Pellis, Sergio

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    Behavior systems approach to object play: stone handling repertoire as a measure of propensity for complex foraging and percussive tool use in the genus Macaca
    (SciKnow Publications, 2017) Pelletier, Amanda N.; Kaufmann, Tatjana; Mohak, Sidhesh; Milan, Riane; Nahallage, Charmalie A. D.; Huffman, Michael A.; Gunst, Noëlle; Rompis, Aida; Wandia, I Nengah; Arta Purta, I Gusti A.; Pellis, Sergio M.; Leca, Jean-Baptiste
    Stone handling (SH), has been identified in four closely related primate species of the Macaca genus. We provide the first ethogram of SH in long-tailed macaques (Macaca fascicularis), a primate species known to use stones for extractive foraging. A total of 62.7 hrs of video recorded data were scored from a population of Balinese long-tailed macaques living in Ubud, Bali, Indonesia, and a total of 36 stone handling patterns were identified. Behavior discovery curves were generated and showed that the minimum threshold of completeness was exceeded for the SH repertoire in this group. A “foraging substitute” hypothesis for the expression of SH was proposed, suggesting that SH consists of performing foraging-like actions on non-edible objects. We used a “behavior systems” framework to test this prediction, finding that all 36 stone handling patterns could be reliably categorized in a foraging behavior system, supporting the hypothesis that stone handling can be considered pseudo-foraging behavior. Our “behavior systems” approach will serve as a foundation for the future testing of the motivational basis of stone handling. Additionally, a comparison of 39 stone handling patterns performed by three macaque species (M. fascicularis, M. fuscata and M. mulatta) showed overlapping behavioral propensities to manipulate stones; however, the differences suggest that long-tailed macaques might be more prone to use stones as percussive tools in a foraging context. This work could offer insights into the development and evolution of complex activities such as percussive stone tool use in early humans.
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    The development of juvenile-typical patterns of play fighting in juvenile rats does not depend on peer-peer play experience in the peri-weaning period
    (eScholarship Publishing, University of California, 2015) Himmler, Brett T.; Himmler, Stephanie M.; Stryjek, Rafal; Modlinska, Klaudia; Pisula, Wojciech; Pellis, Sergio M.
    Play fighting in rats involves attack and defense of the nape. To protect the nape, rats use a variety of defensive tactics, with different strains having specific preferences. Targeting of the nape is established before weaning and defense matures over the course of the week preceding and the week proceeding weaning. Thus, it is possible that experience from engaging in immature forms of play is needed to consolidate the nape as the playful target and for the development of the juvenile-typical pattern of defense. Two experiments were conducted to evaluate this possibility. For the first experiment, male rats were reared over the week post-weaning in either pairs or alone, and their play tested with unfamiliar partners when juveniles (31-34 days). For the second experiment, during the week preceding weaning, male and female rats were placed into one of three conditions: (1) with the mother and no peers, (2) with same-sex siblings but no mother, or (3) with both the mother and same-sex siblings. The subjects were tested in same-sex, samecondition pairs when juveniles (31-34 days). Rats from all conditions, in both experiments, attacked the nape during play fighting and developed the same juvenile-typical patterns of playful defense. This suggests that the experience of peer-peer play in the peri-weaning period is not necessary for the development of the attack and defense components of juvenile-typical play.
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    The development of strain typical defensive patterns in the play fighting of laboratory rats
    (eScholarship Publishing, University of California, 2014) Himmler, Stephanie M.; Lewis, Jena M.; Pellis, Sergio M.
    During play fighting, rats attack and defend the nape, which if contacted is nuzzled with the snout. While all strains of rats use the same suite of defensive tactics to protect the nape, different strains use some tactics more frequently. This study tests two hypotheses for this strain difference: (1) each strain has a preference for using particular tactics and (2) strain differences in defense are a byproduct of strain differences in patterns of nape attack. Juvenile Long-Evans (LE) and Sprague-Dawley (SD) males, raised in same strain quads from shortly after weaning to the early juvenile period (i.e., 24-31 days), were tested with unfamiliar same-strain and different-strain partners (Experiment 1) and LE and SD males raised in mixed LE-SD quads were tested with both familiar (Experiment 2) and unfamiliar same-strain and different-strain partners. If hypothesis (1) were true, they would maintain strain-typical defense patterns irrespective of the strain of the attacking partner, whereas if hypothesis (2) were true, it would vary with the strain of the attacking partner. Hypothesis (1) was supported in the first experiment; all the rats maintained their strain-typical patterns regardless of the partner’s strain. However, Experiments 2 and 3 supported neither hypothesis, as each animal displayed strain-divergent behavior when playing with partners of either strain. Given that in Experiments 2 and 3, subjects were reared in mixed-strain groups, it is possible that, during the early juvenile period, play fighting experiences shape strain-typical patterns of use of defensive tactics.
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    Is play a behavior system, and, if so, what kind?
    (Elsevier, 2019) Pellis, Sergio M.; Pellis, Vivien C.; Pelletier, Amanda; Leca, Jean-Baptiste
    Given that many behavior patterns cluster together in sequences that are organized to solve specific problems (e.g., foraging), a fruitful perspective within which to study behaviors is as distinct ‘behavior systems’. Unlike many behavior systems that are widespread (e.g., anti-predator behavior, foraging, reproduction), behavior that can be relegated as playful is diverse, involving behavior patterns that are typically present in other behavior systems, sporadic in its phylogenetic distribution and relatively rare, suggesting that play is not a distinct behavior system. Yet the most striking and complex forms of play have the organizational integrity that suggests that it is a behavior system. One model that we develop in this paper, involves three stages of evolutionary transition to account for how the former can evolve into the latter. First, play-like behavior emerges from the incomplete development of other, functional behavior systems in some lineages. Second, in some of those lineages, the behavior patterns typical of particular behavior systems (e.g., foraging) are reorganized, leading to the evolution of specific ‘play behavior systems’. Third, some lineages that have independently evolved more than one such play behavior system, coalesce these into a ‘super system’, allowing some animals to combine behavior patterns from different behavior systems during play. Alternative models are considered, but irrespective of the model, the overall message from this paper is that the conceptual framework of the behavior system approach can provide some new insights into the organization and diversity of play present in the animal kingdom.
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    Pinning in the play fighting of rats: a comparative perspective with methodological recommendations
    (eScholarship Publishing, University of California, 2016) Himmler, Stephanie M.; Himmler, Brett T.; Stryjek, Rafal; Modlinska, Klaudia; Pisula, Wojciech; Pellis, Sergio M.
    During play fighting, rats attack and defend the nape of the neck and during the course of this competitive interaction, they may adopt a configuration in which one animal stands over its supine partner (i.e., pin). Because the pin configuration is typically frequent and relatively easy to identify, it has been widely used as a marker to detect the effects of experimental treatments. In the present study, the frequency of pinning during standardized, 10-min trials in three strains of rats, Long Evans hooded (LE), Sprague-Dawley (SD) and wild (WWCPS), was compared. LE and SD had higher rates than WWCPS rats (#/min: 6.5, 5.5, 1.5, respectively). When adjusted for strain differences in the frequency of attacks, SD as well as WWCPS rats had lower rates of pinning compared to LE rats. Both SD and WWCPS rats were less likely to use tactics of defense that promote pinning. Moreover, while the majority of the pins achieved in LE rats arose from the defender actively rolling over onto its back, the majority of pins in WWCPS rats arose because one partner pushed the other onto its back. SD rats were intermediate in this regard. Finally, once they do adopt the pin configuration, SD rats are less likely to remain supine than LE and WWCPS rats. That is, both SD and WWCPS rats have significantly fewer pins than LE rats, but a different combination of factors account for this. These data highlight the need to use a battery of measures for ascertaining the effects of experimental manipulations on play. Some suggested guidelines are provided.
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    Play fighting revisited: its design features and how they shape our understanding of its mechanism and functions
    (Frontiers Media, 2024) Pellis, Sergio M.; Pellis, Vivien C.; Ham, Jackson R.
    Play fighting has been one of the most intensely studied forms of play and so has provided some of our deepest insights into the understanding of play in general. As the label implies, this behavior resembles serious fighting, in that the animals compete for an advantage over one another, but unlike true aggression, for play fighting to remain playful, it also incorporates a degree of cooperation and reciprocity – restrained competition seems to be its hallmark. Despite these common features, it should be noted that both the advantage competed over and the mechanisms by which restraint is achieved varies across species. Such variation mitigates simple generalities. For example, how empirical support for a proposed adaptive function in one species not being replicated in another, is to be interpreted. What has emerged over the past few decades is that play fighting is diverse, varying across several dimensions, some superficial, some fundamental, making choosing species to compare a challenge. In this paper,we explore various design features that constitute play fighting and the ways these can be modified across different species and lineages of species. Given that a major pillar of ethology is that description precedes explanation, having a good grasp of the behavioral diversity of play fighting is an essential starting point for detailed analyses of the mechanisms and functions of play. We show that commonalities across species likely involve different mechanisms than do species idiosyncrasies, and that different styles of play fighting likely afford different adaptive opportunities
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    Quality not quantity: deficient juvenile play experiences lead to altered medial prefrontal cortex neurons and sociocognitive skill deficits
    (Wiley, 2024) Ham, Jackson R.; Szabo, Madeline; Annor-Bediako, Jessica; Stark, Rachel A.; Iwaniuk, Andrew N.; Pellis, Sergio M.
    Reduced play experience over the juvenile period leads to adults with impoverished social skills and to anatomical and physiological aberrations of the neurons found in the medial prefrontal cortex (mPFC). Even rearing rats from high-playing strains with low-playing strains show these developmental consequences. In the present study, we evaluated whether low-playing rats benefit from being reared with higher playing peers. To test this, we reared male Fischer 344 rats (F344), typically thought to be a low-playing strain, with a Long–Evans (LE) peer, a relatively high-playing strain. As juveniles, F344 rats reared with LE rats experienced less play and lower quality play compared to those reared with another F344. As adults, the F344 rats reared with LE partners exhibited poorer social skills and the pyramidal neurons of their mPFC had larger dendritic arbors than F344 rats reared with same-strain peers. These findings show that being reared with a more playful partner does not improve developmental outcomes of F344 rats, rather the discordance in the play styles of F344 and LE rats leads to poorer outcomes.
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    Specific 50-kHv vocalizations are tightly linked to particular types of behavior in juvenile rats anticipating play
    (Public Library of Science, 2017) Burke, Candace J.; Kisko, Theresa M.; Swiftwolfe, Hilarie; Pellis, Sergio M.; Euston, David R.
    Rat ultrasonic vocalizations have been suggested to be either a byproduct of physical movement or, in the case of 50-kHz calls, a means to communicate positive affect. Yet there are up to 14 distinct types of 50-kHz calls, raising issues for both explanations. To discriminate between these theories and address the purpose for the numerous 50-kHz call types, we studied single juvenile rats that were waiting to play with a partner, a situation associated with a high number of 50-kHz calls. We used a Monte-Carlo shuffling procedure to identify vocalization-behavior correlations that were statistically different from chance. We found that certain call types (“split”, “composite” and “multi-step”) were strongly associated with running and jumping while other call types (those involving “trills”) were more common during slower movements. Further, non-locomotor states such as resting and rearing were strongly predictive of a lack of vocalizations. We also found that the various sub-types of USVs can be clustered into 3–4 categories based on similarities in the way they are used. We did not find a one-to-one relationship between any movements and specific vocalizations, casting doubt on the motion byproduct theory. On the other hand, the use of specific calls during specific behaviors is problematic for the affect communication hypothesis. Based on our results, we suggest that ultrasonic calls may serve to coordinate moment-to-moment social interactions