The role of pheromones in freshwater fishes

Journal of Fish Biology

Volumn 73, Issue 1, 2008, Pages 1-16

  Burnard, D ^a,b   Gozlan, R E ^c   Griffiths, S W ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b LANCASTER UNIVERSITY   (United Kingdom)

^c BOURNEMOUTH UNIVERSITY   (United Kingdom)

Author keywords

Chemoreception; Communication; Induced behaviour; Invasive species

Indexed keywords

GOBIO; LEUCASPIUS DELINEATUS; PETROMYZON; PETROMYZON MARINUS; PISCES; PSEUDORASBORA PARVA; VERTEBRATA;

EID: 46749104535     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2008.01872.x     Document Type: Review

References (97)

1. Almeida, O. G., Miranda, A., Frade, P., Hubbard, P. C., Barata, E. N. Canario, A. V. (2005). Urine as a social signal in the Mozambique tilapia (Oreochromis mossambicus). Chemical Senses 30, i309 i310.
2. Arbuckle, W. J., Bélanger, A. J., Corkum, L. D., Zielinski, B. S., Li, W., Yun, S. S., Bachynski, S. Scott, A. P. (2005). In vitro biosynthesis of novel 5β-reduced steroids by the testis of the round goby, Neogobius melanstomus. General and Comparative Endocrinology 140, 1 13.
3. Barreto, R. E. Hoffmann, A. (2007). Alarm substance induces hypoventilation in pintado catfish. Comparative Biochemistry and Physiology B 148, S38.
4. Becker, D., Galili, N. Degani, G. (1992). GCMS-identified steroids and steroid glucoronides in gonads and holding water of Trichogaster trichopterus (Anabantidae, Pallas 1770). Comparative Biochemistry and Physiology B 103, 15 19.
5. Belanger, R. M., Corkum, L. D. Zielinski, B. S. (2006). Differential behavioral responses by reproductive and non-reproductive male round gobies (Neogobius melanostomus) to the putative pheromone estrone. Comparative Biochemistry and Physiology A 147, 77 83.
6. Bentley, M. G. Watson, G. J. (2000). Making scents of sex underwater. Biologist 47, 251 254.
7. Bhatt, J. P. Sajwan, M. S. (2001). Ovarian steroid sulphate functions as priming pheromone in male Barilius bendelisis (Ham.). Journal of Biosciences 26, 253 263.
8. 2α. Chemical Senses 18, 427 436.
9. Brennan, P. A. Keverne, E. B. (2004). Something in the air? New insights into mammalian pheromones. Current Biology 14, 81 89.
10. Brönmark, C. Hansson, L. A. (2000). Chemical communication in aquatic systems: an introduction. Oikos 88, 103 109. doi: 10.1034/j.1600-0706. 2000.880112.x
11. Brown, G. E. Brown, J. A. (1993). Social dynamics in salmonid fishes: do kin make better neighbours? Animal Behaviour 45, 863 871.
12. Brown, G. E. Dreier, V. M. (2002). Predator inspection behaviour and attack cone avoidance in a characin fish: the effects of predator diet and prey experience. Animal Behaviour 63, 1175 1181.
13. Brown, G. E., Chivers, D. P. Smith, R. J. F. (1995a). Fathead minnows avoid conspecific and heterospecific alarm pheromones in the faeces of northern pike. Journal of Fish Biology 47, 387 393. doi: 0022-1112/95/090387+07
14. Brown, G. E., Chivers, D. P. Smith, R. J. F. (1995b). Localized defecation by pike: a response to labelling by cyprinid alarm pheromone? Behavioral Ecology and Sociobiology 36, 105 110.
15. 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, 313 320. doi: 10.1111/j.1095-8649.1996.tb01429.x
16. Brown, G., Godin, J. G. Pedersen, J. (1999). Fin-flicking behaviour: a visual and predator alarm signal in a characin fish, Hemigrammus erythrozonus. Animal Behaviour 58, 469 475.
17. Brown, G. E., Adrian, J. C. Jr., Smyth, E., Leet, H. Brennan, S. (2000). Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxide. Journal of Chemical Ecology 26, 139 154.
18. Brown, G. E., LeBlanc, V. J. Porter, L. E. (2001). Ontogenetic changes in the response of largemouth bass (Micropterus salmoides, Centrarchidae, Perciformes) to heterospecific alarm pheromones. Ethology 107, 401 414. doi: 10.1046/j.1439-0310.2001.00671.x
19. Brown, G. E., Adrian, J. C. Jr., Naderi, N. T., Harvey, M. C. Kelly, J. M. (2003). Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: conservation of the Ostariophysan alarm pheromone. Journal of Chemical Ecology 29, 1781 1796.
20. Butenandt, A., Beckmann, R., Stamm, D. Hecker, E. (1959). Über den Sexuallockstoff des Seidenspinners Bombyx mori. Zeitschrift für Naturforschung B 14, 283 284.
21. Chivers, D. P. Smith, R. J. F. (1998). Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Euroscience 5, 338 352.
22. Chivers, D. P., Brown, G. E. Smith, R. J. F. (1996). The evolution of chemical alarm signals: attracting predators benefits alarm signal senders. American Naturalist 148, 649 659.
23. Chivers, D. P., Mirza, R. S. Johnston, J. G. (2002). Learned recognition of heterospecific alarm cues enhances survival during encounters with predators. Behaviour 139, 929 938.
24. Chivers, D. P., Wisenden, B. D., Hindman, C. J., Michalak, T. A., Kusch, R. C., Kaminskyj, S. G. W., Jack, K. L., Ferrari, M. C. O., Pollock, R. J., Halbgewachs, C. F., Pollock, M. S., Alemadi, S., James, C. T., Savaloja, R. K., Goater, C. P., Corwin, A., Mirza, R. S., Kiesecker, J. M., Brown, G. E., Adrian, J. C. Jr., Krone, P. H., Blaustein, A. R. Mathis, A. (2007). Epidermal 'alarm substance' cells of fishes are maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proceedings of the Royal Society of London B 274, 2611 2619.
25. Chotkowski, M. A. Marsden, J. E. (1999). Round goby and mottled sculpin predation on trout eggs and fry: field predictions from laboratory experiments. Journal of Great Lakes Research 25, 26 35.
26. 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, 1269 1284.
27. Colombo, L., Marconato, A., Belvedere, P. A. Friso, C. (1980). Endocrinology of teleost reproduction: a testicular steroid pheromone in the black goby, Gobius jozo L. Bolletino di Zoologia 47, 355 364.
28. Corkum, L. D. (2004). Pheromone signalling in conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 14, 327 331.
29. Corkum, L. D. Belanger, R. M. (2007). Use of chemical communication in the management of freshwater aquatic species that are vectors of human diseases or are invasive. General and Comparative Endocrinology 153, 401 417.
30. Courtenay, S. C., Quinn, T. P., Dupuis, H. M. C., Groot, C. P. A. Larkin, P. A. (2001). Discrimination of family-specific odours by juvenile coho salmon: roles of learning and odour concentration. Journal of Fish Biology 58, 107 125. doi: 10.1111/j.1095-8649.2001.tb00502.x
31. Dubs, D. O. L. Corkum, L. D. (1996). Behavioural interactions between round gobies (Neogobius melanostomus) and mottled sculpins (Cottus bairdi). Journal of Great Lakes Research 22, 838 844.
32. Essington, T. E. Sorensen, P. W. (1996). Overlapping sensitivities of brook trout and brown trout to putative hormonal pheromones. Journal of Fish Biology 48, 1027 1029. doi: 10.1111/j.1095-8649.1996.tb01499.x
33. Fässler, S. M. M. Kaiser, M. J. (in press). Phylogenetically mediated anti-predator responses in bivalve molluscs. Marine Ecology Progress Series.
34. Fine, M. J., Vrieze, L. A. Sorensen, P. W. (2004). Evidence that petromyzontid lampreys employ a common migratory pheromone that is partially comprised of bile acids. Journal of Chemical Ecology 30, 2091 2110.
35. Fisher, H. S. Rosenthal, G. G. (2006). Female swordtail fish use chemical cues to select well-fed mates. Animal Behaviour 72, 721 725.
36. Friesen, R. G. Chivers, D. P. (2006). Underwater video reveals strong avoidance of alarm cues by prey fishes. Ethology 112, 339 345. doi: 10.1111/j.1439-0310.2006.01160.x
37. Gammon, D. B., Li, W., Scott, A. P., Zielinski, B. S. Corkum, L. D. (2005). Behavioural responses of female Neogobius melanostomus to odours of conspecifics. Journal of Fish Biology 67, 615 626. doi: 10.1111/j.0022-1112. 00762.x
38. Gozlan, R. E., St-Hilaire, S., Feist, S. W., Martin, P. Kent, M. L. (2005). Disease threats on European fish. Nature 435, 1045.
39. Griffiths, S. W., Armstrong, J. D. Metcalfe, N. B. (2003). The cost of aggregation: juvenile salmon avoid sharing winter refuges with siblings. Behavioral Ecology 14, 602 606.
40. Hänfling, B., Bolton, P., Harley, M. Carvalho, G. R. (2005). A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and non indigenous carp species (Carassius spp. and Cyprinus carpio). Freshwater Biology 50, 403 417.
41. Hartman, E. J. Abrahams, M. V. (2000). Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proceedings of the Royal Society of London, Series B 267, 571 575.
42. Hiscock, M. J. Brown, J. A. (2000). Kin discrimination in juvenile brook trout (Salvelinus fontalis) and the effect of odour concentration on kin preferences. Canadian Journal of Zoology 78, 278 282.
43. van den Hurk, R. Resink, J. W 1992). Male reproductive system as sex pheromone producer in teleost fish. Journal of Experimental Zoology 261, 204 213.
44. Irvine, I. A. S. Sorensen, P. W. (1993). Acute olfactory sensitivity of wild common carp, Cyprinus carpio, to goldfish hormonal sex pheromones is influenced by gonadal maturity. Canadian Journal of Zoology 71, 2199 2210.
45. Johnson, N. S., Siefkes, M. K. Li, W. (2005). Capture of ovulating sea lampreys in traps baited with spermiating male sea lampreys. North American Journal of Fisheries Management 25, 67 72.
46. Johnson, N. S., Luehring, M. A., Siefkes, M. K. Li, W. (2006). Mating pheromone reception and induced behaviour in ovulating female sea lamprey. North American Journal of Fisheries Management 26, 88 96.
47. 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, 416 421.
48. Katsel, P., Dmitrieva, T. M., Valeyev, R. B. Kozlov, Y. P 1992). Sex pheromones of male yellowfin baikal sculpin (Cottocomephorus grewingki): isolation and chemical studies. Journal of Chemical Ecology 18, 2003 2010.
49. Kelly, J. M., Adrian, J. C. Jr. Brown, G. E. (2006). Can the ratio of aromatic skeletons explain cross-species responses within evolutionarily conserved Ostariophysan alarm cues?: testing the purine-ratio hypothesis. Chemoecology 16, 93 96.
50. Kikuyama, S., Yamamoto, K., Iwata, T. Toyoda, F. (2002). Peptide and protein pheromones in amphibians. Comparative Biochemistry and Physiology B 132, 69 74.
51. Kobayashi, M., Sorensen, P. W. Stacey, N. E. (2002). Hormonal and pheromonal control of spawning behaviour in the goldfish. Fish Physiology and Biochemistry 26, 71 84.
52. Laberge, F. Hara, T. J 2003). Behavioural and electrophysiological responses to F-prostaglandins, putative spawning pheromones, in three salmonid fishes. Journal of Fish Biology 62, 206 221. doi: 10.1046/j.1095-8649.2003. 00020.x
53. Leary, R. F., Allendorf, F. W. Sage, G. K. (1995). Hybridization and introgression between introduced and native fish. American Fisheries Society Symposium 15, 91 101.
54. Leduc, A. O. H. C., Noseworthy, M. K., Adrian, J. C. Jr. Brown, G. E. (2003). Detection of conspecific and heterospecific alarm signals by juvenile pumpkinseed under weak acidic conditions. Journal of Fish Biology 63, 1331 1336. doi: 10.1046/j.1095-8649.2003.00230.x
55. LeMaster, M. P. Mason, R. T. (2002). Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. Journal of Chemical Ecology 28, 1269 1285.
56. Li, W., Scott, A. P., Siefkes, M. J., Yan, H., Liu, Q., Yun, S. S. Gage, D. A. (2002). Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science 296, 138 141.
57. Lower, N., Scott, A. P. Moore, A 2004). Release of sex steroids into the water by roach. Journal of Fish Biology 64, 16 33. doi: 10.1111/j.1095-8649. 2004.00278.x
58. Magurran, A. E., Irving, P. W., Henderson, P. A. (1996). Is there a fish alarm pheromone? A wild study and critique. Proceedings of the Royal Society of London B 263, 1551 1556.
59. Manchester, S. J. Bullock, J. M. (2000). The impacts of non-native species on UK biodiversity and the effectiveness of control. Journal of Applied Ecology 37, 845 864. doi: 10.1046/j.1365-2664.2000.00538.x
60. Mann, K. D., Turnell, E. R., Atema, J. Gerlach, G. (2003). Kin recognition in juvenile zebrafish (Danio rerio) based on olfactory cues. Biological Bulletin 205, 224 225.
61. Martín, J. López, P. (2000). Chemoreception, symmetry and mate choice in lizards. Proceedings of the Royal Society London B 267, 1265 1269.
62. Milinski, M. (2003). The function of mate choice in sticklebacks: optimizing Mhc genetics. Journal of Fish Biology 63 (Suppl. A 1 16. doi: 10.1046/j.1095-8649.2003.00215.x
63. Mirza, R. S. Chivers, D. P. (2001). Chemical alarm signals enhance survival of brook charr (Salvelinus fontinalis) during encounters with predatory chain pickerel (Esox niger). Ethology 107, 989. doi: 10.1046/j.1439-0310.2001. 00729.x
64. Moore, A. Waring, C. P. (1996). Electrophysiological and endocrinological evidence that F-series prostaglandins function as priming pheromones in mature male Atlantic salmon (Salmo salar) parr. The Journal of Experimental Biology 199, 2307 2316.
65. 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, 443 470.
66. Nichols, S. J., Kennedy, G., Crawford, E., Allen, J., French, J. III., Black, G., Blowin, M., Hickey, J., Chernyak, S., Haas, R. Thomas, M. (2003). Assessment of lake sturgeon (Acipenser fulvescens) spawning efforts in the lower St Clair River, Michigan. Journal of Great Lakes Research 29, 383 391.
67. Ogata, H., Kitamura, S. Takashima, F 1994). Release of 13, 14-dihydro-15-keto-prostaglandin F2α, a sex pheromone, to water by cobitid loach following ovulatory stimulation. Fisheries Science 60, 143 148.
68. Olsén, K. H., Bjerselius, R., Petersson, E., Järvi, T., Mayer, I. Hedenskog, M. (2000). Lack of species-specific primer effects of odours from female Atlantic salmon, Salmo salar, and brown trout, Salmo trutta. Oikos 88, 213 220. doi: 10.1034/j.1600-0706.2000.880123.x
69. Olsén, K. H., Sawisky, G. R. Stacey, N. E. (2006). Endocrine and milt responses of male crucian carp (Carassius carassius L.) to periovulatory females under field conditions. General and Comparative Endocrinology 149, 294 302.
70. Poling, K. R., Fraser, E. J. Sorensen, P. W. (2001). The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comparative Biochemistry and Physiology B 129, 645 651.
71. Rasmussen, L. E. I., Lee, T. D., Roelofs, W. L., Zhano, A. J. Daves, G. D. (1996). Insect pheromones in elephants. Nature 379, 684.
72. Renaud, C. B. (1997). Conservation status of northern hemisphere lamprey (Petromyzontidae). Journal of Applied Ichthyology 13, 143 148. doi: 10.1111/j.1439-0426.1997.tb00114.x
73. Resink, J. W., Schoonen, W. G. E. J., Albers, P. C. II., File, D. M., Notenboom, C. D., van den Hurk, R. van Oordt, P. G. W. J 1989). The chemical nature of sex attracting pheromones from the seminal vesicle of the African catfish, Clarias gariepinus. Aquaculture 83, 153 166.
74. Sala, O. E., Chaplin, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L. F., Jackson, R. B., Kinzig, A., Leemans, R., Lodge, D. M., Mooney, H. A., Oesterheld, M., Poff, L., Sykes, T., Walker, B. H., Walker, M. Wall, D. H. (2000). Global biodiversity scenarios for the year 2100. Science 287, 1770 1774.
75. Smith, R. J. F. (1997). Does one result trump all others? A response to Magurran, Irving and Henderson. Proceedings of the Royal Society of London B 264, 445 450.
76. Sorensen, P. W. Scott, A. P. (1994). The evolution of hormonal sex pheromones in teleost fish: poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Physiologica Scandinavica 152, 191 205.
77. Sorensen, P. W. Stacey, N. E. (2004). Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes. New Zealand Journal of Marine and Freshwater Research 38, 399 417.
78. Sorensen, P. W., Murphy, C. A., Loomis, K., Maniak, P. Thomas, P. (2004). Evidence that 4-pregnen-17,20β,21-triol-3-one functions as a maturation-inducing hormone and pheromonal precursor in the percid fish, Gymnocephalus cernuus. General and Comparative Endocrinology 139, 1 11.
79. Sorensen, P. W., Fine, J. M., Dvornikovs, V., Jeffrey, C. S., Shao, F., Wang, J., Vrieze, L. A., Anderson, K. R. Hoye, T. R. (2005). Mixture of new sulphated steroids functions as a migratory pheromone in the sea lamprey. Nature Chemical Biology 1, 324 328.
80. Stabell, O. B. (1984). Homing and olfaction in salmonids: a critical review with special reference to the Atlantic salmon. Biological Reviews 59, 333 388.
81. Stacey, N. E. Cardwell, J. R. (1995). Hormones as sex pheromones in teleost fish: widespread distribution among freshwater species. In Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish (Goetz, F. W. Thomas, P., eds pp. 244 248. Austin : University of Texas.
82. Stacey, N. E. Sorensen, P. W. (1986). 17α,20β-Dihydroxy-4- pregnen-3-one: a steroidal primer pheromone increasing milt volume in the goldfish, Carassius auratus. Canadian Journal of Zoology 64, 2412 2417.
83. Stacey, N. E. Sorensen, P. W. (1991). Function and evolution of fish hormonal pheromones. In Biochemistry and Molecular Biology of Fishes (Hochachka, P. W. Mommsen, T. P., eds pp. 109 135. Amsterdam : Elsevier.
84. Stacey, N. E. Sorensen, P. W. (2002). Fish hormonal pheromones. In Hormones, Brain and Behavior (Pfaff, D. W., Arnold, A. P., Etgen, S., Fahrbach, S. Rubin, R., eds pp. 375 435. New York : Academic Press.
85. Stacey, N. E. Sorensen, P. W. (2006). Reproductive pheromones. In Behaviour and Physiology of Fish (Sloman, K. A., Wilson, R. W. Balshine, S., eds). Fish Physiology Series 24, pp. 359 412. Amsterdam, Elsevier.
86. Stacey, N. E., Chojnacki, A., Narayanan, A., Cole, T. Murphy, C. (2003). Hormonally derived sex pheromones in fish: exogenous cues and signals from gonad to brain. Canadian Journal of Physiology and Pharmacology 81, 329 341.
87. 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, 253 266.
88. Vermeirssen, E. L. M. 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, 180 194.
89. Verspoor, E. Hammart, J. (1991). Introgressive hybridization in fishes: the biochemical evidence. Journal of Fish Biology 39, 309 334. doi: 10.1111/j.1095-8649.1991.tb05094.x
90. Wagner, M. C., Jones, L. M., Twohey, M. B. Sorenson, P. W. (2006). A field test that verifies that pheromones can be useful for sea lamprey (Petromyzon marinus) control in the great lakes. Canadian Journal of Fisheries and Aquatic Science 63, 475 479.
91. Wilson, E. O. Bossert, W. H. (1963). Chemical communication among animals. In Recent Progress in Hormone Research, Vol. 19 (Pincus, G., ed pp. 673 716. New York : Academic Press.
92. Wisenden, B. D. (2000). Olfactory assessment of predation risk in the aquatic environment. Philosophical Transactions of the Royal Society of London B 355, 1205 1208.
93. Wisenden, B. D. Smith, R. J. F. (1998). A re-evaluation of the effect of shoalmate familiarity on the proliferation of alarm substance cells in ostariophysan fishes. Journal of Fish Biology 53, 841 846. doi: 10.1111/j.1095-8649.1998.tb01837.x
94. Wisenden, B. D., Vollbrecht, K. A. Brown, J. L. (2004). Is there a fish alarm cue? Affirming evidence from a wild study. Animal Behaviour 67, 59 67.
95. Yambe, H. Yamazaki, F. (2001). A releaser pheromone that attracts methyltestosterone-treated immature fish in the urine of ovulated female rainbow trout. Fisheries Science 67, 214 220. doi: 10.1046/j.1444-2906.2001.00242.x
96. Zheng, W., Strobeck, C. Stacey, N. (1997). The steroid pheromone 4-pregnen-1α, 20β-diol-3-one increases fertility and paternity in goldfish. Journal of Experimental Biology 200, 2833 2840.
97. Zielinski, B. S., Arbuckle, W. J., Bélanger, A. J., 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, 237 239.