Pheromones in Fishes

Year 2019, Volume: 15 Issue: 2, 252 - 261, 14.06.2019

Gülsemin Şen Ağılkaya , Sahire Karaytuğ , İsa Şen

https://doi.org/10.22392/actaquatr.576789

Abstract

Pheromones are externally secreted organic compounds that are involved in the communication between the individuals
of same species. Many life activities, such as group formation and recognition of individual, alarm communication, parentchild recognition, sexual attraction, as well as synchronized reproduction success and migration in fish are shaped by the
pheromones. Pheromones of fishes can be classified as follows; Alarm Pheromones, Migration Pheromones, Sex
Pheromones, Communication (Social) Pheromones. Having enough knowledge about pheromones, it will be possible to
utilize pheromones in the implementation of incubation management in aquaculture. In the future, the use of specific
pheromones will reduce the damage caused by hormone and drug use in aquaculture. Using chemical markers, cannibalism
inhibitors, growth stimulators, selective attractants and pheromones added to feeds will provide protection and sustainable
production possibilities for endangered species. It can also be argued that pheromones will also contribute to adaptation
studies for the production of new species in aquaculture.

Keywords

Phremones, fish, aquatic

Balıklarda Feromonlar

Abstract

Feromonlar aynı türün bireyleri arasında
iletişimde yer alan eksternal olarak salgılanan organik bileşiklerdir.
Bireylerin grup oluşturmaları ve tanınmaları, alarm iletişimi, ebeveyn-yavru
tanıma, cinsel cazibe, üreme başarısı ve göç gibi senkronize edilen pek çok
yaşamsal faaliyetler, balıklarda feromonlar tarafından şekillendirilmektedir. Balıkların
sahip oldukları feromonları; Alarm Feromonları, Göç Feromonları, Eşey
Feromonları ve İletişim (Sosyal) Feromonları olarak ayırmak ve bunların
nitelikleri hakkında bilgi sahibi olmak mümkündür. Feromonlar hakkında yeterli
düzeyde bilgi sahibi olunması ile su ürünleri yetiştiriciliğinde kuluçkahane
yönetimi uygulamalarında feromonlardan yararlanılabilmesi mümkün olacaktır.
Gelecek dönemlerde spesifik feromonların kullanımı sayesinde su ürünleri
yetiştiriciliğinde hormon ve ilaç kullanımından kaynaklanan zararlar
azaltılabilecektir. Kimyasal belirteçler, kanibalizm inhibitörleri, büyüme
stimülatörleri, seçici cezbediciler ve yemlere eklenen feromonlar kullanılarak
nesli tükenmekte olan türlerin korunması ve sürdürülebilir üretim imkânı ortaya
çıkacaktır. Ayrıca feromonların, su ürünleri yetiştiriciliğinde yeni türlerin
üretimi için adaptasyon çalışmalarına da katkı getireceği ileri sürülebilir.

Keywords

Feromon, balık, sucul, entegre zararlı yönetimi

References

• Barata, E. N., Hubbard, P. C., Almeida, O. G., Miranda, A., & Canário, A. V. (2007). Male urine signals social rank in the Mozambique tilapia (Oreochromis mossambicus). BMC Biology, 5(1), 54.
• Barata, E. N., Fine, J. M., Hubbard, P. C., Almeida, O. G., Frade, P., Sorensen, P. W., & Canário, A. V. (2008). A sterol-like odorant in the urine of Mozambique tilapia males likely signals social dominance to females. Journal of Chemical Ecology, 34(4), 438-449.
• Bardach, J. E., Fujiya, M., & Holl, A. (1965). Detergents: effects on the chemical senses of the fish Ictalurus natalis (le Sueur). Science, 148(3677), 1605-1607.
• Barnett, C. (1981). The role of urine in parent‐offspring communication in a cichlid fish. Zeitschrift für Tierpsychologie, 55(2), 173-182.
• Barnett, C. (1982). The chemosensory responses of young cichlid fish to parents and predators. Animal Behaviour, 30(1), 35-42.
• Bassler, B. L., & Winans, S. C. (2008). Chemical communication among bacteria (p. 279). S. C. Winans, & B. L. Bassler (Eds.). Washington, DC: ASM Press.
• Belanger, R. M., Smith, C. M., Corkum, L. D., & Zielinski, B. S. (2003). Morphology and histochemistry of the peripheral olfactory organ in the round goby, Neogobius melanostomus (Teleostei: Gobiidae). Journal of Morphology, 257(1), 62-71.
• Bloom, H. D., & Perlmutter, A. (1978). Possible pheromone mediated reproductive isolation in two species of cyprinid fishes of the genus, Brachydanio. Journal of Fish Biology, 13(1), 47-50.
• Bodznick, D. (1978). Calcium ion: an odorant for natural water discriminations and the migratory behavior of sockeye salmon. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural and Behavioral Physiology, 127(2), 157-166.
• Brown, S.B., Evans, R.E., Thompson, B.E., & Hara, T.J. (1982). Chemoreception and aquatic pollutants. In: Chemoreception in fish (pp 363–393), Elsevier, Amsterdam.
• Brown, G. E., Brown, J. A., & Wilson, W. R. (1996). The effects of kinship on the growth of juvenile Arctic charr. Journal of Fish Biology, 48(3), 313-320.
• Bryant, B. P., & Atema, J. (1987). Diet manipulation affects social behavior of catfish. Journal of Chemical Ecology, 13(7), 1645-1661.
• Buckland, F. (1880). Natural History of British Fishes, Unwin Pub., London.
• Burnard, D., Gozlan, R. E., & Griffiths, S. W. (2008). The role of pheromones in freshwater fishes. Journal of Fish Biology, 73(1), 1-16.
• Chandrasekhar, K., & Chacko, T. (1970). Effect of electrical stimulation of the olfactory mucosa on the hypothalamo-hypophyseal neurosecretory system in the fresh water teleostean fish, Ophiocephalus punctatus. Indian Journal of Zootomy, 11, 105-113.
• Charlebois, P. M., Corkum, L. D., Jude, D. J., & Knight, C. (2001). The round goby (Neogobius melanostomus) invasion: current research and future needs. Journal of Great Lakes Research, 27(3), 263-266.
• Chidester, F. E. (1924). A critical examination of the evidence for physical and chemical influences on fish migration. Journal of Experimental Biology, 2(1), 79-118.
• Chivers, D. P., & Smith, R. J. F. (1998). Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience, 5(3), 338-352.
• Chivers, D. P., & Mirza, R. S. (2001). Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. In Chemical Signals in Vertebrates 9 (pp. 277-284). Springer, Boston, MA.
• Christie, G. C., & Goddard, C. I. (2003). Sea Lamprey International Symposium (SLIS II): advances in the integrated management of sea lamprey in the Great Lakes. Journal of Great Lakes Research, 29, 1-14.
• Chung-Davidson, Yu-Wen, Mar Huertas, and Weiming Li. (2010). A review of research in fish pheromones." Chemical communication in crustaceans. Springer, New York, NY,. 467-482.
• Cole, K. S., & Smith, R. J. F. (1992). Attraction of female fathead minnows, Pimephales promelas, to chemical stimuli from breeding males. Journal of Chemical Ecology, 18(7), 1269-1284.
• Colombo, L., Marconato, A., Belvedere, P. C., & Friso, C. (1980). Endocrinology of teleost reproduction: a testicular steroid pheromone in the black goby, Gobius jozo L. Italian Journal of Zoology, 47(3-4), 355-364.
• de Caprona, M. D. C. (1974). The effect of chemical stimuli from conspecifics on the behavior of Haplochromis burtoni (Cichlidae, Pisces). Experientia, 30(12), 1394-1395. Doving, K. B., Selset, R., & Thommesen, G. (1980). Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiologica Scandinavica, 108(2), 123-131.
• Fine, J. M., & Sorensen, P. W. (2008). Isolation and biological activity of the multi-component sea lamprey migratory pheromone. Journal of Chemical Ecology, 34(10), 1259-1267.
• Fontaine, M. (1938). La lamproie marine. Sa peche et son importance economique. Bull. Sco. Oceanogr. Fr, 17, 1681-1687.
• Hamdani, E. H., & Døving, K. B. (2005). Specific projection of the sensory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chemical senses, 31(1), 63-67.
• Hara, T.J. (1992). “Fish Chemoreception”, Chapman & Hall, London.
• Hasler, A. D., & Wisby, W. J. (1951). Discrimination of stream odors by fishes and its relation to parent stream behavior. The American Naturalist, 85(823), 223-238.
• Hasler, A. D., & Cooper, J. C. (1976). Chemical cues for homing salmon. Experientia, 32(9), 1091-1093.
• Hasler, A. D. (1983). Synthetic chemicals and pheromones in homing salmon. Control Processes in Fish Physiology, Croom Helm, London, 103-116.
• Hasler, A. D., & Scholz, A. T. (1983). Olfactory imprinting and homing in salmon: Investigations into the mechanism of the imprinting process (Vol. 14). Springer Science & Business Media.
• Hubbard, P. C., Barata, E. N., & Canario, A. V. (2002). Possible disruption of pheromonal communication by humic acid in the goldfish, Carassius auratus. Aquatic toxicology, 60(3-4), 169-183.
• Inland Fisheries Service. (2017). Inland Fisheries Service Carp Management Program, Tasmania, Australia.
• Johnson, R. H., & Nelson, D. R. (1978). Copulation and possible olfaction-mediated pair formation in two species of carcharhinid sharks. Copeia, 1978(3), 539-542.
• Johnston, R. E. (2003). Chemical communication in rodents: from pheromones to individual recognition. Journal of Mammalogy, 84(4), 1141-1162.
• Jude, D. J., Reider, R. H., & Smith, G. R. (1992). Establishment of Gobiidae in the Great Lakes basin. Canadian Journal of Fisheries and Aquatic Sciences, 49(2), 416-421.
• Kasumyan, A. O., & Lebedeva, N. Y. (1979). New data on the nature of the alarm pheromone in cyprinids. Journal of Ichthyology, 19, 109-114.
• Kawabata, K. (1993). Induction of sexual behavior in male fish (Rhodeus ocellatus ocellatus) by amino acids. Amino Acids, 5(3), 323-327.
• Kikuyama, S., Toyoda, F., Iwata, T., Umezawa, K., Takahashi, N., Matsukawa, H., & Miura, S. (1998). Sodefrin, a novel peptide pheromone in the newt cloacal gland. Annals of the New York Academy of Sciences, 839(1), 60-65.
• Lebedeva, N. Y., Lebedev, V. I., & Golovkina, T. V. (1994). Pheromone of the trout--stress inducer. Biophysics, 39(3), 527-530.
• Leduc, A. O., Kelly, J. M., & Brown, G. E. (2004). Detection of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests. Oecologia, 139(2), 318-324.
• Li, W., & Sorensen, P. W. (1997). Highly independent olfactory receptor sites for naturally occurring bile acids in the sea lamprey, Petromyzon marinus. Journal of Comparative Physiology A, 180(4), 429-438.
• Li, W., Scott, A. P., Siefkes, M. J., Yun, S. S., & Zielinski, B. (2003). A male pheromone in the sea lamprey (Petromyzon marinus): an overview. Fish Physiology and Biochemistry, 28(1-4), 259-262.
• Liley, N. R. (1980). Patterns of hormonal control in the reproductive behavior of fish, and their relevance to fish management and culture programs. In ICLARM Conference Proceedings (Philippines).
• Lohmann, K. J., Lohmann, C. M., & Endres, C. S. (2008). The sensory ecology of ocean navigation. Journal of Experimental Biology, 211(11), 1719-1728.
• Malyukina, G. A., Martem'yanov, V. I., & Flerova, G. I. (1982). Alarm pheromone as a stress factor for fish. Vopr. Ikhtiol, 22, 338-341
• Mank, J. E., & Avise, J. C. (2006). The evolution of reproductive and genomic diversity in ray‐finned fishes: insights from phylogeny and comparative analysis. Journal of Fish Biology, 69(1), 1-27.
• Matsumura, K. (1995). Tetradoxin as a pheromone. Nature, 378, 563-564.
• McKaye, K. R., & Barlow, G. W. (1976). Chemical recognition of young by the Midas cichlid, Cichlasoma citrinellum. Copeia, 276-282.
• Miles, S. G. (1968). Rheotaxis of elvers of the American eel (Anguilla rostrata) in the laboratory to water from different streams in Nova Scotia. Journal of the Fisheries Board of Canada, 25(8), 1591-1602.
• Moore, H. H., & Schleen, L. P. (1980). Changes in spawning runs of sea lamprey (Petromyzon marinus) in selected streams of Lake Superior after chemical control. Canadian Journal of Fisheries and Aquatic Sciences, 37(11), 1851-1860.
• Moore, A. (1994). An electrophysiological study on the effects of pH on olfaction in mature male Atlantic salmon (Salmo salar) parr. Journal of Fish Biology, 45(3), 493-502.
• Mosher, C. (1954). Observations on the spawning behavior and the early larval development of the sargassum fish, Histrio histrio (Linnaeus). Zoologica, 39(4), 141-152.
• Müller, D. G., Kawai, H., Stache, B., Fölster, E., & Boland, W. (1990). Sexual pheromones and gamete chemotaxis in Analipus japonicus (Phaeophyceae). Experientia, 46(5), 534-536.
• Murphy, C. A., Stacey, N. E., & Corkum, L. D. (2001). Putative steroidal pheromones in the round goby, Neogobius melanostomus: olfactory and behavioral responses. Journal of Chemical Ecology, 27(3), 443-470.
• Newcombe, C., & Hartman, G. (1973). Some chemical signals in the spawning behavior of rainbow trout (Salmo gairdneri). Journal of the Fisheries Board of Canada, 30(7), 995-997.
• Nordeng, H. (1977). A pheromone hypothesis for homeward migration in anadromous salmonids. Oikos, 28, 155-159.
• Olsén, H. (1999). Present knowledge of kin discrimination in salmonids. Genetica, 104(3), 295-299.
• Pandey, A. K. (2005). Recent advances in fish pheromone research with emphasis on their potential applications in fisheries. Journal of Applied Zoological Researches, 16(2), 210-216.
• Pandey, A. K. (2009). Fish pheromones and their potential applications in breeding, aquaculture and fishery management. In: Recent Advances in Hormonal Physiology of Fish and Shellfish Reproduction (pp. 69-98), Narendra Publishing House, Delhi.
• Pandey, A.K. (2012). Recent Advances In Fish Pheromone Research With Emphasis On Their Potential Applications In Aquaculture And Fishery Management. Journal of Experimental Zoology India, 15(1), 1-22.
• Pfeiffer, W., & Lemke, J. (1973). Untersuchungen zur Isolierung und Identifizierung des Schreckstoffes aus der Haut der Elritze, Phoxinus phoxinus (L.)(Cyprinidae, Ostariophysi, Pisces). Journal of Comparative Physiology, 82(4), 407-410.
• Pfeiffer, W. (1978). Heterocyclic compounds as releasers of the fright reaction in the giant danio, Danio malabaricus (Jerdon)(Cyprinidae, Ostariophysi, Pisces). Journal of Chemical Ecology, 4(6), 665-673.
• Pfeiffer, W. (1982). Chemical signals in communication. In: Chemoreception in Fishes”, (ed: Hara T J), 307-336. Elsevier Sci. Pub.Co., Amsterdam.
• Pfeiffer, W., Riegelbauer, M.G., Scheibleri, B. (1985). Effects of hypothanthine-3(N)-oxide and hypothanthine-1(N)-oxide on central nervous excitation of the black tetra, Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. Journal of Chemical Ecology, 11, 507-524.
• Reed, J. R., Wieland, W., & Kimbrough, T. D. (1972). A study on the biochemistry of alarm substances in fish. In Proc. of the 26th Ann. Conference, SE Assoc. of Game & Fish Commissioners, Knoxville (pp. 608-610).
• Rossi, A. C. (1969). Chemical signals and nest-building in two species of Colisa (Pisces, Anabantidae). Monitore Zoologico Italiano-Italian Journal of Zoology, 3(4), 225-237.
• Saglio, P. (1982). Use of intraspecific biological extracts to trap eels (Anguilla anguilla L.) in the field. Demonstration of the pheromonal attractivity of the skin mucus [freshwaters, intraspecific communication, pheromones]. Acta Oecologica. Oecologia Applicata.
• Scott, A. P., Liley, N. R., & Vermeirssen, E. L. M. (1994). Urine of reproductively mature female rainbow trout, Oncorhynchus mykiss (Walbaum), contains a priming pheromone which enhances plasma levels of sex steroids and gonadotrophin II in males. Journal of Fish Biology, 44(1), 131-147.
• Scott, A. P., & Vermeirssen, E. L. M. (1994). Production of conjugated steroids by teleost gonads and their role as pheromones. Perspectives in Comparative Endocrinology, 645-654.
• Sloman, K. A., Scott, G. R., Diao, Z., Rouleau, C., Wood, C. M., & McDonald, D. G. (2003). Cadmium affects the social behaviour of rainbow trout, Oncorhynchus mykiss. Aquatic Toxicology, 65(2), 171-185.
• Smith, R. J. F., & Murphy, B. D. (1974). Functional morphology of the dorsal pad in fathead minnows (Pimephales promelas Rafinesque). Transactions of the American Fisheries Society, 103(1), 65-72.
• Sorensen, P. W. (1992). Hormonally derived sex pheromones in goldfish: a model for understanding the evolution of sex pheromone systems in fish. The Biological Bulletin, 183(1), 173-177.
• Sorensen, P. W. (1996). Biological responsiveness to pheromones provides fundamental and unique insight into olfactory function. Chemical Senses, 21(2), 245-256.
• Stabell, O. B. (1992). Olfactory control of homing behaviour in salmonids. In Fish chemoreception (pp. 249-270). Springer, Dordrecht.
• Stacey, N. E., & Hourston, A. S. (1982). Spawning and feeding behavior of captive Pacific herring, Clupea harengus pallasi. Canadian Journal of Fisheries and Aquatic Sciences, 39(3), 489-498.
• Stacey, N.E., &Sorensen, P.W. (1986). 17α,20/gb-Dihydroxy-4-pregnen-3-one: a steroidal primer pheromone which increases milt volume in the goldfish, Carassius auratus. Canadian Journal of Zoology, 64, 2412–2417.
• Sveinsson, T., & Hara, T. J. (1995). Mature males of Arctic charr, Salvelinus alpinus, release F-type prostaglandins to attract conspecific mature females and stimulate their spawning behaviour. Environmental Biology of Fishes, 42(3), 253-266.
• Tavolga, W.N. (1956). Visual, chemical and sound stimuli as cues in sex discriminatory behaviour of the gobid fish, Bothygobio soporator. Zoologica, 41, 49-64.
• Taylor, A. H., Tracey, S. R., Hartmann, K., & Patil, J. G. (2012). Exploiting seasonal habitat use of the common carp, Cyprinus carpio, in a lacustrine system for management and eradication. Marine and Freshwater Research, 63(7), 587-597.
• Teeter, J. (1980). Pheromone communication in sea lampreys (Petromyzon marinus): implications for population management. Canadian Journal of Fisheries and Aquatic Sciences, 37(11), 2123-2132.
• Teichmann, H. (1962). Die Chemorezeption der Fische. Ergebnisse der Biologie, 25, 177-205.
• Theissen, D.D., Sturdivant, S.K. (1977). Female pheromone in the black molly fish (Mollinesnsis latipinna). Journal of Chemical Ecology, 3, 207- 217
• Thommessen, G. (1983). Morphology, distribution and specificity of olfactory receptor cells in salmonid fishes. Acta Physiologica Scandinavica, 117, 241-249.
• Timms, A. M., & Kleerekoper, H. (1972). The locomotor responses of male Ictalurus punctatus, the channel catfish, to a pheromone released by the ripe female of the species. Transactions of the American Fisheries Society, 101(2), 302-310.
• Ueda, H., & Shoji, T. (2002). Physiological mechanisms of homing migration in salomon. Fisheries science, 68(sup1), 53-56.
• Von Frisch, K. (1938). Zur Psychologie des Fisch-Schwarmes. Naturwissenschaften, 26, 601–606.
• Vermeirssen, E. L., & Scott, A. P. (1996). Excretion of free and conjugated steroids in rainbow trout (Oncorhynchus mykiss): evidence for branchial excretion of the maturation-inducing steroid, 17, 20β-dihydroxy-4-pregnen-3-one. General and Comparative Endocrinology, 101(2), 180-194.
• Vrieze, L. A., Bjerselius, R., & Sorensen, P. W. (2010). Importance of the olfactory sense to migratory sea lampreys Petromyzon marinus seeking riverine spawning habitat. Journal of Fish Biology, 76(4), 949-964.
• Wagner, C. M., Jones, M. L., Twohey, M. B., & Sorensen, P. W. (2006). A field test verifies that pheromones can be useful for sea lamprey (Petromyzon marinus) control in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences, 63(3), 475-479.
• Waring, C. P., & Moore, A. (1997). Sublethal effects of a carbamate pesticide on pheromonal mediated endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Fish Physiology and Biochemistry, 17(1-6), 203-211.
• White, H.C. (1934). Some facts and theories concerning the Atlantic salmon. Transactions of the American Fisheries Society, 64(1), 360-362.
• Wyatt, T.D. (2003). Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge University Press, Cambridge, United Kingdom.
• Wyatt, T. D. (2009). Fifty years of pheromones. Nature, 457(7227), 262.
• Wysocki, C. J., Preti, G. (2010). Human pheromones: what's purported, what's supported? Sense of Smell Institute White Paper. The Fragrance Foundation, New York.
• Yambem, H., Shindo, M., & Yamazaki, F. (1999). A releaser pheromone that attracts males in the urine of mature female masu salmon. Journal of Fish Biology, 55(1), 158-171.
• Zeng, F., Shu, S., Park, Y. I., & Ramaswamy, S. B. (1997). Vitellogenin and egg production in the moth, Heliothis virescens. Archives of Insect Biochemistry and Physiology: Published in Collaboration with the Entomological Society of America, 34(3), 287-300.
• Zhang, C. (1997). Bile acids as potential pheromones in lake char, Salvelinus namaycush: an electrophysiological, biochemical and behavioural study”, Ph.D. Thesis. University of Manitoba, Winnipeg, Canada.
• Zielinski, B., Arbuckle, W., Belanger, A., Corkum, L. D., Li, W., & Scott, A. P. (2003). Evidence for the release of sex pheromones by male round gobies (Neogobius melanstomus). Fish Physiology and Biochemistry, 28(1-4), 237-239.