Reproductive status influences multisensory integration responses in female round gobies, Neogobius melanostomus

Animal Behaviour

Volumn 83, Issue 5, 2012, Pages 1179-1185

  Kasurak, A V ^a   Zielinski, B S ^a   Higgs, D M ^a  

^a UNIVERSITY OF WINDSOR   (Canada)

Author keywords

Auditory; Enhanced response; Multisensory; Neogobius melanostomus; Olfactory; Pheromone; Round goby

Indexed keywords

AUDITORY CUE; BREEDING SEASON; CHEMICAL CUE; CONSPECIFIC; FEMALE; OLFACTORY CUE; PERCIFORM; PHEROMONE; REPRODUCTIVE STATUS; SIGNALING;

APOLLONIA MELANOSTOMUS; GOBIIDAE; NEOGOBIUS;

EID: 84859714793     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2012.02.008     Document Type: Article

References (67)

1. Acquistapace P., Aquiloni L., Hazlett B.A., Gherardi F. Multimodal communication in crayfish: sex recognition during mate search by male Austropotamobius pallipes. Canadian Journal of Zoology 2002, 80:2041-2045.
2. Akamatsu T., Okumura T., Novarini N., Yan H.K. Empirical refinements applicable to the recording of fish sounds in small tanks. Journal of the Acoustical Society of America 2002, 112:3073-3082.
3. Andersson S., Amundsen T. Ultraviolet colour vision and ornamentation in bluethroats. Proceedings of the Royal Society B 1997, 264:1587-1591.
4. Archard G.A., Cuthill I.C., Partridge J.C., Oosterhout C.V. Female guppies (Poecilia reticulata) show no preference for conspecific chemosensory cues in the field or an artificial flow chamber. Behaviour 2008, 145:1329-1346.
5. Atema J., Kingsford M.J., Gerlach G. Larval reef fish could use odour for detection, retention and orientation to reefs. Marine Ecology Progress Series 2002, 241:151-160.
6. Baker M.A., Weiler E.M. Sex of listener and hormonal correlates of auditory thresholds. British Journal of Audiology 1977, 11:65-68.
7. Barry K.L., Holwell G.I., Herberstein M.E. Multimodal mate assessment by male praying mantids in a sexually cannibalisitic mating system. Animal Behaviour 2010, 79:1165-1172. 10.1016/j.anbehav.2010.02.025.
8. Belanger A.J., Arbuckle W.J., Corkum L.D., Gammon D.B., Li W., Scott A.P., Zielinski B.S. Behavioural and electrophysiological responses by reproductive female Neogobius melanostomus to odours released by conspecific males. Journal of Fish Biology 2004, 65:933-946.
9. Belanger R.M., Corkum L.D., Zielinski B.S. Differential behavioural responses by reproductive and non-reproductive male round gobies (Neogobius melanostomus) to the putative pheromone estrone. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 2007, 147:77-83.
10. Belanger A.J., Bobeica I., Higgs D.M. The effect of stimulus type and background noise on hearing abilities of the round goby, Neogobius melanostomus. Journal of Fish Biology 2010, 77:1488-1504.
11. Belanger R.M., Pachkowski M.D., Stacey N.E. Methyltestosterone-induced changes in electro-olfactogram responses and courtship behaviours of cyprinids. Chemical Senses 2010, 35:65-74.
12. Boyd H., Fabricius E. Observations on the incidence of following of visual and auditory stimuli in naive mallard ducklings (Anas platyrhynchos). Behaviour 1965, 25:1-15.
13. Braun C.B., Coombs S., Fay R.R. What is the nature of multisensory interaction between octavolateralis sub-systems?. Brain, Behavior and Evolution 2002, 59:162-176.
14. Brown A.D., Mussen T.D., Sisneros J.A., Coffin A.B. Reevaluating the use of aminoglycoside antibiotics in behavioral studies of the lateral line. Hearing Research 2011, 272:1-4.
15. Charlebois P.M., Marsden J.E., Goettel R.G., Wolfe R.K., Jude D.J., Rudnicka S. The Round Goby, Neogobius melanostomus (Pallas), a Review of European and North American Literature 1997, Illinois-Indiana Sea Grant Program, Illinois Natural History Survey, Champaign.
16. Clement T.S., Grens K.E., Fernald R.D. Female affiliative preference on reproductive state in the African cichlid fish, Astatotilapia burtoni. Behavioral Ecology 2005, 16:83-88.
17. Cole K.S., Smith R.J.F. Attraction of female fathead minnows, Pimephales promelas, to chemical stimuli from breeding males. Journal of Chemical Ecology 1992, 18:1269-1284.
18. Crow R.T., Liley N.R. A sexual pheromone in the guppy, Poecilia reticulata (Peters). Canadian Journal of Zoology 1979, 57:184-188.
19. Cummings M.E., Bernal X.E., Reynaga R., Rand A.S., Ryan M.J. Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females. Journal of Experimental Biology 2008, 211:1203-1210.
20. Donaldson E.M., Hunter G.A. Induced final maturation, ovulation and spermiation in cultured fish. Fish Physiology. Vol. 9 1983, 351-404. Academic Press, New York. W.S. Hoar, D.J. Randall, E.M. Donaldson (Eds.).
21. Elkind-Hirsch K.E., Stoner W.R., Stach B.A., Jerger J.F. Estrogen influences auditory brainstem responses during the normal menstrual cycle. Hearing Research 1992, 60:143-148.
22. Field A. Discovering Statistics Using SPSS 2009, Sage, Thousand Oaks, California. 3rd edn.
23. Frade P., Hubbard P.C., Barata E.N., Canario A.V.M. Olfactory sensitivity of the Mozambique tilapia to conspecific odours. Journal of Fish Biology 2002, 61:1239-1254.
24. Gammon D.B., Li W., Scott A.P., Zielinski B.S., Corkum L.D. Behavioural responses of female Neogobius melanostomus to odours of conspecifics. Journal of Fish Biology 2005, 67:615-626.
25. García-López á., Couto E., Canario A.V.M., Sarasquete C., Martínez-Rodríguez G. Ovarian development and plasma sex steroid levels in cultured female Senegalese sole Solea senegalensis. Comparative Biochemistry and Physiology A 2007, 146:342-354.
26. Hamdani E.H., Lastein S., Gregersen F., Doving K.B. Seasonal variations in olfactory sensory neurons: fish sensitivity to sex pheromones explained?. Chemical Senses 2008, 33:119-123.
27. Hebets E.A. Attention-altering signal interactions in the multimodal courtship display of the wolf spider Schizocosa uetzi. Behavioral Ecology 2005, 16:75-82.
28. Hebets E.A., Papaj D.R. Complex signal function: developing a framework of testable hypotheses. Behavioral Ecology and Sociobiology 2005, 57:197-214.
29. Hebets E.A., Cuasay K., Rivlin P.K. The role of visual ornamentation in female choice of a multimodal male courtship display. Ethology 2006, 112:1062-1070.
30. Honkavaara J., Koivula M., Korpimaki E., Siitari H., Viitala J. Ultraviolet vision and foraging in terrestrial vertebrates. Oikos 2002, 98:505-511.
31. Katare Y., Scott A.P., Laframboise A.J., Li W., Alyasha'e Z., Caputo C.B., Loeb S.J., Zielinski B. Release of free and conjugated forms of the putative pheromonal steroid, 11-oxo-etiocholanolone, by reproductively mature male round goby (Neogobius melanostomus Pallas, 1814). Biology of Reproduction 2011, 84:288-298.
32. Kereliuk, M. R. 2009. Female round goby (Neogobius melanostomus) behavioural responses to fractionated male conditioned water and to steroids released by males. M.Sc. thesis, University of Windsor.
33. Knudsen E.I., Knudsen P.F. Vision guides the adjustment of auditory localization in young barn owls. Science 1985, 230:545-548.
34. Kulahci I.G., Dornhaus A., Papaj D.R. Multimodal signals enhance decision making in foraging bumble-bees. Proceedings of the Royal Society B 2008, 275:797-802.
35. Kulikova N.I. The effect of chorionic gonadotropin on growth and maturation of the oocytes of the round goby, Neogobius melanostomus. Journal of Ichthyology 1985, 25:86-98.
36. Laframboise A.J., Zielinski B.S. The effect of elevated steroid concentrations released by male round gobies, Neogobius melanostomus, on olfactory responses in females. Journal of Chemical Ecology 2011, 37:260-262.
37. Lengkeek W., Didderen K. Breeding cycles and reproductive behaviour in the river blenny Salaria fluviatilis. Journal of Fish Biology 2006, 69:1837-1844.
38. Lynch K.S., Rand A.S., Ryan M.J., Wilczynski W. Plasticity in female mate choice associated with changing reproductive states. Animal Behaviour 2004, 69:689-699.
39. MacInnis A.J., Corkum L.D. Fecundity and reproductive season of the round goby Neogobius melanostomus in the upper Detroit River. Transactions of the American Fisheries Society 2000, 129:136-144.
40. McLennan D.A. The importance of olfactory signals in the gasterosteid mating system: sticklebacks go multimodal. Biological Journal of the Linnean Society 2003, 80:555-572.
41. McLennan D.A. Changes in response to olfactory cues across the ovulatory cycle in brook sticklebacks, Culaea inconstans. Animal Behaviour 2005, 69:181-188.
42. McLennan D.A., Ryan M.J. Responses to conspecific and heterospecific olfactory cues in the swordtail Xiphophorus cortezi. Animal Behaviour 1997, 54:1077-1088.
43. Marentette J.R., Corkum L.D. Does the reproductive status of male round gobies (Neogobius melanostomus) influence their response to conspecific odours?. Environmental Biology of Fishes 2008, 81:447-455.
44. Meredith M.A., Stein B.E. Visual, auditory, and somatosensory convergence on cells in the superior colliculus results in multisensory integration. Journal of Neurophysiology 1986, 56:640-662.
45. Moller P. Multimodal sensory integration in weakly electric fish: a behavioural account. Journal of Physiology-Paris 2002, 96:547-556.
46. Moller P., Serrier J., Squire A., Boudinot M. Social spacing in the mormyrid fish Gnathonemus petersii (Pisces): a multisensory approach. Animal Behaviour 1982, 30:641-650.
47. Montgomery J.C., Macdonald F., Baker C.F., Carton A.G. Hydrodynamic contributions to multimodal guidance of prey capture behaviour in fish. Brain, Behavior and Evolution 2002, 59:190-198.
48. Myrberg A.A. The role of chemical and visual stimuli in the preferential discrimination of young by the cichlid fish Cichlasoma nigrofasciatum (Günther). Zeitschrift für Tierpsychologie 1975, 37:274-297.
49. New J.G. Multimodal integration in the feeding behaviors of predatory teleost fishes. Brain, Behavior and Evolution 2002, 59:177-189.
50. New J.G., Kang P.Y. Multimodal sensory integration in the strike-feeding behaviour of predatory fishes. Philosophical Transactions of the Royal Society of London, Series B 2000, 355:1321-1324.
51. O'Loghlen A.L., Rothstein S.I. Multimodal signalling in a songbird: male audiovisual displays vary significantly by social context in brown-headed cowbirds. Animal Behaviour 2010, 79:1285-1292. 10.1016/j.anbehav.2010.03.001.
52. Partan S.R. Multisensory animal communication. The Handbook of Multisensory Processes 2004, 225-240. MIT Press, Cambridge, Massachusetts. G.A. Calvert, C. Spence, B.E. Stein (Eds.).
53. Partan S.R., Marler P. Issues in the classification of multimodal communication signals. American Naturalist 2005, 166:231-245.
54. Rogers P.H., Cox M. Underwater sound as a biological stimulus. Sensory Biology of Aquatic Animals 1988, 131-150. Springer-Verlag, New York. J. Atema, R.R. Fay, A.N. Popper, W.N. Tavolga (Eds.).
55. Rollo A., Higgs D. Differential acoustic response specificity and directionality in the round goby, Neogobius melanostomus. Animal Behaviour 2008, 75:1903-1912.
56. Rollo A., Andraso G., Janssen J., Higgs D. Attraction and localization of round goby (Neogobius melanostomus) to conspecific calls. Behaviour 2007, 44:1-21.
57. Satou M., Takeuchi H.A., Takei K., Hasegawa T., Matsushima T., Okumoto N. Characterization of vibrational and visual signals which elicit spawning behaviour in male hime salmon (landlocked red salmon, Onchorhyncus nerkus). Journal of Comparative Physiology A: Neuroethology, Sensory, Neural and Behavioral Physiology 1994, 174:527-537.
58. Schaefer H.M., Levy D.J., Schaefer V., Avery M.L. The role of chromatic and achromatic signals for fruit detection by birds. Behavioral Ecology 2006, 17:784-789.
59. Sisneros J.A. Adaptive hearing in the vocal plainfin midshipman fish: getting in tune for the breeding season and implications for acoustic communication. Integrative Zoology 2009, 4:33-42.
60. Sisneros J.A., Bass A.H. Seasonal plasticity of peripheral auditory frequency sensitivity. Journal of Neuroscience 2003, 23:1049-1058.
61. Smith E.J., Partridge J.C., Parsons K.N., White E.M., Cuthill I.C., Bennett A.T.D., Church S.C. Ultraviolet vision and mate choice in the guppy (Poecilia reticulate). Behavioral Ecology 2002, 13:11-19.
62. Stein B.E., Meredith M.A., Huneycutt W.S., McDade L. Behavioural indices of multisensory integration: orientation to visual cues is affected by auditory stimuli. Journal of Cognitive Neuroscience 1989, 1:12-24.
63. Tavolga W.N. Visual, chemical and sound stimuli as cues in the sex discriminatory behaviour of the gobiid fish Bathygobius soporator. Zoologica 1956, 41:49-65.
64. Uetz G.W., Roberts J.A., Taylor P.W. Multimodal communication and mate choice in wolf spiders: female response to multimodal versus unimodal signals. Animal Behaviour 2009, 78:299-305.
65. Von der Emde G., Bleckmann H. Finding good: senses involved in foraging for insect larvae in the electric fish Gnathonemus petersii. Journal of Experimental Biology 1998, 201:969-980.
66. Wiley R.H., Richards D.G. Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations. Behavioral Ecology and Sociobiology 1978, 3:69-94.
67. Young J.A.M., Marentette J.R., Gross C., McDonald J.I., Verma A., Marsh Rollo S.E., Macdonald P.D.M., Earn D.J.D., Balshine S. Demography and substrate affinity of the round goby (Neogobius melanostomus) in Hamilton Harbour. Journal of Great Lakes Research 2010, 36:115-122.