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Journal of Comparative Physiology A

, Volume 196, Issue 10, pp 701–711 | Cite as

Understanding behavioral responses of fish to pheromones in natural freshwater environments

  • Nicholas S. Johnson
  • Weiming LiEmail author
Review

Abstract

There is an abundance of experimental studies and reviews that describe odorant-mediated behaviors of fish in laboratory microcosms, but research in natural field conditions has received considerably less attention. Fish pheromone studies in laboratory settings can be highly productive and allow for controlled experimental designs; however, laboratory tanks and flumes often cannot replicate all the physical, physiological and social contexts associated with natural environments. Field experiments can be a critical step in affirming and enhancing understanding of laboratory discoveries and often implicate the ecological significance of pheromones employed by fishes. When findings from laboratory experiments have been further tested in field environments, often different and sometimes contradictory conclusions are found. Examples include studies of sea lamprey (Petromyzon marinus) mating pheromones and fish alarm substances. Here, we review field research conducted on fish pheromones and alarm substances, highlighting the following topics: (1) contradictory results obtained in laboratory and field experiments, (2) how environmental context and physiological status influences behavior, (3) challenges and constraints of aquatic field research and (4) innovative techniques and experimental designs that advance understanding of fish chemical ecology through field research.

Keywords

Pheromone Fish physiology Fish behavior Field study Laboratory study 

Abbreviations

3kPZS

3-Keto petromyzonol sulfate

PZS

Petromyzonol sulfate

ACA

Allocholic acid

17,20 βP

17α, 20β-Dihydroxy-4-pregnen-3-one

PGF

Prostaglandin F2α

PIT

Passive integrated transponder

Notes

Acknowledgments

During the preparation of this manuscript, funding was received from the Great Lakes Fishery Commission. Permission was granted by Elsevier to include Fig. 1a. We thank Dr. Stephen Riley, Dr. Michael Wagner, Karen Slaght, Erin Walaszczyk and Mark Luehring for thoughtful comments during the development of the manuscript. This article is Contribution 1568 of the USGS Great Lakes Science Center.

References

  1. Adams MA, Teeter JH, Katz Y, Johnsen PB (1987a) Reproductive pheromones of the landlocked sea lamprey (Petromyzon marinus)—studies on urinary steroids. Ann NY Acad Sci 510:148–151CrossRefGoogle Scholar
  2. Adams MA, Teeter JH, Katz Y, Johnsen PB (1987b) Sex-pheromones of the sea lamprey (Petromyzon marinus)—steroid studies. J Chem Ecol 13:387–395CrossRefGoogle Scholar
  3. Applegate VC (1950) The natural history of the sea lamprey in Michigan. US Department of Interior Fish & Wildlife Service, Special Scientific Report Fisheries, Washington, DCGoogle Scholar
  4. Bhatt JP, Kandwal JS, Nautiyal R (2002) Water temperature and pH influence olfactory sensitivity to pre-ovulatory and post-ovulatory ovarian pheromones in male Barilius bendelisis. J Biosci 27:273–281PubMedCrossRefGoogle Scholar
  5. Bjerselius R, Li W, Teeter JH, Seelye JG, Johnsen PB, Maniak PJ, Grant GC, Polkinghorne CN, Sorensen PW (2000) Direct behavioral evidence that unique bile acids released by larval sea lamprey (Petromyzon marinus) function as a migratory pheromone. Can J Fish Aquat Sci 57:557–569CrossRefGoogle Scholar
  6. Brennan PA, Zufall F (2006) Pheromone communication in vertebrates. Nature 444:308–315PubMedCrossRefGoogle Scholar
  7. Brown GE, Smith RJF (1996) Foraging trade-offs in fathead minnows (Pimephales promelas): acquired predator recognition in the absence of an alarm response. Ethology 102:776–785CrossRefGoogle Scholar
  8. Brown GE, Smith RJF (1998) Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): conditioning hatchery-reared fish to recognize chemical cues of a predator. Can J Fish Aquat Sci 55:611–617CrossRefGoogle Scholar
  9. Brown GE, Chivers DP, Smith RJF (1995) Fathead minnows avoid conspecific and heterospecific alarm pheromones in the feces of northern pike. J Fish Biol 47:387–393Google Scholar
  10. Brown GE, Adrian JC, Smyth E, Leet H, Brennan S (2000) Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxides. J Chem Ecol 26:139–154CrossRefGoogle Scholar
  11. Brown GE, Adrian JC, Patton T, Chivers DP (2001a) Fathead minnows learn to recognize predator odour when exposed to concentrations of artificial alarm pheromone below their behavioural-response threshold. Can J Zool 79:2239–2245CrossRefGoogle Scholar
  12. Brown GE, LeBlanc VJ, Porter LE (2001b) Ontogenetic changes in the response of largemouth bass (Micropterus salmoides, Centrarchidae, Perciformes) to heterospecific alarm pheromones. Ethology 107:401–414CrossRefGoogle Scholar
  13. Brown GE, Adrian JC, Lewis MC, Tower JM (2002a) The effects of reduced pH on chemical alarm signaling in ostariophysan fishes. Can J Fish Aquat Sci 59:1331–1338CrossRefGoogle Scholar
  14. Brown GE, Gershaneck DL, Plata DL, Golub JL (2002b) Ontogenetic changes in response to heterospecific alarm cues by juvenile largemouth bass are phenotypically plastic. Behaviour 139:913–927CrossRefGoogle Scholar
  15. Burnard D, Gozlan RE, Griffiths SW (2008) The role of pheromones in freshwater fishes. J Fish Biol 73:1–16CrossRefGoogle Scholar
  16. Cardwell JR, Stacey NE, Tan ESP, Mcadam DSO, Lang SLC (1995) Androgen increases olfactory receptor response to a vertebrate sex-pheromone. J Comp Physiol A 176:55–61CrossRefGoogle Scholar
  17. Carolsfeld J, Scott AP, Sherwood NM (1997a) Pheromone-induced spawning of Pacific herring. II. Plasma steroids distinctive to fish responsive to spawning pheromone. Horm Behav 31:269–276PubMedCrossRefGoogle Scholar
  18. Carolsfeld J, Tester M, Kreiberg H, Sherwood NM (1997b) Pheromone-induced spawning of Pacific herring. I. Behavioral characterization. Horm Behav 31:256–268PubMedCrossRefGoogle Scholar
  19. Carreau ND, Pyle GG (2005) Effect of copper exposure during embryonic development on chemosensory function of juvenile fathead minnows (Pimephales promelas). Ecotox Environ Safe 61:1–6CrossRefGoogle Scholar
  20. Carton AG, Montgomery JC (2003) Evidence of a rheotactic component in the odour search behaviour of freshwater eels. J Fish Biol 62:501–516CrossRefGoogle Scholar
  21. Chivers DP, Wisenden BD, Smith RJF (1995) The role of experience in the response of fathead minnows (Pimephales promelas) to skin extract of Iowa darters (Etheostoma exile). Behaviour 132:665–674CrossRefGoogle Scholar
  22. Chivers DP, Puttlitz MH, Blaustein AR (2000) Chemical alarm signaling by reticulate sculpins (Cottus perplexus). Environ Biol Fish 57:347–352CrossRefGoogle Scholar
  23. Chivers DP, Wisenden BD, Hindman CJ, Michalak TA, Kusch RC, Kaminskyj SGW, Jack KL, Ferrari MCO, Pollock RJ, Halbgewachs CF, Pollock MS, Alemadi S, James CT, Savaloja RK, Goater CP, Corwin A, Mirza RS, Kiesecker JM, Brown GE, Adrian JC, Krone PH, Blaustein AR, Mathis A (2007) Epidermal ‘alarm substance’ cells of fishes are maintained by non-alarm functions: possible defense against pathogens, parasites and UVB radiation. Proc R Soc Lond B 274:2611–2619CrossRefGoogle Scholar
  24. Defraipont M, Sorensen PW (1993) Exposure to the pheromone 17-alpha, 20-beta-dihydroxy-4-pregnen-3-one enhances the behavioral spawning success, sperm production and sperm motility of male goldfish. Anim Behav 46:245–256CrossRefGoogle Scholar
  25. Denny MW (1988) Biology and the mechanics of the wave-swept environment. Princeton University Press, PrincetonGoogle Scholar
  26. Denny MW (1993) Air and water. Princeton University Press, PrincetonGoogle Scholar
  27. Dulka JG, Stacey NE, Sorensen PW, Vanderkraak GJ (1987) A steroid sex-pheromone synchronizes male–female spawning readiness in goldfish. Nature 325:251–253CrossRefGoogle Scholar
  28. Dvornikovs V, Fine JM, Hoye TR, Jeffrey CS, Shao F, Wang J, Vrieze LA, Anderson KR, Sorensen PW (2006) Isolation and structure elucidation of the sea lamprey migratory pheromone. Chem Senses 31:A82–A83Google Scholar
  29. Ferrari MCO, Trowell JJ, Brown GE, Chivers DP (2005) The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim Behav 70:777–784CrossRefGoogle Scholar
  30. Fine JM, Sisler SP, Vrieze LA, Swink WD, Sorensen PW (2006) A practical method for obtaining useful quantities of pheromones from sea lamprey and other fishes for identification and control. J Great Lakes Res 32:832–838CrossRefGoogle Scholar
  31. Finelli CM, Pentcheff ND, Zimmer-Faust RK, Wethey DS (1999) Odor transport in turbulent flows: constraints on animal navigation. Limnol Oceanogr 44:1056–1071CrossRefGoogle Scholar
  32. Finelli CM, Pentcheff ND, Zimmer RK, Wethey DS (2000) Physical constraints on ecological processes: a field test of odor-mediated foraging. Ecology 81:784–797CrossRefGoogle Scholar
  33. Fisher HS, Wong BBM, Rosenthal GG (2006) Alteration of the chemical environment disrupts communication in a freshwater fish. P Roy Soc B-Biol Sci 273:1187–1193CrossRefGoogle Scholar
  34. Fontaine M (1938) La lamproie marine. Sa peche et son importance economique. B Sco Ocean Fr 17:1681–1687Google Scholar
  35. Fraser EJ, Stacey NE (2002) Isolation increases milt production in goldfish. J Exp Biol 293:511–524Google Scholar
  36. Friesen RG, Chivers DP (2006) Underwater video reveals strong avoidance of chemical alarm cues by prey fishes. Ethology 112:339–345CrossRefGoogle Scholar
  37. Golub JL, Brown GE (2003) Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (Lepomis cyanellus). Behav Ecol Sociobiol 54:113–118Google Scholar
  38. Golub JL, Vermette V, Brown GE (2005) Response to conspecific and heterospecific alarm cues by pumpkinseeds in simple and complex habitats: field verification of an ontogenetic shift. J Fish Biol 66:1073–1081CrossRefGoogle Scholar
  39. Hall D, Suboski MD (1995a) Sensory preconditioning and 2nd-order conditioning of alarm reactions in zebra danio fish (Brachydanio rerio). J Comp Psychol 109:76–84CrossRefGoogle Scholar
  40. Hall D, Suboski MD (1995b) Visual and olfactory stimuli in learned release of alarm reactions by zebra danio fish (Brachydanio rerio). Neurobiol Learn Memory 63:229–240CrossRefGoogle Scholar
  41. Hansler AD, Scholz AT (1983) Olfactory imprinting and homing in salmon. Springer, BerlinGoogle Scholar
  42. Hartman EJ (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. P Roy Soc B-Biol Sci 267:571–575CrossRefGoogle Scholar
  43. Harvey MC, Brown GE (2004) Dine or dash?: Ontogenetic shift in the response of yellow perch to conspecific alarm cues. Environ Biol Fish 70:345–352CrossRefGoogle Scholar
  44. Heuschele J, Candolin U (2007) An increase in pH boosts olfactory communication in sticklebacks. Biology Lett 3:411–413CrossRefGoogle Scholar
  45. Hoye TR, Dvornikovs V, Fine JM, Anderson KR, Jeffrey CS, Muddiman DC, Shao F, Sorensen PW, Wang J (2007) Details of the structure determination of the sulfated steroids PSDS and PADS: new components of the sea lamprey (Petromyzon marinus) migratory pheromone. J Org Chem 72:7544–7550PubMedCrossRefGoogle Scholar
  46. Hubbard PC, Barata EN, Canario AV (2002) Possible disruption of pheromonal communication by humic acid in the goldfish, Carassius auratus. Aquat Toxicol 60:169–183PubMedCrossRefGoogle Scholar
  47. Hurst J, Beynon R (2004) Scent wars: the chemobiology of competitive signaling in mice. BioEssays 26:1288–1298PubMedCrossRefGoogle Scholar
  48. Hurst J, Payne CE, Nevison CM, Marie AD, Humphries RE, Robertson DHL, Cavaggioni A, Beynon TB (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414:631–634PubMedCrossRefGoogle Scholar
  49. Jaensson A, Scott AP, Moore A, Kylin H, Olsen KH (2007) Effects of a pyrethroid pesticide on endocrine responses to female odours and reproductive behaviour in male parr of brown trout (Salmo trutta L.). Aquat Toxicol 81:1–9PubMedCrossRefGoogle Scholar
  50. Johnsen PB, Hasler AD (1980) The use of chemical cues in the upstream migration of coho salmon, Oncorhynchus kisutch Walbaum. J Fish Biol 17:67–73CrossRefGoogle Scholar
  51. Johnson NS, Siefkes MJ, Li W (2005) Capture of ovulating female sea lampreys in traps baited with spermiating male sea lampreys. N Am J Fish Manage 25:67–72CrossRefGoogle Scholar
  52. Johnson NS, Luehring MA, Siefkes MJ, Li W (2006) Mating pheromone reception and induced behavior in ovulating female sea lampreys. N Am J Fish Manage 26:88–96CrossRefGoogle Scholar
  53. Johnson NS, Yun S-S, Thompson HT, Brant CB, Li W (2009) A synthesized pheromone induces upstream movement in female sea lampreys and summons them into traps. P Natl Acad Sci USA 106:1021–1026CrossRefGoogle Scholar
  54. Keller TA, Weissburg MJ (2004) Effects of odor flux and pulse rate on chemosensory tracking in turbulent odor plumes by the blue crab, Callinectes sapidus. Biol Bull 207:44–55PubMedCrossRefGoogle Scholar
  55. Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4:216–226Google Scholar
  56. Kleerekoper H (1969) Olfaction in fishes. Indiana University Press, BloomingtonGoogle Scholar
  57. Kobayashi M, Sorensen PW, Stacey NE (2002) Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol Biochem 26:71–84CrossRefGoogle Scholar
  58. Leduc A, Kelly JM, Brown GE (2004) Detection of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests. Oecologia 139:318–324PubMedCrossRefGoogle Scholar
  59. Li W, Sorensen PW, Gallaher DD (1995) The olfactory system of migratory adult sea lamprey (Petromyzon marinus) is specifically and acutely sensitive to unique bile acids released by conspecific larvae. J Gen Physiol 105:569–587PubMedCrossRefGoogle Scholar
  60. Li W, Scott AP, Siefkes MJ, Yan H, Liu Q, Yun S-S, Gage DA (2002) Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science 296:138–141PubMedCrossRefGoogle Scholar
  61. Li W, Twohey M, Jones M, Wagner M (2007) Research to guide use of pheromones to control sea lamprey. J Great Lakes Res 33(2):70–86CrossRefGoogle Scholar
  62. Locatello L, Mazzoldi C, Rasotto MB (2002) Ejaculate of sneaker males is pheromonally inconspicuous in the black goby, Gobius niger (Teleostei, Gobiidae). J Exp Zool 293:601–605PubMedCrossRefGoogle Scholar
  63. Losey GS, Hugie DM (1994) Prior anesthesia impairs a chemically mediated fright response in a gobiid fish. J Chem Ecol 20:1877–1883CrossRefGoogle Scholar
  64. Lurling M, Scheffer M (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol Evol 22:374–379PubMedCrossRefGoogle Scholar
  65. Mackie AM, Shelton RGJ (1972) A whole-animal bioassay for the determination of food attractants of the lobster Homarus gannarus. Mar Biol 14:217–221Google Scholar
  66. Magurran AE, Irving PW, Henderson PA (1996) Is there a fish alarm pheromone? A wild study and critique. P Roy Soc B-Biol Sci 263:1551–1556CrossRefGoogle Scholar
  67. Mathis A, Smith RJF (1992) Avoidance of areas marked with a chemical alarm substance by fathead minnows (Pimephales promelas) in a natural habitat. Can J Zool 70:1473–1476CrossRefGoogle Scholar
  68. Mathis A, Chivers DP, Smith RJF (1995) Chemical alarm signals—predator deterrents or predator attractants. Am Nat 145:994–1005CrossRefGoogle Scholar
  69. Mesquita RM, Canario AV, Melo E (2003) Partition of fish pheromones between water and aggregates of humic acids. Consequences for sexual signaling. Environ Sci Technol 37: 742–746PubMedCrossRefGoogle Scholar
  70. Mikheev VN, Wanzenbock J, Pasternak AF (2006) Effects of predator-induced visual and olfactory cues on 0+ perch (Perca fluviatilis L.) foraging behaviour. Ecol Freshw Fish 15:111–117CrossRefGoogle Scholar
  71. Mirza RS, Chivers DP (2000) Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can J Zool 78:2198–2208CrossRefGoogle Scholar
  72. Mirza RS, Chivers DP (2001) Chemical alarm signals enhance survival of brook charr (Salvelinus fontinalis) during encounters with predatory chain pickerel (Esox niger). Ethology 107:989–1005CrossRefGoogle Scholar
  73. Mirza RS, Chivers DP (2002) Brook char (Salvelinus fontinalis) can differentiate chemical alarm cues produced by different age/size classes of conspecifics. J Chem Ecol 28:555–564PubMedCrossRefGoogle Scholar
  74. Moore PA, Grills JL (1999) Chemical orientation to food by the crayfish Orconectes rusticus: influence of hydrodynamics. Anim Behav 58:953–963PubMedCrossRefGoogle Scholar
  75. Moore A, Lower N (2001) The impact of two pesticides on olfactory-mediated endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Comp Biochem Phys B 129:269–276CrossRefGoogle Scholar
  76. Moore HH, Schleen IP (1980) Changes in spawning runs of sea lamprey (Petromyzon-marinus) in selected streams of Lake Superior after chemical control. Can J Fish Aquat Sci 37:1851–1860CrossRefGoogle Scholar
  77. Moore A, Waring CP (1998) Mechanistic effects of a triazine pesticide on reproductive endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Pestic Biochem Phys 62:41–50CrossRefGoogle Scholar
  78. Moore A, Waring CP (1999) Reproductive priming in mature male Atlantic salmon parr exposed to the sound of redd cutting. J Fish Biol 55:884–887CrossRefGoogle Scholar
  79. Moore A, Waring CP (2001) The effects of a synthetic pyrethroid pesticide on some aspects of reproduction in Atlantic salmon (Salmo salar L.). Aquat Toxicol 52:1–12PubMedCrossRefGoogle Scholar
  80. More L (2006) Mouse major urinary proteins trigger ovulation via the vomeronasal organ. Chem Senses 31:393–401PubMedCrossRefGoogle Scholar
  81. Neff BD (2003) Decisions about parental care in response to perceived paternity. Nature 422:716–719PubMedCrossRefGoogle Scholar
  82. Pearson WH (1977) Chemoreception in the blue crab, Callinectus sapidus. Biol Bull 153:346–354CrossRefGoogle Scholar
  83. Pickering AD, Pottinger TG, Carragher J, Sumpter JP (1987) The effects of acute and chronic stress on the levels of reproductive hormones in the plasma of mature male brown trout, Salmo trutta L. Gen Comp Endocr 68:249–259PubMedCrossRefGoogle Scholar
  84. Pollock MS, Chivers DP, Mirza RS, Wisenden BD (2003) Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. Environ Biol Fish 66:313–319CrossRefGoogle Scholar
  85. Pollock MS, Friesen RG, Pollock RJ, Kusch RC, Chivers DP (2005) The avoidance response of fathead minnows to chemical alarm cues: understanding the effects of donor gender and breeding condition. Chemoecology 15:205–209CrossRefGoogle Scholar
  86. Pottinger TG (1992) The influence of social interaction on the acclimation of rainbow trout, Oncorhynchus mykiss (Walbaum) to chronic stress. J Fish Biol 41:435–447CrossRefGoogle Scholar
  87. Riley SC, Tatara CP, Scheurer JA (2005) Aggression and feeding of hatchery-reared and naturally reared steelhead (Oncorhynchus mykiss) fry in a laboratory flume and a comparison with observations in natural streams. Can J Fish Aquat Sci 62:1400–1409CrossRefGoogle Scholar
  88. Scholz NL, Truelove NK, French BL, Berejikian BA, Quinn TP, Casillas E, Collier TK (2000) Diazinon disrupts antipredator and homing behaviors in chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 57:1911–1918CrossRefGoogle Scholar
  89. Scott AP, Ellis T (2007) Measurement of fish steroids in water—a review. Gen Comp Endocr 153:392–400PubMedCrossRefGoogle Scholar
  90. Scott AP, Liley NR, Vermeirssen ELM (1994) Urine of reproductively mature female rainbow-trout, Oncorhynchus-mykiss (Walbaum), contains a priming pheromone which enhances plasma-levels of sex steroids and gonadotropin-II in males. J Fish Biol 44:131–147CrossRefGoogle Scholar
  91. Scott AP, Sloman KA, Rouleau C, Wood CM (2003) Cadmium disrupts behavioral and physiological responses to alarm substances in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 206:1779–1790PubMedCrossRefGoogle Scholar
  92. Sherman ML, Moore PA (2001) Chemical orientation of brown bullheads, Ameiurus nebulosus, under different flow conditions. J Chem Ecol 27:2301–2318PubMedCrossRefGoogle Scholar
  93. Siefkes MJ, Winterstein SR, Li W (2005) Evidence that 3-keto petromyzonol sulphate specifically attracts ovulating female sea lamprey, Petromyzon marinus. Anim Behav 70:1037–1045CrossRefGoogle Scholar
  94. Sloman KA, Armstrong JD (2002) Physiological effects of dominance hierarchies: laboratory artefacts or natural phenomena. J Fish Biol 61:1–23CrossRefGoogle Scholar
  95. Smith RJF (1981) Effect of food deprivation on the reaction of Iowa darters (Etheostoma exile) to skin extract. Can J Zool 59:558–560CrossRefGoogle Scholar
  96. Smith RJF (1997) Does one result trump all others? A response to Magurran, Irving and Henderson. P Roy Soc B-Biol Sci 264:445–450CrossRefGoogle Scholar
  97. Sorensen PW (1992) Hormonally derived sex-pheromones in goldfish—a model for understanding the evolution of sex-pheromone systems in fish. Biol Bull 183:173–177CrossRefGoogle Scholar
  98. Sorensen PW, Stacey NE (2004) Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes. New Zeal J Mar Fresh 38:399–417CrossRefGoogle Scholar
  99. Sorensen PW, Vrieze LA (2003a) The chemical ecology and potential application of the sea lamprey migratory pheromone. J Great Lakes Res 29:66–84CrossRefGoogle Scholar
  100. Sorensen PW, Vrieze LA (2003b) The chemical ecology and potential application of the sea lamprey migratory pheromone. J Great Lakes Res 29:66–84CrossRefGoogle Scholar
  101. Sorensen PW, Stacey NE, Chamberlain KJ (1989) Differing behavioral and endocrinological effects of two female sex pheromones on male goldfish. Horm Behav 23:317–332PubMedCrossRefGoogle Scholar
  102. Sorensen PW, Christensen TA, Stacey NE (1998) Discrimination of pheromonal cues in fish: emerging parallels with insects. Curr Opin Neurobiol 8:458–467PubMedCrossRefGoogle Scholar
  103. Sorensen PW, Fine JM, Dvornikovs V, Jeffrey CS, Shao F, Wang J, Vrieze LA, Anderson KR, Hoye TR (2005) Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat Chem Biol 1:324–328PubMedCrossRefGoogle Scholar
  104. Spehr M, Kelliher KR, Li H-H, Boehm T, Leinders-Zufall T, Zufall F (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 26:1961–1970PubMedCrossRefGoogle Scholar
  105. Stacey N (2003) Hormones, pheromones and reproductive behavior. Fish Physiol Biochem 28:229–235CrossRefGoogle Scholar
  106. Stacey N, Chojnacki A, Narayanan A, Cole T, Murphy C (2003) Hormonally derived sex pheromones in fish: exogenous cues and signals from gonad to brain. Can J Physiol Pharm 81:329–341CrossRefGoogle Scholar
  107. Teeter J (1980) Pheromone communication in sea lampreys (Petromyzon-marinus)—implications for population management. Can J Fish Aquat Sci 37:2123–2132CrossRefGoogle Scholar
  108. von Frisch K (1938) Zur Psychologie des Fischschwarmes. Naturwissenschaften 26:601–606CrossRefGoogle Scholar
  109. von Frisch K (1941) Über einen Schreckstoff der Fischhaut und seine biologische Bedeutung. Z vergl Physiol 29:46–145CrossRefGoogle Scholar
  110. Vrieze LA, Sorensen PW (2001) Laboratory assessment of the role of a larval pheromone and natural stream odor in spawning stream localization by migratory sea lamprey (Petromyzon marinus). Can J Fish Aquat Sci 58:2374–2385CrossRefGoogle Scholar
  111. Wagner CM, Jones ML, Twohey MB, Sorensen PW (2006) A field test verifies that pheromones can be useful for sea lamprey (Petromyzon marinus) control in the Great Lakes. Can J Fish Aquat Sci 63:475–479CrossRefGoogle Scholar
  112. Wagner CM, Twohey MB, Fine JM (2009) Conspecific cueing in the sea lamprey: do reproductive migrations consistently follow the most intense larval odour? Anim Behav 78:593–599CrossRefGoogle Scholar
  113. Weissburg MJ, Zimmer-Faust RK (1994) Odor plumes and how blue crabs use them in finding prey. J Exp Biol 197:349–375PubMedGoogle Scholar
  114. Wisenden BD (2008) Active space of chemical alarm cue in natural fish populations. Behaviour 145:391–407CrossRefGoogle Scholar
  115. Wisenden BD, Chivers DP, Smith RJF (1994) Risk-sensitive habitat use by brook stickleback (Culaea inconstans) in areas associated with minnow alarm pheromone. J Chem Ecol 20:2975–2983CrossRefGoogle Scholar
  116. Wisenden BD, Klitzke J, Nelson R, Friedl D, Jacobson PC (2004a) Predator-recognition training of hatchery-reared walleye (Stizostedion vitreum) and a field test of a training method using yellow perch (Perca flavescens). Can J Fish Aquat Sci 61:2144–2150CrossRefGoogle Scholar
  117. Wisenden BD, Vollbrecht KA, Brown JL (2004b) Is there a fish alarm cue? Affirming evidence from a wild study. Anim Behav 67:59–67CrossRefGoogle Scholar
  118. Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, New YorkCrossRefGoogle Scholar
  119. Yambe H, Yamazaki F (2001) A releaser pheromone that attracts methyltestosterone-treated immature fish in the urine of ovulated female rainbow trout. Fisheries Sci 67:214–220CrossRefGoogle Scholar
  120. Yambe H, Munakata A, Kitamura S, Aida K, Fusetani N (2003) Methyltestosterone induces male sensitivity to both primer and releaser pheromones in the urine of ovulated female masu salmon. Fish Physiol Biochem 28:279–280CrossRefGoogle Scholar
  121. Yambe H, Kitamura S, Kamio M, Yamada M, Matsunaga S, Fusetani N, Yamazaki F (2006) l-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. P Natl Acad Sci USA 103:15370–15374CrossRefGoogle Scholar
  122. Yun S-S, Scott AP, Li W (2003) Pheromones of the male sea lamprey, Petromyzon marinus L.: structural studies on a new compound, 3-keto allocholic acid, and 3-keto petromyzonol sulfate. Steroids 68:297–304PubMedCrossRefGoogle Scholar
  123. Zimmer RK, Commins JE, Browne KA (1999) Regulatory effects of environmental chemical signals on search behavior and foraging success. Ecology 80:1432–1446CrossRefGoogle Scholar
  124. Zimmer-Faust RK, Finelli CM, Pentcheff ND, Wethey DS (1995) Odor plumes and animal navigation in turbulent water-flow—a field-study. Biol Bull 188:111–116CrossRefGoogle Scholar

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© US Government 2010

Authors and Affiliations

  1. 1.Department of Fisheries and WildlifeMichigan State UniversityEast LansingUSA
  2. 2.Great Lakes Science Center, Hammond Bay Biological StationUSGSMillersburgUSA

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