Many teleost species respond with fright reactions to olfactory cues from injured skin of conspecifics, but they may also display responses to skin extracts of heterospecific fish. In the present study, we exposed crucian carp to skin extracts of conspecifics and three cross-order species of fish (brown trout, pike, and perch). Behavioural experiments showed that conspecific skin extracts induced fright reactions in crucian carp; extracts of brown trout induced such behaviour less frequently, while extracts of perch and pike were poor inducers of fright responses. The olfactory bulb is chemo-topically organized, and different sub-sets of neurons respond to functionally related odorants that mediate distinct behaviours. Accordingly, behavioural responses to an alarm signal should be reflected by activation of the neurons mediating fright reaction. Extracellular recordings from single units in the olfactory bulb showed that the relay neurons activated by conspecific skin extracts were also activated by extracts of brown trout, whereas extracts of perch and pike less frequently activated these units. Thus, the difference in behavioural responses matched the differences in the neural responses, indicating that skin extracts of heterospecific fish are more likely to induce fright behaviour when the responding sub-set of olfactory neurons is similar to the sub-set responding to conspecific extracts. Our results suggest that responses to injured heterospecific fish rely on chemical resemblance between odorants from heterospecific and conspecific skin, and need not be based on any form of associative learning.
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Barlow H.B. (1972). Single units and sensation: a neuron doctrine for perceptual psychology? — Perception 1: 371-394.
BeLanger A.J. , Arbuckle W.J. , Corkum L.D. , Gammon D.B. , Li W. , Scott A.P. , Zielinski B.S. (2004). Behavioural and electrophysiological responses by reproductive female Neogobius melanostomus to odours released by conspecific males. — J. Fish Biol. 65: 933-946.
Brown G.E. , Smith R.J.F. (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: 611-617.
Chivers D.P. , Smith R.J.F. (1994a). Intra- and interspecific avoidance of areas marked with skin extract from brook sticklebacks (Culaea inconstans) in a natural habitat. — J. Chem. Ecol. 20: 1517-1524.
Chivers D.P. , Smith R.J.F. (1994b). The role of experience and chemical alarm signalling in predator recognition by fathead minnows, Pimephales promelas. — J. Fish Biol. 44: 273-285.
Døving K.B. , Hamdani E.H. , Höglund E. , Kasumyan A.O. , Tuvikene A. (2005). A review on the chemical and physiological basis of alarm reactions in cyprinids. — In: Fish chemosenses ( Reuter K. , Kapoor B.G. , eds). Science Publishers, Enfield, NH, p. 133-163.
Døving K.B. , Lastein S. (2009). The alarm reaction in fishes-odorants, modulation of responses, neural pathways. — Ann. N.Y. Acad. Sci. 1170: 413-423.
Døving K.B. , Selset R. (1980). Behavior patterns in cod released by electrical stimulation of olfactory tract bundlets. — Science 207: 559-560.
Ferrari M.C.O. , Trowell J.J. , Brown G.E. , Chivers D.P. (2005). The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. — Anim. Behav. 70: 777-784.
Friedrich R.W. , Korsching S.I. (1998). Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. — J. Neurosci. 18: 9977-9988.
Friedrich R.W. , Laurent G. (2004). Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. — J. Neurophysiol. 91: 2658-2669.
Gibson A.K. , Mathis A. (2006). Opercular beat rate for rainbow darters Etheostoma caeruleam exposed to chemical stimuli from conspecific and heterospecific. — J. Fish Biol. 69: 224-232.
Hamdani E.H. , Døving K.B. (2003). Sensitivity and selectivity of neurons in the medial region of the olfactory bulb to skin extract from conspecifics in crucian carp, Carassius carassius. — Chem. Senses 28: 181-189.
Hamdani E.H. , Døving K.B. (2006). Functional organization of the olfactory system in fish. — In: Fish communication ( Collin S.P. , Moller P. , Kapoor B.G. , eds). Science Publishers, Enfield, NH, p. 223-257.
Hamdani E.H. , Døving K.B. (2007). The functional organization of the fish olfactory system. — Prog. Neurobiol. 82: 80-86.
Hamdani E.H. , Kasumyan A. , Døving K.B. (2001). Is feeding behaviour in crucian carp mediated by the lateral olfactory tract? — Chem. Senses 26: 1133-1138.
Hamdani E.H. , Stabell O.B. , Alexander G. , Døving K.B. (2000). Alarm reaction in the crucian carp is mediated by the medial bundle of the medial olfactory tract. — Chem. Senses 25: 103-109.
Heikkinen L.I. (2010). Anatomiske og fysiologiske egenskaper ved den interbulbære forbindelsen i luktesystemet hos karuss, Carassius carassius. — MSc Thesis, University of Oslo, Oslo.
Hubel D.H. (1957). Tungsten microelectrode for recording from single units. — Science 125: 549-550.
Kasumyan A.O. , Ponomarev V.Y. (1987). Biochemical features of alarm pheromone in fish of the order cypriniformes. — J. Evol. Biochem. Physiol. 23: 20-24.
Kimbrell G.M. , Weinrott M.R. , Morris E.K. , Scheid J. , Sangston D. (1970). Alarm pheromone and avoidance conditioning in goldfish, Carassius auratus. — Nature 225: 754.
Lastein S. , Hamdani E.H. , Døving K.B. (2006). Gender distinction in neural discrimination of sex pheromones in the olfactory bulb of crucian carp, Carassius carassius. — Chem. Senses 31: 69-77.
Lastein S. , Hamdani E.H. , Døving K.B. (2008a). Single unit responses to skin odorants from conspecifics and heterospecifics in the olfactory bulb of crucian carp Carassius carassius. — J. Exp. Biol. 211: 3529-3535.
Lastein S. , Höglund E. , Mayer I. , Øverli Ø. , Døving K.B. (2008b). Female crucian carp, Carassius carassius, lose predator avoidance behavior when getting ready to mate. — J. Chem. Ecol. 34: 1487-1491.
Lastein S. , Höglund E. , Øverli Ø. , Døving K.B. (2008c). Effects of antalarmin, a CRF receptor 1 antagonist, on fright reaction and endocrine stress response in crucian carp (Carassius carassius). — J. Comp. Physiol. 194: 1007-1012.
Lawrence B.J. , Smith R.J.F. (1989). Behavioral-response of solitary fathead minnows, Pimephales promelas, to alarm substance. — J. Chem. Ecol. 15: 209-219.
Lee B.B. (1999). Single units and sensation: a retrospect. — Perception 28: 1493-1508.
Li C. , Lu G. , Orti G. (2008). Optimal data partitioning and a test case for ray-finned fishes (Actinopterygii) based on ten nuclear loci. — Syst. Biol. 57: 519-539.
Magurran A.E. (1989). Acquired recognition of predator odor in the european minnow (Phoxinus phoxinus). — Ethology 82: 216-223.
Mathis A. , Smith R.J.F. (1993). Intraspecific and cross-superorder responses to chemical alarm signals by Brook stickleback. — Ecology 74: 2395-2404.
Mathuru A.S. , Kibat C. , Cheong W.F. , Shui G. , Wenk M.R. , Friedrich R.W. , Jesuthasan S. (2012). Chondroitin fragments are odorants that trigger fear behavior in fish. — Curr. Biol. 22: 538-544.
Nikonov A.A. , Caprio J. (2001). Electrophysiological evidence for a chemotopy of biologically relevant odors in the olfactory bulb of the channel catfish. — J. Neurophysiol. 86: 1869-1876.
Pfeiffer W. (1963). Alarm substances. — Experientia 19: 1-11.
Pfeiffer W. (1977). Distribution of fright reaction and alarm substance cells in fishes. — Copeia: 653-665.
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. — Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129: 645-651.
Pollock M.S. , Chivers D.P. (2004). The effects of density on the learned recognition of heterospecific alarm cues. — Ethology 110: 341-349.
Schutz F. (1956). Vergleichende Untersuchungen über die Schreckreaktion bei Fischen und deren verbreitung. — Z. Vergl. Physiol. 38: 84-135.
Smith R.J.F. (1982). Reaction of Percina nigrofasciata, Ammocrypta beani, and Etheostoma swaini (Percidae, Pisces) to conspecific and intergeneric skin extracts. — Can. J. Zool. 60: 1067-1072.
Stabell O.B. , Lwin M.S. (1997). Predator-induced phenotypic changes in crucian carp are caused by chemical signals from conspecifics. — Environ. Biol. Fish 49: 145-149.
von Frisch K. (1938). Zur Psychologie des Fisch-Schwarmes. — Naturwissenschaften 26: 601-606.
von Frisch K. (1941). Über einen Schreckstoff der Fischhaut und seine biologische Beteutung. — Z. Vergl. Physiol. 29: 46-145.
Weltzien F.A. , Höglund E. , Hamdani el H. , Døving K.B. (2003). Does the lateral bundle of the medial olfactory tract mediate reproductive behavior in male crucian carp? — Chem. Senses 28: 293-300.
Yaksi E. , Judkewitz B. , Friedrich R.W. (2007). Topological reorganization of odor representations in the olfactory bulb. — PLoS Biol. 5: 1453-1473.
Zippel H.P. , Gloger M. , Nasser S. , Wilcke S. (2000). Odour discrimination in the olfactory bulb of goldfish: contrasting interactions between mitral cells and ruffed cells. — Phil. Trans. R. Soc. Lond. B: Biol. 355: 1229-1332.
All Time | Past 365 days | Past 30 Days | |
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Many teleost species respond with fright reactions to olfactory cues from injured skin of conspecifics, but they may also display responses to skin extracts of heterospecific fish. In the present study, we exposed crucian carp to skin extracts of conspecifics and three cross-order species of fish (brown trout, pike, and perch). Behavioural experiments showed that conspecific skin extracts induced fright reactions in crucian carp; extracts of brown trout induced such behaviour less frequently, while extracts of perch and pike were poor inducers of fright responses. The olfactory bulb is chemo-topically organized, and different sub-sets of neurons respond to functionally related odorants that mediate distinct behaviours. Accordingly, behavioural responses to an alarm signal should be reflected by activation of the neurons mediating fright reaction. Extracellular recordings from single units in the olfactory bulb showed that the relay neurons activated by conspecific skin extracts were also activated by extracts of brown trout, whereas extracts of perch and pike less frequently activated these units. Thus, the difference in behavioural responses matched the differences in the neural responses, indicating that skin extracts of heterospecific fish are more likely to induce fright behaviour when the responding sub-set of olfactory neurons is similar to the sub-set responding to conspecific extracts. Our results suggest that responses to injured heterospecific fish rely on chemical resemblance between odorants from heterospecific and conspecific skin, and need not be based on any form of associative learning.
All Time | Past 365 days | Past 30 Days | |
---|---|---|---|
Abstract Views | 430 | 62 | 7 |
Full Text Views | 49 | 2 | 0 |
PDF Views & Downloads | 22 | 4 | 0 |