Вкусовая привлекательность изомеров аминокислот для цихлидовых рыб (Cichlidae)

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Abstract

Представлены результаты сравнения вкусовой привлекательности L-α- и D-α-изомеров аланина, аспарагиновой и глутаминовой кислот, триптофана, а также L-α- и L-β-изомеров аланина для мозамбикской Oreochromis mossambicus и нильской O. niloticus тиляпий, золотого меланохрома Melanochromis auratus, апельсинового неолампрологуса Neolamprologus leleupi и цихлазомы Хартвега Vieja hartwegi. Потребление агар-агаровых гранул с L-α- и D-α-изомерами аспарагиновой и глутаминовой кислот и триптофана различается у мозамбикской тиляпии и цихлазомы Хартвега, аланина и триптофана – у золотого меланохрома, аспарагиновой кислоты и триптофана – у апельсинового неолампрологуса, аспарагиновой кислоты – у нильской тиляпии. Вкусовая привлекательность L-α- и L-β-изомеров аланина достоверно разная у мозамбикской тиляпии, апельсинового неолампрологуса и цихлазомы Хартвега. Пищевое поведение, проявляемое цихлидами в ходе оросенсорного тестирования гранул, сходное и мало зависит от вкусовой привлекательности гранул. Все цихлиды совершают небольшое число отверганий и повторных схватываний гранул, большинство цихлид удерживают гранулы в ротовой полости многократно дольше по времени в опытах, завершающихся потреблением. Разные вкусовые свойства оптических и структурных изомеров аминокислот для исследованных цихлид указывают на видовую специфичность вкусовых предпочтений у рыб и свидетельствуют о том, что эти вещества являются важными химическими регуляторами трофических отношений в водных сообществах.

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About the authors

А. Д. Левина

Московский государственный университет

Author for correspondence.
Email: alex_kasumyan@mail.ru
Russian Federation, Москва

А. О. Касумян

Московский государственный университет

Email: alex_kasumyan@mail.ru
Russian Federation, Москва

References

  1. Виноградская М.И., Михайлова Е.С., Касумян А.О. 2017. Вкусовые предпочтения, оросенсорное тестирование и генерация звуков при питании у жемчужного гурами Trichopodus leerii (Osphronemidae) // Вопр. ихтиологии. Т. 57. № 3. С. 324–337. https://doi.org/10.7868/S004287521703016X
  2. Касумян A.O. 2016. Вкусовая привлекательность и физико-химические и биологические свойства свободных аминокислот (на примере рыб) // Журн. эволюц. биохимии и физиологии. Т. 52. № 4. С. 245–254.
  3. Касумян А.О., Исаева О.М. 2023. Вкусовые предпочтения карповых рыб (Cyprinidae). Сравнительное исследование // Вопр. ихтиологии. Т. 63. № 1. С. 81–109. https://doi.org/10.31857/S0042875223010071
  4. Касумян А.О., Левина А.Д. 2023. Сравнение вкусовой рецепции и пищевого поведения у нильской тиляпии Oreochromis niloticus (Cichlidae) разного возраста // Там же. Т. 63. № 4. С. 462–471. https://doi.org/10.31857/S0042875223030086
  5. Касумян А.О., Михайлова Е.С. 2017. Вкусовая привлекательность стереоизомеров и других производных аминокислот для рыб // Журн. эволюц. биохимии и физиологии. Т. 53. № 4. С. 282–287.
  6. Aragão C., Conceição L.E.C., Dinis M.T., Fyhn H.-J. 2004. Amino acid pools of rotifers and Artemia under different conditions: nutritional implications for fish larvae // Aquaculture. V. 234. № 1–4. P. 429–445. https://doi.org/10.1016/j.aquaculture.2004.01.025
  7. Blais J., Rico C., van Oosterhout C. et al. 2007. MHC adaptive divergence between closely related and sympatric African cichlids // PLоS One. V. 2. № 8. Article e734. https://doi.org/10.1371/journal.pone.0000734
  8. Brawand D., Wagner C.E., Li Y.I. et al. 2014. The genomic substrate for adaptive radiation in African cichlid fish // Nature. V. 513. № 7518. P. 375–381. https://doi.org/10.1038/nature13726
  9. Bruckner H., Hausch M. 1990. D-amino acids in food: detection and nutritional aspects // Chirality and biological activity. N.Y.: Alan R. Liss, Inc. P. 129–136.
  10. Burress E.D. 2015. Cichlid fishes as models of ecological diversification: patterns, mechanisms, and consequences // Hydrobiologia. V. 748. № 1. P. 7–27. https://doi.org/10.1007/s10750-014-1960-z
  11. Caprio J. 1975. High sensitivity of catfish taste receptors to amino acids // Comp. Biochem. Physiol. Pt. A. Physiol. V. 52. № 1. P. 247–251. https://doi.org/10.1016/s0300-9629(75)80160-5
  12. Caprio J., Shimohara M., Marui T. et al. 2015. Amino acid specificity of fibers of the facial/trigeminal complex innervating the maxillary barbel in the Japanese sea catfish, Plotosus japonicus // Physiol. Behav. V. 152. Pt. A. P. 288–294.
  13. http://doi.org/10.1016/j.physbeh.2015.10.011
  14. Corrigan J.J. 1969. D-amino acids in animals // Science. V. 164. № 3876. P. 142–149. https://doi.org/10.1126/science.164.3876.142
  15. Danley P.D., Husemann M., Chetta J. 2012. Acoustic diversity in Lake Malawi’s rock-dwelling cichlids // Environ. Biol. Fish. V. 93. № 1. P. 23–30. https://doi.org/10.1007/s10641-011-9886-z
  16. DeLorenzo L., DeBrock V., Carmona Baez A. et al. 2022. Morphometric and genetic description of trophic adaptations in cichlid fishes // Biology. V. 11. № 8. Article 1165. https://doi.org/10.3390/biology11081165
  17. Falco F., Stincone P., Cammarata M., Brandelli A. 2020. Amino acids as the main energy source in fish tissues // Aquac. Fish. Stud. V. 3. № 1. P. 1–11. https://doi.org/10.31038/AFS.2020223
  18. Felbeck H., Wiley D. 1987. Free D-amino acids in the tissues in marine bivalves // Biol. Bull. V. 173. № 1. P. 252–259. https://doi.org/10.2307/1541877
  19. Froese R., Pauly D. (eds.). 2022. FishBase. World Wide Web electronic publication. (www.fishbase.org. Version 08/2022).
  20. Gill A.B., Hart P.J.B. 1996. Unequal competition between three-spined stickleback, Gasterosteus aculeatus L., encountering sequential prey // Anim. Behav. V. 51. № 3. P. 689–698. https://doi.org/10.1006/anbe.1996.0072
  21. Hara T.J. 2007. Gustation // Sensory systems neuroscience. N.Y.: Acad. Press. P. 45–96. https://doi.org/10.1016/S1546-5098(06)25002-7
  22. Hara T.J., Sveinsson T., Evans R.E., Klaprat D.A. 1993. Morphological and functional characteristics of the olfactory and gustatory organs of three Salvelinus species // Can. J. Zool. V. 71. № 2. P. 414–423. https://doi.org/10.1139/Z93-058
  23. Hofmann C.M., O’Quin K.E., Marshall N.J. et al. 2009. The eyes have it: regulatory and structural changes both underlie cichlid visual pigment diversity // PLoS Biol. V. 7. № 12. Article e1000266. https://doi.org/10.1371/journal.pbio.1000266
  24. Iwasaki K., Kasahara T., Sato M. 1985. Gustatory effectiveness of amino acids in mice: behavioral and neurophysiological studies // Physiol. Behav. V. 34. № 4. P. 531–542. https://doi.org/10.1016/0031-9384(85)90045-9
  25. Jones K.A. 1990. Chemical requirements of feeding in rainbow trout, Oncorhynchus mykiss (Walbaum); palatability studies on amino acids, amides, amines, alcohols, aldehydes, saccharides, and other compounds // J. Fish Biol. V. 37. № 3. P. 413–423. https://doi.org/10.1111/J.1095-8649.1990.TB05872.X
  26. Kasumyan A.O. 2019. The taste system in fishes and the effects of environmental variables // Ibid. V. 95. № 1. P. 155–178. https://doi.org/10.1111/jfb.13940
  27. Kasumyan A., Levina A. 2023. Are the taste preferences similar in closely related fish of the same trophic category? A case of Nile and Mozambique tilapias // Rev. Fish Biol. Fish. V. 33. P. 1371–1386. https://doi.org/10.1007/s11160-023-09763-w
  28. Kasumyan A.O., Mouromtsev G.E. 2020. The teleost fish, blue gourami Trichopodus trichopterus, distinguishes the taste of chemically similar substances // Sci. Rep. V. 10. Article 7487. https://doi.org/10.1038/s41598-020-64556-6
  29. Kawai M., Sekine-Hayakawa Y., Okiyama A., Ninomiya Y. 2012. Gustatory sensation of L- and D-amino acids in humans // Amino Acids. V. 43. № 6. P. 2349–2358. https://doi.org/10.1007/s00726-012-1315-x
  30. Kiyohara S., Yamashita S., Harada S. 1981. High sensitivity of minnow gustatory receptors to amino acids // Physiol. Behav. V. 26. № 6. P. 1103–1108. https://doi.org/10.1016/0031-9384(81)90215-8
  31. Kohbara J., Michel W., Caprio J. 1992. Responses of single facial taste fibres in the channel catfish, Ictalurus punctatus, to amino acids // J. Neurophysiol. V. 68. № 4. P. 1012–1026. https://doi.org/10.1152/jn.1992.68.4.1012
  32. Kohbara J., Oohara K., Masuda T. et al. 2002. Gustatory receptor responses in marbled rockfish Sebastiscus marmoratus // Fish. Sci. V. 68. № 4. P. 862–871. https://doi.org/10.1046/j.1444-2906.2002.00504.x
  33. Konings A. 1991. Neolamprologus mustax (Poll, 1978) // The cichlids yearbook. V. 1. P. 15.
  34. Konings A. 2005. Guide to Tanganyika cichlids. El Paso: Cichlid Press, 192 p.
  35. Levina A.D., Mikhailova E.S., Kasumyan A.O. 2021. Taste preferences and feeding behavior in the facultative herbivore fish, Nile tilapia Oreochromis niloticus // J. Fish Biol. V. 98. № 5. P. 1385–1400. https://doi.org/10.1111/jfb.14675
  36. Li X., Zheng S., Wu G. 2021a. Nutrition and functions of amino acids in fish // Amino acids in nutrition and health. Cham: Springer. P. 133–168. https://doi.org/10.1007/978-3-030-54462-1_8
  37. Li X., Han T., Zheng S., Wu G. 2021b. Nutrition and functions of amino acids in aquatic crustaceans // Ibid. P. 169–198. https://doi.org/10.1007/978-3-030-54462-1_9
  38. Marui T., Evans R.E., Zielinski B., Hara T.J. 1983a. Gustatory responses of the rainbow trout (Salmo gairdneri) palate to amino acids and derivatives // J. Comp. Physiol. V. 153. № 4. P. 423–433. https://doi.org/10.1007/BF00612597
  39. Marui T., Harada S., Kasahara Y. 1983b. Gustatory specificity for amino acids in the facial taste system of the carp, Cyprinus carpio L. // Ibid. V. 153. № 3. P. 299–308. https://doi.org/10.1007/BF00612584
  40. Meredith T.L., Kajiura S.M. 2010. Olfactory morphology and physiology of elasmobranchs // J. Exp. Biol. V. 213. № 20. P. 3449–3456. https://doi.org/10.1242/jeb.045849
  41. Michel W., Caprio J. 1991. Responses of single facial taste fibres in the sea catfish, Arius felis, to amino acids // J. Neurophysiol. V. 66. № 1. P. 247–260. https://doi.org/10.1152/jn.1991.66.1.247
  42. Michel W.C., Kohbara J., Caprio J. 1993. Amino acid receptor sites in the facial taste system of the sea catfish Arius felis // J. Comp. Physiol. A. V. 172. № 2. P. 129–138. https://doi.org/10.1007/BF00189391
  43. Olsén K.H. 1993. Emission rate of amino acids and ammonia and their role in olfactory preference behaviour of juvenile Arctic charr, Salvelinus alpinus (L.) // J. Fish Biol. V. 28. № 3. P. 255–265. https://doi.org/10.1111/j.1095-8649.1986.tb05163.x
  44. Preston R.L. 1987. Occurrence of D-amino acids in higher organisms: a survey of the distribution of D-amino acids in marine invertebrates // Comp. Biochem. Physiol. Pt. B. Comp. Physiol. V. 87. № 1. P. 55–62. https://doi.org/10.1016/0305-0491(87)90470-6
  45. Reinthal P.N. 1990. The feeding habits of a group of herbivorous rock-dwelling cichlid fishes (Cichlidae: Perciformes) from Lake Malawi, Africa // Environ. Biol. Fish. V. 27. № 3. P. 215–233. https://doi.org/10.1007/BF00001674
  46. Ribbink A.J., Marsh B.A., Marsh A.C. et al. 1983. A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi // S. Afr. J. Zool. V. 18. № 3. P. 149–310. https://doi.org/10.1080/02541858.1983.11447831
  47. Ronco F., Matschiner M., Böhne A. et al. 2021. Drivers and dynamics of a massive adaptive radiation in cichlid fishes // Nature. V. 589. № 7840. P. 76–81. https://doi.org/10.1038/s41586-020-2930-4
  48. Schiffman S.S., Sennewald K., Cagnon J. 1981. Comparison of taste qualities and thresholds of D- and L-amino acids // Physiol. Behav. V. 27. № 1. P. 51–57. https://doi.org/10.1016/0031-9384(81)90298-5
  49. Silver W.L., Finger T.E. 1984. Electrophysiological examination of a non-olfactory, non-gustatory chemosense in the searobin, Prionotus carolinus // J. Comp. Physiol. A. V. 154. № 2. P. 167–174. https://doi.org/10.1007/BF00604982
  50. Smith M.P. 2008. Lake Tanganyika cichlids. Hauppauge: Barron’s Educational Ser., 96 p.
  51. Sola C., Tongiorgi P. 1998. Behavioural responses of glass eels of Anguilla anguilla to non-protein amino acids // J. Fish Biol. V. 53. № 6. P. 1253–1262. https://doi.org/10.1111/j.1095-8649.1998.tb00246.x
  52. Tiancheng L., Yiming H. 1994. Gustation and taste organ in the barbel of the African catfish // Acta Hydrobiol. Sinica. V. 18. № 4. P. 316–326.
  53. Velez Z., Hubbard P.C., Hardege J.D. et al. 2007. The contribution of amino acids to the odour of a prey species in the Senegalese sole (Solea senegalensis) // Aquaculture. V. 265. № 1–4. P. 336–342. https://doi.org/10.1016/j.aquaculture.2007.02.029
  54. Wagner C.E. 2021. Ecological opportunity, genetic variation, and the origins of African cichlid radiations // The behavior, ecology and evolution of cichlid fishes. Dordrecht: Springer. P. 79–105. https://doi.org/10.1007/978-94-024-2080-7_3
  55. Wegert S., Caprio J. 1991. Receptor sites for amino acids in the facial taste system of the channel catfish // J. Comp. Physiol. A. V. 168. № 2. P. 201–211. https://doi.org/10.1007/BF00218412
  56. Wu G. 2021. Amino acids: biochemistry and nutrition. Boca Raton: CRC Press, 816 p.
  57. Wu G, Wu Z., Dai Z. et al. 2013. Dietary requirements of “nutritionally nonessential amino acids” by animals and humans // Amino Acids. V. 44. № 4. P. 1107–1113. https://doi.org/10.1007/s00726-012-1444-2
  58. Yamamoto Y., Shibata H., Ueda H. 2013. Olfactory homing of chum salmon to stable compositions of amino acids in natal stream water // Zool. Sci. V. 30. № 8. P. 607–612. https://doi.org/10.2108/zsj.30.607
  59. Yoshii K., Kamo N., Kurihara K., Kobatake Y. 1979. Gustatory responses of eel palatine receptors to amino acids and carboxylic acids // J. Gen. Physiol. V. 74. № 3. P. 301–317. https://doi.org/10.1085/jgp.74.3.301
  60. Yuma M. 1994. Food habits and foraging behaviour of benthivorous cichlid fishes in Lake Tanganyika // Environ. Biol. Fish. V. 39. № 2. P. 173–182. https://doi.org/10.1007/BF00004935
  61. Yuma M. 1998. Food resources of shrimp-eating cichlid fishes in Lake Tanganyika // Ibid. V. 52. № 1–3. P. 371–378. https://doi.org/10.1023/A:1007370204240

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2. Fig. 1. Parameters of the taste response to granules with amino acid isomers and Chironomidae extract in the Nile Oreochromis niloticus and Mozambique O. mossambicus tilapia, golden melanochrome Melanochromis auratus, orange Neolamprologus Neolamprologus leleupi and Hartweg's cichlazoma Vieja hartwegi: a – the number of grasps of the pellet; b, c – the duration of retention granules after the first setting (b) and during the entire experiment (c). Granule type: 1-3 (0.1 M): 1 – L-α-alanine, 2– D-α-alanine, 3– L-β-alanine; 4-9 (0.01 M): 4– L-α-aspartic acid, 5– D-α-aspartic acid, 6 – L-α-glutamic acid, 7– D-α-glutamic acid, 8– L-α-tryptophan, 9– D-α-tryptophan; 10 – Chironomidae extract (175 g/l), 11 – control; () – average error; differences in the consumption of granules with substances from the control are significant at p: * < 0.05, ** < 0.01, *** < 0.001.

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3. Fig. 2. Parameters of the taste response in experiments that ended with the consumption (n) and rejection (n) of granules with amino acid isomers and Chironomidae extract in the Nile Oreochromis niloticus and Mozambique O. mossambicus tilapia, golden melanochrome Melanochromis auratus, orange Neolamprologus Neolamprologus leleupi and Hartweg's cichlazoma Vieja hartwegi: a – the number of gripping granules; b, c – the duration of retention of the pellet after the first setting (b) and during the entire experiment (c); differences in pairs of experiments are significant at p: * < 0.05, ** < 0.01, *** < 0.001. The rest of the designations are shown in Fig. 1.

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4. Fig. 3. The index of taste attractiveness of amino acid isomers for the Nile Oreochromis niloticus and Mozambique O. mossambicus tilapia, golden melanochrome Melanochromis auratus, orange neolamprologus Neolamprologus leleupi and Hartweg's cichlasoma Vieja hartwegi. The differences in the consumption of granules with different substances are significant at p: ● < 0.05, ●● < 0.01, ●●● < 0.001; ost. See the designations in Fig. 1.

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5. Fig. 4. Parameters of the taste response to granules with amino acids and Chironomidae extract in the Mozambican tilapia Oreochromis mossambicus according to the results of this study (■) and information from: Kasumyan, Levina, 2023 (): a – consumption of granules, b – number of grasps of the pellet; c, d – duration of retention of the pellet after the first setting (c) and throughout the experiment (d). Granule type: 1– L-α-alanine (0.1 M), 2– L-α-aspartic acid (0.01 M), 3– L-α-glutamic acid (0.01 M), 4– L-α-tryptophan (0.1 M), 5 – Chironomidae extract (175 g/l), 6 – control; ost. See notation in Fig. 1.

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