число складок в розетке увеличивается по мере роста рыб. Наибольшее общее число складок у A. polymnus – 24. В розетке у большинства амфиприонов обнаружены интеркалярные (у четырёх видов) и дихотомические (у трёх видов) складки, крайне редко встречающиеся у других рыб. Нетипичные складки возникают в онтогенезе рыб позже обычных, но в разных частях розетки, их численность у амфиприонов различается, у отдельных особей A. polymnus они преобладают. Уклон медиальной и латеральной сторон розетки в сторону входных отверстий вентиляционных мешков (A. polymnus, A. frenatus) рассматривается как структурная адаптация, улучшающая водообмен у поверхности обонятельных складок и получение рыбами запаховой информации. Связь между устройством органа обоняния и эврибионтностью амфиприонов, их специализацией и прочностью ассоциации с симбионтными актиниями не выявлена. Изложено представление об эволюционном тренде от просто устроенного органа обоняния (A. clarkii) к морфологически более сложному (A. polymnus и A. frenatus) в роде Amphiprion после раннего отделения от общего ствола подрода Actinicola (A. ocellaris, A. percula).

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About the authors

Н. И. Пащенко

Московский государственный университет

Author for correspondence.
Email: visitgrusha@gmail.com
Russian Federation, Москва

Л. Т. К. Оань

Приморское отделение Совместного российско-вьетнамского тропического научно-исследовательского и технологического центра

Email: visitgrusha@gmail.com
Viet Nam, Нячанг

А. О. Касумян

Московский государственный университет; Институт проблем экологии и эволюции РАН

Email: visitgrusha@gmail.com
Russian Federation, Москва; Москва

References

  1. Астахов Д.А. 2002. Видовой состав анемоновых рыб (Perciformes, Pomacentridae) и симбиотических актиний (Cnidaria, Actiniaria) провинции Ханьхоа (Южный Вьетнам) // Вопр. ихтиологии. Т. 42. № 1. С. 41–55.
  2. Астахов Д.А. 2015. Материалы по фауне анемоновых рыб (Pomacentridae, Amphiprioninae) и их симбиотических актиний (Cnidaria, Actiniaria) на рифах островов Ли Сон (Южно-Китайское море, Центральный Вьетнам) // Там же. Т. 55. № 5. С. 618–621. https://doi.org/10.7868/S0042875215050033
  3. Астахов Д.А., Савинкин О.В., Пономарев С.А. 2016. Фауна анемоновых рыб (Pomacentridae, Amphiprioninae) и их симбиотических актиний (Cnidaria, Actiniaria) на рифах островов Фу Куи, Кон Сон и Ан Тхой (Южно-Китайское море, Южный Вьетнам и Сиамский залив) и обзор фауны этих групп из прибрежных вод Вьетнама // Там же. Т. 56. № 6. С. 670–684. https://doi.org/10.7868/S0042875216060011
  4. Касумян А.О., Пащенко Н.И., Оань Л.Т.К. 2021. Морфология органа обоняния анабаса Anabas testudineus (Anabantidae, Perciformes) // Зоол. журн. Т. 100. № 1. С. 40–56. https://doi.org/10.31857/S0044513420110045
  5. Пащенко Н.И., Касумян А.О. 2017. Развитие органа обоняния в онтогенезе карповых рыб (Cyprinidae, Teleostei) // Вопр. ихтиологии. Т. 57. Вып. 1. С. 96–111. https://doi.org/10.7868/S0042875217010106
  6. Пащенко Н.И., Касумян А.О. 2019. Морфология и вентиляция органа обоняния у индо-тихоокеанской рыбы-сержанта Abudefduf vaigiensis (Pomacentridae, Perciformes) // Там же. Т. 59. № 2. С. 154–161. https://doi.org/10.1134/S0042875219010132
  7. Пащенко Н.И., Оань Л.Т.К., Касумян А.О. 2022. Морфология и вентиляция органа обоняния у шестиполосой рыбы-сержанта Abudefduf sexfasciatus (Pomacentridae) // Там же. Т. 62. № 3. С. 282–293. https://doi.org/10.31857/S0042875222030158
  8. Allen G.R. 1972. The anemonefishes: their classification and biology. Neptune City: T.F.H. Publ., 288 p.
  9. Allen G.R. 1980. Anemonefishes of the world: species, care and breeding. Mentor: Aquarium Systems, 104 p.
  10. Allen G.R. 1991. Damselfishes of the World. Melle: Mergus, 271 p.
  11. Allen G.R. 2000. Family Pomacentridae (damselfishes) // Ruffles Bull. Zool. Suppl. 8. P. 626–627.
  12. Almany G.R., Berumen M.L., Thorrold S.R. et al. 2007. Local replenishment of coral reef fish populations in a marine reserve // Science. V. 316. № 5825. P. 742–744. https://doi.org/10.1126/science.1140597
  13. Arvedlund M., Kavanagh K. 2009. The senses and environmental cues used by marine larvae of fish and decapod crustaceans to find tropical coastal ecosystems // Ecological connectivity among tropical coastal ecosystems. Dordrecht: Springer. P. 135–184. https://doi.org/10.1007/978-90-481-2406-0_5
  14. Arvedlund M., Nielsen L.E. 1996. Do the anemonefish Amphiprion ocellaris (Pisces: Pomacentridae) imprint themselves to their host sea anemone Heteractis magnifica (Anthozoa: Actinidae)? // Ethology. V. 102. № 2. P. 197–211. https://doi.org/10.1111/j.1439-0310.1996.tb01118.x
  15. Arvedlund M., McCormick M.I., Fautin D.G., Bildsøe M. 1999. Host recognition and possible imprinting in the anemonefish Amphiprion melanopus (Pisces: Pomacentridae) // Mar. Ecol. Prog. Ser. V. 188. P. 207–218. https://doi.org/10.3354/meps188207
  16. Arvedlund M., Bundgaard I., Nielsen L.E. 2000a. Host imprinting in anemonefishes (Pisces: Pomacentridae): does it dictate spawning site preferences? // Environ. Biol. Fish. V. 58. № 2. P. 203–213. https://doi.org/10.1023/A:1007652902857
  17. Arvedlund M., Larsen K., Winsor H. 2000b. The embryonic development of the olfactory system in Amphiprion melanopus (Perciformes: Pomacentridae) related to the host imprinting hypothesis // J. Mar. Biol. Assoc. U.K. V. 80. № 6. P. 1103–1109. https://doi.org/10.1017/S0025315400003179
  18. Arvedlund M., Brolund T.M., Nielsen L.E. 2003. Morphology and cytology of the olfactory organs in small juvenile Dascyllus aruanus and Amphiprion ocellaris (Pisces: Pomacentridae) // Ibid. V. 83. № 6. P. 1321–1326. https://doi.org/10.1017/S0025315403008762
  19. Biology of Damselfishes. 2016. Boca Raton: CRC Press, 340 p. https://doi.org/10.1201/9781315373874
  20. Astakhov D.A. 2021. Gap in the Continuous Range of Amphiprion clarkii (Pomacentridae) in the Gulf of Thailand (South China Sea). Possible Causes // J. Ichthyol. V. 61. № 6. P. 808–817. https://doi.org/10.1134/S0032945221060023
  21. Bridge T., Scott A., Steinberg D. 2012. Abundance and diversity of anemonefishes and their host sea anemones at two mesophotic sites on the Great Barrier Reef, Australia // Coral Reefs. V. 31. № 4. P. 1057–1062. https://doi.org/10.1007/s00338-012-0916-x
  22. Brolund T.M., Nielsen L.E., Arvedlund M. 2003. Do juvenile Amphiprion ocellaris Cuvier (Pisces: Pomacentridae) recognize conspecifics by chemical or visual cues? // J. Mar. Biol. Assoc. U.K. V. 83. № 5. P. 1127–1136. https://doi.org/10.1017/S0025315403008385h
  23. Burke da Silva K., Nedosyko A. 2016. Sea anemones and anemonefish: a match made in Heaven // The Cnidaria, past, present and future. Cham: Springer. P. 425–438. https://doi.org/10.1007/978-3-319-31305-4_27
  24. Buston P.M. 2004. Territory inheritance in clownfish // Proc. R. Soc. Lond. B. V. 271. Suppl. 4. P. S252–S254. https://doi.org/10.1098/rsbl.2003.0156
  25. Buston P.M., García M.B. 2007. An extraordinary life span estimate for the clown anemonefish Amphiprion percula // J. Fish Biol. V. 70. № 6. P. 1710–1719. https://doi.org/10.1111/j.1095-8649.2007.01445.x
  26. Cleveland A., Verde E.A., Lee R.W. 2011. Nutritional exchange in a tropical tripartite symbiosis: direct evidence for the transfer of nutrients from anemonefish to host anemone and zooxanthellae // Mar. Biol. V. 158. № 3. P. 589–602. https://doi.org/10.1007/s00227-010-1583-5
  27. Colleye O., Vandewalle P., Lanterbecq D. et al. 2011. Interspecific variation of calls in clownfishes: degree of similarity in closely related species // BMC Evol. Biol. V. 11. Article 365. https://doi.org/10.1186/1471-2148-11-365
  28. Colleye O., Iwata E., Parmentier E. 2016. Clownfishes // Biology of damselfishes. Boca Raton: CRC Press. P. 246–266. https://doi.org/10.1201/9781315373874
  29. Daly M., Brugler M.R., Cartwright P. et al. 2007. The phylum Cnidaria: a review of phylogenetic patterns and diversity 300 years after Linnaeus // Zootaxa. V. 1668. P. 127–182. https://doi.org/10.5281/zenodo.180149
  30. Dixson D.L., Jones G.P., Munday P.L. et al. 2008. Coral reef fish smell leaves to find island homes // Proc. R. Soc. B. V. 275. № 1653. P. 2831–2839. https://doi.org/10.1098/rspb.2008.0876
  31. Dixson D.L., Munday P.L., Pratchett M., Jones G.P. 2011. Ontogenetic changes in responses to settlement cues by Anemonefish // Coral Reefs. V. 30. № 4. P. 903–910. https://doi.org/10.1007/s00338-011-0776-9
  32. Døving K.B. 1986. Functional properties of the fish olfactory system // Progress in Sensory Physiology. V. 6. Berlin; Heidelberg: Springer. P. 39–104. https://doi.org/10.1007/978-3-642-70411-6_2
  33. Døving K.B., Kasumyan A.O. 2008. Chemoreception // Fish Larval Physiology. Boca Raton: CRC Press. P. 331–394. https://doi.org/10.1201/9780429061608-15
  34. Elliott J.K., Mariscal R.N. 2001. Coexistence of nine anemonefish species: differential host and habitat utilization, size and recruitment // Mar. Biol. V. 138. № 1. P. 23–36. https://doi.org/10.1007/s002270000441
  35. Elliott J.K., Lougheed S.C., Bateman B. et al. 1999. Molecular phylogenetic evidence for the evolution of specialization in anemone fishes // Proc. R. Soc. Lond. B. V. 266. № 1420. P. 677–685. https://doi.org/10.1098/rspb.1999.0689
  36. Fautin D.G., Allen G.R. 1997. Field guide to anemonefishes and their host sea anemones. Perth: West. Aust. Mus., 159 p.
  37. Feeney W.E., Brooker R.M. 2017. Anemonefishes // Curr. Biol. V. 27. № 1. P. R6–R8. https://doi.org/10.1016/j.cub.2016.07.046
  38. Froese R., Pauly D. (eds.). 2023. FishBase. World Wide Web electronic publication (www.fishbase.org. Version 03/2023).
  39. Garwood R.J., Behnsen J., Ramsey A.T. et al. 2020. The functional nasal anatomy of the pike, Esox lucius L. // Comp. Biochem. Physiol. Pt. A. Mol. Integr. Physiol. V. 244. Article 110688. https://doi.org/10.1016/j.cbpa.2020.110688
  40. Hattori A. 1995. Coexistence of two anemonefishes, Amphiprion clarkii and A. perideraion, which utilize the same host sea anemone // Environ. Biol. Fish. V. 42. № 4. P. 345–353. https://doi.org/10.1007/BF00001464
  41. Hobbs J.-P.A., Frisch A.J., Ford B.M. et al. 2013. Taxonomic, spatial and temporal patterns of bleaching in anemones inhabited by anemonefishes // PLоS One. V. 8. № 8. Article e70966. https://doi.org/10.1371/journal.pone.0070966
  42. Holl A. 1965. Vergleichende morphologische und histologische Untersuchungen am Geruchsorgan der Knochenfische // Z. Morph. Ökol. Tiere. V. 54. № 6. P. 707–782. https://www.jstor.org/stable/43262175
  43. Iwata E., Manbo J. 2013. Territorial behaviour reflects sexual status in groups of false clown anemonefish (Amphiprion ocellaris) under laboratory conditions // Acta Ethol. V. 16. № 2. P. 97–103. https://doi.org/10.1007/s10211-012-0142-0
  44. Jones G.P., Planes S., Thorrold S.R. 2005. Coral reef fish larvae settle close to home // Curr. Biol. V. 15. № 14. P. 1314–1318. https://doi.org/10.1016/j.cub.2005.06.061
  45. Jones G.P., Srinivasan M., Galbraith G.F. et al. 2022. Saving Nemo. Extinction risk, conservation status, and effective management strategies for anemonefishes // Evolution, development and ecology of anemonefishes: model organisms for marine science. Boca Raton: CRC Press. P. 285–297. https://doi.org/10.1201/9781003125365-30
  46. Kasumyan A.O. 2004. The olfactory system in fish: structure, function, and role in behavior // J. Ichthyol. V. 44. Suppl. 2. P. S180–S223.
  47. Kavanagh K.D., Alford R.A. 2003. Sensory and skeletal development and growth in relation to the duration of the embryonic and larval stages in damselfishes (Pomacentridae) // Biol. J. Linn. Soc. V. 80. № 2. P. 187–206. https://doi.org/10.1046/j.1095-8312.2003.00229.x
  48. Klann M., Mercader M., Salis P. et al. 2022. Anemonefishes // Handbook of marine model organisms in experimental biology. Boca Raton: CRC Press. P. 443–464. https://doi.org/10.1201/9781003217503-24
  49. Kleerekoper H. 1969. Olfaction in fishes. Bloomington: Ind. Univ. Press, 222 p.
  50. Lara M.R. 2008. Development of the nasal olfactory organs in the larvae, settlement-stages and some adults of 14 species of Caribbean reef fishes (Labridae, Scaridae, Pomacentridae) // Mar. Biol. V. 154. № 1. P. 51–64. https://doi.org/10.1007/s00227-007-0899-2
  51. Litsios G., Pearman P.B., Lanterbecq D. et al. 2014. The radiation of the clownfishes has two geographical replicates // J. Biogeogr. V. 41. № 11. P. 2140–2149. https://doi.org/10.1111/jbi.12370
  52. Madduppa H.H., Timm J., Kochzius M. 2018. Reduced genetic diversity in the clown anemonefish Amphiprion ocellaris in exploited reefs of Spermonde Archipelago, Indonesia // Front. Mar. Sci. V. 5. Article 80. https://doi.org/10.3389/fmars.2018.00080
  53. Manassa R.P., Dixson D.L., McCormick M.I., Chivers D.P. 2013a. Coral reef fish incorporate multiple sources of visual and chemical information to mediate predation risk // Anim. Behav. V. 86. № 4. P. 717–722. https://doi.org/10.1016/j.anbehav.2013.07.003
  54. Manassa R.P., McCormick M.I., Chivers D.P., Ferrari M.C.O. 2013b. Social learning of predators in the dark: understanding the role of visual, chemical and mechanical information // Proc. R. Soc. B. V. 280. № 1765. Article 20130720. https://doi.org/10.1098/rspb.2013.0720
  55. Miyagawa K., Hidaka T. 1980. Amphiprion clarkii juvenile: innate protection against and chemical attraction by symbiotic sea anemones // Proc. Jpn. Acad. Ser. B. V. 56. № 6. P. 356–361. https://doi.org/10.2183/pjab.56.356
  56. Miyagawa-Kohshima K., Odoriba S., Okabe D. et al. 2014. Embryonic learning of chemical cues via the parents’ host in anemonefish (Amphiprion ocellaris) // J. Exp. Mar. Biol. Ecol. V. 457. P. 160–172.
  57. http://doi.org/10.1016/j.jembe.2014.04.004
  58. Moyer J.T. 1980. Influence of temperate waters on the behavior of the tropical anemonefish Amphiprion clarkii at Miyake-jima, Japan // Bull. Mar. Sci. V. 30. Suppl. 1. P. 261–272.
  59. Moyer J.T., Steene R.C. 1979. Nesting behavior of the anemonefish Amphiprion polymnus // Jpn. J. Ichthyol. V. 26. № 2.
  60. http://doi.org/10.11369/jji1950.26.209
  61. Murphy B.F., Leis J.M., Kavanagh K.D. 2007. Larval development of the Ambon damselfish Pomacentrus amboinensis, with a summary of pomacentrid development // J. Fish. Biol. V. 71. № 2. P. 569–584. https://doi.org/10.1111/j.1095-8649.2007.01524.x
  62. Nelson J.S. 2006. Fishes of the World. Hoboken: John Wiley and Sons, 601 p.
  63. Nguyen H.-T.T., Tran A.-N.T., Ha L.T.L. et al. 2019. Host choice and fitness of anemonefish Amphiprion ocellaris (Perciformes: Pomacentridae) living with host anemones (Anthozoa: Actiniaria) in captive conditions // J. Fish Biol. V. 94. № 6. P. 937–947. https://doi.org/10.1111/jfb.13910
  64. Nguyen H.-T.T., Dang B.T., Glenner H., Geffen A.J. 2020. Cophylogenetic analysis of the relationship between anemonefish Amphiprion (Perciformes: Pomacentridae) and their symbiotic host anemones (Anthozoa: Actiniaria) // Mar. Biol. Res. V. 16. № 2. P. 117–133. https://doi.org/10.1080/17451000.2020.1711952
  65. Pryor S.H., Hill R., Dixson D.L. et al. 2020. Anemonefish facilitate bleaching recovery in a host sea anemone // Sci. Rep. V. 10. Article 18586. https://doi.org/10.1038/s41598-020-75585-6
  66. Randall J.E., Allen G.R., Steene R.C. 1997. Fishes of the Great Barrier Reef and Coral Sea. Bathurst: Crawford House Publ., 580 р.
  67. Ricciardi F., Boyer M., Ollerton J. 2010. Assemblage and interaction structure of the anemonefish-anemone mutualism across the Manado region of Sulawesi, Indonesia // Environ. Biol. Fish. V. 87. № 4. P. 333–347. https://doi.org/10.1007/s10641-010-9606-0
  68. Roopin M., Chadwick N.E. 2009. Benefits to host sea anemones from ammonia contributions of resident anemonefish // J. Exp. Mar. Biol. Ecol. V. 370. № 1–2. P. 27–34. https://doi.org/10.1016/j.jembe.2008.11.006
  69. Roux N., Lecchini D. 2015. Clownfish chemically recognized their sea-anemone host at settlement // Vie Milieu. V. 65. № 1. P. 17–20.
  70. Roux N., Salis P., Lambert A. et al. 2019. Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris) // Devel. Dyn. V. 248. № 7. P. 545–568. https://doi.org/10.1002/dvdy.46
  71. Shuman C.S., Hodgson G., Ambrose R.F. 2005. Population impacts of collecting sea anemones and anemonefish for the marine aquarium trade in the Philippines // Coral Reefs. V. 24. № 4. P. 564–573. https://doi.org/10.1007/s00338-005-0027-z
  72. Tang K.L., Stiassny M.L.J., Mayden R.L., DeSalle R. 2021. Systematics of Damselfishes // Ichthyol. Herpetol. V. 109. № 1. 258–318. https://doi.org/10.1643/i2020105
  73. Yamamoto M. 1982. Comparative morphology of fish olfactory organ in teleosts // Chemoreception in fishes N.Y.: Elsevier. P. 39–59.
  74. Yamamoto M., Ueda K. 1979. Comparative morphology of fish olfactory epithelium. X. Perciformes, Beryciformes, Scorpaeniformes, and Pleuronectiformes // J. Fac. Sci. Univ. Tokyo. V. 14. P. 273–297.
  75. Zeiske E., Theisen B., Breucker H. 1992. Structure, development, and evolutionary aspects of the peripheral olfactory system // Fish chemoreception. Dordrecht: Springer. P. 13–39. https://doi.org/10.1007/978-94-011-2332-7_2

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2. Fig. 1. Location of the olfactory organ in amphiprions: a, b – Amphiprion clarkii TL 11.0 cm; c – A. polymnus TL 8.7 cm, d – A. frenatus TL 9.7 cm, d – A. ocellaris TL 5.3 cm; e – A. perideraion TL 8.0 cm, top left view. Here and in Fig. 2: H – nostril; G – eye; HF – upper jaw. Scale, mm: a – 5.0; b, d, d – 1.0; c – 0.5; e – 2.0.

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3. Fig. 2. The nostril of amphiprions: a, b – A. polymnus TL 12.5 and 2.43 cm; c – A. polymnus TL 14.0 cm, view from the olfactory cavity; d – Amphiprion clarkii TL 11.0 cm; d – A. frenatus TL 9.7 cm; e – A. perideraion TL 8.0 cm. Directions (↔): D–V – dorsoventral, R–K – rostrocaudal. Scale: 0.5 mm.

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4. Fig. 3. Diagram of the olfactory socket of Amphiprion clarkii (a) and A. polymnus (b): C – septa of the central fold; folds: (*) – forked, (+) – unrelated to the septa.

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5. Fig. 4. Olfactory socket in amphiprions: a – Amphiprion clarkii TL 11.0 cm, b – A. perideraion TL 8.0 cm, c – A. ocellaris TL 5.3 cm, d – A. polymnus TL 8.0 cm; d – A. frenatus TL 9.7, 10.0 and 12.5 cm, respectively. LM, EM – holes lacrimal and ethmoidal ventilation bags; N – nasale; (→) – intercalary folds, (↑→) – dichotomous fold. The remaining symbols are shown in Fig. 2, 3. Scale, mm: a, b – 0.5; c–i – 1.0.

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6. Fig. 5. The shape of the folds located in the caudal part of the olfactory rosette: a, b – Amphiprion clarkii, A. frenatus and A. ocellaris; c, d – A. polymnus; e, e – A. perideraion; a, c, d – side view of the fold; b, d, e – vertical profile of the fold.

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7. 6. Atypical folds in the olfactory socket of Amphiprion polymnus: a, b – horizontally dichotomous folds with narrowly and widely diverging blades, respectively; c – vertically dichotomous fold, d–e – intercalary fold (→) at different stages of formation.

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8. Fig. 7. Atypical folds in the olfactory socket of amphiprions: a, b, c, d – Amphiprion polymnus TL 8.2, 12.0, 9.2 and 8.0 cm, respectively; d – A. frenatus TL 9.8 cm; e – A. perideraion TL 7.0 cm; (*) – thickening of the distal parts of the folds, (▽) – unusual secondary folding. The rest of the designations are shown in Fig. 2, 4. Scale: 1.0 mm.

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9. Рис. 8. Обитает в обособленной зоне от наземной части тела (TL) у амфиприона полимнуса (●, --), A. clarkii (▲, ---) и A. frenatus (■, − · −).

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10. Fig. 9. Phylogenetic relationships of fish of the genus Amphiprion (according to: Tang et al., 2021); an increase in the number of asterisks (★) reflects the morphological complexity of the olfactory organ in the studied species.

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