Abstract
There is a paucity of data about the effects of aging on an individual’s response to scent marks in terrestrial mammals. In a recent series of experiments on the arvicoline rodent, the meadow vole, Microtus pennsylvanicus, age of the subject had different effects on three odor-related behaviors: self-grooming, scent marking, and over-marking, suggesting that age of the vole may also affects its ability to identify and discriminate among the scent marks of different conspecifics. We used a habituation/test paradigm to test the hypothesis that aging affects the ability of meadow voles (Microtus pennsylvanicus) to identify individual differences in the scent marks of two conspecifics. In experiments 1 and 2, 2–3-month-old, 5–7-month-old, and 10–12-month-old voles that were exposed four successive times to the scent mark of an opposite-sex conspecific or a same-sex conspecific habituated to the scent mark of these donors. Later, during the test phase, 2–3-, 5–7-, and 10–12-month-old voles spent more time investigating the scent mark of a novel donor than that of the familiar donor. Thus, 2–12-month-old voles behave as if the scent marks of the donors were individually distinct. In contrast, in both experiments 1 and 2, 15–18-month-old voles failed to habituate to the scent mark of the familiar donor. In addition, during the test phase, 15–18-month-old voles spent similar amounts of time investigating the scent mark of the novel donor and that of the familiar donor. In experiment 3, 15–18-month-old voles could distinguish between the scent mark of a male and that of a female donor, spending more time investigating the scent mark of the opposite-sex conspecific to that of the same-sex conspecific. Thus, 15–18-month-old voles can no longer distinguish between the scent marks of two same-sex conspecifics but can discriminate between the scent marks of a male and a female conspecific. The data suggest that age of the vole may influence its ability to identify and discriminate among the scent marks of different same-sex conspecifics. The consequences of such impairment in social recognition may result in a trade-off between survival and mating success for older voles.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Beck CW, Powell LA (2000) Evolution of female mate choice based on male age: are older males better mates? Evol Ecol Res 2:107–118
Boonstra R (1994) Population cycles in microtines: the senescence hypothesis. Evol Ecol 8:196–219
Boraty Z, Koteja P (2009) The association between body mass, metabolic rates and survival of bank voles. Funct Ecol 23:330–339
Brennan MJ, Allen D, Aleman D, Azmitia EC, Quartermain D (1984) Age differences in within-session habituation of exploratory behavior: effects of stimulus complexity. Behav Neural Biol 42:61–72
Brown RE, Macdonald DW (eds) (1985) Social odours in mammals. Oxford University Press, Oxford, UK
Doty RL, Kamath V (2014) The influences of age on olfaction: a review. Front Psychol 5:20. doi:10.3389/fpsyg.2014.00020
Ferkin MH (1999) Attractiveness of opposite-sex odor and responses to it vary with age and sex in meadow voles (Microtus pennsylvanicus). J Chem Ecol 4:757–769
Ferkin MH (2010) Age affects over-marking of opposite-sex scent marks in meadow voles. Ethology 116:24–31
Ferkin MH (2011) Odor-related behavior and cognition in meadow voles, Microtus pennsylvanicus (Arvicolidae, Rodentia). Folia Zool 60:262–276
Ferkin MH (2015) The response of rodents to scent marks: four broad hypotheses. Horm Behav 68:43–52
Ferkin MH, Johnston RE (1995) Meadow voles, Microtus pennsylvanicus, use multiple sources of scent for sex recognition. Anim Behav 49:37–44
Ferkin MH, Leonard ST (2008) Age of the subject and scent donor affects the amount of time that voles self-groom when they are exposed to odors of opposite-sex conspecifics. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates 11. Springer, New York, pp 281–289
Ferkin MH, Li HZ (2005) A battery of olfactory-based screens for phenotyping the social and sexual behaviors of mice. Physiol Behav 85:489–499
Ferkin MH, Sorokin ES, Johnston RE (1996) Self-grooming as a sexually dimorphic communicative behaviour in meadow voles, Microtus pennsylvanicus. Anim Behav 51:801–810
Ferkin MH, Dunsavage J, Johnston RE (1999) Meadow voles can discriminate between the top and bottom scent of an over-mark and prefer the top scent. J Comp Psychol 113:43–51
Fischer K, Perlick J, Galetz T (2008) Residual reproductive value and male mating success: older males do better. Proc R Soc B 275:1517–1524
Gallagher M, Rapp PR (1997) The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 48:339–370
Halpin ZT (1974) Individual differences in the biological odors of the Mongolian gerbil (Meriones unguiculatus). Behav Biol 11:253–259
Halpin ZT (1980) Individual odors and individual recognition: review and commentary. Biol Behav 5:233–248
Halpin ZT (1986) Individual odors among mammals: origins and functions. Adv Study Behav 16:39–70
Heth G, Todrank J, Johnston RE (1999) Similarity in the qualities of individual odors among kin and species in Turkish (Mesocricetus brandti) and golden (Mesocricetus auratus) hamsters. J Comp Psychol 113:321–326
Hurst JL, Beynon RJ (2004) Scent wars: the chemobiology of competitive signaling in mice. Bioassays 26:1288–1298
Johnston RE, Chiang G, Tung C (1994) The information in scent over-marks of golden hamsters. Anim Behav 48:323–330
Johnston RE, Munver R, Tung C (1995) Scent counter marks: selective memory for the top scent by golden hamsters. Anim Behav 49:1435–1442
Johnston RE (1993) Memory for individual scent in hamsters (Mesocricetus auratus) as assessed by habituation methods. J Comp Psychol 107:201–207
Johnston RE (2003) Chemical communication in rodents: from pheromones to individual recognition. J Mammal 84:1141–1162
Johnston RE (2008) Individual odors and social communication: individual recognition, kin recognition, and scent over‐marking. Adv Study Behav 38:439–505
Johnston RE, Bullock T (2001) Individual recognition and the nature of individual representations in golden hamsters. Anim Behav 61:545–557
Johnston RE, Derzie A, Chiang G, Jernigan P, Lee HC (1993) Individual scent signatures in golden hamsters: evidence for specialization of function. Anim Behav 45:1061–1070
Kaur AW, Ackels T, Kuo T-H, Cichy A, Dey S, Hays C, Kateri M, Logan DW, Marton TF, Spehr M, Stowers L (2014) Murine pheromone proteins constitute a context-dependent combinatorial code governing multiple social behaviors. Cell 157:676–688
Keevin TM, Halpin ZT, McCurdy N (1981) Individual and sex-specific odors in male and female eastern chipmunks (Tamias striatus). Behav Biol 6:329–338
Keller BL (1985) Reproductive patterns. In: Tamarin RH (ed) Biology of new world Microtus, vol 8. Amer Soc Mammal Sp Publ, Lawrence, KS, pp 725–778
Kokko H (1998) Good genes, old age and life-history trade-offs. Evol Ecol 12:739–750
Lai S-C, Johnston RE (1994) The repertoire of individual odors in Djungarian hamsters, Phodopus campbelli. Ethology 96:117–126
Madison DM (1980) An integrated view of the social biology of Microtus pennsylvanicus. Biologist 62:20–33
Manning JT (1985) Choosy females and correlates of male age. J Theor Biol 116:349–354
Markowska AL, Stone WS, Ingram DK, Reynolds J, Gold PE, Conti LS, Pontecorvo MJ, Wenk GL, Olton DS (1989) Individual differences in aging: behavioral and neurobiological correlates. Neurobiol Aging 10:31–43
Matzel LD, Light KR, Wass C, Colas-Zelin D, Denman-Brice A, Waddel AC, Kolata S (2011) Longitudinal attentional engagement rescues mice from age-related cognitive declines and cognitive inflexibility. Learn Mem 18:345–356
Mayeaux DJ, Johnston RE (2002) Discrimination of individual odors by hamsters (Mesocricetus auratus) varies with the location of those odors. Anim Behav 64:269–281
McGuire BM, Novak MA (1984) A comparison of maternal behavior in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster), and pine vole (M. pinetorum). Anim Behav 32:1132–1141
McGuire B, Pizzuto T, Getz LL (1990) Potential for social interaction in a natural population of prairie voles (Microtus ochrogaster). Can J Zool 68:391–398
Mertl AS (1975) Discrimination of individuals by scent in a primate. Behav Biol 14:505–509
Milligan SR (1982) Induced ovulation in mammals. Oxf Rev Reprod Biol 4:1–46
Nadeau JH (1985) Ontogeny. In: Tamarin RH (ed) Biology of new world Microtus, vol 8. Amer Soc Mammal Sp Publ, Lawrence, KS, pp 254–285
Negus NC, Berger PJ (1988) Cohort analysis: environmental cues and diapause in microtine rodents. In: Boyce MS (ed) Evolution of life histories of mammals, theory and pattern. Yale University Press, New Haven, CT, pp 65–74
Newman KS, Halpin ZT (1988) Individual odours and mate recognition in the prairie vole, Microtus ochrogaster. Anim Behav 36:1779–1787
Partridge L, Endler JA (1987) Life history constraints on the effects of sexual selection. In: Bradbury JW, Andersson MB (eds) Sexual selection: testing the alternatives. Wiley, New York, pp 265–277
Promislow DEL (1991) Senescence in natural populations of mammals: a comparative study. Evolution 45:1869–1877
Rezende EL, Gomes FR, Malisch JL, Chappell MA, Garland T Jr (2006) Maximal oxygen consumption in relation to subordinate traits in lines of house mice selectively bred for high voluntary wheel running. J Appl Physiol 101:477–485
Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071
Roberts SC (2007) Scent marking. In: Wolff JO, Sherman PW (eds) Evolution of life histories of mammals, theory and pattern. Chicago University Press, Chicago, IL, pp 255–267
Rose MR (1991) Evolutionary biology of aging. Oxford University Press, New York
Sabau RM, Ferkin MH (2013) Food restriction affects the mass of dams and pups and the amount of maternal behavior provided by female meadow voles, Microtus pennsylvanicus. J Mammal 94:1068–1076
Shao R, Lee TMC (2014) Aging and risk taking: toward an integration of cognitive, emotional, and neurobiological perspectives. Neurosci Neuroecon 3:47–62
Sheridan M, Tamarin RH (1988) Space use, longevity, and reproductive success in meadow voles. Behav Ecol Sociobiol 22:85–90
Shukitt-Hale B, Casadesus G, Cantu-Castelvetri I, Joseph JA (2001) Effect of age on object exploration, habituation, and response to spatial and nonspatial change. Behav Neurosci 115:1059–1064
Slade NA (1995) Failure to detect senescence in persistence of some grassland rodents. Ecology 76:863–870
Smith T (2006) Individual olfactory signatures in common marmosets (Callithrix jacchus). Am J Primatol 68:585–604
Tamarin RH, Reich LM, Moyer CA (1984) Meadow vole cycles within fences. Can J Zool 62:1796–1804
Tang-Martinez Z, Bixler A (2009) Individual discrimination by odors in sibling prairie voles (Microtus ochrogaster). J Chem Ecol 35:400–404
Thom MD, Hurst JL (2004) Individual recognition by scent. Ann Zool Fennici 41:765–787
Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43
Todrank J, Heth G, Johnston RE (1998) Kin recognition in golden hamsters: evidence for kinship odours. Anim Behav 55:377–386
Wilson DA, Stevenson RJ (2006) Learning to smell: olfactory perception from neurobiology to behavior. The Johns Hopkins University Press, Baltimore, MD
Wyatt TD (2014) Pheromones and animal behavior. Chemical signals and signatures, 2nd edn. Cambridge University Press, Cambridge, UK
Acknowledgments
We thank Malle Carrasco, Dr. Bruce Schulte, and two anonymous reviewers for reading this manuscript and providing helpful suggestions. The research was supported by NIH grants HD 049525 and an ARRA supplement and NSF grant IOB 0444553 to MHF and funds from the Vice Provost of Research and the Department of Biological Sciences at the University of Memphis. This manuscript is dedicated to Dr. Robert E. Johnston, a pioneer and leader in the field of chemical communication in mammals.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this paper
Cite this paper
Ferkin, M.H., Vlautin, C.T., Pierson, L.M. (2016). Age-Related Effects on Individual Discrimination Among Meadow Voles, Microtus pennsylvanicus . In: Schulte, B., Goodwin, T., Ferkin, M. (eds) Chemical Signals in Vertebrates 13. Springer, Cham. https://doi.org/10.1007/978-3-319-22026-0_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-22026-0_9
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-22025-3
Online ISBN: 978-3-319-22026-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)