Behavioral responses of sea lamprey (Petromyzon marinus) to a putative alarm cue derived from conspecific and heterospecific sources

In: Behaviour
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  • 1 Michigan State University, Department of Fisheries and Wildlife, 480 Wilson Road, 13 Natural Resources Building, East Lansing, MI, 48824, USA

The sea lamprey, Petromyzon marinus, exhibits a spectacular alarm response to the odor emitted from decayed conspecifics that may differ substantially in function from the well-characterized system in ostariophysan fishes. Here, we report a series of three laboratory experiments designed to characterize the behavioral responses of migratory-phase lampreys to a set of odors derived from conspecific and heterospecific tissues, determine whether sex or sexual maturation alters these responses, and ascertain if the putative alarm substance derives from a particular region of the body. A number of the findings were consistent with the prevailing predator-avoidance paradigm for fish alarm substances released from the skin after predator attack in that: (1) dilute odors derived from freshly ground skin were highly repellent; (2) the substance is contained in the organism early in life; (3) the odor derived from a close relative was avoided whereas those of a distant relative were not; and (4) upon sexual maturity female response to the alarm substance was attenuated. Two interesting patterns arose that differed substantially from the prevailing paradigm: (1) conspecific odors remained repellent after 96 h of aerobic decay; and (2) the cue was emitted from multiple areas of the body, not just the skin, and the repellency of the odor derived from any tissue increased in accordance with its mass. A persistent cue emitted from several sources suggests a broader ecological function than the detection and avoidance of a predator.

  • Abrahams M.V., Dill L.M. (1989). A determination of the energetic equivalence of the risk of predation. — Ecology 70: 999-1007.

  • Almeida P.R., Quintella B.R., Dias N.M. (2002). Movement of radio-tagged anadromous sea lamprey during the spawning migration in the River Mondego (Portugal). — Hydrobiologia 483: 1-8.

    • Search Google Scholar
    • Export Citation
  • Applegate V.C. (1950). Natural history of the sea lamprey in Michigan. Wildlife Service Special Scientific Report. — Fisheries 55: 1-237.

    • Search Google Scholar
    • Export Citation
  • Bednekoff P.A. (1996). Risk-sensitive foraging, fitness, and life histories: where does reproduction fit into the big picture?Am. Zool. 36: 471-483.

    • Search Google Scholar
    • Export Citation
  • Bergstedt R.A., Seelye J.G. (1995). Evidence for a lack of homing by sea lamprey. — Trans. Am. Fish. Soc. 124: 235-239.

  • Blanchet S., Bernatchez L., Dodson J.J. (2007). Behavioural and growth responses of a territorial fish (Atlantic salmon, Salmo salar, L.) to multiple predatory cues. — Ethology 113: 1061-1072.

    • Search Google Scholar
    • Export Citation
  • Bouwma P., Hazlett B.A. (2001). Integration of multiple predator cues by the crayfish, Orconectes propinquus. — Anim. Behav. 61: 771-776.

    • Search Google Scholar
    • Export Citation
  • Briones-Fourzán P., Lozano-Álvarez E. (2008). Coexistence of congeneric spiny lobsters on coral reefs: differences in conspecific aggregation patterns and their potential antipredator benefits. — Coral Reefs 27: 275-287.

    • Search Google Scholar
    • Export Citation
  • Brown G.E., Rive A.C., Ferrari M.C.O., Chivers D.P. (2006). The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk. — Behav. Ecol. Sociobiol. 61: 9-16.

    • Search Google Scholar
    • Export Citation
  • Bryer P.J., Mirza R.S., Chivers D.P. (2001). Chemosensory assessment of predation risk by slimy sculpins (Cottus cognatus): responses to alarm, disturbance, and predator cues. — J. Chem. Ecol. 27: 533-546.

    • Search Google Scholar
    • Export Citation
  • Carreau-Green N.D., Mirza R.S., Martínez M.L., Pyle G.G. (2008). The ontogeny of chemically mediated antipredator responses of fathead minnows Pimephales promelas. — J. Fish Biol. 73: 2390-2401.

    • Search Google Scholar
    • Export Citation
  • Chivers D.P., Smith R.J.F. (1998). Chemical alarm signaling in aquatic predator–prey systems: a review and prospectus. — Ecoscience 5: 338-352.

    • Search Google Scholar
    • Export Citation
  • Cochran P.A., Leistein A.A., Sneen M.E. (1992). Cases of predation and parasitism on lampreys in Wisconsin. — J. Freshw. Ecol. 7: 435-436.

  • Cochran P.A., Lyons J. (2004). Field and laboratory observations on the ecology and behavior of the silver lamprey (Ichthyomyzon unicuspis) in Wisconsin. — J. Freshw. Ecol. 19: 245-253.

    • Search Google Scholar
    • Export Citation
  • Dalesman S., Rundle S.D., Bilton D.T., Cotton P.A. (2007). Phylogenetic relatedness and ecological interactions determine antipredator behavior. — Ecology 88: 2462-2467.

    • Search Google Scholar
    • Export Citation
  • Døving K.B., Lastein S. (2009). The alarm reaction in fishes: odorants, modulations of responses, neural pathways. — In: International symposium on olfaction and taste ( Finger T.E., ed.). Wiley-Blackwell, Boston, MA, p.  413-423.

    • Search Google Scholar
    • Export Citation
  • Døving K.B., Westerberg H., Johnsen P.B. (1985). Role of olfaction in the behavioral and neuronal responses of Atlantic salmon, Salmo salar, to hydrographic stratification. — Can. J. Fish. Aquat. Sci. 42: 1658-1667.

    • Search Google Scholar
    • Export Citation
  • Downing S.W., Novales R.R. (1971). The fine structures of lamprey epidermis II. Club cells. — J. Ultrastruct. Res. 35: 295-303.

  • Ferrari M.C.O., Capitania-Kwok T., Chivers D.P. (2006). The role of learning in the acquisition of threat-sensitive responses to predator odours. — Behav. Ecol. Sociobiol. 60: 522-527.

    • Search Google Scholar
    • Export Citation
  • Ferrari M.C.O., Messier F., Chivers D.P. (2007). Degradation of chemical alarm cues under natural conditions: risk assessment by larval woodfrogs. — Chemoecology 17: 263-266.

    • Search Google Scholar
    • Export Citation
  • Ferrari M.O., Wisenden B.D., Chivers D.P. (2010). Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. — Can. J. Zool. 88: 698-724.

    • Search Google Scholar
    • Export Citation
  • Fine J.M., Vrieze L.A., Sorensen P.W. (2004). Evidence that petromyzontid lampreys employ a common migratory pheromone that is partially comprised of bile acids. — J. Chem. Ecol. 30: 2091-2110.

    • Search Google Scholar
    • Export Citation
  • Gall B.G., Mathis A. (2011). Ontogenetic shift in response to amphibian alarm cues by banded sculpins (Cottus carolinae). — Copeia: 5-8.

    • Search Google Scholar
    • Export Citation
  • Gende S.M., Quinn T.P., Wilson M.F. (2001). Consumption choice by bears feeding on salmon. — Oecologia 127: 372-382.

  • Golub J.L., Brown G.E. (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: 113-118.

    • Search Google Scholar
    • Export Citation
  • Hamdani E.H., Døving K.B. (2007). The functional organization of the fish olfactory system. — Prog. Neurobiol. 82: 80-86.

  • Harvey M.C., Brown G.E. (2004). Dine or dash? Ontogenetic shift in the response of yellow perch to conspecific alarm cues. — Environ. Biol. Fishes 70: 345-352.

    • Search Google Scholar
    • Export Citation
  • Hazlett B.A. (1999). Responses to multiple chemical cues by the crayfish Orconectes virilis. — Behaviour 136: 161-171.

  • Imre I., Brown G.E., Bergstedt R.A., McDonald R. (2010). Use of chemosensory cues as repellents for sea lamprey: potential directions for population management. — J. Great Lakes Res. 36: 790-793.

    • Search Google Scholar
    • Export Citation
  • Johnson N.S., Yun S.S., Thompson H.T., Brant C.O., Li W. (2009). A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps. — Proc. Natl. Acad. Sci. USA 106: 1021-1026.

    • Search Google Scholar
    • Export Citation
  • Kats L.B., Dill K.M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. — Ecoscience 5: 361-394.

  • Kim J.W., Brown G.E., Dolinsek I.J., Brodeur N.N., Leduc A.O.H.C., Grant J.W.A. (2009). Combined effects of chemical and visual information in eliciting antipredator behaviour in juvenile Atlantic salmon, Salmo salar. — J. Fish Biol. 74: 1280-1290.

    • Search Google Scholar
    • Export Citation
  • Kobayashi M., Sorensen P.W., Stacey N.E. (2002). Hormonal and pheromonal control of spawning behavior in the goldfish. — Fish Physiol. Biochem. 26: 71-84.

    • Search Google Scholar
    • Export Citation
  • Laframboise A.J., Ren X., Chang S., Dubuc R., Zielinski B.S. (2007). Olfactory sensory neurons in the sea lamprey display polymorphisms. — Neurosci. Lett. 414: 277-281.

    • Search Google Scholar
    • Export Citation
  • Lastein S., Höglund E., Mayer I., Øverli Ø., Døving K.B. (2008). Female crucian carp, Carassius carassius, lose predator avoidance behavior when getting ready to mate. — J. Chem. Ecol. 34: 1487-1491.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • Lima S.L., Dill L.M. (1990). Behavioural decisions made under the risk of predation: a review and prospectus. — Can. J. Zool. 68: 619-640.

    • Search Google Scholar
    • Export Citation
  • Littell R.C., Stroup W.W., Freund R.J. (2002). SAS® for linear models. — SAS Institute, Cary, NC.

  • Luehring M.A., Wagner C.M., Li W. (2011). The efficacy of two synthesized sea lamprey sex pheromone components as a trap lure when placed in direct competition with natural male odors. — Biol. Inv. 13: 1589-1597.

    • Search Google Scholar
    • Export Citation
  • Manion P.J., Hanson L.H. (1980). Spawning behavior and fecundity of lampreys from the upper three Great Lakes. — Can. J. Fish. Aquat. Sci. 37: 1635-1640.

    • Search Google Scholar
    • Export Citation
  • Manion P.J., Smith B.R. (1978). Biology of larval and metamorphosing sea lampreys, Petromyzon marinus, of the 1960 year class in the Big Garlic River, Michigan. Part 2. — Great Lakes Fishery Commission Technical Report No. 30. Great Lakes Fishery Commission, Ann Arbor, MI.

  • Marcus J.P., Brown G.E. (2003). Response of pumpkinseed sunfish to conspecific chemical alarm cues: an interaction between ontogeny and stimulus concentration. — Can. J. Zool. 81: 1671-1677.

    • Search Google Scholar
    • Export Citation
  • Mathis A. (2009). Alarm responses as a defense: chemical alarm cues in nonostariophysan fishes. — In: Fish defenses, Volume 2: Pathogens, parasites and predators ( Zaccone G., Perrière C., Mathis A., Kapoor B.G., eds). Science Publishers, Enfield, NH, p.  323-386.

    • Search Google Scholar
    • Export Citation
  • Mathis A., Smith R.J.F. (1993). Fathead minnows, Pimephales promelas, learn to recognize northern pike, Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike’s diet. — Anim. Behav. 46: 645-656.

    • Search Google Scholar
    • Export Citation
  • Mathuru A.S., Kibat C., Cheong W.F., Shui G., Wenk M.R., Friedrich R.W., Jesuthansan S. (2012). Chondroitin fragments are odorants that trigger fear behavior in fish. — Curr. Biol. 22: 538-544.

    • Search Google Scholar
    • Export Citation
  • McLean F., Barbee N.C., Swearer S.E. (2007). Avoidance of native versus non-native predator odours by migrating whitebait and juveniles of the common galaxiid, Galaxias maculatus. — NZ. J. Mar. Freshw. Res. 41: 175-184.

    • Search Google Scholar
    • Export Citation
  • McNamara J.M., Dall S.R.X. (2010). Information is a fitness enhancing resource. — Oikos 119: 231-236.

  • Metcalfe N.B., Huntingford F.A., Thorpe J.E. (1987). The influence of predation risk on the feeding motivation and foraging strategy of juvenile Atlantic salmon. — Anim. Behav. 35: 901-911.

    • Search Google Scholar
    • Export Citation
  • Mirza R.S., Chivers D.P. (2001). Are chemical alarm cues conserved within salmonid fishes?J. Chem. Ecol. 27: 1641-1655.

  • Mirza R.S. (2009). The nose knows: chemically mediated antipredator defenses in ostariophysans. — In: Fish defenses, Volume 2: Pathogens, parasites and predators ( Zaccone G., Perrière C., Mathis A., Kapoor B.G., eds). Science Publishers, Enfield, NH, p.  291-322.

    • Search Google Scholar
    • Export Citation
  • Mirza R.S., Chivers D.P. (2003). Response of juvenile rainbow trout to varying concentrations of chemical alarm cue: response thresholds and survival during encounters with predators. — Can. J. Zool. 81: 88-95.

    • Search Google Scholar
    • Export Citation
  • Mirza R.S., Scott J.J., Chivers D.P. (2001). Differential responses of male and female red swordtails to chemical alarm cues. — J. Fish Biol. 59: 716-728.

    • Search Google Scholar
    • Export Citation
  • Moore P., Crimaldi J. (2004). Odor landscapes and animal behavior: tracking odor plumes in different physical worlds. — J. Mar. Sys. 49: 55-64.

    • Search Google Scholar
    • Export Citation
  • Olsson O., Brown J.S., Smith H.G. (2002). Long- and short-term state-dependent foraging under predation risk: an indication of habitat quality. — Anim. Behav. 63: 981-989.

    • Search Google Scholar
    • Export Citation
  • Pfeiffer W. (1962). The fright reaction of fish. — Biol. Rev. 37: 495-511.

  • Pfeiffer W. (1977). Distribution of fright reaction and alarm substance cells in fishes. — Copeia: 653-665.

  • Pfeiffer W., Pletcher T.E. (1964). Club cells and granular cells in the skin of lampreys. — J. Fish. Res. Board Can. 21: 1083-1088.

  • Richardson M.K., Admiraal J., Wright G.M. (2010). Developmental anatomy of lampreys. — Biol. Rev. Camb. Philos. Soc. 85: 1-33.

  • Rohr J.R., Madison D.M., Sullivan A.M. (2002). The ontogeny of chemically-mediated antipredator behaviours in Newts (Notophthalmus viridescens): responses to injured and non-injured conspecifics. — Behaviour 139: 1043-1060.

    • Search Google Scholar
    • Export Citation
  • Schmidt K.A., Dall S.R.X., Van Gils J.A. (2010). The ecology of information: an overview on the ecological significance of making informed decisions. — Oikos 119: 304-316.

    • Search Google Scholar
    • Export Citation
  • Schütz F. (1956). Vergleichende Untersuchungen uber die Schreck- reaktion bei Fischen und deren Verbreitung. — Z. Vgl. Physiol. 38: 84-135.

    • Search Google Scholar
    • Export Citation
  • Shabani S., Kamio M., Derby C.D. (2008). Spiny lobsters detect conspecific blood-borne alarm cues exclusively through olfactory sensilla. — J. Exp. Biol. 211: 2600-2608.

    • Search Google Scholar
    • Export Citation
  • Siefkes M.J., Bergstedt R.A., Twohey M.B., Li W. (2003). Chemosterilization of male sea lampreys does not affect sex pheromone release. — Can. J. Fish. Aquat. Sci. 60: 23-31.

    • Search Google Scholar
    • Export Citation
  • Sih A. (1980). Optimal foraging: partial consumption of prey. — Am. Nat. 116: 281-290.

  • Smith R.J.F. (1976). Seasonal loss of alarm substance cells in North American Cyprinoid fishes and its relation to abrasive spawning. — Can. J. Zool. 54: 1172-1182.

    • Search Google Scholar
    • Export Citation
  • Smith R.J.F. (1979). Alarm reaction of Iowa and Johnny darters to chemicals from injured conspecifics. — Can. J. Zool. 57: 1278-1282.

    • Search Google Scholar
    • Export Citation
  • Smith R.J.F. (1992). Alarm signals in fishes. — Rev. Fish Biol. Fish. 2: 33-63.

  • Sorensen P.W., Fine J.M., Dvornikovs V., Jeffrey C.S., Shao J.F., Wang J.Z., Vrieze L.A., Anderson K.A., Hoye T.R. (2005). Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. — Nature Chem. Biol. 1: 324-328.

    • Search Google Scholar
    • Export Citation
  • Sower S.A., Plisetskaya E., Gorbman A. (1985). Steroid and thyroid hormone profiles following a single injection of partly purified salmon gonadotropin or GnRH analogues in male and female sea lamprey. — J. Exp. Zool. 235: 403-408.

    • Search Google Scholar
    • Export Citation
  • Vrieze L.A., Bergstedt R.A., Sorensen P.W. (2011). Olfactory-mediated stream-finding behavior of migratory adult sea lamprey (Petromyzon marinus). — Can. J. Fish. Aquat. Sci. 63: 523-533.

    • Search Google Scholar
    • Export Citation
  • Wagner R.H., Danchin É. (2010). A taxonomy of biological information. — Oikos 119: 203-209.

  • 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. — Can. J. Fish. Aquat. Sci. 63: 475-479.

    • Search Google Scholar
    • Export Citation
  • Wagner C.M., Twohey M.B., Fine J.M. (2009). Conspecific cueing in the sea lamprey: do reproductive migrations consistently follow the most intense larval odor?Anim. Behav. 78: 593-599.

    • Search Google Scholar
    • Export Citation
  • Wagner C.M., Stroud E.M., Meckley T.D. (2011). A deathly odor suggests a new sustainable tool for controlling a costly invasive species. — Can. J. Fish. Aquat. Sci. 68: 1157-1160.

    • Search Google Scholar
    • Export Citation
  • Waldman J., Grunwald C., Wirgin I. (2008). Sea lamprey Petromyzon marinus: an exception to the rule of homing in anadromous fishes. — Biol. Lett. 4: 659-662.

    • Search Google Scholar
    • Export Citation
  • Webster M.M., Laland K. (2011). Reproductive state affects reliance on public information in sticklebacks. — Proc. R. Soc. Lond. B Biol. 278: 619-627.

    • Search Google Scholar
    • Export Citation
  • Williams J.L., Snyder W.E., Wise D.H. (2001). Sex-based differences in antipredator behavior in the spotted cucumber beetle (Coleoptera: Chrysomelidae). — Entomol. Soc. Am. 30: 327-332.

    • Search Google Scholar
    • Export Citation
  • Wigley R.L. (1959). Life history of the sea lamprey of Cayuga Lake, New York. — Fish. Bull. U.S. Fish Wildl. Serv., Washington 59: 561-616.

    • Search Google Scholar
    • Export Citation
  • Wisenden B.D. (2008). Active space of chemical alarm cue in natural fish populations. — Behaviour 145: 391-407.

  • Wisenden B.D., Chivers D.P. (2006). The role of public chemical information in antipredator behaviour. — In: Communication in Fishes, Vol. 1 ( Ladich F., Collin S.P., Moller P., Kapoor B.G., eds). Science Publishers, Enfield, NH, p.  259-278.

    • Search Google Scholar
    • Export Citation
  • Wisenden B.D., Chivers D.P., Smith R.J.F. (1995). Early warning in the predation sequence: a disturbance pheromone in Iowa darters (Etheostoma exile). — J. Chem. Ecol. 21: 1469-1480.

    • Search Google Scholar
    • Export Citation
  • Wisenden B.D., Cline A., Sparkes T.C. (1999). Survival benefit to antipredator behavior in the amphipod Gammarus minus (Crustacea: Amphipoda) in response to injury-released chemical cues from conspecifics and heterospecifics. — Ethology 105: 407-414.

    • Search Google Scholar
    • Export Citation
  • Wisenden B.D., Rugg M.L., Korpi N.L., Fuselier L.C. (2009). Lab and field estimates of active time of chemical alarm cues of a cyprinid fish and an amphipod crustacean. — Behaviour 146: 1423-1442.

    • Search Google Scholar
    • Export Citation
  • Wisenden B.D., Binstock C.L., Knoll K.E., Linke A.D., Demuth B.S. (2010). Risk-sensitive information gathering by cyprinids following release of chemical alarm cues. — Anim. Behav. 79: 1101-1107.

    • Search Google Scholar
    • Export Citation
  • Yao M., Rosenfeld J., Attridge S., Sidhu S., Aksenov V., Rollo C.D. (2009). The ancient chemistry of avoiding risks of predation and disease. — Evol. Biol. 36: 267-281.

    • Search Google Scholar
    • Export Citation
  • Zhao X., Ferrari M.C.O., Chivers D.P. (2006). Threat-sensitive learning of predator odours by a prey fish. — Behaviour 143: 1103-1121.

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