Animal Cognition

, Volume 18, Issue 6, pp 1231–1242 | Cite as

Seasonal variation in attention and spatial performance in a wild population of the African striped mouse (Rhabdomys pumilio)

  • Audrey MailleEmail author
  • Neville Pillay
  • Carsten Schradin
Original Paper


Cognitive flexibility describes the reversible changes of cognition in response to environmental changes. Although various environmental factors such as temperature, photoperiod and rainfall change seasonally, seasonal variation in cognitive performance has been reported in merely a few birds and mammals. We assessed whether cognitive performance in a wild population of African striped mice Rhabdomys pumilio, from the Succulent Karoo semidesert of South Africa, differed between summer and winter. In order to measure cognitive performance, striped mice were trapped in the field, tested under laboratory conditions at our research station and returned to the field within 5 h. We measured attention and spatial memory using the standardized orientation response test and the Barnes maze test. Males tested during summer oriented faster toward a predator-stimulus but made more errors and took longer to locate a shelter than males tested during winter. In contrast, females’ performance did not differ between the two seasons. We discuss how the faster orientation in males during winter might be the consequence of lower temperatures and/or prolonged food restriction. We suggest that the enhancement of spatial performance during winter might be due to a greater motivation for future dispersal in male striped mice, as spring represents the breeding season.


Cognitive flexibility Seasonality Orientation response Spatial memory Sex differences 



This research was supported by a fellowship (to CS) of the University of Strasbourg Institute for Advanced Study. This study was made possible by the administrative and technical support of the Succulent Karoo Research Station (registered South African NPO 122-134), where fieldwork took place. We thank Ivana Schoepf, Chi-Hang Yuen, Patrick Brunner and Andrea Del Mela Gorrino for assistance in data collection. We also thank Bernard Thierry for helpful discussions about the methodology.

Compliance with Ethical Standards

Ethical approval

Animal ethical clearance was provided by the University of the Witwatersrand, Johannesburg, South Africa (No. 2013/50/2A). All procedures were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest

Supplementary material

Online resource 1

Orientation response test. A mouse (identified with ear tags and red/blonde hair dye) placed in a transparent box facing a white screen, orients its head toward the raptor-stimulus that appeared at the left bottom of the screen and slides in a rightward motion. The raptor-stimulus presentation lasts 5 s. (MP4 8310 kb)

Online resource 2

Barnes maze test—bat trial. A mouse (placed in transparent circular box at the center of the Barnes maze) is released, nose-pokes 4 incorrect holes and then locates the correct hole providing access to an escape box. A bat toy hanging above the maze mimics the presence of a flying predator. Pictures of rocks and plants (photographed in the natural habitat of the population of mice tested) that are placed on the walls and curtains surrounding the maze provide visual landmarks to the mice. (MP4 2635 kb)


  1. Abrams PA (1994) Should prey overestimate the risk of predation? Am Nat 144:317–328CrossRefGoogle Scholar
  2. Aimé P, Duchamp-Viret P, Chaput MA et al (2007) Fasting increases and satiation decreases olfactory detection for a neutral odor in rats. Behav Brain Res 179:258–264. doi: 10.1016/j.bbr.2007.02.012 CrossRefPubMedGoogle Scholar
  3. Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioural study in the rat. J Comp Physiol Psychol 93:74–104CrossRefPubMedGoogle Scholar
  4. Bowman RE (2005) Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan. J Neuroendocrinol 17:526–535. doi: 10.1111/j.1365-2826.2005.01335.x CrossRefPubMedGoogle Scholar
  5. Buchanan KL, Grindstaff JL, Pravosudov VV (2013) Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution. Trends Ecol Evol 28:290–296. doi: 10.1016/j.tree.2013.02.004 PubMedCentralCrossRefPubMedGoogle Scholar
  6. Canals M, Rosenmann M, Bozinovic F (1989) Energetics and geometry of huddling in small mammals. J Theor Biol 141:181–189CrossRefPubMedGoogle Scholar
  7. Chatelain M, Halpin CG, Rowe C (2013) Ambient temperature influences birds’ decisions to eat toxic prey. Anim Behav 86:733–740. doi: 10.1016/j.anbehav.2013.07.007 PubMedCentralCrossRefPubMedGoogle Scholar
  8. Clayton NS, Cristol DA (1996) Effects of photoperiod on memory and food storing in captive marsh tits, Parus palustris. Anim Behav 52:715–726. doi: 10.1006/anbe.1996.0216 CrossRefGoogle Scholar
  9. Clayton NS, Reboreda JC, Kacelnik A (1997) Seasonal changes of hippocampus volume in parasitic cowbirds. Behav Process 41:237–243. doi: 10.1016/S0376-6357(97)00050-8 CrossRefGoogle Scholar
  10. Cowling RM, Esler KJ, Rundel PW (1999) Namaqualand, South Africa—an overview of a unique winter-rainfall desert ecosystem. Plant Ecol 142:3–21. doi: 10.1023/A:1009831308074 CrossRefGoogle Scholar
  11. Dal-Pan A, Pifferi F, Marchal J et al (2011) Cognitive performances are selectively enhanced during chronic caloric restriction or resveratrol supplementation in a primate. PLoS One 6:e16581. doi: 10.1371/journalpone.0016581 PubMedCentralCrossRefPubMedGoogle Scholar
  12. Ferrari MCO (2014) Short-term environmental variation in predation risk leads to differential performance in predation-related cognitive function. Anim Behav 95:9–14. doi: 10.1016/j.anbehav.2014.06.001 CrossRefGoogle Scholar
  13. Galea LAM, McEwen B (1999) Sex and seasonal changes in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 89:955–964. doi: 10.1016/S0306-4522(98)00345-5 CrossRefPubMedGoogle Scholar
  14. Galea LAM, Kavaliers M, Ossenkopp K-P et al (1994) Sexually dimorphic spatial learning varies seasonally in two populations of deer mice. Brain Res 635:18–26. doi: 10.1016/0006-8993(94)91419-2 CrossRefPubMedGoogle Scholar
  15. Galea LAM, Kavaliers M, Ossenkopp KP (1996) Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol 199:195–200PubMedGoogle Scholar
  16. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274. doi: 10.1146/annurev.physiol.66.032102.115105 CrossRefPubMedGoogle Scholar
  17. Geiser F, Goodship N, Pavey CR (2002) Was basking important in the evolution of mammalian endothemy? Naturwissenschaften 89:412–414CrossRefPubMedGoogle Scholar
  18. Gilsenan MB, de Bruin EA, Dye L (2009) The influence of carbohydrate on cognitive performance: a critical evaluation from the perspective of glycaemic load. Br J Nutr 101:941–949. doi: 10.1017/S0007114508199019 CrossRefPubMedGoogle Scholar
  19. Isler K, van Schaik CP (2006) Metabolic costs of brain size evolution. Biol Lett 2:557–560. doi: 10.1098/rsbl.2006.0538 PubMedCentralCrossRefPubMedGoogle Scholar
  20. Jašarević E, Williams SA, Roberts RM et al (2012) Spatial navigation strategies in Peromyscus: a comparative study. Anim Behav 84:1141–1149. doi: 10.1016/j.anbehav.2012.08.015 PubMedCentralCrossRefPubMedGoogle Scholar
  21. Kotrschal A, Taborsky B (2010) Environmental change enhances cognitive abilities in fish. PLoS Biol 8:e1000351. doi: 10.1371/journalpbio.1000351 PubMedCentralCrossRefPubMedGoogle Scholar
  22. Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480. doi: 10.1016/S0959-4388(00)00237-3 CrossRefPubMedGoogle Scholar
  23. Maille A, Schradin C (submitted) Eco-physiology of cognition: How environmentally-induced changes in physiology affect cognitive performance? Biol RevGoogle Scholar
  24. McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol 156:1–18. doi: 10.1016/j.cbpa.2010.01.002 CrossRefPubMedGoogle Scholar
  25. Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233CrossRefGoogle Scholar
  26. Pillay N, Rymer TL (2015) Alloparenting enhances the emotional, social and cognitive performance of female African striped mice, Rhabdomys pumilio. Anim Behav 99:43–52. doi: 10.1016/j.anbehav.2014.10.003 CrossRefGoogle Scholar
  27. Popović N, Madrid JA, Rol MÁ et al (2010) Barnes maze performance of Octodon degus is gender dependent. Behav Brain Res 212:159–167. doi: 10.1016/j.bbr.2010.04.005 CrossRefPubMedGoogle Scholar
  28. Pravosudov VV, Clayton NS (2001) Effects of demanding foraging conditions on cache retrival accuracy in food-caching mountain chickadees (Poecile gambeli). Proc Biol Sci 268:363–368. doi: 10.1098/rspb.2000.1401 PubMedCentralCrossRefPubMedGoogle Scholar
  29. Pyter LM, Trainor BC, Nelson RJ (2006) Testosterone and photoperiod interact to affect spatial learning and memory in adult male white-footed mice (Peromyscus leucopus). Eur J Neurosci 23:3056–3062. doi: 10.1111/j.1460-9568.2006.04821.x CrossRefPubMedGoogle Scholar
  30. Raynaud J, Schradin C (2013) Regulation of male prolactin levels in an opportunistically breeding species, the African striped mouse. J Zool 290:287–292. doi: 10.1111/jzo.12040 CrossRefGoogle Scholar
  31. Rodriguiz RM, Wetsel WC (2006) Assessments of cognitive deficits in mutant mice. In: Levin ED, Buccafusco JJ (eds) Animal models of cognitive impairement. CRC Press, Boca Raton (FL), pp 223–280Google Scholar
  32. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24. doi: 10.1016/S0016-6480(02)00064-3 CrossRefPubMedGoogle Scholar
  33. Rosch H (2001) The identification and description of the management units of the Goegap Nature Reserve. Koedoe 44:17–30CrossRefGoogle Scholar
  34. Roth TC, Brodin A, Smulders TV et al (2010) Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus. Philos Trans R Soc B 365:915–931. doi: 10.1098/rstb.2009.0208 CrossRefGoogle Scholar
  35. Rymer T, Schradin C, Pillay N (2008) Social transmission of information about novel food in two populations of the African striped mouse, Rhabdomys pumilio. Anim Behav 76:1297–1304. doi: 10.1016/j.anbehav.2008.06.014 CrossRefGoogle Scholar
  36. Scantlebury M, Bennett NC, Speakman JR, Pillay N, Schradin C (2006) Huddling in groups leads to daily energy savings in free-living African four-striped grass mice, Rhabdomys pumilio. Funct Ecol 20:166–173CrossRefGoogle Scholar
  37. Scantlebury M, Krackow S, Pillay N, Bennett N, Schradin C (2010) Basking is affected by season and influences oxygen consumption in desert-living striped mice. J Zool 281:132–139CrossRefGoogle Scholar
  38. Schradin C (2006) Whole-day follows of striped mice (Rhabdomys pumilio), a diurnal murid rodent. J Ethol 24:37–43. doi: 10.1007/s10164-005-0158-2 CrossRefGoogle Scholar
  39. Schradin C, Pillay N (2005) Demography of the striped mouse (Rhabdomys pumilio) in the succulent karoo. Mammalian Biology-Zeitschrift für Säugetierkunde 70:84–92. doi: 10.1016/j.mambio.2004.06.004 CrossRefGoogle Scholar
  40. Schradin C, Pillay N (2006) Female striped mice (Rhabdomys pumilio) change their home ranges in response to seasonal variation in food availability. Behav Ecol 17:452–458. doi: 10.1093/beheco/arj047 CrossRefGoogle Scholar
  41. Schradin C, Krackow S, Schubert M et al (2007) Regulation of activity in desert-living striped mice: the importance of basking. Ethology 113:606–614CrossRefGoogle Scholar
  42. Sherry DF, Hoshooley JS (2009) The seasonal hippocampus of food-storing birds. Behav Process 80:334–338. doi: 10.1016/j.beproc.2008.12.012 CrossRefGoogle Scholar
  43. Solianik R, Skurvydas A, Mickevičienė D, Brazaitis M (2014) Intermittent whole-body cold immersion induces similar thermal stress but different motor and cognitive responses between males and females. Cryobiology 69:323–332. doi: 10.1016/j.cryobiol.2014.08.007 CrossRefPubMedGoogle Scholar
  44. Solmsen N, Johannesen J, Schradin C (2011) Highly asymmetric fine-scale genetic structure between sexes of African striped mice and indication for condition dependent alternative male dispersal tactics. Mol Ecol 20:1624–1634. doi: 10.1111/j.1365-294X.2011.05042.x CrossRefPubMedGoogle Scholar
  45. Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251–258. doi: 10.1016/S0166-2236(00)01558-7 CrossRefPubMedGoogle Scholar
  46. Yanai S, Okaichi Y, Okaichi H (2004) Long-term dietary restriction causes negative effects on cognitive functions in rats. Neurobiol Aging 25:325–332. doi: 10.1016/S0197-4580(03)00115-5 CrossRefPubMedGoogle Scholar
  47. Yaskin VA (2011) Seasonal changes in hippocampus size and spatial behaviour in mammals and birds. Biol Bull Rev 1:279–288. doi: 10.1134/S2079086411030108 CrossRefGoogle Scholar
  48. Yaskin VA (2013) Seasonal modulation of sex-related differences in hippocampus size and spatial behaviour in bank voles, Clethrionomys glareolus (Rodentia, Cricetidae). Russ J Ecol 44:221–226. doi: 10.1134/S1067413613030156 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Audrey Maille
    • 1
    • 2
    • 3
    Email author
  • Neville Pillay
    • 3
  • Carsten Schradin
    • 1
    • 2
    • 3
    • 4
  1. 1.UMR 7178CNRSStrasbourgFrance
  2. 2.IPHC-DEPEUniversité de StrasbourgStrasbourgFrance
  3. 3.School of Animal, Plant and Environmental SciencesUniversity of the WitwatersrandJohannesburgSouth Africa
  4. 4.University of Strasbourg Institute for Advanced Study (USIAS)StrasbourgFrance

Personalised recommendations