Personality and behavioral syndromes in two Peromyscus species: presence, lack of state dependence, and lack of association with home range size

Abstract

One common theme of adaptive hypotheses for the existence of stable individual differences in behavior (personality) or persistent correlations among behaviors (behavioral syndromes) is an association between intrinsic state (e.g., body size, mass, metabolism) and the behavioral traits of interest. Empiricists are tasked with assessing whether there is an association between intrinsic state and behavior, but the statistical methods to appropriately quantify the among-individual correlation between intrinsic state and behavior have only recently become widely known. We conducted a multiyear study in wild mice of two Peromyscus species (Peromyscus leucopus noveboracensis and Peromyscus maniculatus gracilis) to assess the existence of stable individual differences in four different behaviors (presence of animal personality, as assessed by quantifying repeatabilities) and one measure of intrinsic state (body mass), the degree of association between these four behaviors (presence of behavioral syndromes), and the association of these behavioral traits with body mass using multivariate methods that allowed us to estimate the within-individual (residual) component and the among-individual component. We used standardized behavioral tests to measure struggle time (time spent struggling when removed from the trap) and exploration time (time spent exploring a novel surface) and used open-field trials to measure whether or not an individual entered the open field plus the total time it spent active in the open field. In P. leucopus, we assessed whether coarse but quick methods of assessing animal personality (struggle or exploration time) correlate with behavior using more in-depth estimates obtained by open-field trials. Additionally, we tested the ecological relevance of our personality measures by assessing their association with home range size in P. leucopus. In both species, struggle time, exploration time, and body mass were significantly repeatable and there was a significant among-individual correlation between struggle time and exploration time. However, in both species, there was no evidence for an among-individual correlation between our measure of intrinsic state (body mass) and personality traits. In one species (P. leucopus), we found that individuals that spent more time struggling or exploring a novel surface were also more likely to emerge into an open field and spent more time being active in an open field, but these four behavioral measures were not associated with home range size. Our results suggest among-individual correlation among these different behaviors but no among-individual correlation between behavior and intrinsic state.

Significance statement

Over the past 15 years, it has become clear that nonhuman animals exhibit “personalities”: some individuals consistently differ in their behavior, and there is limited flexibility in their behavior when they experience environmental change. Biologists have now been searching for why and how animal personalities exist and their ecological and evolutionary consequences. Some explanations have focused on how condition or “internal state” may cause variation in animal personalities. In this study, we show that two species of wild mice exhibit personalities and that their personality traits are associated with one another, in that mice that were less docile were also more active, exploratory, and bold. We then show that their personality traits were not linked with body mass, suggesting a lack of association between internal state and personality. Our results provide important insights into the causes of personality in nonhuman animals.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Data availability

All raw data used in these analyses are available on FigShare account of Ben Dantzer (https://figshare.com/authors/Ben_Dantzer/5903843).

References

  1. Bates D, Maechler M, Bolker B et al (2015) Package ‘lme4’. Convergence 12:2

    Google Scholar 

  2. Baumgartner JM, Hoffman SM (2019) Comparison of the responses of two Great Lakes lineages of Peromyscus leucopus to climate change. J Mammal 100:354–364. https://doi.org/10.1093/jmammal/gyz063

    Article  Google Scholar 

  3. Beckmann C, Biro PA (2013) On the validity of a single (boldness) assay in personality research. Ethology 119:937–947. https://doi.org/10.1111/eth.12137

    Article  Google Scholar 

  4. Bedford NL, Hoekstra HE (2015) The natural history of model organisms: Peromyscus mice as a model for studying natural variation. Elife 4:e06813. https://doi.org/10.7554/eLife.06813

    Article  PubMed Central  Google Scholar 

  5. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783. https://doi.org/10.1016/j.anbehav.2008.12.022

    Article  PubMed  PubMed Central  Google Scholar 

  6. Biro PA, Dingemanse NJ (2009) Sampling bias resulting from animal personality. Trends Ecol Evol 24:66–67 https://doi-org.proxy.lib.umich.edu/10.1016/j.tree.2008.11.001

    Article  Google Scholar 

  7. Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368. https://doi.org/10.1016/j.tree.2008.04.003

    Article  PubMed  PubMed Central  Google Scholar 

  8. Blumstein DT, Daniel JC (2007) Quantifying behavior the Jwatcher way. Sinaeur Associates Inc., Sunderland, MA

    Google Scholar 

  9. Boon AK, Réale D, Boutin S (2007) The interaction between personality, offspring fitness and food abundance in North American red squirrels. Ecol Lett 10:1094–1104. https://doi.org/10.1111/j.1461-0248.2007.01106.x

    Article  PubMed  Google Scholar 

  10. Boon AK, Réale D, Boutin S (2008) Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117:1321–1328. https://doi.org/10.1111/j.0030-1299.2008.16567.x

    Article  Google Scholar 

  11. Boyer N, Réale D, Marmet J, Pisanu B, Chapuis JL (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538–547. https://doi.org/10.1111/j.1365-2656.2010.01659.x

    Article  PubMed  Google Scholar 

  12. Brehm AM, Mortelliti A (2018) Mind the trap: large-scale field experiment shows that trappability is not a proxy for personality. Anim Behav 142:101–112. https://doi.org/10.1016/j.anbehav.2018.06.009

    Article  Google Scholar 

  13. Brehm AM, Mortelliti A, Maynard GA, Zydlewski J (2019) Land use change and the ecological consequences of personality in small mammals. Ecol Lett 22:1387–1395. https://doi.org/10.1111/ele.13324

    Article  PubMed  Google Scholar 

  14. Brehm AM, Tironi S, Mortellitic A (2020) Effects of trap confinement on personality measurements in two terrestrial rodents. PLoS One 15:e0221136. https://doi.org/10.1371/journal.pone.0229220

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Brommer JE (2013) On between-individual and residual (co) variances in the study of animal personality: are you willing to take the “individual gambit”? Behav Ecol Sociobiol 67:1027–1032. https://doi.org/10.1007/s00265-013-1527-4

    Article  Google Scholar 

  16. Brommer JE (2017) Multivariate mixed models in R-MCMCglmm examples. https://github.com/JonBrommer/Multivariate-Mixed-Models-in-R/wiki/MCMCglmm-examples. Accessed 1 May 2020

  17. Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519. https://doi.org/10.1016/j.ecolmodel.2006.03.017

    Article  Google Scholar 

  18. Careau V, Bininda-Emonds ORP, Thomas DW, Réale D, Humphries MM (2009) Exploration strategies map along fast–slow metabolic and life history continua in muroid rodents. Funct Ecol 23:150–156. https://doi.org/10.1111/j.1365-2435.2008.01468.x

    Article  Google Scholar 

  19. Careau V, Thomas D, Pelletier F, Turki L, Landry F, Garant D, Réale D (2011) Genetic correlation between resting metabolic rate and exploratory behaviour in deer mice (Peromyscus maniculatus). J Evol Biol 24:2153–2163. https://doi.org/10.1111/j.1420-9101.2011.02344.x

    CAS  Article  PubMed  Google Scholar 

  20. Carter AJ, Heinsohn R, Goldizen AW, Biro PA (2012) Boldness, trappability and sampling bias in wild lizards. Anim Behav 83:1051–1058. https://doi.org/10.1016/j.anbehav.2012.01.033

    Article  Google Scholar 

  21. Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475. https://doi.org/10.1111/brv.12007

    Article  Google Scholar 

  22. Cooper EB, Taylor RW, Kelley AD, Martinig AR, Boutin S, Humphries MM, Dantzer B, Lane JE, McAdam AG (2017) Personality is correlated with natal dispersal in North American red squirrels (Tamiasciurus hudsonicus). Behaviour 154:939–961. https://doi.org/10.1163/1568539X-00003450

    Article  Google Scholar 

  23. Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc Lond B 277:1571–1579. https://doi.org/10.1098/rspb.2009.2128

    Article  Google Scholar 

  24. Dall SR, Griffith SC (2014) An empiricist guide to animal personality variation in ecology and evolution. Front Ecol Evol 2:3. https://doi.org/10.3389/fevo.2014.00003

    Article  Google Scholar 

  25. Dantzer B (2020a) Data for Tables 1 3 S4 and S5. figshare. Dataset, https://doi.org/10.6084/m9.figshare.13242494.v1

  26. Dantzer B (2020b) Data for Tables 2 and S3. figshare. Dataset, https://doi.org/10.6084/m9.figshare.13242506.v1

  27. Dawson WM (1932) Inheritance of wildness and tameness in mice. Genetics 17:296

    CAS  Article  Google Scholar 

  28. De Villemereuil P, Schielzeth H, Nakagawa S, Morrissey M (2016) General methods for evolutionary quantitative genetic inference from generalized mixed models. Genetics 204:1281–1294. https://doi.org/10.1534/genetics.115.186536

    Article  PubMed  PubMed Central  Google Scholar 

  29. Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behavior 142:1159–1184. https://doi.org/10.1163/156853905774539445

    Article  Google Scholar 

  30. Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Philos Trans R Soc B 365:3947–3958. https://doi.org/10.1098/rstb.2010.0221

    Article  Google Scholar 

  31. Dingemanse NJ, Both C, van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B 270:741–747. https://doi.org/10.1098/rspb.2002.2300

    Article  Google Scholar 

  32. Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 271:847–852. https://doi.org/10.1098/rspb.2004.2680

    Article  Google Scholar 

  33. Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of ‘syndrome deviation’ in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548. https://doi.org/10.1007/s00265-012-1416-2

    Article  Google Scholar 

  34. Dochtermann NA, Jenkins SH (2007) Behavioural syndromes in Merriam's kangaroo rats (Dipodomys merriami): a test of competing hypotheses. Proc R Soc Lond B 274:2343–2349. https://doi.org/10.1098/rspb.2007.0622

    Article  Google Scholar 

  35. Dochtermann NA, Royauté R (2019) The mean matters: going beyond repeatability to interpret behavioural variation. Anim Behav 153:147–150. https://doi.org/10.1016/j.anbehav.2019.05.012

    Article  Google Scholar 

  36. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  37. Duckworth RA (2010) Evolution of personality: developmental constraints on behavioral flexibility. Auk 127:752–758. https://doi.org/10.1525/auk.2010.127.4.752

    Article  Google Scholar 

  38. Duckworth RA, Badyaev AV (2007) Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci USA 104:15017–15022. https://doi.org/10.1073/pnas.0706174104

    CAS  Article  PubMed  Google Scholar 

  39. Feldman M, Ferrandiz-Rovira M, Espelta JM, Muñoz A (2019) Evidence of high individual variability in seed management by scatter-hoarding rodents: does ‘personality’ matter? Anim Behav 150:167–174. https://doi.org/10.1016/j.anbehav.2019.02.009

    Article  Google Scholar 

  40. Forkosh O, Karamihalev S, Roeh S, Alon U, Anpilov S, Touma C, Nussbaumer M, Flachskamm C, Kaplick PM, Shemesh Y, Chen A (2019) Identity domains capture individual differences from across the behavioral repertoire. Nat Neurosci 22:2023–2028. https://doi.org/10.1038/s41593-019-0516-y

    CAS  Article  PubMed  Google Scholar 

  41. Fraser DF, Gilliam JF, Daley MJ, Le AN, Skalski GT (2001) Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. Am Nat 158:124–135. https://doi.org/10.1086/321307

    CAS  Article  PubMed  Google Scholar 

  42. Garamszegi LZ, Herczeg G (2012) Behavioural syndromes, syndrome deviation and the within-and between-individual components of phenotypic correlations: when reality does not meet statistics. Behav Ecol Sociobiol 66:1651–1658. https://doi.org/10.1007/s00265-012-1439-8

    Article  Google Scholar 

  43. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86. https://doi.org/10.1037/0033-2909.127.1.45

    CAS  Article  PubMed  Google Scholar 

  44. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. J Stat Softw 33(2):1–22. http://www.jstatsoft.org/v33/i02/

  45. Hadfield JD, Wilson AJ, Garant D, Sheldon BC, Kruuk LE (2010) The misuse of BLUP in ecology and evolution. Am Nat 175:116–125. https://doi.org/10.1086/648604

    Article  PubMed  Google Scholar 

  46. Harris SM, Descamps S, Sneddon LU, Bertrand P, Chastel O, Patrick SC (2020) Personality predicts foraging site fidelity and trip repeatability in a marine predator. J Anim Ecol 89:68–79. https://doi.org/10.1111/1365-2656.13106

    Article  PubMed  Google Scholar 

  47. Herborn KA, Macleod R, Miles WT, Schofield AN, Alexander L, Arnold KE (2010) Personality in captivity reflects personality in the wild. Anim Behav 79:835–843. https://doi.org/10.1016/j.anbehav.2009.12.026

    Article  Google Scholar 

  48. Hertel AG, Leclerc M, Warren D, Pelletier F, Zedrosser A, Mueller T (2019) Don't poke the bear: using tracking data to quantify behavioural syndromes in elusive wildlife. Anim Behav 147:91–104. https://doi.org/10.1016/j.anbehav.2018.11.008

    Article  Google Scholar 

  49. Holtmann B, Santos ES, Lara CE, Nakagawa S (2017) Personality-matching habitat choice, rather than behavioural plasticity, is a likely driver of a phenotype–environment covariance. Proc R Soc B 284:20170943. https://doi.org/10.1098/rspb.2017.0943

    Article  PubMed  Google Scholar 

  50. Houslay TM, Wilson AJ (2017) Avoiding the misuse of BLUP in behavioural ecology. Behav Ecol 28:948–952. https://doi.org/10.1093/beheco/arx023

    Article  PubMed  PubMed Central  Google Scholar 

  51. Houston AI (2010) Evolutionary models of metabolism, behaviour and personality. Philos Trans R Soc B 365:3969–3975. https://doi.org/10.1098/rstb.2010.0161

    Article  Google Scholar 

  52. Houston A, McNamara J (1999) Models of adaptive behavior. Cambridge University Press, Cambridge, UK

    Google Scholar 

  53. Howard WE, Evans FC (1961) Seeds stored by prairie deer mice. J Mammal 42:260–263. https://doi.org/10.2307/1376847

    Article  Google Scholar 

  54. Huang P, Kimball RT, Mary CMS (2018) Does the use of a multi-trait, multi-test approach to measure animal personality yield different behavioural syndrome results? Behaviour 155:115–150. https://doi.org/10.1163/1568539X-00003480

    Article  Google Scholar 

  55. Jolly CJ, Webb JK, Gillespie GR, Hughes NK, Phillips BL (2019) Bias averted: personality may not influence trappability. Behav Ecol Sociobiol 73:129. https://doi.org/10.1007/s00265-019-2742-4

    Article  Google Scholar 

  56. Jönsson KI (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78:57–66. https://doi.org/10.2307/3545800

    Article  Google Scholar 

  57. Kalcounis-Rueppell MC, Petric R, Marler CA (2018) The bold, silent type: predictors of ultrasonic vocalizations in the genus Peromyscus. Front Ecol Evol 6:198. https://doi.org/10.3389/fevo.2018.00198

    Article  Google Scholar 

  58. Kluen E, Siitari H, Brommer JE (2014) Testing for between individual correlations of personality and physiological traits in a wild bird. Behav Ecol Sociobiol 68:205–213. https://doi.org/10.1007/s00265-013-1635-1

    Article  Google Scholar 

  59. Koolhaas JM, Korte SM, de Boer SF, van der Vegt BJ, van Reenen CG, Hopster H, de Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935. https://doi.org/10.1016/S0149-7634(99)00026-3

    CAS  Article  Google Scholar 

  60. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13

    Article  Google Scholar 

  61. Lapiedra O, Schoener TW, Leal M, Losos JB, Kolbe JJ (2018) Predator-driven natural selection on risk-taking behavior in anole lizards. Science 360:1017–1020. https://doi.org/10.1126/science.aap9289

    CAS  Article  PubMed  Google Scholar 

  62. Laskowski KL, Pearish S, Bensky M, Bell AM (2015) Predictors of individual variation in movement in a natural population of threespine stickleback (Gasterosteus aculeatus). Adv Ecol Res 52:65–90. https://doi.org/10.1016/bs.aecr.2015.01.004

    Article  PubMed  PubMed Central  Google Scholar 

  63. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. https://doi.org/10.1139/z90-092

    Article  Google Scholar 

  64. Luttbeg B, Sih A (2010) Risk, resources and state-dependent adaptive behavioural syndromes. Philos Trans R Soc B 365:3977–3990. https://doi.org/10.1098/rstb.2010.0207

    Article  Google Scholar 

  65. Maiti U, Sadowska ET, ChrzĄścik KM, Koteja P (2019) Experimental evolution of personality traits: open-field exploration in bank voles from a multidirectional selection experiment. Curr Zool 65:375–384. https://doi.org/10.1093/cz/zoy068

    Article  PubMed  Google Scholar 

  66. Martin JG, Réale D (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318. https://doi.org/10.1016/j.anbehav.2007.05.026

    Article  Google Scholar 

  67. Michelangeli M, Wong BB, Chapple DG (2016) It’s a trap: sampling bias due to animal personality is not always inevitable. Behav Ecol 27:62–67. https://doi.org/10.1093/beheco/arv123

    Article  Google Scholar 

  68. Minderman J, Reid JM, Hughes M, Denny MJ, Hogg S, Evans PG, Whittingham MJ (2010) Novel environment exploration and home range size in starlings Sturnus vulgaris. Behav Ecol 21:1321–1329. https://doi.org/10.1093/beheco/arq151

    Article  Google Scholar 

  69. Moscarella RA, Hoffman SMG, Myers P, Yahnke C, Lundrigan BL (2019) Genetic and demographic analysis of invasive Peromyscus leucopus in the northern Great Lakes Region. J Mammal 100:345–353. https://doi.org/10.1093/jmammal/gyz053

  70. Myers P, Lundrigan BL, Kopple BV, Lacey EA (2005) Climate change and the distribution of Peromyscus in Michigan: is global warming already having an impact. In: Lacey EA, Myers P (eds) Mammalian diversification: from chromosomes to phylogeography (a celebration of the career of James L. Patton). University of California Press, Berkeley, pp 101–125

    Google Scholar 

  71. Myers P, Lundrigan BL, Hoffman SM, Haraminac AP, Seto SH (2009) Climate-induced changes in the small mammal communities of the Northern Great Lakes Region. Glob Chang Biol 15:1434–1454. https://doi.org/10.1111/j.1365-2486.2009.01846.x

    Article  Google Scholar 

  72. Niemelä PT, Dingemanse NJ (2018) Meta-analysis reveals weak associations between intrinsic state and personality. Proc R Soc B 285:20172823. https://doi.org/10.1098/rspb.2017.2823

    Article  PubMed  Google Scholar 

  73. Niemelä PT, Lattenkamp EZ, Dingemanse NJ (2015) Personality-related survival and sampling bias in wild cricket nymphs. Behav Ecol 26:936–946. https://doi.org/10.1093/beheco/arv036

    Article  Google Scholar 

  74. Nilsen EB, Pedersen S, Linnell JD (2008) Can minimum convex polygon home ranges be used to draw biologically meaningful conclusions? Ecol Res 23:635–639. https://doi.org/10.1007/s11284-007-0421-9

    Article  Google Scholar 

  75. Perals D, Griffin AS, Bartomeus I, Sol D (2017) Revisiting the open-field test: what does it really tell us about animal personality? Anim Behav 123:69–79. https://doi.org/10.1016/j.anbehav.2016.10.006

    Article  Google Scholar 

  76. van de Pol M, Wright J (2009) A simple method for distinguishing within-versus between-subject effects using mixed models. Anim Behav 77:753–758. https://doi.org/10.1016/j.anbehav.2008.11.006

    Article  Google Scholar 

  77. R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org. Accessed 4 May 2020

  78. Réale D, Gallant BY, Leblanc M, Festa-Bianchet M (2000) Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav 60:589–597. https://doi.org/10.1006/anbe.2000.1530

    Article  PubMed  Google Scholar 

  79. Réale D, Berteaux D, McAdam AG, Boutin S (2003) Lifetime selection on heritable life-history traits in a natural population of red squirrels. Evolution 57:2416–2423. https://doi.org/10.1111/j.0014-3820.2003.tb00253.x

    Article  PubMed  Google Scholar 

  80. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318. https://doi.org/10.1111/j.1469-185X.2007.00010.x

    Article  PubMed  PubMed Central  Google Scholar 

  81. Réale D, Dingemanse NJ, Kazem AJ, Wright J (2010) Evolutionary and ecological approaches to the study of personality. Philos Trans R Soc B 365:3937–3946. https://doi.org/10.1098/rstb.2010.0222

    Article  Google Scholar 

  82. Santicchia F, Gagnaison C, Bisi F, Martinoli A, Matthysen E, Bertolino S, Wauters LA (2018) Habitat-dependent effects of personality on survival and reproduction in red squirrels. Behav Ecol Sociobiol 72:134. https://doi.org/10.1007/s00265-018-2546-y

    Article  Google Scholar 

  83. Sih A, Bell A, Johnson JC (2004a) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. https://doi.org/10.1016/j.tree.2004.04.009

    Article  PubMed  PubMed Central  Google Scholar 

  84. Sih A, Bell AM, Johnson JC, Ziemba RE (2004b) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277. https://doi.org/10.1086/422893

    Article  PubMed  Google Scholar 

  85. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289. https://doi.org/10.1111/j.1461-0248.2011.01731.x

    Article  PubMed  Google Scholar 

  86. Sih A, Mathot KJ, Moiron M, Montiglio PO, Wolf M, Dingemanse NJ (2015) Animal personality and state–behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50–60. https://doi.org/10.1016/j.tree.2014.11.004

    Article  PubMed  Google Scholar 

  87. Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495–502. https://doi.org/10.1006/anbe.2001.1953

    Article  Google Scholar 

  88. Stephens RB, Anderson EM, Wendt SR, Meece JK (2014) Field identification of sympatric Peromyscus leucopus noveboracensis and P. maniculatus gracilis in Wisconsin from external measurements. Am Midl Nat 171:139–146. https://doi.org/10.1674/0003-0031-171.1.139

    Article  Google Scholar 

  89. Stickel LF (1968) Home range and travels. In: King LF (ed) Biology of Peromyscus (Rodentia). American Society of Mammalogy, Stillwater, OK, pp 373–411

    Google Scholar 

  90. Stoffel MA, Nakagawa S, Schielzeth H (2017) rptR: Repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644. https://doi.org/10.1111/2041-210X.12797

    Article  Google Scholar 

  91. Vander Wall SB, Thayer TC, Hodge JS, Beck MJ, Roth JK (2001) Scatter-hoarding behavior of deer mice (Peromyscus maniculatus). West N Am Nat 61:109–113

    Google Scholar 

  92. Villegas-Ríos D, Réale D, Freitas C, Moland E, Olsen EM (2018) Personalities influence spatial responses to environmental fluctuations in wild fish. J Anim Ecol 87:1309–1319. https://doi.org/10.1111/1365-2656.12872

    Article  PubMed  PubMed Central  Google Scholar 

  93. Wey TW, Vrana PB, Mabry KE (2017) Mating system as a possible driver of behavioral diversity in Peromyscus. Behav Ecol Sociobiol 71:163. https://doi.org/10.1007/s00265-017-2392-3

    Article  Google Scholar 

  94. Wilson DS (1998) Adaptive individual differences within single populations. Philos Trans R Soc B 353:199–205. https://doi.org/10.1098/rstb.1998.0202

    Article  Google Scholar 

  95. Wilson DS, Coleman K, Clark AB, Biederman L (1993) Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): An ecological study of a psychological trait. J Comp Psychol 107:250–260. https://doi.org/10.1037/0735-7036.107.3.250

    Article  Google Scholar 

  96. Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26. https://doi.org/10.1111/j.1365-2656.2009.01639.x

    Article  PubMed  Google Scholar 

  97. Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Philos Trans R Soc B 365:3959–3968. https://doi.org/10.1098/rstb.2010.0215

    Article  Google Scholar 

  98. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461. https://doi.org/10.1016/j.tree.2012.05.001

    Article  Google Scholar 

  99. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584. https://doi.org/10.1038/nature05835

    CAS  Article  Google Scholar 

  100. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x

    Article  Google Scholar 

Download references

Acknowledgments

Thanks to Joseph Baumgartner, Abigale Bristol, Modeline Celestine, Daniel Nondorf, Mari Angel Rodriguez, and Francesca Santicchia for helping to collect some of the behavioral data. Thanks to Alisande and David Read, as well as John Russell, who allowed us to study mice on their properties, and to the staffs of the Pigeon River Country State Forest and the Seney National Wildlife Refuge for assistance with sampling. Finally, thanks to two anonymous reviewers and especially to Ned Dochtermann for comments that helped improve this manuscript.

Funding

We appreciate the funding support provided by the University of Michigan (to BD) and Miami University (to SMGH) and the logistical support provided by the University of Michigan Biological Station and University of Michigan Museum of Zoology.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ben Dantzer.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethics approval

All of our trapping and handling procedures were approved by Animal Care and Use Committees of the University of Michigan (#PRO00009067) and Miami University (#874_2021_Mar). We acquired permission to carry out these procedures from areas owned or managed by the University of Michigan (Cheboygan and Livingston Counties), the United States National Forest Service (Chippewa and Delta Counties), the United States Fish and Wildlife Service (Schoolcraft County), the State of Michigan (Menominee and Otsego Counties), or private landowners (Washtenaw County). All applicable international, national, and/or institutional guidelines for the use of animals were followed.

Ethical statement

All data presented are original, have not been fabricated or manipulated, and have not been published previously. All authors have made sufficient contributions to be included as authors and consent to publish the data.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by N. A Dochtermann

Supplementary Information

ESM 1

(DOCX 509 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Underhill, V., Pandelis, G.G., Papuga, J. et al. Personality and behavioral syndromes in two Peromyscus species: presence, lack of state dependence, and lack of association with home range size. Behav Ecol Sociobiol 75, 9 (2021). https://doi.org/10.1007/s00265-020-02951-9

Download citation

Keywords

  • Animal personality,
  • Behavioral syndromes,
  • MCMCglmm,
  • Mice,
  • Pace-of-life