The alarm cue obstruction hypothesis: isopods respond to alarm cues, but do not respond to dietary chemical cues from predatory bluegill

in Behaviour
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Predator avoidance behaviours occur when prey detect a predator but the predator has not yet detected and identified prey. These defences are critical because they prevent predation at the earliest possible stages when prey have the best chance of escape. We tested for predator avoidance behaviours in an aquatic macroinvertebrate (Caecidotea intermedius; order Isopoda) in a series of three experiments. The first experiment attempted to determine if isopods possess alarm cues by exposing them to stimuli from macerated conspecifics. We then exposed isopods to kairomones from non-predatory tadpoles (Rana catesbiana) and predatory fish (Lepomis macrochirus) that had been fed a benign diet. Finally, we exposed isopods to kairomones of predatory fish that had been fed a diet exclusively of isopods. We found that isopods did not respond to any kairomone cues or dietary cues from any potential predator, but did reduce activity in response to alarm cues. These results suggest that isopods exhibit predator avoidance responses toward chemical cues in a limited setting (they do not respond unless the information suggests an attack has occurred in the immediate past) or that bluegill have the ability to modify or mask the alarm cues from their prey.



BrodieE.D.IIIBrodieE.D.Jr. (1999). Predator–prey arms races. — Bioscience 49: 557-568.

BrodieE.D.Jr.FormanowiczD.R.Jr.BrodieE.D.III (1991). Predator avoidance and antipredator mechanisms: distinct pathways to survival. — Ethol. Ecol. Evol. 3: 73-77.

BrownG.B.EisnerT.WhittakerA.C. (1970). Allomones and kairomones: transpecific chemical messengers. — Bioscience 20: 21-22.

BrownG.E. (2003). Learning about danger: chemical alarm cues and local risk assessment in prey fishes. — Fish Fish. 4: 227-234.

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

CrowlT.A.CovichA.P. (1990). Predator-induced life-history shifts in a freshwater snail. — Science 247: 949-951.

EndlerJ.A. (1986). Defense against predators. — In: Predator–prey relationships ( FederM.E.LauderG.V., eds). University of Chicago Press, Chicago, IL, p.  109-134.

FeminellaJ.W.HawkinsC.P. (1994). Tailed frog tadpoles differentially alter their feeding behavior in response to non-visual cues from four predators. — J. N. Am. Benthol. Soc. 13: 310-320.

FerrariM.C.O.MessierF.ChiversD.P. (2008). Degradation of chemical alarm cues under natural conditions: risk assessment by larval woodfrogs. — Chemoecology 17: 263-266.

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.

GracaM.A.S.MaltbyL.CalowP. (1993). Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus: feeding strategies. — Oecologia 93: 139-144.

HarrisS.GreenK.K.PetterssonL.B. (2013). Predator faunas past and present: quantifying the influence of waterborne cues in divergent ecotypes of the isopod Asellus aquaticus. — Oecologia 173: 791-799.

HolomuzkiJ.R.HatchettL.A. (1994). Predator avoidance costs and habituation to fish chemicals by a stream isopod. — Freshw. Biol. 32: 585-592.

HolomuzkiJ.R.ShortT.M. (1988). Habitat use and fish avoidance behaviors by the stream-dwelling isopod Lirceus fontinalis. — Oikos 52: 79-86.

HolomuzkiJ.R.ShortT.M. (1990). Ontogenetic shifts in habitat use and activity in a stream-dwelling isopod. — Ecography 13: 300-307.

HopkinsG.R.GallB.G.BrodieE.D.Jr. (2011). Ontogenetic shift in efficacy of antipredator mechanisms in a top aquatic predator, Anax junius (Odonata: Aeshnidae). — Ethology 117: 1093-1100.

HoweN.R.HarrisL.G. (1978). Transfer of the sea anemone pheromone, anthopleurine, by the nudibranch Aeolidia papillosa. — J. Chem. Ecol. 4: 551-561.

JacobsenH.P.StabellO.B. (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.

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

KeastA. (1970). Food specializations and bioenergetic interrelations in the fish faunas of some small ontario waterways. — In: Marine food chains ( SteeleJ.H., ed.). Oliver and Boyd, Edinburgh, p.  377-411.

KeefeM. (1992). Chemically mediated avoidance behavior in wild brook trout, salvelinus fontinalis: the response to familiar and unfamiliar predaceous fishes and the influence of fish diet. — Can. J. Zool. 70: 288-292.

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.

MathisA.SmithR.J.F. (1993). Chemical alarm signals increase the survival time of fathead minnows (Pimephales promelas) during encounters with northern pike (Esox lucius). — Behav. Ecol. 4: 260-265.

MirzaR.S.ChiversD.P. (2003). Fathead minnows learn to recognize heterospecific alarm cues they detect in the diet of a known predator. — Behaviour 140: 1359-1370.

MooreJ.W. (1975). The role of algae in the diet of Asellus aquaticus L. and Gammarus pulex L.J. Anim. Ecol. 44: 719-730.

RohrJ.R.MadisonD.M. (2001). A chemically mediated trade-off between predation risk and mate search in newts. — Anim. Behav. 62: 863-869.

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.

SchrammH.L.Jr.JirkaK.J. (1989). Epiphytic macroinvertebrates as a food resource for bluegills in Florida lakes. — Trans. Am. Fish. Soc. 118: 416-426.

ShortT.M.HolomuzkiJ.R. (1992). Indirect effects of fish on foraging behaviour and leaf processing by the isopod Lirceus fontinalis. — Freshw. Biol. 27: 91-97.

SmithR.J.F. (1977). Chemical communication as adaptation: alarm substance of fish. — In: Chemical signals in vertebrates. Springer, Berlin, p.  303-320.

SmithR.J.F. (1992). Alarm signals in fishes. — Rev. Fish Biol. Fish. 2: 33-63.

SutrisnoR.SchotteP.M.WisendenB.D. (2014). Chemical arms race between predator and prey: a test of predator digestive countermeasures against chemical labeling by dietary cues of prey. — J. Freshw. Ecol. 29: 17-23.

VollmerK.L.GallB.G. (2014). Complex predator–prey interactions between the rusty crayfish (Orconectes rusticus) and invertebrate and vertebrate prey within their native range. — J. Freshw. Ecol. 29: 1-11.

WilsonD.J.LefcortH. (1993). The effect of predator diet on the alarm response of red-legged frog, Rana aurora, tadpoles. — Anim. Behav. 46: 1017-1019.

WisendenB.D.ClineA.SparkesT.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.

WisendenB.D.RuggM.L.KorpiN.L.FuselierL.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.

WoosterD.SihA. (1995). A review of the drift and activity responses of stream prey to predator presence. — Oikos 73: 3-8.


  • The mean (±SE) difference in the number of lines crossed between pre-stimulus and post-stimulus periods when isopods were exposed to either a blank control or alarm cues from macerated conspecifics. Isopods significantly decreased movement when exposed to alarm cues (t-test, t=3.84, N=40, p<0.001).

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  • The mean (±SE) difference in the number of lines crossed between pre-stimulus and post-stimulus periods when isopods were exposed to either a blank control, nonpredatory tadpole kairomones, or predatory fish kairomones. Tadpoles and fish were maintained on a nonisopod diet. Isopods did not significantly change behaviour when exposed to any treatment (one-way ANOVA, F2,73=1.41, p=0.25).

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  • The mean (±SE) difference in the number of lines crossed between pre-stimulus and post-stimulus periods when isopods were exposed to either a blank control or cues from fish that had been wax worms or isopods. Isopods did not change behaviour when exposed to any treatment (one-way ANOVA, F2,94=0.063, p=0.94).

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