INTRODUCTION

This chapter considers cognition in great apes as integrated systems that orchestrate the many abilities that great apes express, systems for which satisfactory characterizations remain elusive. In part, difficulties owe to research trends. Empirical studies have been guided by diverse and sometimes contradictory models, questions, measures, tasks, and living conditions. Performance levels have proven inconsistent across individuals, rearing conditions, and testing conditions, and evidence is patchy across species for virtually any facet of cognition. Evidence on wild great apes, the most important from an evolutionary perspective, is especially patchy because research has favored captives; much of what is available was collected for other purposes, so it was neither described nor analyzed with cognition in mind. The issues at stake are also hard–felt ones that touch on the human–nonhuman boundary, so entrenched beliefs infect how the literature is interpreted and even what of it is read.

Attempts have none the less been made to develop an integrated model of great ape cognition using available evidence. They include both edited survey volumes (Matsuzawa 2001a; Parker, Mitchell & Miles 1999; Russon, Bard & Parker 1996) and integrative reviews, three of the latter as major books (Byrne 1995 (RWB), Parker & McKinney 1999 (P&M); Tomasello & Call 1997 (T&C)) and others as articles (e.g., Byrne 1997; Suddendorf & Whiten 2001; Thompson & Oden 2000; Whiten & Byrne 1991). My aim is not to analyze this terrain, yet again, in detail, but to offer a compact mise à date to ground evolutionary reconstruction.

INTRODUCTION

This chapter will focus on aspects of great ape gestural communication that have implications for cognition and human language. From an evolutionary perspective, gestures may provide an important link across primate species in communicative systems. As a researcher interested in the development of language in human infants, and its precursors, I will stress similar developments, or their absence, in great apes. These developments will include communicative gestures, symbolic gestures, sign acquisition, and sign combinations.

Gesture has a very broad usage; here it will be restricted to movements of the hand, arm, head, and body with communicative functions. Postural and tactile gestures, as well as facial expressions, although often communicative, are not a focus because their implications for language are unclear. It must be kept in mind, however, that visual communication is a complex, redundant system in which these various components are usually combined (Marler 1965).

I will begin with a brief review of communicative gestures according to their functions and then focus on specific gestures involved in exchange, requests involving cognizance of agency, and pointing, as well as on the degree to which great ape gestures are intentional and inventive. These are the kinds of gestures and their characteristics that are related to the development of language in human infants. I then discuss the extent to which apes display symbolic gestures, both in captivity and in the wild, because such gestures in human infants emerge during the transition to language.

The existence of avian species in which social groups consist of more than a reproductive pair and individuals other than the parents feed offspring has been known for more than a century (Boland and Cockburn 2002), and active research on cooperatively breeding species has been ongoing since Skutch (1961) reviewed the important questions raised by such systems. Both the theoretical approach to evolutionary questions raised by cooperative breeding and the empirical investigation of such systems have changed greatly in these 40 years. In the first compilation of articles focused on cooperative breeding in birds Stacey and Koenig (1990a) presented summary chapters on long-term studies of cooperatively breeding birds, including several of the best-known species at the time. Research on those species yielded many of the data on which the theoretical foundation for our understanding of the evolution of cooperative breeding has been built.

The focus of Stacey and Koenig (1990a) on long-term behavioral and ecological studies was relevant because of the importance of such studies to identifying the costs and benefits of individual behaviors. Although the importance of long-term studies is no less significant today, it is also the case that with the advent of new techniques (particularly paternity analysis, phylogenetic methods, comparative analysis, and theoretical approaches such as reproductive skew theory), a questions-based approach to cooperative breeding has flourished and is reflected in the focus of this volume, in which conceptual issues relevant to the biology of all cooperatively breeding species, both birds and mammals, are examined.

INTRODUCTION

Is the intelligence of monkeys and apes primarily a “Machiavellian” adaptation for social life, an ecological adaptation for resource exploitation, or both a social and an ecological adaptation? How can we evaluate these competing models of intelligent adaptation? Are great apes really smarter than monkeys? How can we assess the cognitive complexity of social life? Are the social organizations and/or social roles of great apes more complex than those of monkeys? If they are, do different developmental and acquisition processes underlie that greater complexity, and which models are useful for studying those processes? Similarly, how is socioecological knowledge distributed and transmitted from one generation to the next, and what models are useful for studying this process? All these questions plague efforts to characterize great ape cognition and to reconstruct its evolution.

Systematic evaluation of social and/or ecological hypotheses about primate cognition calls for an integrated framework for comparing the sophistication of social organization and socialization in wild primates. Despite keen interest in specific topics in social cognition (e.g., social learning, social communication), a comprehensive ecologically based framework for comparing primate social cognition is currently lacking.

In this chapter, I propose such a framework. Specifically, this comparison can be made in terms of (1) the number, function, and composition of activity subgroups within primate range groups; (2) the social roles the members of these activity subgroups play; and (3) the typical routines or scripts in which these roles are played.

INTRODUCTION

Unlike the majority of the larger mammals, which are terrestrial herbivores, omnivores, or insectivores, nonhuman primates have created unique niches as arboreal insectivores, frugivores, or folivores. Primates now play important roles as fruit consumers and seed dispersers in tropical forests (Gautier–Hion et al. 1985; Terborgh 1986). However, food is still the primary limiting factor of primate populations because of its sparse distribution, physical protection (hard shells, spines, etc.), and toxic secondary compounds (Feeny 1976; Freeland & Janzen 1974; Milton 1984). Primates have evolved different strategies to cope with these dietary difficulties, and their specializations have influenced both anatomy and behavior.

Primates have evolved various features of gastrointestinal anatomy and the digestive system to cope with such dietary constraints. Leaves in particular are high in structural carbohydrates and are difficult to digest. Folivorous primates need more time to digest and absorb important food components to satisfy nutritional requirements. Specialization in gut morphology has raised the capacity of some primates to consume structural carbohydrates and detoxify secondary compounds (Kay & Davies 1994; Milton 1986). For example, the Colobinae have evolved a sacculated fermenting chamber in the stomach in which microbial fermentation precedes digestion and absorption (Bauchop & Martucci 1968; Chivers & Hladik 1980). Some secondary compounds are degraded during fermentation in the alkaline stomach environment before absorption. As an alternative strategy, a number of more folivorous primates, including howler monkeys, gorillas, bamboo lemurs, and sportive lemurs, have evolved an enlarged caecum or colon in which bacterial fermentation is activated (Stevens & Hume 1995).

Cooperative breeding (hereafter often abbreviated as CB) is an umbrella label that includes a diverse array of mating and social systems (Ligon 1999). For example, Brown (1987) lists 13 separate categories of CB (see also Chapter 5). The variability in the forms of CB is due to differences in both the strength and the forms of selection on helping behaviors, mating strategies, and other aspects of group living. Here we follow the commonly employed definition of avian cooperative breeding, which is that it involves the existence of social units composed of two or more breeding birds, plus one or more (often presumed) non-breeding “helpers-at-the-nest” (Brown 1987; Edwards and Naeem 1993). It is the feeding of young birds by the helpers – also referred to as alloparental behavior – that characterizes cooperative breeding and that has made it of singular interest.

For most of the history of CB studies, researchers have sought ecological factors that might have promoted the evolutionary development of CB. This search has met with limited success, in part because ecological and climatic considerations, in themselves, offer little predictive power beyond the fact that north-temperate-zone species are unlikely to be cooperative breeders (Heinsohn et al. 1990; Mumme 1992a; Cockburn 1996). Even in tropical and subtropical areas, where cooperative breeders occur most frequently, one typically cannot offer a good guess, based solely on environmental conditions, as to whether or not a given species will prove to exhibit CB.

Cooperative breeding occurs where more than two individuals contribute to a single brood of young, so it is certain that some individuals cannot be parents of some of the young they are rearing. By universal acclaim, studies of this phenomenon represent some of the most heroic field studies ever initiated, with several researchers following the fate of individuals within groups for decades (Stacey and Koenig 1990a).

Despite the admirable and detailed data achieved in these studies, there has been remarkably little crossing over from the study of avian cooperation into the burgeoning literature concerned with sexual selection. Indeed, a lot of research on cooperative breeding birds totally ignores the sex of the “helpers” that have prompted so much interest (Wright et al. 1999). No doubt part of the reason for ignoring gender arises because some cooperatively breeding birds are sexually monomorphic even as adults. Until recently, such monomorphism precluded identification of the sex of helpers without difficult and intrusive surgery. In addition, lack of obvious dimorphism or dichromatism might have been taken to indicate that sexual selection was of restricted importance in these species. However, as pointed out by Burley (1981), sexual conflict can lead to selection for concealing sexual identity. Such selection for indistinguishability may be particularly important in group-living species.

This chapter looks anew at the role of sex differences in the evolution of cooperative breeding, prompted by several considerations.

ENVIRONMENTS OF NATURAL SELECTION

Understanding the evolution of great ape cognition depends on identifying past adaptive settings and the factors that influenced early ape cognitive responses. Reconstructing past environments is not sufficient for developing and testing evolutionary arguments. It is the sequence of selective environments in which ancestral apes lived that is essential to determining how great ape mental abilities evolved. This requires us to assess the ways in which environmental settings (i.e., specific habitat reconstructions), trends (e.g., cooling, drying), and variability (e.g., seasonality and long-term oscillation) affected the resources and survival regimes of ancestral great apes – and thus posed adaptive problems in the places where they lived and the time periods when they evolved. This chapter investigates the evolutionary adaptability of great apes in light of local, regional, and global paleoenvironments; the geographic patterns of ape evolution; and the cognitive, social, environmental, and dietary characteristics of living great apes.

PRIOR HYPOTHESES OF GREAT APE COGNITIVE EVOLUTION

Although attempts to define unique aspects of great ape cognition have generated much debate (e.g., Tomasello & Call 1997), great apes appear to have achieved levels of cognitive sophistication and flexibility unknown in other nonhuman primates.

INTRODUCTION

Our preoccupation with large brain size and why it evolved originally arose from interest in the evolution of traits that we consider to be special in our own species. Humans are generally thought to be more intelligent, behaviorally flexible, and culturally complex than other primate species. In humans, these complex behaviors are usually linked to the relatively large brain size that is also a key feature of Homo sapiens. Understanding the evolution of large brains may therefore help us to understand the evolution of complex behaviors and abilities. This requires identifying the costs and benefits of large brain size, in order to explain why large brains evolved in a few primate taxa but not in most, or in other mammal groups.

Compared to other mammals, haplorhine primates also have large brains (relative to body size), the relative brain size of humans is still larger, and those of the great apes are not exceptional within the group (Figure 8.1). However, a range of studies has found that the intellectual capacities of the great apes are significantly different from those of other haplorhine primates (e.g., Byrne 1995, 1999a; Russon, Bard & Parker 1996; and Blake, Chapter 5, Byrne, Chapter 3, Parker, Chapter 4, Russon, Chapter 6, this volume). This suggests that a large brain size relative to body size is not the only factor that may be important in determining levels of intelligence in primates.

Cooperatively breeding birds are species in which social groups comprise at least three individuals that share parental care at a single nest. Although same-sex group members are sometimes non-relatives (Davies 1992, the majority of cooperative breeders exhibit delayed dispersal of offspring, which subsequently forgo reproduction and become non-reproductive helpers at the nests of parents or other close relatives. Group formation, social interactions, and reproduction within groups are characterized by both cooperation and competition among family members (Mumme 1997). In many cases, helpers derive indirect fitness benefits by increasing the productivity of their parents' nest. However, because helping at the nest only partially compensates helpers for failing to breed independently, helpers usually pay a net fitness cost by helping instead of breeding on their own (Stacey and Koenig 1990a).

Because most helping appears to represent a “best of a bad job” strategy, rather than an adaptive peak, it has become clear that we can understand the evolution of kin-based helping only by investigating why offspring forgo personal reproduction in the first place, and the associated question of why offspring, once they postpone personal reproduction, remain on their natal territories (Emlen 1982a). The decision to delay dispersal should be the key to the formation of family units, hence the aim of this chapter is to explore the selective basis of delayed dispersal. The selective factors favoring postponement of reproduction and helping are discussed in Chapter 3.

The route leading to cooperative breeding in multigenerational family groups involves a series of decisions.

The primary objective of conservation is to preserve biodiversity. Biodiversity encompasses not only distinct life forms such as species and subspecies, but also unique adaptations such as cooperative breeding. Cooperatively breeding birds exhibit a variety of distinctive traits that render some species unusually vulnerable to, or resistant to, habitat loss, degradation, and fragmentation, and to the problems inherent to small populations. Especially relevant are extreme philopatry, sensitivity to habitat quality, and the presence of large numbers of non-breeding adults (helpers). To our knowledge, no one has previously assessed how cooperative breeders as a group are faring against the threats to their continued existence they currently face. In this chapter we conduct such an assessment and examine the interaction between the distinctive features of cooperative breeders and the various threats to biodiversity.

In the absence of a body of previous work, we take a simplistic approach and look for broad, general patterns rather than attempting complex analyses. The existing data simply will not support the latter, compelling us to propose hypotheses rather than test them. We fully recognize that, given the diverse ecologies of cooperatively breeding birds (Chapter 5), there will be numerous exceptions to any generalization made about the group. We also recognize that many generalizations will apply to some of the diverse array of cooperative breeding systems but not others, for example to systems with singular breeders assisted by natal helpers but not to systems with plural breeders.

INTRODUCTION

In this part the contributors explore a variety of attributes of the paleobiology of fossil hominoids that may contribute to an understanding of the evolution of great ape intelligence. Our request to these experts, in each topic that is the focus of their contributions, was to focus attention on the way in which a single aspect of paleobiology may inform this issue. This is a twoedged sword. Many authors, most of whom had thought relatively little about the broader question of great ape intelligence (myself included), found new insights from the data they have long been contemplating from other perspectives. On the other hand, since we asked contributors to restrict themselves to a focused topic, many readers may feel that each contributor thinks their area of interest is the one most likely to “explain” great ape cognitive evolution. Nothing could be farther from the truth. All the contributors to this part of the volume recognize that their topic, whether it is environment and ecology, diet, locomotion, size, or life history, is one piece of the puzzle. When authors in this part of the book reach conclusions on the relevance of a specific aspect of fossil ape paleobiology to understanding great ape cognition, it is because the editors pushed them to do it, and all know that each attribute is but a facet of a very complex problem.

INTRODUCTION

It has become almost axiomatic in discussions of brain size increase within primates that causation lies with cognition. However, it is also worth exploring other possible causative factors. For instance, it has long been known that within mammals, brain size is broadly correlated with the pace of life history (see Deaner, Barton & van Schaik 2003; van Schaik & Deaner 2003, and references therein). It is not surprising therefore that large-brained great apes have greatly prolonged life histories compared with smaller-brained monkeys (Harvey & Clutton-Brock 1985; Harvey, Martin & Clutton- Brock 1987; Kelley 1997). In discussions of the life-history/brain size relationship, particularly concerning human evolution, the arrow of causation is almost universally suggested to point from brain size to life history. In this view, life-history changes are passive consequences of selection for brain size and by implication, cognitive capacity. However, this is contradicted by a substantial body of theory and empirical evidence pointing to species demographics in the shaping of life history. The relationship between brain size and life history could also be due to correlations to another variable, such as body size, without any direct cause-and-effect relationship between the two, but this seems unlikely (van Schaik & Deaner 2003; and below).

There are further difficulties with the proposition that selection for enhanced cognitive capacity leads to increasing brain size.