Abstract
Numerous studies have examined how predator diets influence prey responses to predation risk, but the role predator diet plays in modulating prey responses remains equivocal. We reviewed 405 predator–prey studies in 109 published articles that investigated changes in prey responses when predators consumed different prey items. In 54 % of reviewed studies, prey responses were influenced by predator diet. The value of responding based on a predator’s recent diet increased when predators specialized more strongly on particular prey species, which may create patterns in diet cue use among prey depending upon whether they are preyed upon by generalist or specialist predators. Further, prey can alleviate costs or accrue greater benefits using diet cues as secondary sources of information to fine tune responses to predators and to learn novel risk cues from exotic predators or alarm cues from sympatric prey species. However, the ability to draw broad conclusions regarding use of predator diet cues by prey was limited by a lack of research identifying molecular structures of the chemicals that mediate these interactions. Conclusions are also limited by a narrow research focus. Seventy percent of reviewed studies were performed in freshwater systems, with a limited range of model predator–prey systems, and 98 % of reviewed studies were performed in laboratory settings. Besides identifying the molecules prey use to detect predators, future studies should strive to manipulate different aspects of prey responses to predator diet across a broader range of predator–prey species, particularly in marine and terrestrial systems, and to expand studies into the field.
Similar content being viewed by others
References
Alexander GJ (1996) Thermal physiology of Hemachatus haemachatus and its implications to range limitation. PhD thesis, University of the Witwatersrand, Johannesburg, South Africa
Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci 95:8113–8118
Batabyal A, Gosavi S, Gramapurohit N (2014) Determining sensitive stages for learning to detect predators in larval bronzed frogs: importance of alarm cues in learning. J Biosci 39:701–710
Belden LK, Wildy EL, Hatch AC, Blaustein AR (2000) Juvenile western toads, Bufo boreas, avoid chemical cues of snakes fed juvenile, but not larval, conspecifics. Anim Behav 59:871–875
Bell RD, Rypstra AL, Persons MH (2006) The effect of predator hunger on chemically mediated antipredator responses and survival in the wolf spider Pardosa milvina (Araneae: Lycosidae). Ethology 112:903–910
Bourdeau PE (2010a) An inducible morphological defence is a passive by-product of behaviour in a marine snail. Proc R Soc 277:455–462
Bourdeau PE (2010b) Cue reliability, risk sensitivity and inducible morphological defense in a marine snail. Oecologia 162:987–994
Brodin T, Mikolajewski DJ, Johansson F (2006) Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae. Oecologia 148:162–169
Bronmark C, Pettersson LB (1994) Chemical cues from piscivores induce a change in morphology in crucial carp. Oikos 70:396–402
Brooker RM, Munday PL, Chivers DP, Jones GP (2015) You are what you eat: diet-induced chemical crypsis in a coral-feeding reef fish. Proc R Soc B 282:20141887
Brown GE, Cowan J (2000) Foraging trade-offs and predator inspection in an ostariophysan fish: switching from chemical to visual cues. Behaviour 137:181–195
Brown GE, Godin J (1999) Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish. Anim Behav 57:475–481
Brown GE, Schwarzbauer EM (2001) Chemical predator inspection and attack cone avoidance in a characin fish: the effects of predator diet. Behaviour 138:727–739
Brown GE, Smith RJF (1996) Foraging trade-offs in fathead minnows (Pimephales promelas, Osteichthyes, Cyprinidae): acquired predator recognition in the absence of an alarm response. Ethology 102:776–785
Brown GE, Zachar MM (2002) Chemical predator inspection in a characin fish (Hemigrammus erythrozonus, Characidae, Ostariophysi): the effects of mixed predator diets. Ethology 108:451–461
Brown GE, Chivers DP, Smith RJF (1995) Localized defecation by pike: a response to labelling by cyprinid alarm pheromone? Behav Ecol Sociobiol 36:105–110
Brown GE, Chivers DP, Smith RJF (1996) Effects of diet on localized defecation by northern pike, Esox lucius. J Chem Ecol 22:467–475
Brown GE, Adrian JC, Smyth E, Leet H, Brennan S (2000a) Ostariophysan alam pheromones: laboratory and field tests of the functional significance of nitrogen oxides. J Chem Ecol 26:139–154
Brown GE, Paige J, Godin J (2000b) Chemically mediated predator inspection behaviour in the absence of predator visual cues by a characin fish. Anim Behav 60:315–321
Brown GE, Golub JL, Plata DL (2001) Attack cone avoidance during predator inspection visits by wild finescale dace (Phoxinus neogaeus): the effects of predator diet. J Chem Ecol 27:1657–1666
Brown GE, Adrian JC, Naderi NT, Harvey MC, Kelly JM (2003) Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: conservation of the ostariophysan alarm pheromone. J Chem Ecol 29:1781–1796
Brown GE, Foam PE, Cowell HE, Fiore PG, Chivers DP (2004) Production of chemical alarm cues in convict cichlids: the effects of diet, body condition and ontogeny. Ann Zool Fenn 41:487–499
Brown GE, Ferrari MCO, Elvidge CK, Ramnarine I, Chivers DP (2013) Phenotypically plactic neophobia: a response to variable predation risk. Proc R Soc A 280:20122712
Bryan JE, Larkin PA (1972) Food specialization by individual trout. J Fish Res Board Can 29:1615–1624
Cai F, Wu Z, He N, Wang Z, Huang C (2011) Can native species crucian carp Carassius auratus recognizes the introduced red swamp crayfish Procambarus clarkii? Curr Zool 57:330–339
Chivers DP, Mirza RS (2001) Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. Chem Signals Vertebr 9:277–284
Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:338–352
Chivers DP, Brown GE, Smith JF (1995) Acquired recognition of chemical stimuli from Pike, Esox lucius, by Brook Sticklebacks, Culaea inconstans (Osteichthyes, Gasterosteidae). Ethology 99:234–242
Chivers DP, Wisenden BD, Smith RJF (1996) Damselfly larvae learn to recognize predators from chemical cues in the predator’s diet. Anim Behav 52:315–320
Chivers DP, Wildy EL, Blaustein AR (1997) Eastern long-toed salamander (Ambystoma macrodactylum colurnbianum) larvae recognize cannibalistic conspecifics. Ethology 103:187–197
Chivers DP, Mirza RS, Johnston JG (2002) Learned recognition of heterospecific alarm cues enhances survival during encounters with predators. Behaviour 139:929–938
Chivers DP, Zhao X, Ferrari MCO (2007) Linking morphological and behavioural defences: prey fish detect the morphology of conspecifics in the odour signature of their predators. Ethology 113:733–739
Covich AP, Crowl TA (1990) Predator-induced life history shifts in a fresh-water snail. Science 246:949–951
Crawford BA, Hickman CR, Luhring TM (2012) Testing the threat-sensitive hypothesis with predator familiarity and dietary specificity. Ethology 118:41–48
Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205:489–511
Dixson DL, Pratchett MS, Munday PL (2012) Reef fishes innately distinguish predators based on olfactory cues associated with recent prey items rather than individual species. Anim Behav 84:45–51
Ferrari MCO, Brown MR, Pollock MS, Chivers DP (2007) The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators. Chemoecology 17:157–161
Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724
Flynn AM, Smee DL (2010) Behavioral plasticity of the soft-shell clam, Mya arenaria (L.), in the presence of predators increases survival in the field. J Exp Mar Biol Ecol 383:32–38
Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466–467
Fraser DF, Gilliam JF (1992) Nonlethal impacts of predator invasion: facultative suppression of growth and reproduction. Ecology 3:959–970
Greene HW (1997) Snakes. The evolution of mystery in nature. University of California Press, Berkeley
Griffiths CL, Richardson CA (2006) Chemically induced predator avoidance behaviour in the burrowing bivalve Macoma balthica. J Exp Mar Biol Ecol 331:91–98
Grostal P, Dicke M (2000) Recognising one’s enemies: a functional approach to risk assessment by prey. Behav Ecol Sociobiol 47:258–264
Hay ME (2009) Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Ann Rev Mar Sci 1:193–212
Hettyey A, Zsarnoczai S, Vincze K, Hoi H, Laurila A (2010) Interactions between the information content of different chemical cues affect induced defences in tadpoles. Oikos 119:1814–1822
Hews DK (1988) Alarm response in larval western toads, Bufo boreas: release of larval chemicals by a natural predator and its effects on predator capture efficiency. Anim Behav 36:125–133
Hirvonen H, Ranta E, Piironen J, Laurila A, Peuhkuri N (2000) Behavioural responses of naïve Arctic charr young to chemical cues from salmonid and non-salmonid fish. Oikos 88:191–199
Hoefler CD, Durso LC, McIntyre KD (2012) Chemical-mediated predator avoidance in the European house cricket (Acheta domesticus) is modulated by predator diet. Ethology 118:431–437
Howe NR, Harris LG (1978) Transfer of the sea anemone pheromone, Anthopleurine, by the nudibranch Aeolidia papillosa. J Chem Ecol 4:551–561
Huryn AD, Chivers DP (1999) Contrasting behvaioral responses by detritivorous and predatory mayflies to chemicals released by injured conspecifics and their predators. J Chem Ecol 25:2729–2740
Jachner A (1997) The response of bleak to predator odour of unfed and recently fed pike. J Fish Biol 50:878–886
Jackson RR, Li D (2004) One-encounter search-image formation by araneophagic spiders. Anim Cogn 7:247–254
Jacobsen HP, Stabell OB (1999) Predator-induced alarm responses in the common periwinkle, Littorina littorea: dependence on season, light conditions, and chemical labelling of predators. Mar Biol 134:551–557
Jacobsen HP, Stabell OB (2004) Antipredator behaviour mediated by chemical cues: the role of conspecific alarm signalling and predator labelling in the avoidance response of a marine gastropod. Oikos 104:43–50
Jones HM, Paszkowski CA (1997) Effects of exposure to predatory cues on territorial behaviour of male fathead minnows. Environ Biol Fishes 49:97–109
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394
Kesavaraju B, Juliano SA (2010) Nature of predation risk cues in container systems: mosquito responses to solid residues from predation. Entomol Soc Am 103:1038–1045
Kiesecker JM, Chivers DP, Anderson M, Blaustein AR (2002) Effect of predator diet on life history shifts of red-legged frogs, Rana aurora. J Chem Ecol 28:1007–1015
Large SI, Smee DL (2010) Type and nature of cues used by Nucella lapillus to evaluate predation risk. J Exp Mar Biol Ecol 396:10–17
Large SI, Smee DL (2012) Biogeographic variation in behavioral and morphological responses to predation risk. Oecologia. doi:10.1007/s00442-012-2450-5
Large S, Smee D, Trussell G (2011) Environmental conditions influence the frequency of prey responses to predation risk. Mar Ecol Prog Ser 422:41–49
Large SI, Torres P, Smee DL (2012) Behavior and morphology of Nucella lapillus influenced by predator type and predator diet. Aquat Biol 16:189–196
Laurila A, Kujasalo J, Ranta E (1997) Different antipredator behavior in two anuran tadpoles: effects of predator diet. Behav Ecol Sociobiol 40:329–336
Laurila A, Kujasalo J, Ranta E (1998) Predator-induced changes in life history in two anuran tadpoles: effects of predator diet. Oikos 83:307–317
Levri EP (1998) Perceived predation risk, parasitism, and the foraging behavior of a freshwater snail (Potamopyrgus antipodarum). Can J Zool 76:1878–1884
Li D, Jackson RR (2005) Influence of diet-related chemical cues from predators on the hatching of egg-carrying spiders. J Chem Ecol 31:333–342
Licht T (1989) Discriminating between hungry and satiated predators: the response of guppies (Poecilia reticulata) from high and low predation sites. Ethology 82:238–243
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Madison DM, Maerz JC, McDarby JH (1999) Optimization of predator avoidance by salamanders using chemical cues: diet and diel effects. Ethology 105:1073–1086
Madison DM, Sullivan AM, Maerz JC, McDarby JH, Rohr JR (2002) A complex, cross-taxon, chemical releaser of antipredator behavior in amphibians. J Chem Ecol 28:2271–2282
Magalhaes S, Tudorache C, van Maanen R, Sabelis MW, Janssen A (2004) Diet of intraguild predators affects antipredator behavior in intraguild prey. Behav Ecol 16:364–370
Magurran A (1989) Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology 82:216–223
Manek AK, Ferrari MCO, Niyogi S, Chivers DP (2014) The interactive effects of multiple stressors on physiological stress responses and club cell investment in fathead minnows. Sci Total Environ 476–477:90–97
Marquis O, Saglio P, Neveu A (2004) Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. Arch Fur Hydrobiol 160:153–170
Mathis A, Smith RJF (1993) Chemical labeling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas). J Chem Ecol 19:1967–1979
Mathis A, Unger S (2012) Learning to avoid dangerous habitat types by aquatic salamanders, Eurycea tynerensis. Ethology 118:57–62
Mathis A, Chivers DP, Smith RJF (1993) Population differences in responses of fathead minnows (Pimephales promelas) to visual and chemical stimuli from predators. Ethology 93:31–40
Melcer T, Chiszar D (1989) Striking prey creates a specific chemical search image in rattlesnakes. Anim Behav 37:477–486
Meng R, Janssen A, Nomikou M, Zhang QW, Sabelis MW (2006) Previous and present diets of mite predators affect antipredator behaviour of whitefly prey. Exp Appl Acarol 38:113–124
Mirza RS, Chivers DP (2001a) Do juvenile yellow perch use diet cues to assess the level of threat posed by intraspecific predators? Behaviour 138:1249–1258
Mirza RS, Chivers DP (2001b) Learned recognition of heterospecific alarm signals: the importance of a mixed predator diet. Ethology 107:1007–1018
Mirza RS, Chivers DP (2003) Predator diet cues and the assessment of predation risk by juvenile brook charr: do diet cues enhance survival? Can J Zool 81:126–132
Mogali SM, Saidapur SK, Shanbhag BA (2012) Tadpoles of the bronze frog (Rana temporalis) assess predation risk before evoking antipredator defense behavior. Ethology 30:379–386
Morishita VR, Barreto R (2011) Black sea urchins evaluate predation risk using chemical signals from a predator and injured con- and heterospecific prey. Mar Ecol Prog Ser 435:173–181
Mortensen L, Richardson JML (2008) Effects of chemical cues on foraging in damselfly larvae, Enallagma antennatum. J Insect Behav 21:285–295
Munoz NE, Blumstein DT (2012) Multisensory perception in uncertain environments. Behav Ecol 23:457–462
Murray DL, Jenkins CL (1999) Perceived predation risk as a function of predator dietary cues in terrestrial salamanders. Anim Behav 57:33–39
Nolte DL, Mason JR, Epple G, Aronov E, Campbell DL (1994) Why are predator urines aversive to prey? J Chem Ecol 20:1505–1516
Nunes AL, Richter-Boix A, Laurila A (2013) Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study. Oecologia 171:115–127
Osburn DJ, Cramer MJ (2013) Foraging response of Erethizon drosatum and Lepus americanus to specialized and generalized predator scents. Am Midl Nat 169:66–73
Persons MH, Rypstra AL (2000) Preference for chemical cues associated with recent prey in the wolf spider Hogna helluo (Araneae: Lycosidae). Ethology 106:27–35
Persons MH, Walker SE, Rypstra AL, Marshall SD (2001) Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae). Anim Behav 61:43–51
Pillay N, Alexander GJ, Lazenby SL (2003) Responses of striped mice, Rhabdomys pumilio, to faeces of a predatory snake. Behaviour 140:125–135
Preisser EL, Bolnick DI, Benard ME (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509
Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter nonconsumptive effects in predator–prey interactions. Ecology 88:2744–2751
Relyea RA (2000) Trait-mediated indirect effects in larval anurans: reversing competition with the threat of predation. Ecology 81:2278–2289
Relyea RA (2002) Costs of phenotypic plasticity. Am Nat 159:272–282
Roberts LJ, de Leaniz CG (2011) Something smells fishy: predator-naïve salmon use diet cues, not kairomones, to recognize a sympatric mammalian predator. Anim Behav 82:619–625
Rosell F, Holtan LB, Thorsen JG, Heggenes J (2013) Predator-naïve brown trout (Salmo trutta) show antipredator behaviours to scent from an introduced piscivorous mammalian predator fed conspecifics. Ethology 119:303–308
Saglio P, Mandrillon AL (2006) Embryonic experience to predation risk affects tadpoles of the common frog (Rana temporaria). Arch Fur Hydrobiol 166:505–523
Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512
Schoeppner NM, Relyea RA (2009) When should prey respond to consumed heterospecifics? Testing hypotheses of perceived risk. Copeia 2009:190–194
Shin PKS, Yang FY, Chiu MY, Cheung SG (2009) Cues from the predator crab Thalamita danae fed different prey can affect scope for growth in the prey mussel Perna viridis. Mar Freshw Behav Physiol 42:343–355
Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210:1041–1043
Sih A (1984) The behavioral response race between predator and prey. Am Nat 123:143–150
Smee DL, Weissburg MJ (2006a) Hard clams (Mercenaria mercenaria) evaluate predation risk using chemical signals from predators and injured conspecifics. J Chem Ecol 32:605–619
Smee DL, Weissburg MJ (2006b) Clamming up: environmental forces diminish the perceptive ability of bivalve prey. Ecology 87:1587–1598
Stabell OB, Lwin MS (1997) Predator-induced phenotypic changes in crucian carp are caused by chemical signals from conspecifics. Environ Biol Fishes 49:145–149
Stabell OB, Ogbebo F, Primicerio R (2003) Inducible defences in Daphnia depend on latent alarm signals from conspecific prey activated in predators. Chem Senses 28:141–153
Storm JJ, Lima SL (2008) Predator-naive fall field crickets respond to the chemical cues of wolf spiders. Can J Zool 1263:1259–1263
Sullivan AM, Madison DM, Rohr JR (2004) Variation in the antipredator responses of three sympatric Plethodontid salamanders to predator-diet cues. Herpetologica 60:401–408
Sullivan AM, Picard AL, Madison DM (2005) To avoid or not to avoid? Factors influencing the discrimination of predator diet cues by a terrestrial salamander. Anim Behav 69:1425–1433
Sundermann D, Scheumann M, Zimmermann E (2008) Olfactory predator recognition in predator-naive gray mouse lemurs (Micrcebus murinus). J Comp Psychol 122:146–155
Turner GF, Pitcher TJ (1986) Attack abatement: a model for group protection by combined avoidance and dilution. Am Nat 128:228–240
van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585
Vilhuen S, Hirvonen H (2003) Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet. Behav Ecol Sociobiol 55:1–10
Weissburg MJ, Ferner MC, Pisut DP, Smee DL (2002) Ecological consequences of chemically mediated prey perception. J Chem Ecol 28:1953–1970
Weissburg M, Smee DL, Ferner MC (2014) The sensory ecology of nonconsumptive predator effects. Am Nat 184:141–157
Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363
Wildy EL, Blaustein AR (2001) Learned recognition of intraspecific predators in larval long-toed salamanders Ambystoma macrodactylum. Ethology 107:479–493
Wildy EL, Chivers DP, Blaustein AR (1999) Shifts in life-history traits as a response to cannibalism in larval long-toed salamanders (Ambystoma macrodactylum). J Chem Ecol 25:2337–2346
Yamada SB, Navarrete SA, Needham C (1998) Predation induced changes in behavior and growth rate in three populations of the intertidal snail, Littorina sitkana (Philippi). J Exp Mar Biol Ecol 220:213–226
Zhao X, Ferrari MCO, Chivers DP (2006) Threat-sensitive learning of predator odours by a prey fish. Behaviour 143:1103–1121
Acknowledgments
Funding for this work was provided by NSF-MSP ETEAMS Grant #1321319, a TAMU-CC Faculty Enhancement Grant, and the Ruth A. Campbell Professorship to D.L.S. M. Weissburg’s thoughtful comments greatly improved the article.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Michael Heethoff.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Scherer, A.E., Smee, D.L. A review of predator diet effects on prey defensive responses. Chemoecology 26, 83–100 (2016). https://doi.org/10.1007/s00049-016-0208-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-016-0208-y