Animal play and evolution: Seven timely research issues about enigmatic phenomena.

The nature of play in animals has been long debated, but progress is being made in characterizing play and its variants, documenting its distribution across vertebrate and invertebrate taxa, describing its mechanisms and development, and proposing testable theories about its origins, evolution, and adaptive functions. To achieve a deeper understanding of the functions and evolution of play, integrative and conceptual advances are needed in neuroscience, computer modeling, phylogenetics, experimental techniques, behavior development, and inter- and intra-specific variation. The special issue contains papers documenting many of these advances. Here, we describe seven timely areas where further research is needed to understand this still enigmatic class of phenomena more fully. Growing empirical and theoretical evidence reveals that play has been crucial in the evolution of behavior and psychology but has been underestimated, if not ignored, in both empirical and theoretical areas of evolutionary biology and neuroscience. Play research has important ramifications for understanding the evolution of cognition, emotion, and culture, and research on animals can be both informative and transformative.

A review of interspecific social play among nonhuman animals.

Few species play socially with another species, hereafter called interspecific social play (ISP). ISP involves reading and responding appropriately to social cues of other species, often taxonomically remote, and has implications for perception, communication, and cognition. We reviewed information on non-human ISP from both print media and videos from YouTube and Reddit. We found over 200 instances of ISP. The literature predominantly featured wild primates, carnivores, and marine mammals. Carnivores and terrestrial ungulates were common in videos. ISP in avian and reptile species were found in both sources, including instances of playing with mammals. Animals may engage in ISP because it is risky and stimulating, they lack age-appropriate conspecifics, the play motivation is high, or to maintain social bonds in mixed-species groups. Cataloguing ISP uncovers which species are interacting and how. Systematic studies of ISP are difficult and many reports are brief and anecdotal. Minimally, future research should record information about each observation, including the age, sex, and history of participants.

A Descriptive Methodology for Studying the Ontogeny of Object Play and Breed Differences in Dogs (Canis lupus familiaris).

Play behavior is a prominent aspect of juvenile behavior for many animals, yet early development, especially play with objects, has received little attention. Our previous study on object play introduced our general methods, focusing on litter differences in the developmental trajectory of object play and toy preferences. Here, we present a detailed ethogram of more than 30 observed object play behaviors. We focus on breed differences in the development of play in the three following breeds: Welsh Terriers, Vizslas, and standard Poodles. Puppies were video recorded from 3 to 7 weeks of age at half-week intervals upon the introduction of a standard set of five toys into their home environments. Ten minutes of video from each session for each puppy were analyzed using the Noldus Observer XT program. Aside from analyzing individual behaviors, they were also grouped into three behavioral categories. These were behaviors that occurred only in a solitary context, only in a social context, or in both contexts. Solitary object play developed first, and social object play developed later across breeds. There was a significant three-way interaction between breed, developmental age, and the context in which play occurred. Pairwise comparisons within each breed, age, and context are discussed, but a prominent result is that the onset of many behaviors occurred later in Welsh Terriers compared to the other breeds.

Comparing the ontogeny, neurobiology, and function of social play in hamsters and rats.

Syrian hamsters show complex social play behavior and provide a valuable animal model for delineating the neurobiological mechanisms and functions of social play. In this review, we compare social play behavior of hamsters and rats and underlying neurobiological mechanisms. Juvenile rats play by competing for opportunities to pin one another and attack their partner's neck. A broad set of cortical, limbic, and striatal regions regulate the display of social play in rats. In hamsters, social play is characterized by attacks to the head in early puberty, which gradually transitions to the flanks in late puberty. The transition from juvenile social play to adult hamster aggression corresponds with engagement of neural ensembles controlling aggression. Play deprivation in rats and hamsters alters dendritic morphology in mPFC neurons and impairs flexible, context-dependent behavior in adulthood, which suggests these animals may have converged on a similar function for social play. Overall, dissecting the neurobiology of social play in hamsters and rats can provide a valuable comparative approach for evaluating the function of social play.

How comparative was (is) the Journal of Comparative Psychology? A reptilian perspective.

[Correction Notice: An Erratum for this article was reported in Vol 135(3) of Journal of Comparative Psychology (see record 2021-87304-004). In the article "How Comparative Was (Is) the Journal of Comparative Psychology? A Reptilian Perspective" by Gordon M. Burghardt (Journal of Comparative Psychology. Advance online publication. August 5, 2021. http://doi.org/10.1037/com0000290), the phrase in the introduction that includes the Dewbury (1998) citation also includes an extra word. The phrase should appear as Dewbury (1998) noted that the focus. The year of publication for the Journal of Animal Behavior that appears in the third line of the Method section should appear as (1911-1917). The last sentence in the first paragraph of the Method section should appear as The 8,911 entries over this 110-year period constituted the data analyzed here in detail. The first sentence of the Results section should appear as The Journal of Animal Behavior published 238 articles in its 7-year run. The last phrase of the first paragraph of the Results section should appear as and 8,635 published items of the JCP and JCPP....] Comparative psychology, and particularly the Journal of Comparative Psychology, has been criticized for a lack of taxon diversity. The nature and consequences of the critiques are discussed and assessed by analyzing the representation of nonavian reptiles in the journal over its 100-year existence. Although reptiles are indeed rare in the journal, their representation has greatly increased in recent decades, and especially since about 1980. More interestingly, the mix among the major reptilian groups: turtles, lizards, snakes, and crocodylians, has shifted. First turtles predominated in studies, but in recent decades, snakes were far more prominent. In the last 50 years of the journal, there were 10 times the number of articles on snakes than in the first 50 years, turtles declined, and lizards increased greatly, although their totals remained less than half the number of snake articles. Crocodylians only appeared in the first several volumes in the 1920s and never again. The predominance of snakes, not known for their cognitive prowess, in a journal viewed increasingly as an outlet for work on comparative cognition, is discussed. Finally, it appears that the low representation of reptile behavioral research is not peculiar to the Journal of Comparative Psychology, but animal behavior journals more generally. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Behavior in Free-Living American Black Bear Dens: Parturition, Maternal Care, and Cub Behavior.

Denning behavior has long remained the least observed aspect of bear behavior. During 2010-2013, we used webcams, microphones, the internet, and 14,602 h of archived video to document the denning behaviors of two adult wild black bears (Ursus americanus) as they gave birth and cared for four litters through six winters in northeastern Minnesota. Observations included types of dens, labor, pre-parturient genital swelling, birthing positions, post-partum vocalizations, mothers removing amniotic tissues and warming newborn cubs in sub-freezing temperatures, frequency of nursing, cubs establishing nipple order, yearlings suckling, the ingestion of snow and icicles, the ingestion of foot pads, urination and defecation in latrine areas, toilet-licking, eye opening, reciprocal tongue-licking, play, rapid eye movement (REM) sleep and possible dreaming, and reactions to wildlife intruders. The use of this new method for observing natural bear dens allowed the identification of many behaviors undescribed for any species of wild bear in dens. We also discuss the need for future studies and how the depth and duration of black bear hibernation varies with body condition and geographic region.

A place for emotions in behavior systems research.

Although issues of motivation, including appetitive searching behavior, have been crucial aspects of behavior systems approaches since their inception, as well as in the ethological research and models that inspired them, emotions and affect have been noticeably absent in such analyses. Emotions and affect may have been lying below the surface all the time, however, as motivation, emotion, and cognitive processing are embedded in all aspects of behavior, including conditioning and learning. Here a brief case is made that emotions and related hedonic processes, can and should be explicitly incorporated into behavior systems approaches. Evidence from recent behaviorist, neuroscience, and animal behavior (including human) studies suggest that emotions may, just as motivational drives, lead to appetitive searching and avoidance, both general and focal, as well as consummatory acts with emotional consequences and satiation. Research testing these claims, as well as theoretical formulations and evaluations, would be timely and extend the reach of behavior systems approaches to a far wider swath of psychological research than it has engaged with hitherto.

Development of social play in hamsters: Sex differences and their possible functions.

In several rodent species social play appears to be necessary for proper deployment of species-specific patterns of aggressive and reproductive behavior. Specifically, in male Syrian hamsters (Mesocricetus auratus), play has been linked to the development of adult aggression. We quantified several types of social play behavior in same-sex peer groups of Syrian hamsters three times per week for three consecutive weeks after weaning, which included postnatal days 22-42 (PD22 to PD42). Male hamsters increased playful contact during PD36-PD42, whereas females showed peak playful contact during PD29-PD35. These findings suggest that the motivation for social play increases during mid-adolescence in males, but dissipates in females. To investigate the effects of social play deprivation, one hamster per litter remained pair-housed with its mother forthree weeks after weaning its littermates. In adulthood, both play-deprived and play-exposed animals received acute social defeat stress followed by social interaction testing. Play deprivation led to increased defeat-induced social avoidance in both males and females. In males, play deprivation increased fighting back during social defeat stress, whereas in females it reduced aggressive behavior during conditioned defeat testing. We suggest that social play deprivation disrupts neural circuits regulating aggression in a sex-specific manner, perhaps related to sex differences in territorial defense, but has similar effects on neural circuits regulating stress responsivity. Overall, these findings suggest that juvenile social play functions to promote coping with stress and appropriate social behavior in adulthood.

Wallace Craig's Appetites and aversions as constituents of instincts: A centennial appreciation.

Wallace Craig's "Appetites and Aversions as Constituents of Instincts," one of the seminal articles in animal behavior, comparative psychology, and ethology, appeared 100 years ago this year. The influence of this classic article is continuing and perhaps even expanding. Here we review the major ideas Craig offered in the article, provide a brief sketch of his scientific career and historical context, and examine the impact of the article on ethological and instinct theory. We also review some current applications of his work in diverse areas and discuss why it is cited more now than in earlier decades, especially in articles on causal mechanisms. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Toward a Theory of the Evolution of Fair Play.

Juvenile animals of many species engage in social play, but its functional significance is not well understood. This is especially true for a type of social play called fair play (Fp). Social play often involves behavioral patterns similar to adult behaviors (e.g., fighting, mating, and predatory activities), but young animals often engage in Fp behaviors such as role-reversals and self-handicapping, which raises the evolutionary problem of why Fp exists. A long-held working hypothesis, tracing back to the 19th century, is that social play provides contexts in which adult social skills needed for adulthood can be learned or, at least, refined. On this hypothesis, Fp may have evolved for adults to acquire skills for behaving fairly in the sense of equitable distribution of resources or treatment of others. We investigated the evolution of Fp using an evolutionary agent-based model of populations of social agents that learn adult fair behavior (Fb) by engaging in Fp as juveniles. In our model, adults produce offspring by accumulating resources over time through foraging. Adults can either behave selfishly by keeping the resources they forage or they can pool them, subsequently dividing the pooled resources after each round of foraging. We found that fairness as equitability was beneficial especially when resources were large but difficult to obtain and led to the evolution of Fp. We conclude by discussing the implications of this model, for developing more rigorous theory on the evolution of social play, and future directions for theory development by modeling the evolution of play.

Do tiger keelback snakes (Rhabdophis tigrinus) recognize how toxic they are?

Animals that depend on defensive chemicals acquired from food may face a decision when attempting to deter predatory attacks: Should they exhibit antipredator behavior that relies on the toxicity of the sequestered chemicals or should they adopt other behaviors that can avoid predation without using the chemical defense, such as flight? Thus, it is reasonable to assume that animals that sequester prey toxins have evolved the ability to flexibly change their antipredator responses according to the amount of toxin-resource they have consumed. We tested this hypothesis using an Asian snake, Rhabdophis tigrinus, that sequesters toxins from toads consumed as food and stores them in specialized organs back of the head, called nuchal glands. We reared hatchling snakes from toad-free and toad-rich islands on controlled diets and examined their subsequent antipredator responses after 3 and 6 month feeding. Juveniles from a toad-free island that had been fed a diet including toads for 3 months showed antipredator displays associated with the nuchal glands more frequently than those that had been fed a diet without toads. They showed a similar, but less clear, tendency after 6 months feeding. Juveniles from the toad-rich island did not show a clear tendency of dietary effect. We discuss possible reasons for the different dietary effects between the 2 populations and between the ages. Our results, along with previous related phenomena in other animals, suggest that the ability of self-toxicity-recognition may be widespread in animals that sequester defensive toxins from facultative food. (PsycINFO Database Record

Metabolic rate associates with, but does not generate covariation between, behaviours in western stutter-trilling crickets, Gryllus integer.

The causes and consequences of among-individual variation and covariation in behaviours are of substantial interest to behavioural ecology, but the proximate mechanisms underpinning this (co)variation are still unclear. Previous research suggests metabolic rate as a potential proximate mechanism to explain behavioural covariation. We measured the resting metabolic rate (RMR), boldness and exploration in western stutter-trilling crickets, Gryllus integer, selected differentially for short and fast development over two generations. After applying mixed-effects models to reveal the sign of the covariation, we applied structural equation models to an individual-level covariance matrix to examine whether the RMR generates covariation between the measured behaviours. All traits showed among-individual variation and covariation: RMR and boldness were positively correlated, RMR and exploration were negatively correlated, and boldness and exploration were negatively correlated. However, the RMR was not a causal factor generating covariation between boldness and exploration. Instead, the covariation between all three traits was explained by another, unmeasured mechanism. The selection lines differed from each other in all measured traits and significantly affected the covariance matrix structure between the traits, suggesting that there is a genetic component in the trait integration. Our results emphasize that interpretations made solely from the correlation matrix might be misleading.

Short-term exposure to predation affects body elemental composition, climbing speed and survival ability in Drosophila melanogaster.

Factors such as temperature, habitat, larval density, food availability and food quality substantially affect organismal development. In addition, risk of predation has a complex impact on the behavioural and morphological life history responses of prey. Responses to predation risk seem to be mediated by physiological stress, which is an adaptation for maintaining homeostasis and improving survivorship during life-threatening situations. We tested whether predator exposure during the larval phase of development has any influence on body elemental composition, energy reserves, body size, climbing speed and survival ability of adult Drosophila melanogaster. Fruit fly larvae were exposed to predation by jumping spiders (Phidippus apacheanus), and the percentage of carbon (C) and nitrogen (N) content, extracted lipids, escape response and survival were measured from predator-exposed and control adult flies. The results revealed predation as an important determinant of adult phenotype formation and survival ability. D. melanogaster reared together with spiders had a higher concentration of body N (but equal body C), a lower body mass and lipid reserves, a higher climbing speed and improved adult survival ability. The results suggest that the potential of predators to affect the development and the adult phenotype of D. melanogaster is high enough to use predators as a more natural stimulus in laboratory experiments when testing, for example, fruit fly memory and learning ability, or when comparing natural populations living under different predation pressures.

A dark cuticle allows higher investment in immunity, longevity and fecundity in a beetle upon a simulated parasite attack.

Cuticle melanism in insects is linked to a number of life history traits: a positive relationship is hypothesized between melanism, immune function, fecundity and lifespan. However, it is not clear how activation of the immune system affects trade-offs between life history traits in female mealworm beetles (Tenebrio molitor) differing in cuticle melanization. The females with tan, brown and black cuticles examined in the present study did not differ in the intensity of encapsulation response, fecundity and longevity when their immune system was not activated. However, we found that immune activation and cuticle melanization have a significant effect on life history traits. Offspring number and lifespan decreased in females with tan and brown cuticles, while the fecundity and lifespan of black females were not affected. Importantly, we inserted the implants again and found a significant decrease in the strength of encapsulation response in females with tan and brown cuticles. In contrast, black females increased melanotic reactions against the nylon implant, suggesting immunological priming. The results show that cuticle melanization plays an important adaptive role under the risk of being infected, while the lack of these benefits before the insertion of nylon monofilaments suggests that there are costs associated with an activated immunity system.

Social play in juvenile hamsters alters dendritic morphology in the medial prefrontal cortex and attenuates effects of social stress in adulthood.

Social play is a fundamental aspect of behavioral development in many species. Social play deprivation in rats alters dendritic morphology in the ventromedial prefrontal cortex (vmPFC) and we have shown that this brain region regulates responses to social defeat stress in Syrian hamsters. In this study, we tested whether play deprivation during the juvenile period disrupts dendritic morphology in the prefrontal cortex and potentiates the effects of social defeat stress. At weaning, male hamsters were either group-housed with peers or pair-housed with their mother, with whom they do not play. In adulthood, animals received acute social defeat stress or no-defeat control treatment. The hamsters were then tested for a conditioned defeat response in a social interaction test with a novel intruder, and were also tested for social avoidance of a familiar opponent. Brains were collected for Golgi-Cox staining and analysis of dendritic morphology in the infralimbic (IL), prelimbic (PL), and orbitofrontal cortex (OFC). Play-deprived animals showed an increased conditioned defeat response and elevated avoidance of a familiar opponent compared with play-exposed animals. Furthermore, play-deprived animals showed increased total length and branch points in apical dendrites of pyramidal neurons in the IL and PL cortices, but not in the OFC. These findings suggest that social play deprivation in juvenile hamsters disrupts neuronal development in the vmPFC and increases vulnerability to the effects of social stress in adulthood. Overall, these results suggest that social play is necessary for the natural dendritic pruning process during adolescence and promotes coping with stress in adulthood. (PsycINFO Database Record

Rough-and-tumble play as a window on animal communication.

Rough-and-tumble play (RT) is a widespread phenomenon in mammals. Since it involves competition, whereby one animal attempts to gain advantage over another, RT runs the risk of escalation to serious fighting. Competition is typically curtailed by some degree of cooperation and different signals help negotiate potential mishaps during RT. This review provides a framework for such signals, showing that they range along two dimensions: one from signals borrowed from other functional contexts to those that are unique to play, and the other from purely emotional expressions to highly cognitive (intentional) constructions. Some animal taxa have exaggerated the emotional and cognitive interplay aspects of play signals, yielding admixtures of communication that have led to complex forms of RT. This complexity has been further exaggerated in some lineages by the development of specific novel gestures that can be used to negotiate playful mood and entice reluctant partners. Play-derived gestures may provide new mechanisms by which more sophisticated communication forms can evolve. Therefore, RT and playful communication provide a window into the study of social cognition, emotional regulation and the evolution of communication systems.

Why can't we all just get along? Integration needs more than stories.

As astutely noted by the authors of this provocative article, it is time for evolutionary psychology (EP) to be incorporated into clinical and educational interventions. However, two issues from this article are raised in the current commentary: some historical misconceptions of the evolutionary label and a lack of clear and specific guidelines for developing or improving interventions based on EP.

Black Bear Reactions to Venomous and Non-venomous Snakes in Eastern North America.

Bears are often considered ecological equivalents of large primates, but the latter often respond with fear, avoidance, and alarm calls to snakes, both venomous and non-venomous, there is sparse information on how bears respond to snakes. We videotaped or directly observed natural encounters between black bears (Ursus americanus) and snakes. Inside the range of venomous snakes in Arkansas and West Virginia, adolescent and adult black bears reacted fearfully in seven of seven encounters upon becoming aware of venomous and non-venomous snakes; but in northern Michigan and Minnesota where venomous snakes have been absent for millennia, black bears showed little or no fear in four encounters with non-venomous snakes of three species. The possible roles of experience and evolution in bear reactions to snakes and vice versa are discussed. In all areas studied, black bears had difficulty to recognize non-moving snakes by smell or sight. Bears did not react until snakes moved in 11 of 12 encounters with non-moving timber rattlesnakes (Crotalus horridus) and four species of harmless snakes. However, in additional tests in this study, bears were repulsed by garter snakes that had excreted pungent anal exudates, which may help explain the absence of snakes, both venomous and harmless, in bear diets reported to date.