Abstract
The pace-of-life syndrome (POLS) theory provides an evolutionary explanation for the existence of consistent among-individual variation in behaviour, or animal personality. Herein, individuals with a fast lifestyle are considered to be bolder and should take more risks resulting in a lower life expectancy compared to shyer individuals with a slower lifestyle. However, this assumption depends on the levels of intra-specific competition that the individuals experience which has rarely been tested in species that experience large changes in competition on a very short time scale. We used the multimammate mice (Mastomys natalensis) as a model system to study the POLS assumption by investigating the effects of two personality traits (exploration and stress-sensitivity) on survival, maturation (a proxy for reproductive investment) and recapture probability during one population cycle (Nindividuals = 201). Such a cycle consists of two phases in which the levels of intra-specific competition vary drastically. We found that only one personality trait, namely stress-sensitivity, had a negative effect on both survival and recapture probability but none of them affected maturation. This suggests that less stress-sensitive individuals take more risks in the wild and have a higher survival probability compared to high stress-sensitive individuals. However, the effect of personality on survival was only present during the population decrease phase, when the levels of intra-specific competition are high due to a scarcity of food. This suggests that seasonal changes in competition might be important in the evolution and maintenance of animal personalities in species whose population dynamics have a clear seasonal component.
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References
Ademola OJ, Vanden Broecke B, Leirs H et al (2021) Effects of forest disturbance on the fitness of an endemic rodent in a biodiversity hotspot. Ecol Evol 11:2391–2401. https://doi.org/10.1002/ece3.7214
Andreassen HP, Sundell J, Ecke F et al (2020) Population cycles and outbreaks of small rodents: ten essential questions we still need to solve. Oecologia. https://doi.org/10.1007/s00442-020-04810-w
Araya-Ajoy YG, Bolstad GH, Brommer J et al (2018) Demographic measures of an individual’s “pace of life”: fecundity rate, lifespan, generation time, or a composite variable? Behav Ecol Sociobiol 72:75. https://doi.org/10.1007/s00265-018-2477-7
Barber I, Dingemanse NJ (2010) Parasitism and the evolutionary ecology of animal personality. Philos Trans R Soc B 365:4077–4088. https://doi.org/10.1098/rstb.2010.0182
Bergeron P, Montiglio P-O, Réale D et al (2013) Disruptive viability selection on adult exploratory behaviour in eastern chipmunks. J Evol Biol 26:766–774. https://doi.org/10.1111/jeb.12081
Bergvall UA, Schäpers A, Kjellander P, Weiss A (2011) Personality and foraging decisions in fallow deer, Dama dama. Anim Behav 81:101–112. https://doi.org/10.1016/j.anbehav.2010.09.018
Biro PA (2013) Are most samples of animals systematically biased? Consistent individual trait differences bias samples despite random sampling. Oecologia 171:339–345. https://doi.org/10.1007/s00442-012-2426-5
Borremans B, Hughes NK, Reijniers J et al (2014) Happily together forever: temporal variation in spatial patterns and complete lack of territoriality in a promiscuous rodent. Popul Ecol 56:109–118. https://doi.org/10.1007/s10144-013-0393-2
Borremans B, Sluydts V, Makundi RH, Leirs H (2015) Evaluation of short-, mid- and long-term effects of toe clipping on a wild rodent. Wildl Res 42:143. https://doi.org/10.1071/WR14109
Boyer N, Réale D, Marmet J et al (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
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
Burnham KP, Anderson DR (2004) Model selection and multimodel inference. Springer New York, New York
Carere C, Maestripieri D (2013) Animal personalities: behavior, physiology, and evolution. University of Chicago Press, Chicago
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
Carter AJ, Feeney WE, Marshall HH et al (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475. https://doi.org/10.1111/brv.12007
Choquet R, Lebreton J-D, Gimenez O et al (2009a) U-CARE: utilities for performing goodness of fit tests and manipulating CApture-REcapture data. Ecography (Cop) 32:1071–1074. https://doi.org/10.1111/j.1600-0587.2009.05968.x
Choquet R, Rouan L, Pradel R (2009b) Program E-surge: a software application for fitting multievent models. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling Demographic Processes in marked populations. Springer US, Boston, pp 845–865
Dammhahn M, Almeling L (2012) Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim Behav 84:1131–1139. https://doi.org/10.1016/j.anbehav.2012.08.014
Dammhahn M, Dingemanse NJ, Niemelä PT, Réale D (2018) Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav Ecol Sociobiol 72:62. https://doi.org/10.1007/s00265-018-2473-y
Dhellemmes F, Finger J, Smukall MJ et al (2020) Personality-driven life history trade-offs differ in two subpopulations of free-ranging predators. J Anim Ecol 1365–2656:13283. https://doi.org/10.1111/1365-2656.13283
Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc London Ser B Biol Sci 271:847–852. https://doi.org/10.1098/rspb.2004.2680
Dingemanse NJ, Wright J, Kazem AJN et al (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138. https://doi.org/10.1111/j.1365-2656.2007.01284.x
Dingemanse NJ, Moiron M, Araya-Ajoy YG et al (2020) Individual variation in age-dependent reproduction: fast explorers live fast but senesce young? J Anim Ecol 89:601–613. https://doi.org/10.1111/1365-2656.13122
Dougherty LR, Guillette LM (2018) Linking personality and cognition: a meta-analysis. Philos Trans R Soc B Biol Sci 373:20170282. https://doi.org/10.1098/rstb.2017.0282
Eccard JA, Herde A (2013) Seasonal variation in the behaviour of a short-lived rodent. BMC Ecol 13:43. https://doi.org/10.1186/1472-6785-13-43
File SE, Wardill AG (1975) Validity of head-dipping as a measure of exploration in a modified hole-board. Psychopharmacologia 44:53–59. https://doi.org/10.1007/BF00421184
Frame JD, Baldwin JM, Gocke DJ, Troup JM (1970) Lassa fever, a new virus disease of man from West Africa. I. Clinical description and pathological findings. Am J Trop Med Hyg 19:670–676
Garamszegi LZ, Eens M, Török J (2009) Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim Behav 77:803–812. https://doi.org/10.1016/j.anbehav.2008.12.012
Gelman A, Su Y-S, Yajima M, et al (2020) arm: data analysis using regression and multilevel/hierarchical models. R package version 1.11–2. https://CRAN.R-project.org/package=arm
Getz LL, Hofmann JE, McGuire B, Dolan TW III (2001) Twenty-five years of population fluctuations of Microtus ochrogaster and M. pennsylvanicus in three habitats in East-Central Illinois. J Mammal 82:22–34. https://doi.org/10.1644/1545-1542(2001)082%3c0022:TFYOPF%3e2.0.CO;2
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
Hadfield JD, Wilson AJ, Garant D et al (2010) The misuse of BLUP in ecology and evolution. Am Nat 175:116–125. https://doi.org/10.1086/648604
Hämäläinen A, Immonen E, Tarka M, Schuett W (2018) Evolution of sex-specific pace-of-life syndromes: causes and consequences. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-018-2466-x
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
Jolly CJ, Webb JK, Gillespie GR et al (2019) Bias averted: personality may not influence trappability. Behav Ecol Sociobiol 73:129. https://doi.org/10.1007/s00265-019-2742-4
Kennis J, Sluydts V, Leirs H, van Hooft WFP (2008) Polyandry and polygyny in an African rodent pest species, Mastomys natalensis. Mammalia 72:150–160. https://doi.org/10.1515/MAMM.2008.025
Krebs CJ (1970) Microtus population biology: behavioral changes associated with the population cycle in M. Ochrogaster and M Pennsylvanicus Ecology 51:34–52. https://doi.org/10.2307/1933598
Krebs CJ (2013) Population fluctuations in rodents. The University of Chicago Press, Chicago
Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model.’ Philos Trans R Soc London Ser B Biol Sci 359:873–890. https://doi.org/10.1098/rstb.2003.1437
Le Cœur C, Thibault M, Pisanu B et al (2015) Temporally fluctuating selection on a personality trait in a wild rodent population. Behav Ecol 26:1285–1291. https://doi.org/10.1093/beheco/arv074
Le Galliard J-F, Paquet M, Mugabo M (2015) An experimental test of density-dependent selection on temperament traits of activity, boldness and sociability. J Evol Biol 28:1144–1155. https://doi.org/10.1111/jeb.12641
Lebreton JD, Pradel R (2002) Multistate recapture models: modelling incomplete individual histories. J Appl Stat 29:353–369. https://doi.org/10.1080/02664760120108638
Leirs H, Stuyck J, Verhagen R, Verheyen W (1990) Seasonal variation in growth of Mastomys natalensis (Rodentia: Muridae) in Morogoro, Tanzania. Afr J Ecol 28:298–306. https://doi.org/10.1111/j.1365-2028.1990.tb01164.x
Leirs H, Verhagen R, Verheyen W (1993) Productivity of different generations in a population of Mastomys natalensis rats in Tanzania. Oikos 68:53–60
Leirs H, Verhagen R, Verheyen W (1994) The basis of reproductive seasonality in Mastomys rats (Rodentia: Muridae) in Tanzania. J Trop Ecol 10:55–66
Leirs H, Stenseth NC, Nichols JD et al (1997) Stochastic seasonality and nonlinear density-dependent factors regulate population size in an African rodent. Nature 389:176–180. https://doi.org/10.1038/38271
Mariën J, Sluydts V, Borremans B et al (2018) Arenavirus infection correlates with lower survival of its natural rodent host in a long-term capture-mark-recapture study. Parasit Vectors 11:90. https://doi.org/10.1186/s13071-018-2674-2
Martin JGA, 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
Mathot KJ, Frankenhuis WE (2018) Models of pace-of-life syndromes (POLS): a systematic review. Behav Ecol Sociobiol 72:41. https://doi.org/10.1007/s00265-018-2459-9
Mayamba A, Vanden BB, Leirs H et al (2020) Fitness of the pestiferous small rodent Mastomys natalensis in an agroecosystem in Mayuge district, Lake Victoria Crescent, Uganda. Mammalia 84:344–353. https://doi.org/10.1515/mammalia-2019-0101
Mella VSA, Ward AJW, Banks PB, McArthur C (2015) Personality affects the foraging response of a mammalian herbivore to the dual costs of food and fear. Oecologia 177:293–303. https://doi.org/10.1007/s00442-014-3110-8
Michelangeli M, Wong BBM, 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
Millar AJS, Hickling GJ (1990) Fasting endurance and the evolution of mammalian body size. Funct Ecol 4:5–12
Mlyashimbi ECM, Mariën J, Kimaro DN et al (2018) Relationships between seasonal changes in diet of Multimammate rat ( Mastomys natalensis ) and its breeding patterns in semi-arid areas in Tanzania. Cogent Food Agric 4:1507509. https://doi.org/10.1080/23311932.2018.1507509
Mlyashimbi ECM, Vanden Broecke B, Mariën J et al (2019) Soil type influences population dynamics and survival of the Multimammate rat (Mastomys natalensis) in semi-arid areas in Tanzania. Crop Prot. https://doi.org/10.1016/j.cropro.2019.05.023
Moiron M, Laskowski KL, Niemelä PT (2020) Individual differences in behaviour explain variation in survival: a meta-analysis. Ecol Lett 23:399–408. https://doi.org/10.1111/ele.13438
Montiglio P-O, Garant D, Thomas D, Réale D (2010) Individual variation in temporal activity patterns in open-field tests. Anim Behav 80:905–912. https://doi.org/10.1016/j.anbehav.2010.08.014
Montiglio P-O, Garant D, Pelletier F, Réale D (2012) Personality differences are related to long-term stress reactivity in a population of wild eastern chipmunks, Tamias striatus. Anim Behav 84:1071–1079. https://doi.org/10.1016/j.anbehav.2012.08.010
Montiglio P-O, Dammhahn M, Dubuc Messier G, Réale D (2018) The pace-of-life syndrome revisited: the role of ecological conditions and natural history on the slow-fast continuum. Behav Ecol Sociobiol 72:116. https://doi.org/10.1007/s00265-018-2526-2
Mulungu LS, Mahlaba TA, Massawe AW et al (2011) Dietary differences of the multimammate mouse, Mastomys natalensis (Smith, 1834), across different habitats and seasons in Tanzania and Swaziland. Wildl Res 38:640–646. https://doi.org/10.1071/WR11028
Mulungu LS, Mlyashimbi ECM, Ngowo V et al (2014) Food preferences of the multi-mammate mouse, Mastomys natalensis, in irrigated rice habitats in Tanzania. Int J Pest Manag 60:1–8. https://doi.org/10.1080/09670874.2013.871759
Myers JH (2018) Population cycles: generalities, exceptions and remaining mysteries. Proc R Soc B Biol Sci 285:20172841. https://doi.org/10.1098/rspb.2017.2841
Nicolaus M, Tinbergen JM, Ubels R et al (2016) Density fluctuations represent a key process maintaining personality variation in a wild passerine bird. Ecol Lett 19:478–486. https://doi.org/10.1111/ele.12584
Odhiambo RO, Makundi RH, Leirs H, Verhagen R (2008) Dietary selection in Mastomys natalensis (Rodentia: Muridae) in the maize agro-ecosystems of central and southwestern Tanzania. Mammalia 72:169–177. https://doi.org/10.1515/MAMM.2008.007
Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer New York, New York
Pogány Á, Vincze E, Szurovecz Z et al (2018) Personality assortative female mating preferences in a songbird. Behaviour 155:481–503. https://doi.org/10.1163/1568539X-00003500
Pollock KH (1982) A capture-recapture design robust to unequal probability of capture. J Wildl Manage 46:752–757. https://doi.org/10.2307/3808568
Pradel R (2005) Multievent: an extension of multistate capture-recapture models to uncertain states. Biometrics 61:442–447. https://doi.org/10.1111/j.1541-0420.2005.00318.x
Pradel R, Sanz-Aguilar A (2012) Modeling trap-awareness and related phenomena in capture-recapture studies. PLoS ONE 7:e32666. https://doi.org/10.1371/journal.pone.0032666
Pradel R, Wintrebert CMA, Gimenez O (2003) A proposal for a goodness-of-fit test to the Arnason-Schwarz multisite capture-recapture model. Biometrics 59:43–53
Réale D, Reader SM, Sol D et al (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318. https://doi.org/10.1111/j.1469-185X.2007.00010.x
Réale D, Garant D, Humphries MM et al (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B Biol Sci 365:4051–4063. https://doi.org/10.1098/rstb.2010.0208
Rödel HG, Zapka M, Talke S et al (2015) Survival costs of fast exploration during juvenile life in a small mammal. Behav Ecol Sociobiol 69:205–217. https://doi.org/10.1007/s00265-014-1833-5
Royauté R, Berdal MA, Garrison CR, Dochtermann NA (2018) Paceless life? A meta-analysis of the pace-of-life syndrome hypothesis. Behav Ecol Sociobiol 72:64. https://doi.org/10.1007/s00265-018-2472-z
Santicchia F, Gagnaison C, Bisi F et al (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
Santicchia F, Van Dongen S, Martinoli A et al (2020) Measuring personality traits in Eurasian red squirrels: a critical comparison of different methods. Ethology 00:1–15. https://doi.org/10.1111/eth.13117
Schuett W, Tregenza T, Dall SRX (2010) Sexual selection and animal personality. Biol Rev 85:217–246. https://doi.org/10.1111/j.1469-185X.2009.00101.x
Sluydts V, Crespin L, Davis S et al (2007) Survival and maturation rates of the African rodent, Mastomys natalensis: density-dependence and rainfall. Integr Zool 2:220–232. https://doi.org/10.1111/j.1749-4877.2007.00065.x
Sluydts V, Davis S, Mercelis S, Leirs H (2009) Comparison of multimammate mouse (Mastomys natalensis) demography in monoculture and mosaic agricultural habitat: Implications for pest management. Crop Prot 28:647–654. https://doi.org/10.1016/j.cropro.2009.03.018
Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455. https://doi.org/10.1093/beheco/arm144
Smolinsky AN, Bergner CL, LaPorte JL, Kalueff AV (2009) Analysis of grooming behavior and its utility in studying animal stress, anxiety, and depression. In: Gould TD (ed) Mood and anxiety related phenotypes in mice. Humana Press, Totowa, pp 21–36
Stuber EF, Araya-Ajoy YG, Mathot KJ et al (2013) Slow explorers take less risk: a problem of sampling bias in ecological studies. Behav Ecol 24:1092–1098. https://doi.org/10.1093/beheco/art035
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
Vanden Broecke B, Borremans B, Mariën J et al (2018) Does exploratory behavior or activity in a wild mouse explain susceptibility to virus infection? Curr Zool 64:585–592. https://doi.org/10.1093/cz/zox053
Vanden Broecke B, Mariën J, Sabuni CA et al (2019) Relationship between population density and viral infection: a role for personality? Ecol Evol 9:10213–10224. https://doi.org/10.1002/ece3.5541
Vanden Broecke B, Bongers A, Mnyone L et al (2021) Nonlinear maternal effects on personality in a rodent species with fluctuating densities. Curr Zool 67:1–9. https://doi.org/10.1093/cz/zoaa032
Ward AJW, Thomas P, Hart PJB, Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 55:561–568. https://doi.org/10.1007/s00265-003-0751-8
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139. https://doi.org/10.1080/00063659909477239
Wilson ADM, Binder TR, McGrath KP et al (2011) Capture technique and fish personality: angling targets timid bluegill sunfish, Lepomis macrochirus. Can J Fish Aquat Sci 68:749–757. https://doi.org/10.1139/f2011-019
Wright J, Bolstad GH, Araya-Ajoy YG, Dingemanse NJ (2019) Life-history evolution under fluctuating density-dependent selection and the adaptive alignment of pace-of-life syndromes. Biol Rev 94:230–247. https://doi.org/10.1111/brv.12451
Ziwa MH, Matee MI, Kilonzo BS, Hang’ombe BM (2013) Evidence of Yersinia pestis DNA in rodents in plague outbreak foci in Mbulu and Karatu Districts, northern Tanzania. Tanzan J Health Res 15:1–8. https://doi.org/10.4314/thrb.v15i3.1
Acknowledgements
We would like to that the staff at the Pest Management Center (Sokoine University of Agriculture) for their excellent assistance during the fieldwork, specifically Shabani Lutea, Goefrey Sabuni, Omary Kibwana, Baraka Edson, Maddy Wheatley, Aurelia Bongers and Steven Van den Panhuyzen. Special thanks to Bert Thys for his assistance during the whole process.
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BVB was funded by the Ph.D. fellowship from the Research Foundation Flanders (FWO) (Grant ID: 11A0817N).
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BVB, JM, AM, EM and HL conceived and designed the study. BVB collected the data with the support of JM, CAS and AM. BVB and VS performed the data analysis with input from JM, EM and HL. The first draft was written by BVB and all authors contributed substantially to revisions.
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All experimental procedures were approved by the University of Antwerp Ethical Committee for Animal Experimentation (LA1100135) and adhered to the EEC Council Directive 2010/63/EU and followed the Animal Ethics guidelines of the Research Policy of Sokoine University of Agriculture.
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Vanden Broecke, B., Sluydts, V., Mariën, J. et al. The effects of personality on survival and trappability in a wild mouse during a population cycle. Oecologia 195, 901–913 (2021). https://doi.org/10.1007/s00442-021-04897-9
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DOI: https://doi.org/10.1007/s00442-021-04897-9