Repeatability and Consistency of Individual Behaviour in Juvenile and Adult Eurasian Harvest Mice

Sci Nat (2017) 104:10 DOI 10.1007/s00114-017-1430-3 ORIGINAL PAPER Repeatability and consistency of individual behaviour in juvenile and adult Eurasian harvest mice Andrea C. Schuster1 & Teresa Carl 1 & Katharina Foerster1 Received: 10 May 2016 /Revised: 9 January 2017 /Accepted: 11 January 2017 # The Author(s) 2017. This article is published with open access at Springerlink.com Abstract Knowledge on animal personality has provided in cognitive performance, and in its relationship to animal new insights into evolutionary biology and animal ecology, personality, we suggest that it is important to gather more data as behavioural types have been shown to affect fitness. on the repeatability and consistency of cognitive traits. Animal personality is characterized by repeatable and consistent between-individual behavioural differences throughout Keywords Animal personality . Repeatability . Consistency . time and across different situations. Behavioural repeatability Spatialcognition .Eurasianharvestmouse .Micromysminutus within life history stages and consistency between life history stages should be checked for the independence of sex and age, as recent data have shown that males and females in some Introduction species may differ in the repeatability of behavioural traits, as well as in their consistency. We measured the repeatability Over the last decades, the interest in individual variation in and consistency of three behavioural and one cognitive traits behaviour within animal species has increased rapidly. in juvenile and adult Eurasian harvest mice (Micromys Consistent between-individual differences in behaviours, minutus). We found that exploration, activity and boldness known as animal personality, coping styles or behavioural were repeatable in juveniles and adults. Spatial recognition syndromes (Koolhaas et al. 1999;Sihetal.2004; Réale measured in a Y Maze was only repeatable in adult mice. et al. 2007), have been analysed in all main animal taxa to Exploration, activity and boldness were consistent before date. This is due to the relevance of animal personality as an and after maturation, as well as before and after first sexual important component of animal ecology and its effects on contact. Data on spatial recognition provided little evidence fitness (Thomas et al. 2016). In wild populations, animal per- for consistency. Further, we found some evidence for a litter sonality could be linked to differences in reproductive success effect on behaviours by comparing different linear mixed (Reale et al. 2000;Bothetal.2005), parental care (Budaev models. We concluded that harvest mice express animal per- et al. 1999) and survival (Dingemanse et al. 2004;Boonetal. sonality traits as behaviours were repeatable across sexes and 2007), and even to different life history strategies (e.g. Vetter consistent across life history stages. The tested cognitive trait et al. 2016). Animal personality is specified as consistent showed low repeatability and was less consistent across life between-individual behavioural differences throughout time history stages. Given the rising interest in individual variation and across situations (Réale et al. 2007). In many species, individuals behave repeatably when tested in the same behav- Communicated by: Paul Tyler ioural test more than once. In a meta-analysis, the mean repeatability value was 0.37 (reviewed by Bell et al. 2009). In * Andrea C. Schuster general, the term repeatability is used when assessing the ac- [email protected] curacy of specific measurements (Nakagawa and Schielzeth 2010). In animal personality research, repeatability specifies the proportion of between-individual variance relative to the 1 Department of Comparative Zoology, Institute for Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 28, total phenotypic variance in a population for repeated mea- 72076 Tübingen, Germany sures of the same behaviour (Dingemanse et al. 2010). 10 Page 2 of 14 Sci Nat (2017) 104:10 The repeatability of a specific behaviour is usually calcu- Réale et al. (2007) proposed measuring animal personality lated based on repeated observations in the same context and based on five behavioural traits that confer non-overlapping life history phase. Repeatability estimates from observations information on an animal’s behaviour and have been shown to across contexts or life history phases have also been reported affect fitness-relevant traits in a number of species: boldness, as Brepeatability^, but the alternative terms, cross-context re- activity, exploration, sociability and aggression. We here in- peatability (e.g. Laskowski and Bell 2013) or consistency (e.g. vestigated three of these traits in Eurasian harvest mice, as we Wuerz and Krüger 2015), allow us to better specify the differ- considered them of particular interest in this solitary species ent information content of these estimates. The proportion of (see also below): boldness (the tendency of an individual to between-individual variance among measurements from dif- take risks), activity (the general activity level of an individual) ferent contexts or life history phases characterizes the stability and exploration (an individual’s reaction to a new situation, of individual behaviour across a longer time interval or across for instance, novel objects or novel environments; see also changes in the environment. We here restrict the use of the Réale et al. 2007). Exploration was a consistent trait over a term repeatability to estimates of the proportion of between- significant part of an individual’s lifetime in great tits (Parus individual variance from observations within the same life major; Dingemanse et al. 2002) and zebra finches history phase. We define consistency of behavioural traits as (Taeniopygia guttata; David et al. 2012). But while boldness, the proportion of between-individual variance from observa- exploration and activity were repeatable behavioural traits tions at different ontogenetic stages. We use the term person- over short periods of time in small rodents (e.g. Koolhaas ality trait for behavioural traits that are repeatable and consis- et al. 1999; Boon et al. 2007; Lantova et al. 2011; Petelle tent and can hence contribute to animal personality. A behav- et al. 2013), only activity seemed to be consistent across life ioural type is characterized by a particular combination of trait history stages in that group (e.g. Kanda et al. 2012; Herde and expressions in two or more personality traits (Bell 2007). Eccard 2013;butseeGuentheretal.2014). There is growing evidence that behavioural syndromes can Behavioural repeatability within, but no consistency across be less stable across lifetimes than previously assumed (Wuerz life history, phases can arise from developmental changes (see and Krüger 2015; Fischer et al. 2016; but see Gyuris et al. above). However, a simulation study showed that life history 2012). Developmental changes could reveal that underlying trade-offs can promote the evolution of behavioural types that mechanisms of animal personalities (Stamps and Groothuis are specific to particular life history phases (Wolf et al. 2007). 2010b; Trillmich and Hudson 2011) as different experiences Empirical data provided evidence that the level of boldness during development can shape behavioural types. Also, the can vary between individuals depending on expected future hormonal constitution undergoes considerable change during reproductive success: in grey mouse lemurs (Microcebus the phase of vertebrate maturation, and this is likely to influ- murinus), young males had low current but high expected ence individual behavioural consistency (Stamps and future reproductive success, while the opposite was true in Groothuis 2010a). Bell et al. (2009) already suggested to an- older males (Dammhahn 2012). Hence, the trade-off between alyse repeatable behaviours between different age classes the investment into current and future reproduction differed within species to investigate the potential impact of age and between age classes. Dammhahn (2012) found that young individual (sexual) experience on the repeatability and consis- male mouse lemurs were shyer than older males. She hypoth- tency of behavioural traits. Although their meta-analysis could esized that selection favoured young mouse lemurs that ex- not detect any differences in the repeatability of behaviours hibited less risky behaviour because of the expected future between juveniles and adults (Bell et al. 2009), a recent review fitness payoff, while older mouse lemurs benefitted most from by Brommer and Class (2015) reported evidence for lower (also risky) investments into the current reproductive effort. A behavioural repeatability in juveniles. Changes in behavioural trade-off between reproductive states may thus maintain ani- repeatability and consistency across the life history do not mal personality variation in this species (Dammhahn 2012). contradict the existence of animal personality. They rather The repeatability and consistency of behavioural traits can highlight the necessity to investigate personality traits across also differ between the sexes (Schuett et al. 2010). In the different life history phases to fully understand when and how abovementioned grey mouse lemurs, males were, on average, animal personality arises and how long it persists. Recently, bolder than females and boldness was more repeatable in experiments have in fact shown that animal personality (based males than in females (Dammhahn 2012). Schuett

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