Predator recognition of chemical cues in crayfish: diet and experience influence the ability to detect predation threats

in Behaviour
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Abstract

Aquatic prey often alter their morphology, physiology, and/or behaviour when presented with predatory chemical cues which are heavily influenced by the diet of the predator. We tested the roles that diet and prey familiarity with predators play in the ability of prey to recognize predator threats. Odours from two fish, bass and cichlid fed a vegetarian, protein, heterospecific, and a conspecific diet, were collected and presented to virile crayfish in a choice arena. Our results show that crayfish altered their behaviour in the presence of odours containing conspecific, as opposed to heterospecific diets, but only from familiar predators. A reduced anti-predator response was measured with odours from an unfamiliar predator fed conspecific crayfish. Therefore, crayfish may be able to determine different threat levels based on the different dietary cues from a potential predator, but only when the prey have familiarity with the predators.

Predator recognition of chemical cues in crayfish: diet and experience influence the ability to detect predation threats

in Behaviour

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References

  • AcquistapaceP.HazlettB.A. & GherardiF. (2003). Unsuccessful predation and learning of predator cues by crayfish. — J. Crust. Biol. 23: 364-370.

  • Alexander Jr.J.E. & CovichA.P. (1991). Predator avoidance by the freshwater snail Physella virgate in response to the crayfish Procambarus simulans. — Oecologia 87: 435-442.

  • AtemaJ. (1996). Eddy chemotaxis and odor landscapes: exploration of nature with animal sensors. — Biol. Bull. 191: 129-138.

  • BatesD.MaechlerM.BolkerB. & WalkerS. (2015). Fitting linear mixed-effects models using lme4. — J. Stat. Soft. 67: 1-48. DOI:10.18637/jss.v067.i01.

  • BergmanD.A. & MooreP.A. (2003). Field observations of intraspecific agonistic behavior of two crayfish species, Orconectes rusticus and Orconectes virilis, in different habitats. — Biol. Bull. 205: 26-35.

  • BrönmarkC. & MinerJ.G. (1992). Predator-induced phenotypical change in body morphology in crucian carp. — Science 258: 1348-1350.

  • CaiF.WuZ.HeN. & WangZ. (2011). Can native species crucian carp Carassius auratus recognizes the introduced red swamp crayfish Procambarus clarkii?Curr. Zool. 57: 330-339.

  • ChiversD.P. & MirzaR.S. (2001). Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. — Chem. Signal. 9: 19-26.

  • ChiversD.P.WisendenB.D. & SmithR.J.F. (1996). Damselfly larvae learn to recognize predators from chemical cues in the predator’s diet. — Anim. Behav. 52: 315-320.

  • ChiversD.P. & SmithR.J.F. (1998). Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. — Ecoscience 5: 338-352.

  • DalesmanS. & RundleS.D. (2010). Cohabitation enhances the avoidance response to heterospecific alarm cues in a freshwater snail. — Anim. Behav. 79: 173-177.

  • DalesmanS.RundleS.D.ColemanR.A. & CottonP.A. (2006). Cue association and antipredator behaviour in a pulmonate snail, Lymnaea stagnalis. — Anim. Behav. 71: 789-797.

  • DalesmanS.RundleS.D.BiltonD.T. & CottonP.A. (2007). Phylogenetic relatedness and ecological interactions determine antipredator behavior. — Ecology 88: 2462-2467.

  • DixonD.L.PratchettM.S. & MundayP.L. (2012). Reef fishes innately distinguish predators based on olfactory cues associated with recent prey items rather than individual species. — Anim. Behav. 84: 45-51.

  • Ferland-RaymondB. & MurrayD.L. (2008). Predator diet and prey adaptive responses: can tadpoles distinguish between predators feeding on congeneric vs. conspecific prey?Can. J. Zool. 86: 1329-1336.

  • FerrariM.C.RiveA.C.MacNaughtonC.J.BrownG.E. & ChiversD.P. (2008). Fixed vs. random temporal predictability of predation risk: an extension of the risk allocation hypothesis. — Ethology 114: 238-244.

  • FerrariM.C.O.SihA. & ChiversD.P. (2009). The paradox of risk allocation: a review and prospectus. — Anim. Behav. 78: 579-585.

  • FerrariM.C.O.WisendenB.D. & ChiversD.P. (2010). Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. — Can. J. Zool. 88: 698-724.

  • GherardiF.MavutiK.M.PaciniN.TricarioE. & HarperD.M. (2011). The smell of danger: chemical recognition of fish predators by the invasive crayfish Procambarus clarkii. — Freshw. Biol. 56: 1567-1578.

  • GonzaloA.LópezP. & MartínJ. (2007). Iberian green frog tadpoles may learn to recognize novel predators from chemical alarm cues of conspecifics. — Anim. Behav. 74: 447-453.

  • GrasonE.W. (2017). Does cohistory constrain information use? Evidence for generalized risk assessment in nonnative prey. — Am. Nat. 189: 213-226.

  • GrostalP. & DickeM. (2000). Recognising one’s enemies: a functional approach to risk assessment by prey. — Behav. Ecol. Sociobiol. 47: 258-264.

  • HazlettB.A. & SchoolmasterD.R. (1988). Responses of cambarid crayfish to predator odor. — J. Chem. Ecol. 24: 1757-1770.

  • HazlettB.A. (2003). Predator recognition and learned irrelevance in the crayfish Orconectes virilis. — Ethology 109: 765-780.

  • HillA.M.SinarsD.M. & LodgeD.M. (1993). Invasion of an occupied niche by the crayfish Orconectes rusticus: potential importance of growth and mortality. — Oecology 94: 303-306.

  • HothornT.BretzF. & WestfallP. (2008). Simultaneous inference in general parametric models. — Biomet. J. 50: 346-363.

  • JutfeltF.SundinJ.RabyG.D.KrångA. & ClarkT.D. (2016). Two-current choice flumes for testing avoidance and preference in aquatic animals. — Methods Ecol. Evol. 8: 379-390.

  • KatsL.B. & DillL.M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. — Ecoscience 5: 361-394.

  • LargeS.I. & SmeeD.L. (2010). Type and nature of cues used by Nucella lapillus to evaluate predation risk. — J. Exp. Mar. Biol. Ecol. 396: 10-17.

  • LimaS.L. & BednekoffP.A. (1999). Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. — Am. Nat. 153: 649-659.

  • LimaS.L. & DillL.M. (1990). Behavioral decisions made under the risk of predation: a review and prospectus. — Can. J. Zool. 68: 619-640.

  • MachM.E. & BourdeauP.E. (2011). To flee or not to flee? Risk assessment by a marine snail in multiple cue environments. — J. Exp. Mar. Biol. Ecol. 409: 166-171.

  • MarquisO.SaglioP. & NeveuA. (2004). Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. — Arch. Hydrobiol. 160: 153-170.

  • MathisA. & SmithJ.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.

  • McLennanD.A. & RyanM.J. (1997). Responses to conspecific and heterospecific olfactory cues in swordtail Xiphophorus cortezi. — Anim. Behav. 54: 1077-1088.

  • MirzaR.S.ChiversD.P. & GodinJ.G.J. (2001). Brook charr alevins alter timing of nest emergence in response to chemical cues from fish predators. — J. Chem. Ecol. 27: 1775-1785.

  • MirzaR.S.FerrariM.C.KieseckerJ.M. & ChiversD.P. (2006). Responses of American toad tadpoles to predation cues: behavioural response thresholds, threat-sensitivity and acquired predation recognition. — Behaviour 143: 877-889.

  • MooreP.A. (2007). Agonistic behavior in freshwater crayfish: the influence of intrinsic and extrinsic factors on aggressive behavior and dominance. — In: Evolutionary ecology of social and sexual systems: Crustacea as models organisms (DuffyJ.E. & ThielM. eds). Oxford University PressOxford p. 90-114.

  • MurrayD.L. & JenkinsC.L. (1999). Predation risk as a function of predator dietary cues in terrestrial salamanders. — Anim. Behav. 57: 33-39.

  • NunesA.L.Richter-BioxA.LaurilaA. & RebeloR. (2012). Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study. — Oecology 171: 115-127.

  • PeacorK.W. & HazlettB.A. (2006). A test of temporal variation in risk and food stimuli on behavioral tradeoffs in the rusty crayfish, Orconectes rusticus: risk allocation and stimulus degradation. — Ethology 112: 230-237.

  • PollockM.S.ChiversD.P.MirzaR.S. & WisendenB.D. (2003). Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. — Environ. Biol. Fish. 66: 313-319.

  • R Core Team (2018). R: a language and environment for statistical computing. — R Foundation for Statistical ComputingVienna.

  • ReynoldsJ.D. (2011). A review of ecological interactions between crayfish and fish, indigenous and introduced. — Knowl. Manage. Aquat. Ecosyst. 401: 10.

  • RobertsL.J. & de LeanizC.G. (2011). Something smells fishy: predator-naive salmon use diet cues, not kairomones, to recognize a sympatric mammalian predator. — Anim. Behav. 82: 619-625.

  • RosellF.HoltanL.B.ThorsenJ.G. & HeggenesJ. (2013). Predator-naïve brown trout (Salmo trtutta) show antipredator behaviours to scent from an introduced piscivorous mammalian predator fed conspecifics. — Ethology 119: 303-308.

  • RundleS.D. & BrönmarkC. (2001). Inter- and intraspecific trait compensation of defence mechanisms in freshwater snails. — Proc. Roy. Soc. Lond. B: Biol. Sci. 268: 1463-1468.

  • SchererA.E. & SmeeD.L. (2016). A review of predator diet effects on prey defensive responses. — Chemoecology 26: 83-100.

  • SchoeppnerN.M. & RelyeaR.A. (2005). Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. — Ecol. Lett. 8: 505-512.

  • SchoeppnerN.M. & RelyeaR.A. (2009). Interpreting the smells of predation: how alarm cues and kairomones induce different prey defences. — Funct. Ecol. 23: 1114-1121.

  • SteinR.A. & MagnusonJ.J. (1976). Behavioral response of crayfish to a fish predator. — Ecology 57: 751-761.

  • StenzlerD. & AtemaJ. (1977). Alarm response of the marine mud snail, Nassarius obsoletus: specificity and behavioral priority. — J. Chem. Ecol. 3: 159-171.

  • SullivanA.M.PicardA.L. & MadisonD.M. (2005). To avoid or not to avoid? Factors influencing the discrimination of predator diet cues by a terrestrial salamander. — Anim. Behav. 69: 1425-1433.

  • TurnerA.M. & MontgomeryS.L. (2003). Spatial and temporal scales of predator avoidance: experiments with fish and snails. — Ecology 84: 616-622.

  • TurnerA.M. (2008). Predator diet and prey behaviour: freshwater snails discriminate among closely related prey in a predator’s diet. — Anim. Behav. 76: 1211-1217.

  • van OosterhoutF.GoitomE.RoessinkI. & LürlingM. (2014). Lanthanum from a modified clay used in eutrophication control is bioavailable to the marbled crayfish (Procambarus fallax f. virginalis). — PLoS ONE 9: e102410. DOI:10.1371/journal.pone.0102410.

  • WeissburgM. & BeauvaisJ. (2015). The smell of success: the amount of prey consumed by predators determines the strength and range of cascading non-consumptive effects. — PeerJ 3: e1426. DOI:10.7717/peerj.1426.

  • WeissburgM.J.FernerM.C.PisutD.P. & SmeeD.L. (2002). Ecological consequences of chemically mediated prey perception. — J. Chem. Ecol. 28: 1953-1970.

  • WeissburgM.SmeeD.L. & FernerM.C. (2014). The sensory of nonconsumptive predator effects. — Am. Nat. 184: 141-157.

  • WeissburgM.PoulinR.X. & KubanekJ. (2016). You are what you eat: a metabolomics approach to understanding prey responses to diet-dependent chemical cues by predators. — J. Chem. Ecol. 42: 1037-1046.

  • WernerE.E. & AnholtB.R. (1993). Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. — Am. Nat. 142: 242-272.

  • WilsonM.L.WebsterD.R. & WeissburgM.J. (2013). Spatial and temporal variation in the hydrodynamic landscape in intertidal salt marsh systems. — Limnol. Oceanogr. Fluids Environ. 3: 156-172.

  • WisendenB.D. (2000). Olfactory assessment of predation risk in the aquatic environment. — Phil. Trans. Roy. Soc. Lond B: Biol. Sci. 355: 1205-1208.

  • WitteF.GoldschmidtT.WaninkJ.van OijenM.GoudswaardK.Witte-MaasE. & BoutonN. (1992). The destruction of an endemic species flock: quantitative data on the decline of haplochromine cichlids of Lake Victoria. — Environ. Biol. Fish. 34: 1-28.

Figures

  • View in gallery

    Schematic of housing and feeding area for the fish while their odour was not being collected. Water that came from a nearby stream was pumped into the head tank, which then flowed into the troughs through the inflow tubes. Once the head tank troughs were filled to maximum capacity, water was released through the outflow tubes. The numbers and letters were used to identify each individual feeding section.

  • View in gallery

    Schematic of two-current choice flume arena (choice arena). The letters represent the following: (A) inflow tube; (B) baffle plate to decrease turbulence; (C) window screening; (D) honeycomb to ensure constant flow and prevent crayfish from escaping; (E) choice arena for the crayfish; (F) shelter; (G) window screening; (H) flume drains. Water flowed in the direction of A → H.

  • View in gallery

    Schematic of constant head tank which consisted of buckets and barrels to distribute the water to the choice arena. The letters represent the following: (A) y-valve to switch the side of the odour halfway through each trial; (B) submersible water pump to circulate the water. This is not drawn to scale for clarity purposes.

  • View in gallery

    Temporal sequence of odour presentations in choice arena.

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    Mean (± SEM) of amount of time (s) crayfish spent on the side of the choice arena containing fish odour as a function of species and diet. Open circles and dotted lines are for the cichlid odour donors and the black closed squares with solid lines are for the bass odour donors. Capital letters represent significant differences for comparison within a species and across diet and an asterisk represents a significant difference across species for the same diet. All statistical differences are determined using a Tukey-HSD.

  • View in gallery

    Mean (± SEM) of percent time crayfish spent in the shelter on the side with the fish odour as a function of species and diet. Open circles and dotted lines are for the cichlid odour donors and the black closed squares with solid lines are for the bass odour donors. Capital letters represent significant differences for comparison within a species and across diet and an asterisk represents a significant difference across species for the same diet. A and B are for comparisons with the bass treatments whereas W and X are comparisons within cichlid treatments. All statistical differences are determined using a Tukey-HSD.

  • View in gallery

    Mean (± SEM) of walking speed of crayfish on the odour side as a function of species and diet. Open circles and dotted lines are for the cichlid odour donors and the black closed squares with solid lines are for the bass odour donors. Capital letters represent significant differences for comparison within a species and across diet and an asterisk represents a significant difference across species for the same diet. All statistical differences are determined using a Tukey-HSD.

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