Endocrine and Energetic Mediation of Play Behavior in Free-Living Belding's Ground Squirrels

Nunes, Scott; Muecke, Eva-Maria; Anthony, Jessica A.; Batterbee, Aaron S.

doi:10.1006/hbeh.1999.1538

Cited by 56 publications

(60 citation statements)

References 66 publications

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“…The first report of play-fighting among ground squirrels was published in the same year (Steiner, 1971) and only much later systematically dissociated from agonistic behavior (Pellis & Pellis, 1987; Pellis, 1988). More recently, free-living male juveniles of S. richardsonii and S. beldingi were shown to engage in more play fighting than females (Nunes et al, 1999; Pasztor et al, 2001) This sexually dimorphic pattern is also expressed by juvenile laboratory rats (Olioff & Stewart, 1978; Pellis, 2002) and play-fighting was found to be rewarding, as revealed by CPP experiments (Calcagnetti & Schechter, 1992; Siviy, 1998). Physiological studies show that play fighting is influenced by activation of perinatal steroid receptors (Meaney & Stewart, 1981; Olesen, Jessen, Auger, & Auger, 2005) and supported by juvenile reward circuits (Burgdorf, Panksepp, Beinfeld, Kroes, & Moskal, 2006; Siviy, Fleischhauer, Kerrigan, & Kuhlman, 1996; Trezza & Vanderschuren, 2008).…”

Section: Discussionmentioning

confidence: 94%

Social conditioned place preference in the captive ground squirrel (Ictidomys tridecemlineatus): Social reward as a natural phenotype.

Lahvis

Panksepp

Kennedy

et al. 2015

Journal of Comparative Psychology

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Social behaviors of wild animals are often considered within an ultimate framework of adaptive benefits versus survival risks. By contrast, studies of laboratory animals more typically focus on affective aspects of behavioral decisions, whether a rodent derives a rewarding experience from social encounter and how this experience might be initiated and maintained by neural circuits. Artificial selection and inbreeding have rendered laboratory animals more affiliative and less aggressive than their wild conspecifics, leaving open the possibility that social reward is an artifact of domestication. We compared social behaviors of wild and captive population of juvenile 13-lined ground squirrels (Ictidomys tridecemlineatus), the latter 2nd and 3rd generation descendents of wild individuals. At an age corresponding to emergence from the burrow, postnatal day 38, captive squirrels engaged in vigorous social approach and play; these juvenile behaviors declined significantly by postnatal day 56. Similarly, young wild squirrels expressed social proximity and play, affiliative interactions declined with summer’s progression and were replaced by agonistic chasing behaviors. Social conditioned place preference testing (conditioned postnatal days 40–50) indicated that adolescent squirrels derived a rewarding experience from social reunion. Our results support the contention that undomesticated rodents have the capacity for social reward and more generally suggest the possibility that positive affective experiences may support group cohesion and social cooperation in the wild.

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Section: Discussionmentioning

confidence: 94%

Social conditioned place preference in the captive ground squirrel (Ictidomys tridecemlineatus): Social reward as a natural phenotype.

Lahvis

Panksepp

Kennedy

et al. 2015

Journal of Comparative Psychology

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“…Under laboratory conditions, squirrel monkeys that needed to work harder to obtain food, and hence increase foraging time, played at 1% of their normal level (Baldwin and Baldwin 1976). Similarly, Nunes et al (1999) reported that in unprovisioned ground squirrels, a trade-off between time available for feeding and for social activities limited play. Conversely, Sharpe et al (2002) demonstrated that an increase in available energy, instead of simply an increase in available time, contributed to a rise in play rates in free-ranging meerkats.…”

Section: Discussionmentioning

confidence: 95%

“…Troops of langurs (Semnopithecus entellus) in poor-quality habitats played 6-7 times less than troops in rich habitats did (Sommer and Mendoza-Granados 1995). Food supplementation experiments in free-ranging mammals showed that provisioning increases the rate of play (Nunes et al 1999;Sharpe et al 2002). For example, in juvenile meerkats (Suricatta suricatta), mass gain over a 6-wk period correlated positively with rates of play (Sharpe et al 2002).…”

Section: Introductionmentioning

confidence: 93%

Seasonal Effects on Play Behavior in Immature Saimiri sciureus in Eastern Amazonia

Stone

2008

Int J Primatol

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Play behavior is prevalent among most mammalian young, particularly primates. Though several hypotheses address the function of play, researchers have documented information on the potential costs of play and of environmental effects on the occurrence of primate play less well during long-term field studies. I examine seasonal changes in play behavior of immature squirrel monkeys (Saimiri sciureus) across 4 age classes: infants, young juveniles, mid-juveniles, and late juveniles. I observed individuals during 12 mo in Eastern Brazilian Amazonia, an area characterized by highly seasonal rainfall. Play was strongly tied to seasonality, food availability, and changes in diet. The percentage of time spent playing was reduced in the dry season, a period characterized by low fruit availability and an increase in time spent foraging for prey. I suggest that the decrease in play behavior in the dry season is related both to a higher need for energy conservation and to increased time expended in foraging activities.

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“…Play fighting is sensitive to opiate administration (Vanderschuren et al 1997), suggesting hedonia is associated with this self-versus-other, back-and-forth activity (Panksepp 1998). Explanations for the energy demanding behavior among wild mammals include its role in improving emotional responsiveness to unexpected events (Nunes et al 1999; Spinka et al 2001), familiarizing participants with self-handicap and fair behavior (Bekoff 2004), improving abilities to cope with social challenges (van den Berg et al 1999), establishing dominance relationships (Blumstein et al 2013), and helping refine abilities to respond to subtle and ambiguous social signals (Pellis et al 2010). The give-and-take of social play promotes normal brain development (Gordon et al 2003; Pellis and Pellis 2007).…”

Section: Empathymentioning

confidence: 99%

Social Reward and Empathy as Proximal Contributions to Altruism: The Camaraderie Effect

Lahvis

2016

Current Topics in Behavioral Neurosciences

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Natural selection favors individuals to act in their own interests, implying that wild animals experience a competitive psychology. Animals in the wild also express helping behaviors, presumably at their own expense and suggestive of a more compassionate psychology. This apparent paradox can be partially explained by ultimate mechanisms that include kin selection, reciprocity, and multilevel selection, yet some theorists argue such ultimate explanations may not be sufficient and that an additional “stake in others” is necessary for altruism’s evolution. We suggest this stake is the “camaraderie effect,” a by-product of two highly adaptive psychological experiences: social motivation and empathy. Rodents can derive pleasure from access to others and this appetite for social rewards motivates individuals to live together, a valuable psychology when group living is adaptive. Rodents can also experience empathy, the generation of an affective state more appropriate to the situation of another compared to one’s own. Empathy is not a compassionate feeling but it has useful predictive value. For instance, empathy allows an individual to feel an unperceived danger from social cues. Empathy of another’s stance toward one’s self would predict either social acceptance or ostracism and amplify one’s physiological sensitivity to social isolation, including impaired immune responses and delayed wound healing. By contrast, altruistic behaviors would promote well-being in others and feelings of camaraderie from others, thereby improving one’s own physiological well-being. Together, these affective states engender a stake in others necessary for the expression of altruistic behavior.

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Endocrine and Energetic Mediation of Play Behavior in Free-Living Belding's Ground Squirrels

Cited by 56 publications

References 66 publications

Social conditioned place preference in the captive ground squirrel (Ictidomys tridecemlineatus): Social reward as a natural phenotype.

Social conditioned place preference in the captive ground squirrel (Ictidomys tridecemlineatus): Social reward as a natural phenotype.

Seasonal Effects on Play Behavior in Immature Saimiri sciureus in Eastern Amazonia

Social Reward and Empathy as Proximal Contributions to Altruism: The Camaraderie Effect

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