Abstract
Prey species show specific adaptations that allow recognition, avoidance, and defense against predators. This study was undertaken to investigate the processing of a chronic, life-threatening stimulus to Norway rats (Rattus norvegicus). One hundred forty-four Norway rats were tested by repeated presentation of cat urine for 1 h at different days in a defensive withdrawal apparatus. Rats exposed to urine for short periods showed significantly larger defensive behavioral and medial hypothalamic c-fos messenger RNA (mRNA) responses than other groups. These defensive responses habituated shortly after the presentation of cat urine. Serum levels of adrenocorticotropic hormone and corticosterone increased significantly when animals were repeatedly exposed to cat urine. However, the hormonal responses took longer to habituate than the behavioral and molecular responses did. We conclude that the behavioral and c-fos mRNA responses are “primed” for habituation to repeated exposures to cat urine, while the hormonal responses show “resistance.” The results support our hypothesis that the strongest anti-predator responses at three levels would occur during short-term exposure to cat urine and that these responses would subsequently disappear on prolonged exposure. This study assists understanding the way in which the different levels of defensive responses are integrated and react during chronic stress.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amir S, Cain S, Sullivan J, Robinson B, Stewart J (1999) In rats, odor-induced Fos in the olfactory pathways depends on the phase of the circadian clock. Neurosci Lett 272:175–178. doi:10.1016/S0304-3940(99)00609-6
Apfelbach R, Blanchard CD, 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 29:1123–1144. doi:10.1016/j.neubiorev.2005.05.005
Apfelbach R, Soini HA, Vasilieva NY, Novotny MV (2015) Behavioral responses of predator-naïve dwarf hamsters (Phodopus campbelli) to odor cues of the European ferret fed with different prey species. Physiol Behav 146:57–66. doi:10.1016/j.physbeh.2015.04.014
Blanchard RJ, Blanchard DC (1989) Antipredator defensive behaviors in a visible burrow system. J Comp Psychol 103:70–82. doi:10.1037/0735-7036.103.1.70
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 90:331–336. doi:10.1016/j.beproc.2012.03.014
Brachetta V, Schleich CE, Zenuto RR (2016) Source odor, intensity, and exposure pattern affect antipredatory responses in the subterranean rodent Ctenomys talarum. Ethology 122:923–936. doi:10.1111/eth.12568
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 Rev 48:57–73. doi:10.1016/j.brainresrev.2004.08.004
Canteras NS, Chiavegatto S, Valle LER, Swanson LW (1997) Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res Bull 44:297–305. doi:10.1016/S0361-9230(97)00141-X
Cullinan WE, Helmreich DL, Watson SJ (1996) Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. J Comp Neurol 368:88–99. doi:10.1002/(SICI)1096-9861(19960422)368
Dielenberg RA, McGregor IS (1999) Habituation of the hiding response to cat odor in rats (Rattus norvegicus). J Comp Psychol 113:376–387. doi:10.1037/0735-7036.113.4.376
Eilam D, Dayan T, Ben-Eliyahu S (1999) Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim Behav 58:1085–1093. doi:10.1006/anbe.1999.1224
Elvidge CK, Ramnarine I, Brown GE (2014) Compensatory foraging in Trinidadian guppies: effects of acute and chronic predation threats. Curr Zool 3:323–332. doi:10.1093/czoolo/60.3.323
Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ, Datta SR (2011) Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci U S A 108:11235–11240. doi:10.1073/pnas.1103317108
Filaretov AA, Rakitskaya VV (1980) Role of the medial hypothalamus in regulation of the pituitary-adrenocortical system. Neurosci Behav Physiol 10:135–138. doi:10.1007/BF01148449
File SE, Zangrossi JH, Sanders FL, Mabbutt PS (1993) Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiol Behav 54:1109–1111. doi:10.1016/0031-9384(93)90333-B
Filipovic D, Zlatkovic J, Gass P, Inta D (2013) The differential effects of acute vs. chronic stress and their combination on hippocampal parvalbumin and inducible heat shock protein 70 expression. Neuroscience 236:47–54. doi:10.1016/j.neuroscience.2013.01.033
Harris BN, Perea-Rodriguez JP, Saltzman W (2011) Acute effects of corticosterone injection on paternal behavior in California mouse (Peromyscus californicus) fathers. Horm Behav 60:666–675. doi:10.1016/j.yhbeh.2011.09.001
Hawkins LA, Anne EM, John DA (2008) Ontogenetic learning of predator recognition in hatchery-reared Atlantic salmon, Salmo salar. Anim Behav 75:1663–1671. doi:10.1016/j.anbehav.2007.10.019
Hegab IM, Wang A, Yin B et al (2014a) Behavioral and neuroendocrine response of Brandt’s voles, Lasiopodomys brandtii, to odors of different species. Eur J Wildl Res 60:331–340. doi:10.1007/s10344-013-0790-z
Hegab IM, Shang G, Ye M et al (2014b) 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
Hegab IM, Jin Y, Ye M et al (2014c) Defensive responses of Brandt’s voles (Lasiopodomys brandtii) to stored cat feces. Physiol Behav 123:193–199. doi:10.1016/j.physbeh.2013.10.030
Hegab IM, Yang S, Wei WH (2015) The ethological relevance of predator odors to induce changes in prey species. Acta Ethol 18:1–9. doi:10.1007/s10211-014-0187-3
Jankord R, Herman JP (2008) Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann N Y Acad Sci 1148:64–73. doi:10.1196/annals.1410.012
Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2005) Mapping the neural circuit activated by alarm pheromone perception by c-Fos immunohistochemistry. Brain Res 1043:145–154. doi:10.1016/j.brainres.2005.02.061
Leussis MP, Bolivar VJ (2006) Habituation in rodents: a review of behavior, neurobiology, and genetics. Neurosci Biobehav Rev 30:1045–1064. doi:10.1016/j.neubiorev.2006.03.006
Mashoodh R, Wright LD, Hebert K, Perrot-Sinal TS (2008) Investigation of sex differences in behavioural, endocrine, and neural measures following repeated psychological stressor exposure. Behav Brain Res 188:368–379. doi:10.1016/j.bbr.2007.11.018
Masini CV, Sauer S, Campeau S (2005) Ferret odor as a processive stress model in rats: neurochemical, behavioral, and endocrine evidence. Behav Neurosci 119:280–292. doi:10.1037/0735-7044.119.1.280
McSweeney FK, Murphy ES (2009) Sensitization and habituation regulate reinforcer effectiveness. Neurobiol Learn Mem 92:189–198. doi:10.1016/j.nlm.2008.07.002
Monclús R, Palomares F, Tablado Z, Martinez-Fonturbel A, Palme R (2009) Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 158:615–623. doi:10.1007/s00442-008-1201-0
Navarro-Castilla Á, Barja I (2014) Does predation risk, through moon phase and predator cues, modulate food intake, antipredatory and physiological responses in wood mice (Apodemus sylvaticus)? Behav Ecol Sociobiol 68:1505–1512. doi:10.1007/s00265-014-1759-y
Perrot-Sinal TS, Ossenkopp KP, Kavaliers M (1999) Effects of repeated exposure to fox odor on locomotor activity levels and spatial movement patterns in breeding male and female meadow voles (Microtus pennsylvanicus). J Chem Ecol 25:1567–1584. doi:10.1023/A:1020836832455
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation in predator-prey interactions. Ecology 86:501–509. doi:10.1890/04-0719
Rampin O, Bellier C, Maurin Y (2012) Electrophysiological responses of rat olfactory tubercle neurons to biologically relevant odours. Eur J Neurosci 35:97–105. doi:10.1111/j.1460-9568.2011.07940.x
Staples LG, McGregor IS, Apfelbach R et al (2008) Cat odor, but not trimethylthiazoline (fox odor), activates accessory olfactory and defense-related brain regions in rats. Neuroscience 151:937–947. doi:10.1016/j.neuroscience.2007.11.039
Takahashi LK, Nakashima BR, Hong H et al (2005) The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neurosci Biobehav Rev 29:1157–1167. doi:10.1016/j.neubiorev.2005.04.008
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 52:436–444. doi:10.1016/j.yhbeh.2007.06.009
Wernecke KEA, Vincenz D, Storsberg S et al (2015) Fox urine exposure induces avoidance behavior in rats and activates the amygdalar olfactory cortex. Behav Brain Res 279:76–81. doi:10.1016/j.bbr.2014.11.020
Xu HY, Liu YJ, Xu MY et al (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
Yin BF, Fan HM, Li SP et al (2011) Behavioral response of Norway rats (Rattus norvegicus) to odors of different mammalian species. J Pest Sci 84:265–272. doi:10.1007/s10340-011-0351-8
Acknowledgments
This work was supported by the National Basic Research Program of China (973 program, 2007CB109102), the National Natural Science Foundation of China (No. 31370415), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All procedures were approved by the Animal Care and Use Committee of the Faculty of Veterinary Medicine of Yangzhou University.
Additional information
Communicated by: Sven Thatje
Rights and permissions
About this article
Cite this article
Yin, B., Gu, C., Lu, Y. et al. Repeated exposure to cat urine induces complex behavioral, hormonal, and c-fos mRNA responses in Norway rats (Rattus norvegicus). Sci Nat 104, 64 (2017). https://doi.org/10.1007/s00114-017-1484-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-017-1484-2