Testing the predation stress hypothesis: behavioural and hormonal responses to predator cues in Allegheny Mountain dusky salamanders

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?


The predation stress hypothesis posits that exposure to predators and/or predator cues causes release of glucocorticoid hormones which coordinate behavioural responses that facilitate predator avoidance. We measured responses to short-term and repeated exposure to predator-derived kairomones in Allegheny Mountain dusky salamanders (Desmognathus ochrophaeus). Salamanders expressed predator avoidance behaviours (reduced locomotion, reduced mating behaviour) in the presence of predator kairomones. However, plasma glucocorticoids after short-term exposure to predator kairomones were similar to levels after exposure to controls. After repeated exposure to predator-derived kairomones, locomotory activity and plasma glucocorticoids were similar compared to controls. There was no evidence of habituation to predator kairomones. Overall, results did not support the predation stress hypothesis in Allegheny Mountain dusky salamanders in either an acute or chronic context. Use of glucocorticoids to mediate antipredator responses may occur when predation pressure is unpredictable, and when energetic and opportunity costs of linking glucocorticoids to anti-predator responses are low.



AmaralV.C.Santos GomesK.Nunes-de-SouzaR.L. (2010). Increased corticosterone levels in mice subjected to the rat exposure test. — Horm. Behav. 57: 128-133.

BeldenL.K. (2005). Corticosterone and growth in pacific treefrog (Hyla regilla) tadpoles. — Copeia 2005: 424-430.

BlileyJ.M.WoodleyS.K. (2012). The effects of repeated handling and treatment with corticosterone on behavior in an amphibian (Ocoee salamander: Desmognathus ocoee). — Physiol. Behav. 105: 1132-1139.

BoonstraR.HikD.SingletonG.R.TinnikovA. (1998). The impact of predator-induced stress on the snowshoe hare cycle. — Ecol. Monogr. 79: 371-394.

CanoineV.HaydenT.-J.RoweK.GoymannW. (2002). The stress response of european stonechats depends on the type of stressor. — Behaviour 139: 1303-1311.

ClinchyM.SchulkinJ.ZanetteL.Y.SheriffM.J.McGowanP.O.BoonstraR. (2010). The neurological ecology of fear: insights neuroscientists and ecologists have to offer one another. — Front. Behav. Neurosci. 4: 21.

ClinchyM.ZanetteL.BoonstraR.WingfieldJ.C.SmithJ.N. (2004). Balancing food and predator pressure induces chronic stress in songbirds. — Proc. Roy. Soc. Lond. B: Biol. Sci. 271: 2473-2479.

CockremJ.F.SilverinB. (2002). Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). — Gen. Comp. Endocrinol. 125: 248-255.

CreelS.ChristiansonD.LileyS.WinnieJ.A.Jr. (2007). Predation risk affects reproductive physiology and demography of elk. — Science 315: 960.

CreelS.WinnieJ.A.Jr.ChristiansonD. (2009). Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. — Proc. Natl. Acad. Sci. USA 106: 12388-12393.

DahlE.OrizaolaG.WinbergS.LaurilaA. (2012). Geographic variation in corticosterone response to chronic predator stress in tadpoles. — J. Evol. Biol. 25: 1066-1076.

DavisD.R.GaborC.R. (2015). Behavioral and physiological antipredator responses of the San Marcos salamander, Eurycea nana. — Physiol. Behav. 139: 145-149.

DurantS.E.RomeroL.M.TalentL.G.HopkinsW.A. (2008). Effect of exogenous corticosterone on respiration in a reptile. — Gen. Comp. Endocrinol. 156: 126-133.

EppK.GaborC.R. (2008). Innate and learned predator recognition mediated by chemical signals in Eurycea nana. — Ethology 114: 607-615.

FederM.E. (1983). Integrating the ecology and physiology of plethodontid salamanders. — Herpetelogica 39: 291-310.

FischerE.K.HarrisR.M.HofmannH.A.HokeK.L. (2014). Predator exposure alters stress physiology in guppies across timescales. — Horm. Behav. 65: 165-172.

FormanowiczD.Jr.BrodieE.D.Jr. (1993). Size-mediated predation pressure in a salamander community. — Herpetologica 49: 265-270.

GlennemeierK.A.DenverR.J. (2002). Small changes in whole-body corticosterone content affect larval Rana pipiens fitness components. — Gen. Comp. Endocrinol. 127: 16-25.

GruenewaldD.A.HessD.L.WilkinsonC.W.MatusumatoA.M. (1992). Excessive testicular progesterone secretion in age male Fischer 344 rats: a potential casue of age-related gonadotropin suppression and counfounding variable in aging studies. — J. Gerontol. 42: B164-B170.

HairstonN.G. (1986). Species packing in Desmognathus salamanders: experimental demonstration of predation and competition. — Am. Nat. 127: 266-291.

HayesT.ChanR.LichtP. (1993). Interactions of temperature and steroids on larval growth, development, and metamorphosis in a toad (Bufo boreas). — J. Exp. Zool. 266: 206-215.

JohnsonE.C.SullivanA.M. (2014). Antipredator behavior in Desmognathus ochrophaeus: threat-specific responses to chemical stimuli in a foraging context. — Ethology 120: 672-680.

KagawaN.MugiyaY. (2000). Exposure of goldfish (Carassius auratus) to bluegills (Lepomis macrochirus) enhances expression of stress protein 70 mRNA in the brains and increases plasma cortisol levels. — Zool. Sci. 17: 1061-1066.

KalynchukL.E.GregusA.BoudreauD.Perrot-SinalT.S. (2004). Corticosterone increases depression-like behavior, with some effects on predator odor-induced defensive behavior, in male and female rats. — Behav. Neurosci. 118: 1365-1377.

LimaS.L. (1998). Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. — Adv. Stud. Behav. 27: 215-290.

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

MateoJ.M. (2007). Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi). — Behav. Ecol. Sociobiol. 62: 37-49.

McCollumS.A.LeimbergerJ.D. (1997). Predator-induced morphological changes in an amphibian: predation by dragonfiles affects tadpole shape and color. — Oecologia 109: 615-621.

MonclusR.PalomaresF.TabladoZ.Martinez-FonturbelA.PalmeR. (2009). Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. — Oecologia 158: 615-623.

MullerC.Jenni-EiermannS.BlondelJ.PerretP.CaroS.P.LambrechtsM.JenniL. (2006). Effect of human presence and handling on circulating corticosterone levels in breeding blue tits (Parus caeruleus). — Gen. Comp. Endocrinol. 148: 163-171.

NarayanE.J.CockremJ.F.HeroJ.M. (2013). Sight of a predator induces a corticosterone stress response and generates fear in an amphibian. — PLoS One 8: e73564.

NewmanA.E.ZanetteL.Y.ClinchyM.GoodenoughN.SomaK.K. (2013). Stress in the wild: chronic predator pressure and acute restraint affect plasma DHEA and corticosterone levels in a songbird. — Stress 16: 363-367.

PetrankaJ.W. (2010). Salamanders of the United States and Canada. — Smithsonian Institute, Washington, DC.

PreestM.R.CreeA. (2008). Corticosterone treatment has subtle effects on thermoregulatory behavior and raises metabolic rate in the New Zealand common gecko, Hoplodactylus maculatus. — Physiol. Biochem. Zool. 81: 641-650.

RaderschallC.A.MagrathR.D.HemmiJ.M. (2011). Habituation under natural conditions: model predators are distinguished by approach direction. — J. Exp. Biol. 214: 4209-4216.

ReeveB.C.CrespiE.J.WhippsC.M.BrunnerJ.L. (2013). Natural stressors and ranavirus susceptibility in larval wood frogs (Rana sylvatica). — Ecohealth 10: 190-200.

RelyeaR.A.EdwardsK. (2010). What doesn’t kill you makes you sluggish: how sublethal pesticides alter predator–prey interactions. — Copeia: 558-567.

Remage-HealeyL.NowacekD.P.BassA.H. (2006). Dolphin foraging sounds suppress calling and elevate stress hormone levels in a prey species, the Gulf toadfish. — J. Exp. Biol. 209: 4444-4451.

ReskoJ.A.EllinwoodW.E.PasztorL.M.BuhlA.E. (1980). Sex steroids in the umbilical circulation of fetal rhesus monkeys from the time of gonadal differentiation. — J. Clin. Endocrinol. Metab. 50: 900-905.

RicciardellaL.F. (2008). Acidification and stress physiology in a plethodontid salamander, Desmognathus ochrophaeus. — Unpublished M.S., Duquesne University, Pittsburgh, PA.

RicciardellaL.F.BlileyJ.M.FethC.C.WoodleyS.K. (2010). Acute stressors increase plasma corticosterone and decrease activity in a terrestrial salamander (Desmognathus ochrophaeus). — Physiol. Behav. 101: 81-86.

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

RomeroL.M. (2002). Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. — Gen. Comp. Endocrinol. 128: 1-24.

SapolskyR.M. (2002). Endocrinology of the stress response. — In: Behavioral endocrinology ( BeckerJ.B.BreedloveS.M.CrewsD.McCarthyM.M., eds). MIT Press, Cambridge, MA, p.  409-450.

ScheuerleinA.van ’t HofT.J.GwinnerE. (2001). Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris). — Proc. Roy. Soc. Lond. B: Biol. Sci. 268: 1575-1582.

SheriffM.J.KrebsC.J.BoonstraR. (2009). The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. — J. Anim. Ecol. 78: 1249-1258.

ThakerM.LimaS.L.HewsD.K. (2009a). Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs. — Horm. Behav. 56: 51-57.

ThakerM.LimaS.L.HewsD.K. (2009b). Alternative antipredator tactics in tree lizard morphs: hormonal and behavioural responses to a predator encounter. — Anim. Behav. 77: 395-401.

TrompeterW.P.LangkildeT. (2011). Invader danger: lizards faced with novel predators exhibit an altered behavioral response to stress. — Horm. Behav. 60: 152-158.

WackC.L.LovernM.B.WoodleyS.K. (2010). Transdermal delivery of corticosterone in terrestrial amphibians. — Gen. Comp. Endocrinol. 169: 269-275.

WackC.L.DuRantS.E.HopkinsC.D.LovernM.B.FeldhoffR.C.WoodleyS.K. (2012). Elevation of plasma corticosterone increases metabolic rate in a terrestrial salamander. — Comp. Biochem. Physiol. A 161: 153-158.

WellsK.D. (2007). Ecology and behavior of amphibians. — The University of Chicago Press, Chicago, IL.

WoodleyC.M.PetersonM.S. (2003). Measuring responses to simulated predation threat using behavioral and physiological metrics: the role of aquatic vegetation. — Oecologia 136: 155-160.

WoodleyS.K.FreemanP.E.RicciardellaL.F. (2014). Environmental acidification is not associated with altered plasma corticosterone levels in the stream-side salamander, Desmognathus ochrophaeus. — Gen. Comp. Endocrinol. 201: 8-15.


  • Activity of male and female Allegheny Mountain dusky salamanders tested in the presence of non-predator kairomones or predator kairomones for 1 h. An asterisk indicates that predator kairomone exposure significantly decreased activity levels in both males and females, p=0.002.

    View in gallery
  • Plasma CORT levels of male and female Allegheny Mountain dusky salamanders exposed for 45 min to either non-predator kairomones or predator kairomones. No significant difference in CORT levels between the two treatments was present. Sample sizes are indicated within bars.

    View in gallery
  • Plasma CORT levels of male Allegheny Mountain dusky salamanders exposed to either non-predator kairomones or predator kairomones for either 30 min or 3 h. No significant differences in CORT levels among the treatments were present. Sample sizes are indicated within bars.

    View in gallery
  • Activity of male and female Allegheny Mountain dusky salamanders after prolonged exposure to predator kairomones. Subjects were either left undisturbed (no treatment) or were exposed to non-predator kairomones or predator kairomones every day for at least 10 days. Then, activity was measured in the presence of predator kairomones or non-predator kairomones. Although there was no significant effect of prior, prolonged treatment on activity, activity was reduced when tested in the presence of predator rinses compared to non-predator rinses (p=0.001).

    View in gallery
  • Plasma CORT levels of male and female Allegheny Mountain dusky salamanders after prolonged exposure to predator kairomones. Sample sizes are within bars. Subjects were either left undisturbed (no treatment) or were exposed to either non-predator kairomones or predator kairomones every day for at least 10 days. On the final day, subjects were exposed to either non-predator kairomones or predator kairomones and blood was collected 45 min later. There was no effect of prior, prolonged treatment on CORT levels, nor was there an effect of the short-term, acute exposure to predator kairomones compared to non-predator kairomones.

    View in gallery


Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 5 5 2
Full Text Views 4 4 4
PDF Downloads 0 0 0
EPUB Downloads 0 0 0