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The ethological relevance of predator odors to induce changes in prey species

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Abstract

Predator odors are non-intrusive naturalistic stressors of high ethological relevance. Prey species show specific adaptations that allow recognition, avoidance, and defense against predators. For many mammalian species, this includes sensitivity towards predator-derived odors. The typical sources of such odors include predator skin and fur, urine, feces, and anal gland secretions. Avoidance of predator odors has been observed in many mammalian prey species including rats, mice, and voles. Field and laboratory studies show that predator odors have distinctive behavioral effects which include (1) inhibition of or decreased activity; (2) suppression of non-defensive behaviors such as foraging, feeding, and grooming; and (3) shifts to safe habitats or secured locations where such odors are not present. Chronic exposure to predator odor may elicit one of two controversial processes: sensitization and habituation. Some studies have suggested that chronic exposure to predator odors may induce behavioral sensitization while others stated little or even no habituation at all. Finally, prey species respond variably to different degrees of threats, and the odor intensity is a key factor to determine the “optimal” behavioral response. Future research should aim at linking behavioral and neuroendocrine changes for a better understanding of predator–prey interactions.

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References

  • Aaron J, Wirsing KE, Cameron MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79(3):531–537

    Article  Google Scholar 

  • Adamec R, Blundell J, Burton P (2005) Role of NMDA receptors in the lateralized potentiation of amygdala afferent and efferent neural transmission produced by predator stress. Physiol Behav 86(1–2):75–91. doi:10.1016/j.physbeh.2005.06.026

    Article  CAS  PubMed  Google Scholar 

  • Agren G, Zhou Q, Zhong W (1989) Ecology and social behaviour of Mongolian gerbils, Meriones unguiculatus, at Xilin hot, inner Mongolia, China. Anim Behav 37:11–27

    Article  Google Scholar 

  • Apfelbach R, Blanchard DC, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29(8):1123–1144. doi:10.1016/j.neubiorev.2005.05.005

    Article  PubMed  Google Scholar 

  • Beijamini V, Guimaraes FS (2006) c-Fos expression increase in NADPH-diaphorase positive neurons after exposure to a live cat. Behav Brain Res 170(1):52–61

    Article  CAS  PubMed  Google Scholar 

  • Berridge K (1990) Comparative fine structure of action: rules of form and sequence in the grooming patterns of six rodent species. Behavior 113:21–56

    Article  Google Scholar 

  • Berton F, Vogel E, Belzung C (1998) Modulation of mice anxiety in response to cat odor as a consequence of predators diet. Physiol Behav 65(2):247–254

    Article  CAS  PubMed  Google Scholar 

  • Blanchard RJ, Blanchard DC (1989) Antipredator defensive behaviors in a visible burrow system. J Comp Psychol 103(1):70–82

    Article  CAS  PubMed  Google Scholar 

  • Blanchard DC, Griebel G, Blanchard RJ (2003a) Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion. Prog Neuropsychopharmacol Biol Psychiatry 27:1177–1185

    Article  PubMed  Google Scholar 

  • Blanchard DC, Markham C, Yang M, Hubbard D, Madarang E, Blanchard RJ (2003b) Failure to produce conditioning with low-dose trimethylthiazoline or cat feces as unconditioned stimuli. Behav Neurosci 117(2):360–368

    Article  CAS  PubMed  Google Scholar 

  • Borowski Z (1998) Influence of weasel (Mustela nivalis Linneaus, 1776) odour on spatial behaviour of root voles (Microtus oeconomus Pallas, 1776). Can J Zool 76:1799–1804

    Article  Google Scholar 

  • Borowski Z, Owadowska E (2001) Spatial responses of field (Microtus agrestis) and bank (Clethronomys glareolus) voles to weasel (Mustela nivalis) odour in natural habitat. Chemical Signals in Vertebrates. Kluwer/Plenum, New York

    Google Scholar 

  • Borowski Z, Owadowska E (2010) Field vole (Microtus agrestis) seasonal spacing behavior: the effect of predation risk by mustelids. Naturwissenschaften 97(5):487–493

    Article  CAS  PubMed  Google Scholar 

  • Bowen MT, Keats K, Kendig MD, Cakic V, Callaghan PD, McGregor IS (2012) Aggregation in quads but not pairs of rats exposed to cat odor or bright light. Behav Process 90(3):331–336. doi:10.1016/j.beproc.2012.03.014

    Article  Google Scholar 

  • Breese GR, Knapp DJ, Criswell HE, Moy SS, Papadeas ST, Blake BL (2005) The neonate-6-hydroxydopamine-lesioned rat: a model for clinical neuroscience and neurobiological principles. Brain Res Brain Res Rev 48(1):57–73. doi:10.1016/j.brainresrev.2004.08.004

    Article  CAS  PubMed  Google Scholar 

  • Campos KF, Amaral VC, Rico JL, Miguel TT, Nunes-de-Souza RL (2013) Ethopharmacological evaluation of the rat exposure test: a prey–predator interaction test. Behav Brain Res 240:160–170. doi:10.1016/j.bbr.2012.11.023

    Article  CAS  PubMed  Google Scholar 

  • Cressman R, Garay J (2011) The effects of opportunistic and intentional predators on the herding behavior of prey. Ecology 92(2):432–440

    Article  PubMed  Google Scholar 

  • Davis M, Parisi T, Gendelman DS, Tischler M, Kehne JH (1982) Habituation and sensitization of startle reflexes elicited electrically from the brainstem. Science 218(4573):688–690

    Article  CAS  PubMed  Google Scholar 

  • Day HE, Masini CV, Campeau S (2004) The pattern of brain c-fos mRNA induced by a component of fox odor, 2,5-dihydro-2,4,5-trimethylthiazoline (TMT), in rats, suggests both systemic and processive stress characteristics. Brain Res 1025(1–2):139–151. doi:10.1016/j.brainres.2004.07.079

    Article  CAS  PubMed  Google Scholar 

  • Deecke VB, Slater PJ, Ford JK (2002) Selective habituation shapes acoustic predator recognition in harbour seals. Nature 420(6912):171–173. doi:10.1038/nature01030

    Article  CAS  PubMed  Google Scholar 

  • Dickman C (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313–322

    Article  Google Scholar 

  • Dielenberg RA, McGregor IS (1999) Habituation of the hiding response to cat odor in rats (Rattus norvegicus). J Comp Psychol 113(4):376–387

    Article  CAS  PubMed  Google Scholar 

  • Dielenberg RA, McGregor IS (2001) Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 25(7–8):597–609

    Article  CAS  PubMed  Google Scholar 

  • Ellard CG (1996) Laboratory studies of antipredator behavior in the Mongolian gerbil (Meriones unguiculatus): factors affecting response attenuation with repeated presentations. J Comp Psychol 110(2):155–163

    Article  CAS  PubMed  Google Scholar 

  • Endres T, Fendt M (2007) Conditioned behavioral responses to a context paired with the predator odor trimethylthiazoline. Behav Neurosci 121(3):594–601. doi:10.1037/0735-7044.121.3.594

    Article  PubMed  Google Scholar 

  • Fendt M, Siegl S, Steiniger-Brach B (2005) Noradrenaline transmission within the ventral bed nucleus of the stria terminalis is critical for fear behavior induced by trimethylthiazoline, a component of fox odor. J Neurosci 25(25):5998–6004. doi:10.1523/JNEUROSCI.1028-05.2005

    Article  CAS  PubMed  Google Scholar 

  • Fenn MG, Macdonald DW (1995) Use of middens by red foxes: risk reverses rhythms of rats. J Mammal 76:130–136

    Article  Google Scholar 

  • Figueiredo HF, Bodie BL, Tauchi M, Dolgas CM, Herman JP (2003) Stress integration after acute and chronic predator stress: differential activation of central stress circuitry and sensitization of the hypothalamo-pituitary-adrenocortical axis. Endocrinology 144(12):5249–5258. doi:10.1210/en.2003-0713

    Article  CAS  PubMed  Google Scholar 

  • File SE, Zangrossi H Jr, Sanders FL, Mabbutt PS (1993) Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiol Behav 54:1109–1111

    Article  CAS  PubMed  Google Scholar 

  • Fullard JH, Ratcliffe JM, Guignion C (2005) Sensory ecology of predator–prey interactions: responses of the AN2 interneuron in the field cricket, Teleogryllus oceanicus to the echolocation calls of sympatric bats. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191(7):605–618. doi:10.1007/s00359-005-0610-3

    Article  PubMed  Google Scholar 

  • Hacquemand R, Choffat N, Jacquot L, Brand G (2013) Comparison between low doses of TMT and cat odor exposure in anxiety- and fear-related behaviors in mice. Behav Brain Res 238:227–231. doi:10.1016/j.bbr.2012.10.014

    Article  CAS  PubMed  Google Scholar 

  • Haupt M, Eccard JA, Winter Y (2010) Does spatial learning ability of common voles (Microtus arvalis) and bank voles (Myodes glareolus) constrain foraging efficiency? Anim Cogn 13(6):783–791. doi:10.1007/s10071-010-0327-8

    Article  PubMed  Google Scholar 

  • Hegab IM, Ai QW, Yin BF, Yang SM, Wei WH (2013a) Behavioral and neuroendocrine response of Brandt’s voles, Lasiopodomys brandtii, to odors of different species. Eur J Wildl Res. doi:10.1007/s10344-013-0790-z

    Google Scholar 

  • Hegab IM, Shang G, Ye M, Jin Y, Wang A, Yin B, Yang S, Wei W (2013b) Defensive responses of Brandt’s voles (Lasiopodomys brandtii) to chronic predatory stress. Physiol Behav 126:1–7. doi:10.1016/j.physbeh.2013.12.001

    Article  PubMed  Google Scholar 

  • Hegab IM, Jin Y, Ye M, Wang A, Yin B, Yang S, Wei WH (2014) Defensive responses of Brandt’s voles (Lasiopodomys brandtii) to stored cat feces. Physiol Behav 123:193–199

    Article  CAS  PubMed  Google Scholar 

  • Helfman GS (1989) Threat-sensitive predator avoidance in damsel-fish trumpet-fish interactions. Behav Ecol Sociobiol 24:47–58

    Article  Google Scholar 

  • Janitzky K, Stork O, Lux A, Yanagawa Y, Schwegler H, Linke R (2009) Behavioral effects and pattern of brain c-fos mRNA induced by 2,5-dihydro-2,4,5-trimethylthiazoline, a component of fox feces odor in GAD67-GFP knock-in C57BL/6 mice. Behav Brain Res 202(2):218–224. doi:10.1016/j.bbr.2009.03.038

    Article  CAS  PubMed  Google Scholar 

  • Jedrzejewski W, Jedrzejewska B (1990) Effect of a predator’s visit on the spatial distribution of bank voles: experiments with weasels. Can J Zool 68:660–666

    Article  Google Scholar 

  • Kavaliers M, Choleris E (2001) Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci Biobehav Rev 25(7–8):577–586

    Article  CAS  PubMed  Google Scholar 

  • Koivisto E, Pusenius J (2003) Effects of temporal variation in the risk of predation by least weasels (Mustela nivalis) on feeding behavior of field voles (Microtus agrestis). Evol Ecol 17:477–489

    Article  Google Scholar 

  • Leussis MP, Bolivar VJ (2006) Habituation in rodents: a review of behavior, neurobiology, and genetics. Neurosci Biobehav Rev 30(7):1045–1064. doi:10.1016/j.neubiorev.2006.03.006

    Article  PubMed  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Back to the basics of antipredatory vigilance: can nonvigilant animals detect attack? Anim Behav 58(3):537–543

    Article  PubMed  Google Scholar 

  • Luedke AC, Boucher PO, Niel L, Holmes MM (2013) Altered anxiety and defensive behaviors in Bax knockout mice. Behav Brain Res 239:115–120. doi:10.1016/j.bbr.2012.10.056

    Article  CAS  PubMed  Google Scholar 

  • Luttbeg B, Trussell GC (2013) How the informational environment shapes how prey estimate predation risk and the resulting indirect effects of predators. Am Nat 181(2):182–194. doi:10.1086/668823

    Article  PubMed  Google Scholar 

  • Mackenzie L, Nalivaiko E, Beig MI, Day TA, Walker FR (2010) Ability of predator odour exposure to elicit conditioned versus sensitised post-traumatic stress disorder-like behaviours, and forebrain deltaFosB expression, in rats. Neuroscience 169(2):733–742. doi:10.1016/j.neuroscience.2010.05.005

    Article  CAS  PubMed  Google Scholar 

  • Martel G, Dill LM (1993) Chemoreception, risk of predation, feeding and agonistic behaviours in juvenile coho salmon (Oncorhynchus kisutch). Behav Ecol Sociobiol 32:365–370

    Article  Google Scholar 

  • Masini CV, Sauer S, Campeau S (2005) Ferret odor as a processive stress model in rats: neurochemical, behavioral, and endocrine evidence. Behav Neurosci 119(1):280–292. doi:10.1037/0735-7044.119.1.280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • May MD, Bowen MT, McGregor IS, Timberlake W (2012) Rubbings deposited by cats elicit defensive behavior in rats. Physiol Behav 107(5):711–718. doi:10.1016/j.physbeh.2012.03.007

    Article  CAS  PubMed  Google Scholar 

  • McGregor IS, Schrama L, Ambermoon P, Dielenberg RA (2002) Not all ‘predator odours’ are equal: cat odour but not 2,4,5 trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behav Brain Res 129(1–2):1–16

    Article  CAS  PubMed  Google Scholar 

  • Monclus R, Rodel HG, Von Holst D, De Miguel J (2005) Behavioural and physiological responses of naive European rabbits to predator odour. Anim Behav 70:753–761. doi:10.1016/j.anbehav.2004.12.019

    Article  Google Scholar 

  • Norrdahl K, Korpimaki E (1998) Does mobility or sex of voles affect risk of predation by mammalian predators? Ecology 79:226–232

    Article  Google Scholar 

  • Orrock JL, Danielson BJ, Brinkerhoff RJ (2004) Rodent foraging is affected by indirect, but not by direct, cues of predation risk. Behav Ecol 15(3):433–437. doi:10.1093/beheco/arh031

    Article  Google Scholar 

  • Perrot-Sinal TS, Ossenkopp KP, Kavaliers M (1999) Brief predator odour exposure activates the HPA axis independent of locomotor changes. Neuroreport 10(4):775–780. doi:10.1097/00001756-199903170-00021

    Article  CAS  PubMed  Google Scholar 

  • Pitman RK, van der Kolk BA, Orr SP, Greenberg MS (1990) Naloxone-reversible analgesic response to combat-related stimuli in posttraumatic stress disorder. A pilot study. Arch Gen Psychiatry 47(6):541–544

    Article  CAS  PubMed  Google Scholar 

  • Pusenius J, Ostfeld RS (2002) Mammalian predator scent, vegetation cover and tree seedling predation by meadow voles. Ecography 25(4):481–487. doi:10.1016/j.bbr.2006.01.025

    Article  Google Scholar 

  • Sato JJ, Wolsan M, Prevosti FJ, D’Elia G, Begg C, Begg K, Hosoda T, Campbell KL, Suzuki H (2012) Evolutionary and biogeographic history of weasel-like carnivorans (Musteloidea). Mol Phylogenet Evol 63(3):745–757. doi:10.1016/j.ympev.2012.02.025

    Article  PubMed  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Article  Google Scholar 

  • Schmitz OJ, Bradford MA, Strickland MS, Hawlena D (2013) Linking predation risk, herbivore physiological stress and microbial decomposition of plant litter. J Vis Exp (73). doi:10.3791/50061

  • Staples LG, McGgregor IS, Apfelbach R, Hunt GE (2008) Cat odor, but not trimethylthiazoline (fox odor), activates accessory olfactory and defense-related brain regions in rats. Neuroscience 151(4):937–947. doi:10.1016/j.neuroscience.2007.11.039

    Article  CAS  PubMed  Google Scholar 

  • Staples LG, McGregor IS, Hunt GE (2009) Long-lasting FosB/Delta FosB immunoreactivity in the rat brain after repeated cat odor exposure. Neuroci Lett 462(2):157–161. doi:10.1016/j.neulet.2009.06.069

    Article  CAS  Google Scholar 

  • Sullivan T, Crump D, Sullivan D (1988) Use of predator odors as repellents to reduce feeding damage by herbivores. 4. Northern pocket gophers (Thomomys talipoides). J Chem Ecol 14:379–390

    Article  CAS  PubMed  Google Scholar 

  • Sullivan AM, Madison DM, Rohr JR (2004) Variation in the antipredator responses of three sympatric plethodontid salamanders to predator-diet cues. Herpetologica 60(4):401–408. doi:10.1655/03-71

    Article  Google Scholar 

  • Sundell J, Dudek D, Klemme I, Koivisto E, Pusenius J, Ylonen H (2004) Variation in predation risk and vole feeding behaviour: a field test of the risk allocation hypothesis. Oecologia 139(1):157–162. doi:10.1007/s00442-004-1490-x

    Article  PubMed  Google Scholar 

  • Takahashi LK, Nakashima BR, Hong H, Watanabe K (2005) The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neurosci Biobehav Rev 29(8):1157–1167. doi:10.1016/j.neubiorev.2005.04.008

    Article  PubMed  Google Scholar 

  • Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73(1):16–43

    Article  CAS  PubMed  Google Scholar 

  • Tidhar WL, Bonier F, Speakman JR (2007) Sex- and concentration-dependent effects of predator feces on seasonal regulation of body mass in the bank vole Clethrionomys glareolus. Horm Behav 52(4):436–444. doi:10.1016/j.yhbeh.2007.06.009

    Article  PubMed  Google Scholar 

  • Tsigos C, Chrousos GP (2002) Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53(4):865–871

    Article  PubMed  Google Scholar 

  • Vianna DM, Borelli KG, Ferreira-Netto C, Macedo CE, Brandao ML (2003) Fos-like immunoreactive neurons following electrical stimulation of the dorsal periaqueductal gray at freezing and escape thresholds. Brain Res Bull 62(3):179–189

    Article  CAS  PubMed  Google Scholar 

  • Wallace KJ, Rosen JB (2000) Predator odor as an unconditioned fear stimulus in rats: elicitation of freezing by trimethylthiazoline, a component of fox feces. Behav Neurosci 114(5):912–922

    Article  CAS  PubMed  Google Scholar 

  • Willson JD, Hopkins WA (2011) Prey morphology constrains the feeding ecology of an aquatic generalist predator. Ecology 92(3):744–754

    Article  PubMed  Google Scholar 

  • Wilson CA, Vazdarjanova A, Terry AV Jr (2013) Exposure to variable prenatal stress in rats: effects on anxiety-related behaviors, innate and contextual fear, and fear extinction. Behav Brain Res 238:279–288. doi:10.1016/j.bbr.2012.10.003

    Article  PubMed Central  PubMed  Google Scholar 

  • Wood WF, Jeffrey P, Copeland RE, Yates IK, Horsey LR (2009) Potential semiochemicals in urine from free ranging wolverines (Gulo gulo Pallas, 1780). Biochem Syst Ecol 37(5):574–578

    Article  CAS  Google Scholar 

  • Wright LD, Muir KE, Perrot TS (2012) Stress responses of adolescent male and female rats exposed repeatedly to cat odor stimuli, and long-term enhancement of adult defensive behaviors. Dev Psychobiol 55(5):551–567. doi:10.1002/dev.21060

    Article  PubMed  Google Scholar 

  • Wywialowski AP (1987) Habitat structure and predators: choices and consequences for rodent habitat specialists and generalists. Oecologia 72:39–45

    Article  Google Scholar 

  • Xu HY, Liu YJ, Xu MY, Zhang YH, Zhang JX, Wu YJ (2012) Inactivation of the bed nucleus of the stria terminalis suppresses the innate fear responses of rats induced by the odor of cat urine. Neuroscience 221:21–27. doi:10.1016/j.neuroscience.2012.06.056

    Article  CAS  PubMed  Google Scholar 

  • Yin BF, Fan HM, Li SP, Hegab IM, Lu GY, Wei WH (2011) Behavioral response of Norway rats (Rattus norvegicus) to odors of different mammalian species. J Pest Sci 84(3):265–272. doi:10.1007/s10340-011-0351-8

    Article  Google Scholar 

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Acknowledgments

The first author would like to thank the staff members of the Department of Animal Hygiene, Zoonosis and Animal Behavior and Management, College of Veterinary Medicine, Suez Canal University, Egypt. This work was supported by the National Basic Research Program of China (973 program, 2007CB109102), the National Natural Science Foundation of China (no. 31272320 and no. 31370415) and the Priority Academic Program Development of Jiangsu Higher Education Institutions. The authors declare that they have no conflicts of interest.

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  1. Department of Animal Hygiene, Zoonosis and Animal Behavior and Management, College of Veterinary Medicine, Suez Canal University, Ismailia, Egypt

    Ibrahim M. Hegab

  2. Department of Animal Behavior, College of Bioscience and Biotechnology, Yangzhou University, Yangzhou, 225009, Jiangsu, China

    Shushu Kong, Shengmei Yang & Wanhong Wei

  3. Department of Animal Medicine, College of Veterinary Medicine, Yangzhou University, Yangzhou, 225009, Jiangsu, China

    Walaa I. Mohamaden

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  1. Ibrahim M. Hegab
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  2. Shushu Kong
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Hegab, I.M., Kong, S., Yang, S. et al. The ethological relevance of predator odors to induce changes in prey species. acta ethol 18, 1–9 (2015). https://doi.org/10.1007/s10211-014-0187-3

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