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Juvenile social play predicts docility in Belding’s ground squirrels

Juvenile social play predicts docility in Belding’s ground squirrels We evaluated the hypothesis that social play behavior influences the development of temperament in young animals, using docility as a measure of temperament. We observed the play behavior of juvenile Belding’s ground squirrels (Urocitellus beldingi) during the developmental period in which play primarily occurs and conducted behavioral tests measuring docility at the beginning and toward the end of the play interval. Tests involved handling squirrels and recording their responses. We observed a significant but weak association between body mass and docility at the beginning of the play period, suggesting that docility may vary with size or energetic variables. Docility decreased significantly among juveniles over the play interval, and rates of social play were reliable predictors of change in docility. Juveniles who played at higher rates tended to have greater decreases in docility over the play interval, suggesting that social play might refine temperament toward more active responses in U. beldingi. Rates of social play among juveniles were reliable predictors of their scores on docility tests as yearlings, suggesting that possible effects of juvenile play on docility may extend beyond the juvenile period. Among mothers of juveniles in the study, docility during gestation and lactation were reliable predictors of docility after emergence of young from the natal burrow. However, docility of mothers decreased significantly between gestation and emergence of young, suggesting that although squirrels have individual tendencies toward docility, the expression of these tendencies may be influenced by behavioral context. Significance statement This study helps to elucidate ways in which juvenile social play influences the development of young animals. Various studies have suggested that juvenile play inu fl ences motor, social, and cognitive development. Here, we show an association between juvenile social play and development of temperament in Belding’s ground squirrels (Urocitellus beldingi). Juveniles who engaged in play at higher rates across the play interval had greater behavioral shifts from passive toward active responses. Refinements in temperament toward more proactive behavior might have benefits for young animals such as better preparing them to explore, investigate, and gather information about their social and physical environments as they venture away from their natal areas. Keywords Docility · Ground squirrel · Juvenile development · Plasticity · Social play · Temperament Introduction Communicated by A. I Schulte-Hostedde Play occurs in a range of animal taxa but is especially * Scott Nunes prominent in mammals and serves as an important component nunes@usfca.edu of juvenile development in an array of mammalian species James S. Hurst-Hopf (Bekoff and Byers 1998; Burghardt 2005; Pellis et al. 2015). jshursthopf@dons.usfca.edu Pellis et al. (2023) observed in rats (Rattus norvegicus) that Martha P. Monroy Montemayor social elements of play behavior can importantly influence mpmonroy@dons.usfca.edu development of executive functions mediated through Nyla N. Leonardi the prefrontal cortex in mammals, resulting in increased nnleonardi@dons.usfca.edu social competence and greater behavioral flexibility and Department of Biology, University of San Francisco, adaptability during adulthood. Along this line, Spinka et al. San Francisco, CA 94117, U.S.A. Vol.:(0123456789) 1 3 62 Page 2 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 (2001) suggested that juvenile social play in mammals tendencies toward docility tended to be more consistent across may fine tune development of temperament in ways that the lifespan. Moreover, temperament can affect a range of promote emotional stability, behavioral flexibility, and ecologically important variables such as physiological expression of adaptive behavior across a range of situations responses to stress, space use, dispersal, reproductive success, and circumstances. Elements of temperament can exhibit and survival and thus can have an impact on the ability of plasticity in various species during the juvenile period animals to navigate through the life challenges they face when behavior is developing and can be shaped by social, (Réale et al. 2007, 2010; Boon et al. 2008; Baugh et al. 2013; physiological, and ecological factors (Sinn et al. 2008; Petelle Clary et al. 2014; Wauters et al. 2021; Skinner et al. 2022). et al. 2017; DiRienzo et al. 2018; Cabrera et al. 2021). In Temperament can also have important fitness consequences this work, we studied a population of Belding’s ground for individuals, and different temperaments can be adaptive squirrels (Urocitellus beldingi) to evaluate the relationship under different environmental conditions, varying with factors between juvenile social play behavior and the development of such as the prevalence of predators, abundance of resources, temperament. We used docility as a measure of temperament or local population density (Dingemanse et al. 2004; Both to assess whether play behavior might shape or refine et al. 2005; Boon et al. 2007; Colchester and Harrison 2016; elements of temperament in young animals. Behaviors Rasmussen and Belk 2017; Vetter et al. 2016). For example, along the docility spectrum of temperament are generally in stable environments, proactive individuals who are less considered to reflect reactive inclinations that involve docile and respond quickly to environmental stimuli may gathering information before acting or proactive tendencies have an advantage. By contrast, in unstable or unpredictable related to taking immediate action (Réale et al. 2000, 2009; environments, reactive individuals who are more docile and Petelle et al. 2013). Appropriate expression of proactive and gather information before acting may be favored by natural reactive responses may be important to juvenile U. beldingi selection (Sih et al. 2004). as they gather information about their physical and social The expression of juvenile play behavior and the adaptive environments and also during important events later in life benefits of engaging in play can vary among species and such as emigrating from the natal area or defending territories between sexes within a species (Olioff and Stewart 1978; (Nunes and Monroy Montemayor 2023). Meder 1990; Pederson et al. 1990; Pellis et al. 1996; Bekoff Temperament is also referred to as personality and and Byers 1998; Nunes et al. 1999; Maestripieri and Ross includes behavioral tendencies of individuals that are 2004; Burghardt 2005; Paukner and Suomi 2008; Auger consistent and repeatable over time and across situations and Olesen 2009; Wang et al. 2021). Juvenile play can have (Sih et al. 2004; Réale et al. 2007). Temperaments occur benefits that are experienced prominently early in the life along spectra that, for example, can encompass responses of individuals. For example, in horses (Equus caballus), to risks or threats (shyness/caution–boldness) or responses juvenile play is associated with enhanced body condition to novel objects or situations (avoidance–exploration). and increased survival (Cameron et  al. 2008). Play in Behaviors along the docility spectrum are generally white-tailed deer (Odocoileus virginianus) and mule deer measured as responses to being trapped and handled and (Odocoileus hemionus) promotes development of anti- reflect tendencies toward proactive vs. reactive behavior predator behavior and increases behavioral versatility among rather than responses specifically to threats or novelty (Réale juveniles (Carter et al. 2019). Play in geladas (Theropithecus et al. 2000, 2007, 2009; Cooper 2009; Herde and Eccard gelada) improves motor skill and fosters development of 2013; Petelle et al. 2013). For example, Petelle et al. (2015) social relationships (Gallo et  al. 2021). In brown bears observed that docility in yellow-bellied marmots (Marmota (Ursus arctos), play among cubs facilitates increased flaviventris) was inversely related to activity during open survival to the following summer, possibly by relieving field tests but not related to boldness when individuals were stress and reducing stress-related sources of mortality confronted with a potential threat. Docile individuals tend (Fagen and Fagen 2004). In U. beldingi, play behavior to be inclined toward expressing less active behavior across promotes development of motor skill and may contribute to situations or to wait and gather information before acting earlier natal dispersal in young males (Nunes et al. 2004). (Sih et al. 2004; Petelle et al. 2013, 2015, 2017). Juvenile play can also have a range of long-term benefits that Early-life experiences can have important and long-lasting extend beyond the juvenile period. For example, laboratory effects on the development of temperament (Rӧ del and von rats make extensive hand movements during play that Hulst 2009; Rӧdel and Monclús 2011; de Jong et al. 2022). likely promote long-term improvement of their motor and Elements of temperament can be stable across an individual’s manipulation skills (Whishaw et al. 2021). In spotted hyenas lifespan or can exhibit varying degrees of plasticity. For (Crocuta crocuta), play can facilitate social assessment example, Petelle et  al. (2013) observed in yellow-bellied by providing young animals with information about clan marmots that tendencies toward boldness in response to a members with whom they will interact throughout their lives threat were consistent among individuals early in life, whereas (Nolfo et al. 2021). Play behavior in yellow-bellied marmots 1 3 Behavioral Ecology and Sociobiology (2023) 77:62 Page 3 of 12 62 helps to establish dominance relationships that persist into active periods that coincide with the annual growing season adulthood (Blumstein et al. 2013). Rough and tumble play in (Jenkins and Eshelman 1984). Mating begins shortly after juvenile American minks (Neovison vison) is correlated with emergence from hibernation, and females bear at most one longer copulations among males in adulthood and longer litter per year (Morton and Gallup 1975). Males do not periods of precopulatory activity among females possibly begin breeding until they are 2 years old, whereas females facilitating mate choice (Ahloy Dallaire and Mason 2017). may begin reproducing as yearlings (Jenkins and Eshelman Juvenile play in female U. beldingi is associated with greater 1984). Reproductive females defend maternal territories intensity of maternal territorial behavior as a yearling and and aggressively evict intruders from the territories (Nunes increased likelihood of establishing a maternal territory and et al. 2000). Gestation lasts 24–25 days. During lactation, weaning a litter (Nunes 2014). In brown bears, play behavior young remain underground in natal burrows and first emerge as a juvenile is associated with increased long-term survival above ground at 25–28 days of age, near the time of weaning (Fagen and Fagen 2009). (Holekamp et al. 1984; Nunes et al. 1999). Play behavior Prior work with U. beldingi suggested a relationship occurs primarily during juveniles’ first 2 weeks above between juvenile social play and development of ground, with > 97% of play interactions occurring among temperament along the exploration–avoidance axis. Juvenile littermates (Nunes et al. 1999). squirrels who engaged in social play at higher rates and had We captured squirrels using Tomahawk live traps longer play interactions had greater increases across the (Tomahawk Live Trap Company, Hazelhurst, WI, USA) baited developmental period in which play primarily occurs in their with peanut butter and checked traps every 30 min or less tendencies to explore an unfamiliar testing arena (Marks et al. during trapping sessions. Squirrels were fitted with numbered 2017). Shifts in young animals toward greater exploratory metal ear tags (National Band and Tag Company, Newport, behavior may in general promote greater acquisition of KY, USA) at their first capture for long-term identification. information as they venture farther from their natal areas Ear tags of juveniles were painted different colors with nail or begin to integrate themselves into their social groups polish prior to application to aid in identification of individuals (Nunes and Monroy Montemayor 2023). Here, we expanded during observations (Nunes et al. 2015). We also dyed the on the prior work of Marks et al. (2017) to evaluate whether fur of squirrels with unique symbols using black hair dye juvenile social play in U. beldingi might be associated with (Clairol, Stamford, CT, USA) to facilitate visual identification development of other elements of temperament, focusing on of individuals. We observed the territories of reproductive temperament along the docility spectrum. We observed the females daily to determine the dates that their litters first play behavior of juvenile U. beldingi and evaluated other emerged from the natal burrow. We trapped young within 2 factors that might influence the development of temperament days of their r fi st emergence above ground when they could be in young animals, such as body mass and the docility of unambiguously assigned to mothers (Holekamp et al. 1984). their mothers (Mousseau and Fox 1998; Rӧdel and von Hulst We weighed juveniles with spring balance scales (Avinet, 2009). We conducted behavioral tests assessing docility at the Dryden, NY, USA) at their first capture and again 12–14 beginning and toward the end of the primary developmental days after their first appearance above ground and calculated play interval for U. beldingi. We predicted that if social play changes in body mass across this period as a proportion of influences the development of docility, then social play in initial mass. Methods used in the study followed guidelines individuals should be correlated with their changes in docility for wild mammals published by the American Society of across the play interval. Mammalogists (Sikes et al. 2016). Behavioral tests Methods We conducted behavioral tests to evaluate docility of Study animals and general methods U. beldingi. During tests, a handler removed a squirrel from its trap, and the squirrel was held for 30 s with the From May to June 2016 and June to August 2017, we studied handler’s hand positioned around the squirrel’s chest a population of U. beldingi in a 25-ha meadow at Tioga and abdomen and the squirrel’s forelimbs free from Pass (latitude 37.9, longitude −119.2, elevation 2950 m) the handler’s grip (Fig.  1). Squirrels were allowed to in Mono County, CA, USA. Squirrels in this species live in equilibrate in a trap covered by a cloth for at least 2 min in groups but do not have a complex social system compared a quiet area before tests began. Squirrels’ responses during to many other sciurid species (Michener 1983; Wolff and tests were recorded on video, and recordings were later Sherman 2007). The squirrels are diurnal, inhabit alpine viewed by observers to determine docility scores. Scores and subalpine meadows in the western USA, and have an were calculated as the number of seconds during the 30-s 8–9-month hibernation period interspersed with 3–4-month test that squirrels were docile. Docility was defined as 1 3 62 Page 4 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 Fig. 1 Examples of A docile/ passive and B active responses during behavioral tests remaining motionless or displaying slight movements such defined as the 25-day interval prior to lactation (Holekamp as turning the head or repositioning the paws (Fig. 1A). et al. 1984; Nunes et al. 1999). Squirrels were not considered to be docile if they wriggled their bodies or otherwise struggled, used their forelimbs to Observation of juvenile behavior push down on the handler’s glove to try to lift their body free from the handler’s grip, or bit the handler’s glove During the summer of 2016, we observed the play behavior (Fig. 1B). All recordings were scored blindly by the same of 23 juvenile squirrels from 14 different litters who were two observers, and scores for individual squirrels were included in the study as yearlings in 2017. These squirrels averaged. were observed as juveniles for an average of 396 + 16.2 We conducted docility tests for 151 juveniles from 32 (SE) min per individual over an average of 5.9 ± 0.2 (SE) litters at their initial capture after first emerging from the different days during their first 12 days above ground. natal burrow. Docility tests were conducted before any other During the summer of 2017, we observed the behavior handling procedures such as ear-tagging, dye-marking, or of 90 juvenile U. beldingi from 19 litters. These juveniles weighing were performed to prevent the possibility of these were observed for an average of 484.7 + 19.0 (SE) min procedures influencing responses on tests. We observed the per individual over an average of 6.1 ±0.3 (SE) different behavior (see below) of 90 of these juveniles from 19 litters days during their first 12 days above ground. Behavioral during their first 12 days above ground and conducted a observations were conducted between 0700 and 1600 h from second docility test for these 90 juveniles 12–14 days after elevated posts such as boulders and hillsides. We recorded their initial emergence from the natal burrow, toward the end all occurrences of social play during observations and of the period in which play primarily occurs. We note that calculated rates of social play for individuals as the number ten juveniles from nine of the 19 litters disappeared before of play interactions per hour of observation. Specific play they could be re-tested and were omitted from this part of behaviors were defined (Table  1) following descriptions by the study. Marks et al. (2017). We observed specific focal animals, so To evaluate whether possible effects of juvenile play on it was not possible to record behavioral data blindly. docility extended beyond the play period, we conducted docility tests on 23 yearling U. beldingi from 14 different Data analysis litters for whom juvenile play data were available from the previous year. To evaluate whether docility was consistent Continuous variables evaluated in the study included among individual U. beldingi in different contexts, we scores on docility tests, changes in docility scores, body conducted docility tests during different phases of the mass, changes in body mass, and rates of juvenile social reproductive cycle for 30 adult and yearling females who play. Correlations between variables were evaluated with weaned a litter during the study. Tests were performed Pearson’s r. Data were compared between juvenile males at the female’s first capture in the active season either and females using independent t-tests. Scores on docility during gestation or lactation and then again within the first tests for individual U. beldingi at the beginning vs. end of the week after emergence of young from the natal burrow. play interval were compared using paired t-tests. Variances Lactation was defined as the 27-day interval prior to the were pooled when assumptions of homoscedasticity were first appearance of young above ground, and gestation was not met in t-tests. A linear mixed effects model was used 1 3 Behavioral Ecology and Sociobiology (2023) 77:62 Page 5 of 12 62 Table 1 Social play behavior of Behavior Description juvenile U. beldingi Play fighting The juvenile faces another juvenile, typically in a ventrum-to-ventrum hold and pecks at the other juvenile without inflicting bite wounds Tackling The juvenile jumps or pounces on another juvenile, usually from a running start Boxing The juvenile bats with the forepaws at another juvenile Chasing The juvenile follows and pursues another juvenile for > 1 m, while both are running Mounting and play The juvenile climbs on the back of another juvenile and places its forepaws around copulation the other juvenile, grasping in its mouth the other juvenile’s neck, cheek, or back and aligning its pelvis with other juvenile’s pelvis; intromission does not occur Table 2 Results of analysis with linear mixed effects model evaluating different variables as possible predictors of docility at first emergence from the natal burrow for 151 juvenile U. beldingi Predictor of juvenile docility (seconds) Estimate Degrees of freedom F P Juvenile body mass (grams) -0.02 1, 118 11.03 0.001 Docility of mother (seconds) -0.14 1, 188 < 0.001 0.987 to evaluate whether docility of juveniles at first emergence R =0.10 from the natal burrow varied with their body mass or the P =0.001 docility of their mothers. A linear mixed effects model was also used to evaluate whether changes in docility of juveniles across the play interval varied with rates of social play, body mass, changes in body mass, or the docility of their mothers. Litter was included as a random effect in linear mixed effects models to account for possible similarities among 15 littermates. Linear regression was used to evaluate whether docility scores of reproductive females prior to emergence of young from the natal burrow were reliable predictors of docility scores after litter emergence and whether rates of 30 40 50 60 70 80 90 100 110 social play among juvenile squirrels were reliable predictors of their scores on docility tests as yearlings. Assumptions of Body mass (grams) homoscedasticity and normal distribution of residuals were met in statistical analyses. Statistical tests were performed Fig. 2 Association between body mass and scores on docility tests at first emergence from the natal burrow for 151 juvenile U. beldingi with Systat 13.1 (Systat Software Inc., Chicago, IL, USA). Relationships indicated by statistical tests were considered significant when P < 0.05. with the body mass of juveniles but not with the docility of their mothers (Table 2). Docility of juveniles tended to Results decrease as their body mass increased, but the association between these variables was weak (Fig. 2). Initial docility of juveniles Changes in juvenile docility The amount of time juvenile U. beldingi were docile during behavioral tests at their first emergence from the natal bur - The amount of time juveniles were docile during behavio- row did not differ between the sexes (t = 0.53, P = 0.597), ral tests decreased significantly between initial tests at first so data for juvenile males and females were combined for emergence from the natal burrow and re-tests near the end of statistical analysis. Body mass of juveniles at first emergence the play period (Fig. 3, t = 10.55, P < 0.001), indicating a from the natal burrow also did not differ between the sexes shift toward more active responses across the play interval. (t = 0.80, P = 0.428) and was not significantly correlated Changes in docility scores over the play interval, expressed with docility of mothers (r = −0.01, P = 0.947). Juvenile as a proportion of the initial score, did not differ between docility during initial behavioral tests varied significantly juvenile males and females (t =1.18, P = 0.241). Scores 1 3 Docility score(sec) 62 Page 6 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 0.4 R =0.18 0.2 P =0.001 a b 0.0 -0.2 -0.4 -0.6 -0.8 -1.0 0- 212- 14 Social play (interactions/hour of observation) Days afteremergingfromthe natalburrow Fig. 4 Association between social play and changes in docility Fig. 3 Box and whisker plots showing docility scores of 151 individ- scores, expressed as a proportion of the initial score, across the play ual juvenile U. beldingi near their first emergence from the natal bur - interval for 90 juvenile U. beldingi row at the onset of the play interval and 12–14 days after emerging from the natal burrow near the end of the play interval. Boxes delimit the 0.25 and 0.75 quantiles, horizontal lines indicate medians, whisk- ers extend to 1.5 interquartile range, and outliers are plotted as indi- Docility of yearlings and reproductive females vidual points. Letters indicate statistical differences at P < 0.05 To evaluate possible longer-term associations between docility and juvenile play, docility tests were conducted on on initial tests were significantly correlated with scores on 23 yearling U. beldingi for whom juvenile play data from re-tests (r = 0.53, P < 0.001) but not with changes in docility the previous year were available. Among these squirrels, over the play interval (r = −0.13, P = 0.223). the rates of social play as a juvenile were reliable predictors Changes in docility of juveniles varied significantly of scores on docility tests as a yearling (Fig. 5, F = 8.64, 1,21 with social play but not with average body mass across P = 0.008, R = 0.26). In particular, squirrels who engaged the play interval, changes in body mass across the play in social play at higher rates as juveniles tended to be less interval, or docility scores of mothers (Table 3). Higher docile as yearlings (Fig. 5). rates of social play were associated with greater decreases To evaluate consistency in docility among individual in docility and greater shifts toward active responses U. beldingi over time and across situations, we conducted (Fig.  4). We note that there were no significant sex docility tests for a total of 30 reproductive females both prior differences in rates of play (t = 1.31, P = 0.194), body to and after the first emergence of their litters from the natal mass (t = 0.45, P = 0.653), or changes in body mass burrow. Among these females, 12 were first tested during (t = 1.33, P = 0.188), and none of the independent gestation, and 18 were first tested during lactation. Docility variables in this analysis was significantly correlated scores increased significantly between the initial test and with any others (−0.24 < r < 0.16, 0.124 < P < 0.999). re-test for females first tested during gestation (Fig.  6, t = We further note that although changes in docility varied 3.17, P = 0.009) but not for those first tested during lactation with rates of social play, the rates of social play were not (t = 0.75, P = 0.465). Scores on initial docility tests were significantly correlated with initial docility scores (r = reliable predictors of scores on the re-tests for females first −0.15, P = 0.159). tested during gestation (Fig. 7A, F = 13.32, P = 0.004, R 1,10 Table 3 Results of analysis Predictor of change in juvenile docility (proportion of initial score) Estimate Degrees F P with linear mixed effects model of free- evaluating different variables as dom possible predictors of change in docility across the play interval Juvenile social play (interactions/hour) −0.06 1, 68 13.16 0.001 for 90 juvenile U. beldingi Average juvenile body mass during play interval (grams) −0.001 1, 68 0.44 0.511 Change in juvenile body mass (proportion of initial mass) 0.05 1, 68 0.26 0.609 Docility of mother (seconds) 0.004 1, 68 0.74 0.392 1 3 Docility score(sec) Change in docility score (proportionofinitial score) Behavioral Ecology and Sociobiology (2023) 77:62 Page 7 of 12 62 R =0.26 P =0.008 R =0.53 P =0.004 05 10 15 20 25 30 0246 8 Gestationdocilityscore (sec) Social play as juvenile (interactions/hour) Fig. 5 Association between rates of social play as juveniles and scores on docility tests as yearlings for 23 Urocitellus beldingi R =0.48 P =0.001 10 05 10 15 20 25 30 Lactationdocilityscore (sec) Fig. 7 Association between docility scores of reproductive female Urocitellus beldingi after first emergence of litters from the natal bur - GestationPost-emergence row and scores during A lactation and B gestation. Twelve females were sampled during gestation and after emergence of young, and 18 Fig. 6 Box and whisker plots showing docility scores of 12 female females were sampled during lactation and after emergence of young Urocitellus beldingi during the reproductive cycle. Boxes delimit the 0.25 and 0.75 quantiles, horizontal lines indicate medians, whiskers extend to 1.5 interquartile range, and outliers are plotted as individual and responses to restraint (Rӧdel and von Hulst 2009; points. Letters indicate a significant difference between stages of the Rӧdel and Monclús 2011; Rӧdel et al. 2017). Body mass in reproductive cycle at P < 0.05 juvenile U. beldingi at first emergence from the natal burrow is associated with the size of fat reserves (Nunes et al. 1999). = 0.53) as well as those first tested during lactation (Fig.  7B, Smaller juveniles tend to have less body fat and thus might be inclined to be more conservative in their energy usage, F = 16.49, P = 0.001, R = 0.48). 1,16 and development of more docile temperaments might be favored in these individuals. Moreover, smaller juveniles Discussion might be less competitive in agonistic interactions and thus might be favored to have more docile and reactive responses Body mass of juvenile U. beldingi in our study was inversely rather than proactive behavior (Sih et al. 2004; Rӧdel and von Hulst 2009). We note, however, that the association related to docility at juveniles’ r fi st emergence from the natal burrow, with smaller juveniles having more docile and less between body mass and docility in juvenile U. beldingi was weak (Fig.  2), and possible influences of body mass active responses during behavioral tests. Body mass has been shown to influence the developmental trajectory of on docility may be relatively minor. Another possibility is that body mass of U. beldingi at emergence from the natal behavioral tendencies in European rabbits (Oryctolagus cuniculus), including exploratory and aggressive behavior burrow reflected the expression of temperament during 1 3 Docility score(sec) Docility score as yearling (sec) Post-emergence docilityscore (sec) Post-emergence docility score (sec) 62 Page 8 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 lactation. That is, more docile juveniles might have been observed that greater social play among juvenile U. beldingi less likely to seek nursing opportunities or might have been was associated with greater increases in caution in response less successful at competing for milk and thus might have to a potential threat. Thus, temperament appears to be plastic been smaller near the time of weaning (Rӧdel et al. 2017). in U. beldingi during the juvenile period. Moreover, possible We did not observe a significant relationship between the refinements in different elements of temperament associated docility of maternal U. beldingi and the docility of their with social play in U. beldingi might better equip young young. However, we cannot rule out here the possibility squirrels to express adaptive responses across a diverse array that other maternal effects influenced the development of of situations they may encounter as they interact with the docility in juvenile U. beldingi in our study. Temperament world around them. is plastic during the postnatal and juvenile periods in a range Social play of U. beldingi as juveniles in this study was of species (Cabrera et al. 2021), and maternal effects on significantly correlated with their docility as yearlings, the development of temperament and other variables have suggesting that possible effects of social play on docility been suggested to prepare offspring to be successful under may extend beyond the juvenile period in this species. prevailing environmental conditions (Storm and Lima 2010; Play behavior has been shown to have a variety of adaptive Kapheim et al. 2011; Dantzer et al. 2013). Environmental benefits during the juvenile period as well as longer-term stresses experienced by mothers can directly affect the way effects on behavior, reproductive success, and survival in a they raise their young, which in turn can affect the behavior variety of species (Bekoff and Byers 1998; Burghardt 2005; as well as growth, metabolism, and immune and endocrine Cameron et al. 2008; Fagen and Fagen 2009; Blumstein function of offspring (Mousseau and Fox 1998; Weinstock et al. 2013; Nunes 2014; Ahloy Dallaire and Mason 2017; 2001; Hayward and Wingfield 2004). For example, environ- Whishaw et  al. 2021). However, we note that studies of mental stressors and prior experience raising young have meerkats (Suricata suricatta) (Sharpe and Cherry 2003; been observed to influence glucocorticoid concentrations in Sharpe 2005a, b, c) and chimpanzees (Pan troglodytes mothers, and glucocorticoids passed to offspring through schweinfurthii) (Heintz et  al. 2017) did not reveal any milk during lactation can influence development of behavior associations between juvenile play and behavior later in and elements of temperament such as boldness and docility life. These discrepancies in longer-term effects of play may (Hinde et al. 2015; Petelle et al. 2017). reflect different courses in the evolution of play behavior Docility among juvenile U. beldingi in our study among different species (Pellis et al. 2014). decreased over the course of the play interval, with the Among maternal U. beldingi in our study, docility scores behavior of juveniles shifting toward more active responses. of individual females during gestation and lactation were Marks et al. (2017) observed that exploratory behavior of reliable predictors of their docility after young emerged from juvenile U. beldingi increased across the play interval, and the natal burrow, indicating consistency among individuals the amount of time to escape from an unfamiliar testing in their tendencies toward docile responses and aligning arena decreased. Juvenile U. beldingi are unfamiliar with docility in this species with Réale et al.’s (2007) definition above-ground elements of their habitat when they first of temperament. However, we observed a significant emerge from the natal burrow, and reactive responses such increase in the docility of maternal U. beldingi between as passive observation might help naïve squirrels avoid gestation and the emergence of their young from the natal potentially dangerous situations and thus might be favored burrow, indicating that although individual females may be by natural selection. However, as young squirrels spend time predisposed to different degrees of docility, expression of above ground and gain familiarity with their surroundings, docility can be influenced by factors such as reproductive exploration and proactive responses might be favored to help state and may vary across different contexts. Maternal individuals gather additional information about and navigate U. beldingi exhibit peak aggressive behavior during the through their physical and social environments as they begin gestational period when they are competing for burrow to venture farther from their natal home areas (Sih et al. systems and space in which to establish a maternal territory, 2004). and rates of aggression decrease substantially after gestation We observed a significant relationship between social (Nunes et al. 1997, 2000). Thus, changes in docility across play and decreases in docility of juvenile U. beldingi after the reproductive cycle may reflect increases in aggressive emergence from the natal burrow. Juveniles who played at behavior or general tendencies toward more proactive higher rates tended to have greater decreases in docility and responses when establishing a maternal territory. greater shifts toward active responses in behavioral tests. The possible effects of social play on the development Marks et  al. (2017) similarly observed that juvenile U. temperament along the docility spectrum may be mediated beldingi who engaged in social play at higher rates tended by effects on the developing brain. Some elements of brain to have greater increases in exploratory behavior after development are plastic during the postnatal and juvenile emergence from the natal burrow. Shehan (2019) further periods, and a range of experiences after birth can play 1 3 Behavioral Ecology and Sociobiology (2023) 77:62 Page 9 of 12 62 an important role in directing specific aspects of neural Declarations and behavioral development (Johnson 2001; Stiles and Ethics approval The study followed guidelines for use of animals in Jernigan 2010; Kolb and Gibb 2011; Sakai and Sugiyama field research published by the American Society of Mammalogists. 2018). For example, in rats, social play experiences during Work for the study was conducted under permit SC-2008 from the early development are necessary for the establishment of California Department of Fish and Wildlife and permits LVD16018 and LVD17005 from the US Forest Service. Institutional approval for competent social skills and the normal expression of social use of animals in the study was not required by the University of San behavior in adulthood (Pellis et al. 2014; Stark and Pellis Francisco. 2020; Stark et  al. 2021). Juvenile play in rats has also been shown to modify development of areas in the frontal Conflict of interest The authors declare no competing interests. cortex associated with motor and social behavior as well as behavioral flexibility (Bell et al. 2010; Pellis et al. 2010; Open Access This article is licensed under a Creative Commons Attri- bution 4.0 International License, which permits use, sharing, adapta- Himmler et al. 2013, 2017; Burleson et al. 2016). tion, distribution and reproduction in any medium or format, as long Pellis et  al. (2019) proposed that in some species, as you give appropriate credit to the original author(s) and the source, play may comprise a behavioral system devoted to the provide a link to the Creative Commons licence, and indicate if changes expression and regulation of play behaviors. This idea were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated suggests that play arose evolutionarily as non-functional otherwise in a credit line to the material. If material is not included in expression during early development of behaviors that are the article's Creative Commons licence and your intended use is not functional in adulthood. Over time, these behaviors were permitted by statutory regulation or exceeds the permitted use, you will modified by natural selection into specific play behaviors need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . that provided various adaptive benefits to individuals and that were regulated by distinct neural systems (Burghardt 2005; Pellis et al. 2014, 2015). Pellis et al. (2019) noted that in some species, behavior systems related to play may References be complex. 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Juvenile social play predicts docility in Belding’s ground squirrels

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Copyright © The Author(s) 2023
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0340-5443
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10.1007/s00265-023-03341-7
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Abstract

We evaluated the hypothesis that social play behavior influences the development of temperament in young animals, using docility as a measure of temperament. We observed the play behavior of juvenile Belding’s ground squirrels (Urocitellus beldingi) during the developmental period in which play primarily occurs and conducted behavioral tests measuring docility at the beginning and toward the end of the play interval. Tests involved handling squirrels and recording their responses. We observed a significant but weak association between body mass and docility at the beginning of the play period, suggesting that docility may vary with size or energetic variables. Docility decreased significantly among juveniles over the play interval, and rates of social play were reliable predictors of change in docility. Juveniles who played at higher rates tended to have greater decreases in docility over the play interval, suggesting that social play might refine temperament toward more active responses in U. beldingi. Rates of social play among juveniles were reliable predictors of their scores on docility tests as yearlings, suggesting that possible effects of juvenile play on docility may extend beyond the juvenile period. Among mothers of juveniles in the study, docility during gestation and lactation were reliable predictors of docility after emergence of young from the natal burrow. However, docility of mothers decreased significantly between gestation and emergence of young, suggesting that although squirrels have individual tendencies toward docility, the expression of these tendencies may be influenced by behavioral context. Significance statement This study helps to elucidate ways in which juvenile social play influences the development of young animals. Various studies have suggested that juvenile play inu fl ences motor, social, and cognitive development. Here, we show an association between juvenile social play and development of temperament in Belding’s ground squirrels (Urocitellus beldingi). Juveniles who engaged in play at higher rates across the play interval had greater behavioral shifts from passive toward active responses. Refinements in temperament toward more proactive behavior might have benefits for young animals such as better preparing them to explore, investigate, and gather information about their social and physical environments as they venture away from their natal areas. Keywords Docility · Ground squirrel · Juvenile development · Plasticity · Social play · Temperament Introduction Communicated by A. I Schulte-Hostedde Play occurs in a range of animal taxa but is especially * Scott Nunes prominent in mammals and serves as an important component nunes@usfca.edu of juvenile development in an array of mammalian species James S. Hurst-Hopf (Bekoff and Byers 1998; Burghardt 2005; Pellis et al. 2015). jshursthopf@dons.usfca.edu Pellis et al. (2023) observed in rats (Rattus norvegicus) that Martha P. Monroy Montemayor social elements of play behavior can importantly influence mpmonroy@dons.usfca.edu development of executive functions mediated through Nyla N. Leonardi the prefrontal cortex in mammals, resulting in increased nnleonardi@dons.usfca.edu social competence and greater behavioral flexibility and Department of Biology, University of San Francisco, adaptability during adulthood. Along this line, Spinka et al. San Francisco, CA 94117, U.S.A. Vol.:(0123456789) 1 3 62 Page 2 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 (2001) suggested that juvenile social play in mammals tendencies toward docility tended to be more consistent across may fine tune development of temperament in ways that the lifespan. Moreover, temperament can affect a range of promote emotional stability, behavioral flexibility, and ecologically important variables such as physiological expression of adaptive behavior across a range of situations responses to stress, space use, dispersal, reproductive success, and circumstances. Elements of temperament can exhibit and survival and thus can have an impact on the ability of plasticity in various species during the juvenile period animals to navigate through the life challenges they face when behavior is developing and can be shaped by social, (Réale et al. 2007, 2010; Boon et al. 2008; Baugh et al. 2013; physiological, and ecological factors (Sinn et al. 2008; Petelle Clary et al. 2014; Wauters et al. 2021; Skinner et al. 2022). et al. 2017; DiRienzo et al. 2018; Cabrera et al. 2021). In Temperament can also have important fitness consequences this work, we studied a population of Belding’s ground for individuals, and different temperaments can be adaptive squirrels (Urocitellus beldingi) to evaluate the relationship under different environmental conditions, varying with factors between juvenile social play behavior and the development of such as the prevalence of predators, abundance of resources, temperament. We used docility as a measure of temperament or local population density (Dingemanse et al. 2004; Both to assess whether play behavior might shape or refine et al. 2005; Boon et al. 2007; Colchester and Harrison 2016; elements of temperament in young animals. Behaviors Rasmussen and Belk 2017; Vetter et al. 2016). For example, along the docility spectrum of temperament are generally in stable environments, proactive individuals who are less considered to reflect reactive inclinations that involve docile and respond quickly to environmental stimuli may gathering information before acting or proactive tendencies have an advantage. By contrast, in unstable or unpredictable related to taking immediate action (Réale et al. 2000, 2009; environments, reactive individuals who are more docile and Petelle et al. 2013). Appropriate expression of proactive and gather information before acting may be favored by natural reactive responses may be important to juvenile U. beldingi selection (Sih et al. 2004). as they gather information about their physical and social The expression of juvenile play behavior and the adaptive environments and also during important events later in life benefits of engaging in play can vary among species and such as emigrating from the natal area or defending territories between sexes within a species (Olioff and Stewart 1978; (Nunes and Monroy Montemayor 2023). Meder 1990; Pederson et al. 1990; Pellis et al. 1996; Bekoff Temperament is also referred to as personality and and Byers 1998; Nunes et al. 1999; Maestripieri and Ross includes behavioral tendencies of individuals that are 2004; Burghardt 2005; Paukner and Suomi 2008; Auger consistent and repeatable over time and across situations and Olesen 2009; Wang et al. 2021). Juvenile play can have (Sih et al. 2004; Réale et al. 2007). Temperaments occur benefits that are experienced prominently early in the life along spectra that, for example, can encompass responses of individuals. For example, in horses (Equus caballus), to risks or threats (shyness/caution–boldness) or responses juvenile play is associated with enhanced body condition to novel objects or situations (avoidance–exploration). and increased survival (Cameron et  al. 2008). Play in Behaviors along the docility spectrum are generally white-tailed deer (Odocoileus virginianus) and mule deer measured as responses to being trapped and handled and (Odocoileus hemionus) promotes development of anti- reflect tendencies toward proactive vs. reactive behavior predator behavior and increases behavioral versatility among rather than responses specifically to threats or novelty (Réale juveniles (Carter et al. 2019). Play in geladas (Theropithecus et al. 2000, 2007, 2009; Cooper 2009; Herde and Eccard gelada) improves motor skill and fosters development of 2013; Petelle et al. 2013). For example, Petelle et al. (2015) social relationships (Gallo et  al. 2021). In brown bears observed that docility in yellow-bellied marmots (Marmota (Ursus arctos), play among cubs facilitates increased flaviventris) was inversely related to activity during open survival to the following summer, possibly by relieving field tests but not related to boldness when individuals were stress and reducing stress-related sources of mortality confronted with a potential threat. Docile individuals tend (Fagen and Fagen 2004). In U. beldingi, play behavior to be inclined toward expressing less active behavior across promotes development of motor skill and may contribute to situations or to wait and gather information before acting earlier natal dispersal in young males (Nunes et al. 2004). (Sih et al. 2004; Petelle et al. 2013, 2015, 2017). Juvenile play can also have a range of long-term benefits that Early-life experiences can have important and long-lasting extend beyond the juvenile period. For example, laboratory effects on the development of temperament (Rӧ del and von rats make extensive hand movements during play that Hulst 2009; Rӧdel and Monclús 2011; de Jong et al. 2022). likely promote long-term improvement of their motor and Elements of temperament can be stable across an individual’s manipulation skills (Whishaw et al. 2021). In spotted hyenas lifespan or can exhibit varying degrees of plasticity. For (Crocuta crocuta), play can facilitate social assessment example, Petelle et  al. (2013) observed in yellow-bellied by providing young animals with information about clan marmots that tendencies toward boldness in response to a members with whom they will interact throughout their lives threat were consistent among individuals early in life, whereas (Nolfo et al. 2021). Play behavior in yellow-bellied marmots 1 3 Behavioral Ecology and Sociobiology (2023) 77:62 Page 3 of 12 62 helps to establish dominance relationships that persist into active periods that coincide with the annual growing season adulthood (Blumstein et al. 2013). Rough and tumble play in (Jenkins and Eshelman 1984). Mating begins shortly after juvenile American minks (Neovison vison) is correlated with emergence from hibernation, and females bear at most one longer copulations among males in adulthood and longer litter per year (Morton and Gallup 1975). Males do not periods of precopulatory activity among females possibly begin breeding until they are 2 years old, whereas females facilitating mate choice (Ahloy Dallaire and Mason 2017). may begin reproducing as yearlings (Jenkins and Eshelman Juvenile play in female U. beldingi is associated with greater 1984). Reproductive females defend maternal territories intensity of maternal territorial behavior as a yearling and and aggressively evict intruders from the territories (Nunes increased likelihood of establishing a maternal territory and et al. 2000). Gestation lasts 24–25 days. During lactation, weaning a litter (Nunes 2014). In brown bears, play behavior young remain underground in natal burrows and first emerge as a juvenile is associated with increased long-term survival above ground at 25–28 days of age, near the time of weaning (Fagen and Fagen 2009). (Holekamp et al. 1984; Nunes et al. 1999). Play behavior Prior work with U. beldingi suggested a relationship occurs primarily during juveniles’ first 2 weeks above between juvenile social play and development of ground, with > 97% of play interactions occurring among temperament along the exploration–avoidance axis. Juvenile littermates (Nunes et al. 1999). squirrels who engaged in social play at higher rates and had We captured squirrels using Tomahawk live traps longer play interactions had greater increases across the (Tomahawk Live Trap Company, Hazelhurst, WI, USA) baited developmental period in which play primarily occurs in their with peanut butter and checked traps every 30 min or less tendencies to explore an unfamiliar testing arena (Marks et al. during trapping sessions. Squirrels were fitted with numbered 2017). Shifts in young animals toward greater exploratory metal ear tags (National Band and Tag Company, Newport, behavior may in general promote greater acquisition of KY, USA) at their first capture for long-term identification. information as they venture farther from their natal areas Ear tags of juveniles were painted different colors with nail or begin to integrate themselves into their social groups polish prior to application to aid in identification of individuals (Nunes and Monroy Montemayor 2023). Here, we expanded during observations (Nunes et al. 2015). We also dyed the on the prior work of Marks et al. (2017) to evaluate whether fur of squirrels with unique symbols using black hair dye juvenile social play in U. beldingi might be associated with (Clairol, Stamford, CT, USA) to facilitate visual identification development of other elements of temperament, focusing on of individuals. We observed the territories of reproductive temperament along the docility spectrum. We observed the females daily to determine the dates that their litters first play behavior of juvenile U. beldingi and evaluated other emerged from the natal burrow. We trapped young within 2 factors that might influence the development of temperament days of their r fi st emergence above ground when they could be in young animals, such as body mass and the docility of unambiguously assigned to mothers (Holekamp et al. 1984). their mothers (Mousseau and Fox 1998; Rӧdel and von Hulst We weighed juveniles with spring balance scales (Avinet, 2009). We conducted behavioral tests assessing docility at the Dryden, NY, USA) at their first capture and again 12–14 beginning and toward the end of the primary developmental days after their first appearance above ground and calculated play interval for U. beldingi. We predicted that if social play changes in body mass across this period as a proportion of influences the development of docility, then social play in initial mass. Methods used in the study followed guidelines individuals should be correlated with their changes in docility for wild mammals published by the American Society of across the play interval. Mammalogists (Sikes et al. 2016). Behavioral tests Methods We conducted behavioral tests to evaluate docility of Study animals and general methods U. beldingi. During tests, a handler removed a squirrel from its trap, and the squirrel was held for 30 s with the From May to June 2016 and June to August 2017, we studied handler’s hand positioned around the squirrel’s chest a population of U. beldingi in a 25-ha meadow at Tioga and abdomen and the squirrel’s forelimbs free from Pass (latitude 37.9, longitude −119.2, elevation 2950 m) the handler’s grip (Fig.  1). Squirrels were allowed to in Mono County, CA, USA. Squirrels in this species live in equilibrate in a trap covered by a cloth for at least 2 min in groups but do not have a complex social system compared a quiet area before tests began. Squirrels’ responses during to many other sciurid species (Michener 1983; Wolff and tests were recorded on video, and recordings were later Sherman 2007). The squirrels are diurnal, inhabit alpine viewed by observers to determine docility scores. Scores and subalpine meadows in the western USA, and have an were calculated as the number of seconds during the 30-s 8–9-month hibernation period interspersed with 3–4-month test that squirrels were docile. Docility was defined as 1 3 62 Page 4 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 Fig. 1 Examples of A docile/ passive and B active responses during behavioral tests remaining motionless or displaying slight movements such defined as the 25-day interval prior to lactation (Holekamp as turning the head or repositioning the paws (Fig. 1A). et al. 1984; Nunes et al. 1999). Squirrels were not considered to be docile if they wriggled their bodies or otherwise struggled, used their forelimbs to Observation of juvenile behavior push down on the handler’s glove to try to lift their body free from the handler’s grip, or bit the handler’s glove During the summer of 2016, we observed the play behavior (Fig. 1B). All recordings were scored blindly by the same of 23 juvenile squirrels from 14 different litters who were two observers, and scores for individual squirrels were included in the study as yearlings in 2017. These squirrels averaged. were observed as juveniles for an average of 396 + 16.2 We conducted docility tests for 151 juveniles from 32 (SE) min per individual over an average of 5.9 ± 0.2 (SE) litters at their initial capture after first emerging from the different days during their first 12 days above ground. natal burrow. Docility tests were conducted before any other During the summer of 2017, we observed the behavior handling procedures such as ear-tagging, dye-marking, or of 90 juvenile U. beldingi from 19 litters. These juveniles weighing were performed to prevent the possibility of these were observed for an average of 484.7 + 19.0 (SE) min procedures influencing responses on tests. We observed the per individual over an average of 6.1 ±0.3 (SE) different behavior (see below) of 90 of these juveniles from 19 litters days during their first 12 days above ground. Behavioral during their first 12 days above ground and conducted a observations were conducted between 0700 and 1600 h from second docility test for these 90 juveniles 12–14 days after elevated posts such as boulders and hillsides. We recorded their initial emergence from the natal burrow, toward the end all occurrences of social play during observations and of the period in which play primarily occurs. We note that calculated rates of social play for individuals as the number ten juveniles from nine of the 19 litters disappeared before of play interactions per hour of observation. Specific play they could be re-tested and were omitted from this part of behaviors were defined (Table  1) following descriptions by the study. Marks et al. (2017). We observed specific focal animals, so To evaluate whether possible effects of juvenile play on it was not possible to record behavioral data blindly. docility extended beyond the play period, we conducted docility tests on 23 yearling U. beldingi from 14 different Data analysis litters for whom juvenile play data were available from the previous year. To evaluate whether docility was consistent Continuous variables evaluated in the study included among individual U. beldingi in different contexts, we scores on docility tests, changes in docility scores, body conducted docility tests during different phases of the mass, changes in body mass, and rates of juvenile social reproductive cycle for 30 adult and yearling females who play. Correlations between variables were evaluated with weaned a litter during the study. Tests were performed Pearson’s r. Data were compared between juvenile males at the female’s first capture in the active season either and females using independent t-tests. Scores on docility during gestation or lactation and then again within the first tests for individual U. beldingi at the beginning vs. end of the week after emergence of young from the natal burrow. play interval were compared using paired t-tests. Variances Lactation was defined as the 27-day interval prior to the were pooled when assumptions of homoscedasticity were first appearance of young above ground, and gestation was not met in t-tests. A linear mixed effects model was used 1 3 Behavioral Ecology and Sociobiology (2023) 77:62 Page 5 of 12 62 Table 1 Social play behavior of Behavior Description juvenile U. beldingi Play fighting The juvenile faces another juvenile, typically in a ventrum-to-ventrum hold and pecks at the other juvenile without inflicting bite wounds Tackling The juvenile jumps or pounces on another juvenile, usually from a running start Boxing The juvenile bats with the forepaws at another juvenile Chasing The juvenile follows and pursues another juvenile for > 1 m, while both are running Mounting and play The juvenile climbs on the back of another juvenile and places its forepaws around copulation the other juvenile, grasping in its mouth the other juvenile’s neck, cheek, or back and aligning its pelvis with other juvenile’s pelvis; intromission does not occur Table 2 Results of analysis with linear mixed effects model evaluating different variables as possible predictors of docility at first emergence from the natal burrow for 151 juvenile U. beldingi Predictor of juvenile docility (seconds) Estimate Degrees of freedom F P Juvenile body mass (grams) -0.02 1, 118 11.03 0.001 Docility of mother (seconds) -0.14 1, 188 < 0.001 0.987 to evaluate whether docility of juveniles at first emergence R =0.10 from the natal burrow varied with their body mass or the P =0.001 docility of their mothers. A linear mixed effects model was also used to evaluate whether changes in docility of juveniles across the play interval varied with rates of social play, body mass, changes in body mass, or the docility of their mothers. Litter was included as a random effect in linear mixed effects models to account for possible similarities among 15 littermates. Linear regression was used to evaluate whether docility scores of reproductive females prior to emergence of young from the natal burrow were reliable predictors of docility scores after litter emergence and whether rates of 30 40 50 60 70 80 90 100 110 social play among juvenile squirrels were reliable predictors of their scores on docility tests as yearlings. Assumptions of Body mass (grams) homoscedasticity and normal distribution of residuals were met in statistical analyses. Statistical tests were performed Fig. 2 Association between body mass and scores on docility tests at first emergence from the natal burrow for 151 juvenile U. beldingi with Systat 13.1 (Systat Software Inc., Chicago, IL, USA). Relationships indicated by statistical tests were considered significant when P < 0.05. with the body mass of juveniles but not with the docility of their mothers (Table 2). Docility of juveniles tended to Results decrease as their body mass increased, but the association between these variables was weak (Fig. 2). Initial docility of juveniles Changes in juvenile docility The amount of time juvenile U. beldingi were docile during behavioral tests at their first emergence from the natal bur - The amount of time juveniles were docile during behavio- row did not differ between the sexes (t = 0.53, P = 0.597), ral tests decreased significantly between initial tests at first so data for juvenile males and females were combined for emergence from the natal burrow and re-tests near the end of statistical analysis. Body mass of juveniles at first emergence the play period (Fig. 3, t = 10.55, P < 0.001), indicating a from the natal burrow also did not differ between the sexes shift toward more active responses across the play interval. (t = 0.80, P = 0.428) and was not significantly correlated Changes in docility scores over the play interval, expressed with docility of mothers (r = −0.01, P = 0.947). Juvenile as a proportion of the initial score, did not differ between docility during initial behavioral tests varied significantly juvenile males and females (t =1.18, P = 0.241). Scores 1 3 Docility score(sec) 62 Page 6 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 0.4 R =0.18 0.2 P =0.001 a b 0.0 -0.2 -0.4 -0.6 -0.8 -1.0 0- 212- 14 Social play (interactions/hour of observation) Days afteremergingfromthe natalburrow Fig. 4 Association between social play and changes in docility Fig. 3 Box and whisker plots showing docility scores of 151 individ- scores, expressed as a proportion of the initial score, across the play ual juvenile U. beldingi near their first emergence from the natal bur - interval for 90 juvenile U. beldingi row at the onset of the play interval and 12–14 days after emerging from the natal burrow near the end of the play interval. Boxes delimit the 0.25 and 0.75 quantiles, horizontal lines indicate medians, whisk- ers extend to 1.5 interquartile range, and outliers are plotted as indi- Docility of yearlings and reproductive females vidual points. Letters indicate statistical differences at P < 0.05 To evaluate possible longer-term associations between docility and juvenile play, docility tests were conducted on on initial tests were significantly correlated with scores on 23 yearling U. beldingi for whom juvenile play data from re-tests (r = 0.53, P < 0.001) but not with changes in docility the previous year were available. Among these squirrels, over the play interval (r = −0.13, P = 0.223). the rates of social play as a juvenile were reliable predictors Changes in docility of juveniles varied significantly of scores on docility tests as a yearling (Fig. 5, F = 8.64, 1,21 with social play but not with average body mass across P = 0.008, R = 0.26). In particular, squirrels who engaged the play interval, changes in body mass across the play in social play at higher rates as juveniles tended to be less interval, or docility scores of mothers (Table 3). Higher docile as yearlings (Fig. 5). rates of social play were associated with greater decreases To evaluate consistency in docility among individual in docility and greater shifts toward active responses U. beldingi over time and across situations, we conducted (Fig.  4). We note that there were no significant sex docility tests for a total of 30 reproductive females both prior differences in rates of play (t = 1.31, P = 0.194), body to and after the first emergence of their litters from the natal mass (t = 0.45, P = 0.653), or changes in body mass burrow. Among these females, 12 were first tested during (t = 1.33, P = 0.188), and none of the independent gestation, and 18 were first tested during lactation. Docility variables in this analysis was significantly correlated scores increased significantly between the initial test and with any others (−0.24 < r < 0.16, 0.124 < P < 0.999). re-test for females first tested during gestation (Fig.  6, t = We further note that although changes in docility varied 3.17, P = 0.009) but not for those first tested during lactation with rates of social play, the rates of social play were not (t = 0.75, P = 0.465). Scores on initial docility tests were significantly correlated with initial docility scores (r = reliable predictors of scores on the re-tests for females first −0.15, P = 0.159). tested during gestation (Fig. 7A, F = 13.32, P = 0.004, R 1,10 Table 3 Results of analysis Predictor of change in juvenile docility (proportion of initial score) Estimate Degrees F P with linear mixed effects model of free- evaluating different variables as dom possible predictors of change in docility across the play interval Juvenile social play (interactions/hour) −0.06 1, 68 13.16 0.001 for 90 juvenile U. beldingi Average juvenile body mass during play interval (grams) −0.001 1, 68 0.44 0.511 Change in juvenile body mass (proportion of initial mass) 0.05 1, 68 0.26 0.609 Docility of mother (seconds) 0.004 1, 68 0.74 0.392 1 3 Docility score(sec) Change in docility score (proportionofinitial score) Behavioral Ecology and Sociobiology (2023) 77:62 Page 7 of 12 62 R =0.26 P =0.008 R =0.53 P =0.004 05 10 15 20 25 30 0246 8 Gestationdocilityscore (sec) Social play as juvenile (interactions/hour) Fig. 5 Association between rates of social play as juveniles and scores on docility tests as yearlings for 23 Urocitellus beldingi R =0.48 P =0.001 10 05 10 15 20 25 30 Lactationdocilityscore (sec) Fig. 7 Association between docility scores of reproductive female Urocitellus beldingi after first emergence of litters from the natal bur - GestationPost-emergence row and scores during A lactation and B gestation. Twelve females were sampled during gestation and after emergence of young, and 18 Fig. 6 Box and whisker plots showing docility scores of 12 female females were sampled during lactation and after emergence of young Urocitellus beldingi during the reproductive cycle. Boxes delimit the 0.25 and 0.75 quantiles, horizontal lines indicate medians, whiskers extend to 1.5 interquartile range, and outliers are plotted as individual and responses to restraint (Rӧdel and von Hulst 2009; points. Letters indicate a significant difference between stages of the Rӧdel and Monclús 2011; Rӧdel et al. 2017). Body mass in reproductive cycle at P < 0.05 juvenile U. beldingi at first emergence from the natal burrow is associated with the size of fat reserves (Nunes et al. 1999). = 0.53) as well as those first tested during lactation (Fig.  7B, Smaller juveniles tend to have less body fat and thus might be inclined to be more conservative in their energy usage, F = 16.49, P = 0.001, R = 0.48). 1,16 and development of more docile temperaments might be favored in these individuals. Moreover, smaller juveniles Discussion might be less competitive in agonistic interactions and thus might be favored to have more docile and reactive responses Body mass of juvenile U. beldingi in our study was inversely rather than proactive behavior (Sih et al. 2004; Rӧdel and von Hulst 2009). We note, however, that the association related to docility at juveniles’ r fi st emergence from the natal burrow, with smaller juveniles having more docile and less between body mass and docility in juvenile U. beldingi was weak (Fig.  2), and possible influences of body mass active responses during behavioral tests. Body mass has been shown to influence the developmental trajectory of on docility may be relatively minor. Another possibility is that body mass of U. beldingi at emergence from the natal behavioral tendencies in European rabbits (Oryctolagus cuniculus), including exploratory and aggressive behavior burrow reflected the expression of temperament during 1 3 Docility score(sec) Docility score as yearling (sec) Post-emergence docilityscore (sec) Post-emergence docility score (sec) 62 Page 8 of 12 Behavioral Ecology and Sociobiology (2023) 77:62 lactation. That is, more docile juveniles might have been observed that greater social play among juvenile U. beldingi less likely to seek nursing opportunities or might have been was associated with greater increases in caution in response less successful at competing for milk and thus might have to a potential threat. Thus, temperament appears to be plastic been smaller near the time of weaning (Rӧdel et al. 2017). in U. beldingi during the juvenile period. Moreover, possible We did not observe a significant relationship between the refinements in different elements of temperament associated docility of maternal U. beldingi and the docility of their with social play in U. beldingi might better equip young young. However, we cannot rule out here the possibility squirrels to express adaptive responses across a diverse array that other maternal effects influenced the development of of situations they may encounter as they interact with the docility in juvenile U. beldingi in our study. Temperament world around them. is plastic during the postnatal and juvenile periods in a range Social play of U. beldingi as juveniles in this study was of species (Cabrera et al. 2021), and maternal effects on significantly correlated with their docility as yearlings, the development of temperament and other variables have suggesting that possible effects of social play on docility been suggested to prepare offspring to be successful under may extend beyond the juvenile period in this species. prevailing environmental conditions (Storm and Lima 2010; Play behavior has been shown to have a variety of adaptive Kapheim et al. 2011; Dantzer et al. 2013). Environmental benefits during the juvenile period as well as longer-term stresses experienced by mothers can directly affect the way effects on behavior, reproductive success, and survival in a they raise their young, which in turn can affect the behavior variety of species (Bekoff and Byers 1998; Burghardt 2005; as well as growth, metabolism, and immune and endocrine Cameron et al. 2008; Fagen and Fagen 2009; Blumstein function of offspring (Mousseau and Fox 1998; Weinstock et al. 2013; Nunes 2014; Ahloy Dallaire and Mason 2017; 2001; Hayward and Wingfield 2004). For example, environ- Whishaw et  al. 2021). However, we note that studies of mental stressors and prior experience raising young have meerkats (Suricata suricatta) (Sharpe and Cherry 2003; been observed to influence glucocorticoid concentrations in Sharpe 2005a, b, c) and chimpanzees (Pan troglodytes mothers, and glucocorticoids passed to offspring through schweinfurthii) (Heintz et  al. 2017) did not reveal any milk during lactation can influence development of behavior associations between juvenile play and behavior later in and elements of temperament such as boldness and docility life. These discrepancies in longer-term effects of play may (Hinde et al. 2015; Petelle et al. 2017). reflect different courses in the evolution of play behavior Docility among juvenile U. beldingi in our study among different species (Pellis et al. 2014). decreased over the course of the play interval, with the Among maternal U. beldingi in our study, docility scores behavior of juveniles shifting toward more active responses. of individual females during gestation and lactation were Marks et al. (2017) observed that exploratory behavior of reliable predictors of their docility after young emerged from juvenile U. beldingi increased across the play interval, and the natal burrow, indicating consistency among individuals the amount of time to escape from an unfamiliar testing in their tendencies toward docile responses and aligning arena decreased. Juvenile U. beldingi are unfamiliar with docility in this species with Réale et al.’s (2007) definition above-ground elements of their habitat when they first of temperament. However, we observed a significant emerge from the natal burrow, and reactive responses such increase in the docility of maternal U. beldingi between as passive observation might help naïve squirrels avoid gestation and the emergence of their young from the natal potentially dangerous situations and thus might be favored burrow, indicating that although individual females may be by natural selection. However, as young squirrels spend time predisposed to different degrees of docility, expression of above ground and gain familiarity with their surroundings, docility can be influenced by factors such as reproductive exploration and proactive responses might be favored to help state and may vary across different contexts. Maternal individuals gather additional information about and navigate U. beldingi exhibit peak aggressive behavior during the through their physical and social environments as they begin gestational period when they are competing for burrow to venture farther from their natal home areas (Sih et al. systems and space in which to establish a maternal territory, 2004). and rates of aggression decrease substantially after gestation We observed a significant relationship between social (Nunes et al. 1997, 2000). Thus, changes in docility across play and decreases in docility of juvenile U. beldingi after the reproductive cycle may reflect increases in aggressive emergence from the natal burrow. Juveniles who played at behavior or general tendencies toward more proactive higher rates tended to have greater decreases in docility and responses when establishing a maternal territory. greater shifts toward active responses in behavioral tests. The possible effects of social play on the development Marks et  al. (2017) similarly observed that juvenile U. temperament along the docility spectrum may be mediated beldingi who engaged in social play at higher rates tended by effects on the developing brain. Some elements of brain to have greater increases in exploratory behavior after development are plastic during the postnatal and juvenile emergence from the natal burrow. Shehan (2019) further periods, and a range of experiences after birth can play 1 3 Behavioral Ecology and Sociobiology (2023) 77:62 Page 9 of 12 62 an important role in directing specific aspects of neural Declarations and behavioral development (Johnson 2001; Stiles and Ethics approval The study followed guidelines for use of animals in Jernigan 2010; Kolb and Gibb 2011; Sakai and Sugiyama field research published by the American Society of Mammalogists. 2018). For example, in rats, social play experiences during Work for the study was conducted under permit SC-2008 from the early development are necessary for the establishment of California Department of Fish and Wildlife and permits LVD16018 and LVD17005 from the US Forest Service. Institutional approval for competent social skills and the normal expression of social use of animals in the study was not required by the University of San behavior in adulthood (Pellis et al. 2014; Stark and Pellis Francisco. 2020; Stark et  al. 2021). Juvenile play in rats has also been shown to modify development of areas in the frontal Conflict of interest The authors declare no competing interests. cortex associated with motor and social behavior as well as behavioral flexibility (Bell et al. 2010; Pellis et al. 2010; Open Access This article is licensed under a Creative Commons Attri- bution 4.0 International License, which permits use, sharing, adapta- Himmler et al. 2013, 2017; Burleson et al. 2016). tion, distribution and reproduction in any medium or format, as long Pellis et  al. (2019) proposed that in some species, as you give appropriate credit to the original author(s) and the source, play may comprise a behavioral system devoted to the provide a link to the Creative Commons licence, and indicate if changes expression and regulation of play behaviors. This idea were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated suggests that play arose evolutionarily as non-functional otherwise in a credit line to the material. If material is not included in expression during early development of behaviors that are the article's Creative Commons licence and your intended use is not functional in adulthood. Over time, these behaviors were permitted by statutory regulation or exceeds the permitted use, you will modified by natural selection into specific play behaviors need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . that provided various adaptive benefits to individuals and that were regulated by distinct neural systems (Burghardt 2005; Pellis et al. 2014, 2015). Pellis et al. (2019) noted that in some species, behavior systems related to play may References be complex. Social play can be diverse and can involve planning interactions with other individuals as well as Ahloy Dallaire J, Mason GM (2017) Rough-and-tumble play predicts adult sexual behavior in American mink. Anim Behav 123:81–89. responding to the actions of play partners and unfamiliar https:// doi. org/ 10. 1016/j. anbeh av. 2016. 10. 023 circumstances that arise during play interactions (Pellis Auger AP, Olesen KM (2009) Brain sex differences and the organiza- and Pellis 2017; Palagi 2018). We suggest social play in tion of juvenile social play behaviour. J Neuroendocrinol 21:519– juvenile U. beldingi may reinforce behavioral responses 525. https:// doi. org/ 10. 1111/j. 1365- 2826. 2009. 01871.x Baugh AT, van Oers K, Naguib M, Hau M (2013) Initial reactivity and that a function of play in this species might be to refine and magnitude of the acute stress response associated with per- development of temperament and promote responses that sonality in wild great tits (Parus major). Gen Comp Endocrinol help young animals maneuver through their surroundings 189:96–104. https:// doi. org/ 10. 1016/j. ygcen. 2013. 04. 030 and social situations they may encounter. Bekoff M, Byers JA (1998) Animal play: evolutionary, comparative, and ecological processes. Cambridge University Press, Cam- Supplementary Information The online version contains supplementary bridge, UK material available at https:// doi. org/ 10. 1007/ s00265- 023- 03341-7. Bell HC, Pellis SM, Kolb B (2010) Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cor- Acknowledgements We thank Nicole Thometz and Naupaka tices. Behav Brain Res 2017:7–13. https:// doi. org/ 10. 1016/j. bbr. Zimmerman for their valuable insights throughout this work and 2009. 09. 029 assistance with statistical analyses. We further thank two anonymous Blumstein DT, Chung LK, Smith JE (2013) Early play may predict reviewers for suggestions to improve the paper’s conceptual framework later dominance relationships in yellow-bellied marmots (Mar- and statistical analyses. Naomi Logwood, Emma Gibson, Karen Marks, mota flaviventris). Proc R Soc B 280:20130485. https:// doi. org/ and Jennifer Rodriguez provided excellent assistance in the field.10. 1098/ rspb. 2013. 0485 Boon AK, Réale D, Boutin S (2007) The interaction between person- Author contribution JH-H and SN conceived and designed the study. ality, offspring fitness and food abundance in North American All authors contributed to collection of data. JH-H, NL, and SN red squirrels. Ecol Lett 10:1094–1104. https:// doi. org/ 10. 1111/j. contributed to analysis of data. JH-H and SN wrote the first draft of 1461- 0248. 2007. 01106.x the manuscript. All authors contributed to revision of the manuscript Boon AK, Réale D, Boutin S (2008) Personality, habitat use, and their and approved the final manuscript. consequences for survival in North American red squirrels Tami- asciurus hudsonicus. Oikos 117:1321–1328. https:// doi. org/ 10. Funding Open access funding provided by SCELC, Statewide 1111/j. 0030- 1299. 2008. 16567.x California Electronic Library Consortium. This study was supported Both C, Dingemanse NJ, Drent PJ, Tinbergen JM (2005) Pairs of by the Faculty Development Fund and Department of Biology at the extreme avian personalities have highest reproductive success. University of San Francisco. J Anim Ecol 74:667–674. https:// doi. org/ 10. 1111/j. 1365- 2656. 2005. 00962.x Data availability The data reported in this paper are available in a Burghardt GM (2005) The genesis of animal play: testing the limits. supplementary information file. 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Journal

Behavioral Ecology and SociobiologySpringer Journals

Published: Jun 1, 2023

Keywords: Docility; Ground squirrel; Juvenile development; Plasticity; Social play; Temperament

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