Saimiri play in wild, semi-wild, and captive environments

Squirrel monkey (Saimiri sciureus) play behavior was first described almost 30 years ago in studies by Frank DuMond (1968) and John Baldwin (1969, 1971). These early reports were made under the benign observation conditions of the Monkey Jungle facility near Homestead, Florida. The provisioned four acre enclosed forest, referred to in the DuMond and Baldwin papers as a ‘seminatural’ environment, was home to over 100 squirrel monkeys of all ages, as well as other primate species. The extensive descriptions of play behaviors, partner preferences, and ontogeny observed at Monkey Jungle were confirmed a few years later by Baldwin's observations of wild squirrel monkeys in Panama and Costa Rica. At the National Institutes of Health ‘animal farm’ facility at Poolesville, Maryland, I observed monkeys in indoor and outdoor enclosures and found play indistinguishable from the earlier published descriptions. Only the frequency of play, responding to environmental stressors such as food shortages, was variable. It is reassuring that play has a basic conservatism and a reliability of behavior patterns over a wide range of settings, for much of our research has come from studies of captive animals.

At about five weeks of age, infants start to reach out to each other in rudimentary play while mounted on the backs of mothers who are resting side by side. During the second month, the infants slide off their mothers' backs, and wrestle vigorously beside the mothers as they rest, or try to rest. Nervous mothers retrieve very young infants from these earliest play fights. Later, it is rare for a mother to intervene, even if the play gets noisy.

Introduction

Many young mammals play and we still do not really understand why. The play literature abounds with hypotheses and speculation (Fagen 1981, Smith 1982, Baldwin 1986, Martin & Caro 1985), but quantitative support for most functional hypotheses is in frustratingly short supply. There is a wealth of descriptive data, but most of it deals with very basic and superficial aspects of play, such as sex differences in play frequency and the resemblance between play and serious fighting on a very gross level. Studies of play rarely have a strong theoretical underpinning. Undoubtedly, part of the problem results from the lack of precisely worded, falsifiable hypotheses (Caro 1988, Byers & Walker 1995). Compounding this is a tendency for certain ideas to become generally accepted, despite the lack of strong supporting data (e.g., that play is rehearsal for adult behaviors or serves to strengthen social bonds between playmates).

Some of the strongest recent play research addresses topics that are tangential to the function of play, for example the metabolic and fitness costs of play (Caro 1988, 1995; Miller & Byers 1991; Siviy & Atrens 1992) and the relationship between play and perturbations in the social environment such as decreased maternal responsiveness and the onset of weaning (Bateson et al. 1990, Smith 1991, Moore & Power 1992, Terranova & Laviola 1995). There is a need for carefully formulated hypotheses that generate testable predictions and detailed, quantitative data that are directly relevant to tests of these predictions.

In this paper, I will briefly consider several aspects of play that seem inadequately explained by current theory.

Like many other beautiful things, play is ephemeral, and often difficult to study. Play typically occupies a small part of an animal's day, and in most species, occurs only during a circumscribed part of juvenile life. Other types of behavior are more approachable and more forgiving. To study foraging in pronghorn, one can show up at just about any time of day. Missing a week or so of data is not a problem: one can always get more samples, because the animals are always foraging. In contrast, to study play in this (and other) species, one must be prepared to start observations at 5:00 a.m. each day. A missing week means that about 15% of the behavior is missed. Behavioral development is always more difficult to study than adult behavior, and play is more difficult to study than most other aspects of behavioral development. Nevertheless, play is receiving increased attention from many students of behavior studying an increasing number of different taxa, and interdisciplinary efforts are beginning to pay off. It also is becoming clear that a detailed understanding of play allows for strong insights into other aspects of behavior and social ecology. This book, which grew out of a symposium organized by Marc Bekoff and Robert Fagen for the 1996 Animal Behavior Society meetings in Flagstaff, Arizona, presents the thoughts and recent empirical results of many of the leaders in play research. We have not broken down the volume into distinct sections because of extensive overlap among many of the essays, overlap that compels researchers to continue broadly comparative and evolutionary research in this exciting area.

Arnold Schwarzenegger shows us one side of the profound plasticity of the vertebrate muscular–skeletal system. Muscles become larger and bones appropriately remodeled when they experience increased work loads. Parenthetically, although Mr. Schwarzenegger has not been called upon to go topless in his recent films, his continuing apparent bulk under a sports jacket shows that use-specific hypertrophy is not confined to a narrow age range. I shall return to this point later. The anti-Arnold effect, or disuse-specific atrophy, also is well known. It is strikingly illustrated by the rapid loss of muscle and bone mass that occurs in zero gravity. Mammals, including humans, that spend a few days in earth orbit return with substantial reduction in muscle and bone mass (Bodine-Fowler et al. 1992; Cann & Adachi 1983; Morey & Baylink 1978). NASA acknowledges that muscular–skeletal atrophy is the most serious medical problem associated with space flight. Another well-known plastic response in vertebrates is the use-induced gain and disuse-induced loss of aerobic capacity. Here, changes in many organ and enzyme systems are involved (Close 1972; Laughlin et al. 1989; Nieman 1990; Bigard et al. 1991), and the effects are equally as dramatic as Mr. Schwarzenegger's pectoralis muscles. I and most other humans cannot run a single 5 minute mile, but some humans who have trained for marathons can run 26 of these in succession.

Phenotypic plasticity in systems that support strength and endurance is adaptive. The muscular–skeletal system has a way of detecting demands placed upon it, and responds appropriately, building as much, but no more, capability as is called for.

Introduction

In the ongoing commentary on Smith's (1982) target article on play, Moran (1985) wrote a critique entitled ‘Behavioral description and its impact on functional inference.’ In response, Smith (1985) wrote a counter-critique entitled ‘Functional hypotheses and their impact on behavioral description.’ While seemingly at odds, these two points of view are actually complementary. If play fighting did not resemble serious fighting, in at least some crude ways, then it is unlikely that the hypothesis that the former served as practice for the latter (Groos 1898) would ever have been considered. In this regard, description preceded functional inference. However, once formulated, such an hypothesis makes predictions about other features of the behavior, in this case, play fighting, which are not known. Therefore, behavioral description informs functional inference, which in turn, influences further description.

That play fighting functions as a means of refining the skills necessary for combat is an hypothesis which continues to receive widespread support (e.g., Caro 1988; Fagen 1981; Pellis 1981b; Smith 1982; Symons 1978a). Indeed, the hypothesis that play serves as practice is widely endorsed in lay treatments of the topic, as can be ascertained from both television nature documentaries and from popular books. For example, Angier (1995) asserts that ‘through play, animals can rehearse many of the moves they will need as adults’ (p. 133). With regard to play fighting, this hypothesis asserts that this form of play serves to practice the tactics of attack and defense, which would otherwise only occur in dangerous situations (Symons 1978a). The enhancement of fighting skills that such practice affords is often argued to be responsible for shaping the form of play fighting (Smith 1982).

There is no dispute that ungulate sparring is somehow less serious than fighting; that it does not constitute a life or death battle. Sparring resembles a fencing match or cooperative dance in which rules are followed. The game is over after three ‘veneys’, or hits, have been made and the wager is not blood but rather a ‘dish of stewed prunes’. Sparring appears to have, at the very least, a mild energy and small risk of injury cost. Such a behavior, if functionless, would have been weeded out long ago and would not be so popular an activity among a wide range of mammals today. What is the wager – spoils gained or lost – in a sparring match between two young ungulate males? To answer this question, we describe the context in which sparring is observed as well as the common participants in both pronghorn and other species in which sparring has been studied.

What is object play?

Object play is the involvement of inanimate objects of various kinds in an animal's play activities. Fagen (1981) defines 'divertive interactions with an inanimate object … including exploratory manipulation', when describing object play. It is a type of play behaviour familiar to pet cat and dog owners who regularly provide their pets with toys. In the absence of human manufactured toys, domestic, captive and wild animals may use a wide variety of objects such as sticks, rocks, leaves, fruit, feathers, dead prey animals and even items of discarded human bric-a-brac as objects to play with (see Heinrich & Smolker, Chapter 2). Along with other types of play described in other chapters, object play is characterised by boisterousness and appears, anthropomorphically, to be enjoyable. Objects are thrown into the air, chased and captured, pulled to pieces, kicked, shaken and bitten.

Animals of all ages, from diverse taxa, play with objects. While nonhuman primates and carnivorous species such as cats, dogs and bears, are regular performers, other animals also play with objects. Play with twigs, small stones and nutshells by corvids, parrots and other birds is well known (see Heinrich & Smolker, Chapter 2), as is play with human manufactured toys by a wide variety of zoo animals, from turtles to rhinoceroses.

Detailed scientific study aimed specifically at object play has been confined to a small range of species, particularly domestic cats and dogs, some wild canids, laboratory rats, primates, polecats and their domestic counter-parts, ferrets. Domestic species are convenient subjects, because they are easy to house and handle, and are less sensitive to stress induced by captivity.

What concepts have been used to explain the sorts of behavior described in the prologue? The purpose of this chapter is to review the variety of those ideas. The overview is historical in part, but is also organized around Nikolaas Tinbergen's four-part classification of questions that can be posed about behavior - about the evolutionary history and functions of behavior (ultimate questions), and about the immediate regulation and development of behavior (proximate questions). This chapter does not distinguish between the ideas that do and do not form a part of a modern synthesis. Our synthesis is presented in Chapter 2, and is developed from only a portion of the concepts discussed here. The goal in Chapter 2 is to identify that subset of old and new concepts with the greatest capacity to provide an understanding of communicative behavior.

An evolutionary approach: ultimate questions

Natural selection and the functions of behavior

Well over a hundred years ago, Charles Darwin provided the essential elements of the evolutionary framework in which this book is cast. His principle of evolution through natural selection is very powerful, but also so elegantly simple that it can be summarized by just four points (Alcock, 1989). (1) There is variation among the individuals within a species, in body form, physiology, behavior, and so on. (2) Some of this variation is heritable; in other words, some of the distinctive characteristics of individuals can be passed on to their young, so that offspring tend to resemble their parents more than they do other members of the species

Consequences, society, fighting, and the origin of vocal communication

This chapter describes how the consequences of vocalizations have affected their form, i.e., their physical structures. Social consequences of vocalizing result from assessment, but there are other consequences too. If a bird is killed by a predator attracted to its song, the predator's attack is a side-effect, not a social consequence, of singing. Therefore, conspicuous singing, and other communicative behavior, is selected for if, on balance, given side-effects, it results in fitness benefits. Another class of side-effects might accrue during eavesdropping by nontarget individuals (Myrberg, 1981; McGregor & Dabelsteen, 1996). For example, female lions roar to stay in contact with their pridemates and defend their territories against other prides. In doing so, they risk attracting the attention of potentially infanticidal males. Females counteract this eavesdropping by roaring in choruses, which intimidates these males (Grinnell & McComb, 1996). So, both social consequences and side-effects are sources of selection on communication.

Social consequences arise chiefly from assessment. The assessor perceives a signal. It might do nothing, it might run away, it might share, it might copulate, etc. By assessing and acting in its own interest, the assessor provides feedback to the manager to determine what has been accomplished. This process drives the evolution of communication. But what if the assessor does not act in the manager's interest at all? The only road left for the manager is to change the assessor's behavior physically by fighting and this is common enough. And here we have a hint about the possible evolutionary origin of communication - communication substitutes for fighting over resources.

Historical antecedents are discussed in Chapter 1. This chapter introduces what communication encompasses. Not all historical concepts and ideas described in Chapter 1 are included. The goal here is to provide a new synthesis to guide future research, emphasizing the central role that

assessment and regulatory processes play in communication.

Placing assessment on a par with management

Many species of small temperate birds form winter feeding flocks, sometimes consisting of several species (Sullivan, 1984), which they maintain by repeatedly contact calling. The downy and hairy woodpeckers, blackcapped chickadees, tufted titmice, and white-breasted nuthatches that forage together often emit such contact calls throughout the day, but may cease abruptly with signs of danger, such as when a flock member emits an antipredator call, or a hawk is detected.

Animal Vocal Communication: A New Approach results from our belief that the field of animal communication needs new blood. We have tried, independently, to convince colleagues that the informational perspective is not adequate as a concept or methodology to understand either the evolution or the process of vocal communication. In 1987, we began to collaborate on this book, deciding on the order of authors with the toss of a coin.

We have attempted to include in this book those aspects of theory that we feel have ‘staying power,’ i.e., those that suggest and provide the best questions and will not lead to blind alleys. Game theory, in particular, has increased in popularity. It deals with frequency dependence – the concept that the success of an animal's behavior depends on the relative frequency with which it occurs in the animal's own population. A game-theoretic approach can be contrasted with studies of adaptation that deal with structure, function and with nonsocial activities as well as with social behavior. Adaptation suggests optimization, such as the optimal shape of a bird's wing for soaring flight. But both of these approaches have staying power; they are complementary to each other rather than in conflict. A behavioral strategy will not work if someone else can do it better because they have the better structural design. It is the latter that affects the outcome of evolutionary competition.

Carolina wren

A male Carolina wren was widowed in the flash of a sharp-shinned hawk's attack. It was late September, but singing and pairbonding are possible throughout the year for this wren, as is the case with tropical-living birds, even though the hawk struck in the State of Maryland, USA. The widowed male continued to sing and otherwise defend his permanent year-round territory using a repertoire of 42 song types. He sang one type 5 to 120 times before switching to another. During the two months after he became independent from his parents, his song-learning phase, he had learned 85% of his song types from neighboring males; he learned the remaining 15% while dispersing or from males more distant from his territory and not found in his neighbors' repertoires. At 9:00 a.m. a stranger wren was detected. The male approached it with plumage fluffed, quickly sang three song types without the usual pause between them, then attacked. The intruder gave high-pitched pi-zeet calls, an appeasement or friendly call between mates or siblings. It then gave high pee pee pee calls as the resident male continued to attack, producing short growls during each attack flight. Between attacks, the resident male also uttered harsh, low chirrs between attacks. The intruder fled silently. At 10:30 a.m. a second intruder was detected.

Why the informational perspective is inadequate

Convey versus accomplish

Major problems in the use of ideas and language have occurred in attempts to understand communication. Words often carry additional conceptual baggage that is counterproductive rather than useful. One of the difficulties about using such words is that they are liable to beg the question of causal links between process and product (Bateson, 1990). Concepts should focus attention on the processes relevant to communication. It has been seen that the concept of information is not equal to that task (Chapters 1-4). One reason for this is that it is not easy to ask what is conveyed over a longer time period than that immediately following the acoustic signal. It is, however, possible to ask what is accomplished over much longer periods of time. Indeed, time, long or short, must pass before accomplishment can be described.

The concept of information tends to draw attention to each signal-response couplet, thereby disposing us to treat communication as a chain of such couplets. In contrast, the regulatory process in A/M emphasizes the many time frames in which communicative behavior and its effects are patterned. The ultimate products of communicative behavior consist of evolutionary changes (Chapters 1-3), whereas the most proximate effects consist of the immediate impact of communication on participating individuals (Chapters 2 and 4). For both time scales, effects occur due to the interaction between processes of assessment and management (A/M). A/M describes interactions among communicants in the context of the logic of natural (and sexual) selection.

This chapter is not divided as Chapter 2 is, into separate sections on assessment and management. Instead, it considers the integrated proximate functioning of these two processes, discussing the contributions of perception, cognition, motivation, and emotion to the interacting operation of assessment and management both within and between individuals. These multileveled interactions are most clearly highlighted in the last section of this chapter, in which the development of communicative abilities is explored. The adoption of an A/M approach has provided a framework for dealing with the dynamics of social interaction.

The material here may seem a bit off the point for those readers expecting a treatment dealing exclusively with vocal communication. Time is spent exploring broader issues, of how perception, cognition, motivation, and emotion work in general, not just during communication, and of how interactions between individuals not only result from management and assessment, but also influence those two processes. This latter point, that the dynamics of interaction among individuals is the arena of communication, is convergent with the same consistent theme in the writings of John Smith (1997), even though its source lies in a very different, noninformational starting point from Smith's. We share with Smith this message: if we are to continue progressing in our understanding of communication, we must return systematic descriptive research on the broader contexts of communicative behavior to its former highpriority position. With this theme, we ally ourselves once more with Tinbergen (1963), whose seminal paper on the aims and methods of ethology featured not only sections on his four questions, but also an initial section entitled ‘Observation and Description.’