Introduction

Given the significant influence of seasonality patterns on many aspects of modern human and non-human primate tropical ecology (Foley 1993; Jablonski et al. 2000), it is reasonable to assume that factors associated with seasonality provided key selective forces in the evolution of the human lineage in Equatorial Africa. Reconstructing the climatic and ecological context of early hominin innovations ultimately is critical for interpreting their adaptive significance, and much research has focused on establishing links between hominin evolutionary events and global, regional, and local environmental perturbations (Brain 1981; Grine 1986; Vrba et al. 1989, 1995; Bromage & Schrenk 1999). Attempts to correlate hominin evolution with climatic trends have typically invoked models of progressively more arid and seasonal terrestrial conditions in Africa, ultimately resulting in the expansion of grassland ecosystems. Alternative interpretations of the Pliocene fossil record of east Africa suggest pulses (Vrba 1985) or multiple episodes (Bobe & Eck 2001; Bobe et al. 2002; Bobe & Behrensmeyer 2004) of high faunal turnover correlated with major global climatic change, set within a gradual shift from forest dominance to more open habitats.

While long-term trends or abrupt turnover events may have influenced human evolution, it has become evident that climatic control of mammalian evolution, including hominins, in Equatorial Africa is much more complex than supposed previously and that this region is characterized by almost continuous flux and oscillation of climatic patterns driven primarily by orbital forcing (e.g. Rossignol-Strick et al. 1982; Pokras & Mix 1987; deMenocal 1995; Kutzbach et al. 1996; Thompson et al. 2002; Hughen et al. 2004).

Introduction

Seasonality in Primates is about the impact of seasonality on the lives of primates. Because the vast majority of primates live in the tropics, most of the chapters in this book focus on aspects of seasonality in primates, including humans, and early hominins living in the tropics. Contributors to this book explore the various responses of primates to environmental seasonality, and their implications for reconstructing our own journey toward becoming human, beginning some seven million years ago. In this chapter, I synthesize the results of these contributions (Table 19.1) and examine the degree, if any, to which responses of primates to seasonality can be extrapolated to the behavior of extinct humans inhabiting mosaic habitats of the tropics.

It will become readily apparent to the reader that this endeavor yields as many questions as it provides insights, a consequence of an imperfect fossil record, the difficulties inherent in documenting seasonality in the distant past (e.g. see Chapter 8), and the paucity of empirical data available directly linking behavioral responses of hominins to environmental flux. Many of the contributions do, nevertheless, provide predictions of how hominins may have responded to increasing seasonality based upon studies of living primate and human populations, and while evaluations of these predictions are limited, they do provide new directions for future research. An important result that emerges from this synthesis is the proposition that hominins may not have responded in the same way to seasonality as did the other primates.

Introduction

The nature of the relationship between organisms and their environment has figured prominently in studies of evolution and ecology for over a century. Of particular interest has been the investigation of how climatic and environmental changes influence the course of animal evolution, and specifically how important environmental change may be relative to other factors such as migration, predation, and competition, if, in fact, its influence can be isolated sufficiently from these others to be tested. Some of the important questions that have been framed on this topic include: How are animals buffered against their environment? Why do different species appear to respond differently to environmental change? What kinds and degrees of environmental change are sufficient to induce range shifts or the “retuning” of anatomical or physiological tolerances? How directly or immediately do climatic and environmental change influence the origination or extinction of species? These questions have been the subject of many recent and important studies of mammalian evolution and diversification (e.g. Vrba [1985]; McKinney [1998]; Behrensmeyer et al. [1997]; Alroy et al. [2000]; Hooker [2000]) and have begun to figure prominently in discussions of the more specific context of primate evolution (e.g. Reed [1999]; Jablonski et al. [2000]). Different species of mammals have responded differently to changing patterns of environmental seasonality through time, coping by means of combinations of geographical range shifts and evolution of new ecological strategies, or not coping by extinction (Hooker 2000; Jablonski et al. 2000).

Introduction

A primate's activity cycle is one of its most fundamental characteristics as it determines when an individual engages in the basic behaviors required for survival. The allocation of activity over a single 24-hour period varies substantially across and even within species. Although the biological mechanisms that regulate vertebrate activity cycles and the abiotic cues associated with them have been the subject of much research, there has been relatively less emphasis on the adaptive and evolutionary correlates of the different ways in which animals distribute activity and rest across the 24-hour day.

Most primates display either a nocturnal or a diurnal activity cycle. Although diurnality frequently is associated with haplorhine primates, along with their superior visual acuity and trichromatic vision (at least in the catarrhines), several strepsirrhine species are also habitually day-active (Tattersall 1982; Mittermeier et al. 1994), and at least three taxa display an X-linked polymorphism that permits trichromacy in females (Tan & Li 1999). Furthermore, not all haplorhines are diurnal; exceptions include the tarsier and the owl monkey, taxa that secondarily evolved a nocturnal activity cycle from diurnal ancestors (Martin 1990).

The morphological and behavioral dichotomy that exists between nocturnal and diurnal species is striking, especially within the visually adapted primate order, and it would seem difficult to shift from day activity to night activity, or vice versa, once adaptations for either of these activity periods have evolved. Nonetheless, a third activity cycle observed in primates requires such transitions between day and night activity.

Introduction

The past 40 years of great-ape field research have seen the accumulation of a wealth of data that can be used to make predictions about the behavior of early hominins. We have only just begun, however, to undertake great-ape field studies that incorporate a physiological component in the wild. Understanding how the energetic and reproductive systems of living hominoids respond to environmental variation allows us to build more informed models with which to reconstruct the behavior, morphology, and responses to ecological pressures that were present in great-ape and human ancestors.

Fruit is the favored, although not always the most common, food of the great apes, and all ape populations that rely on fruit experience fluctuations in its availability. Given the importance of fruit in ape diets, such fluctuations are likely to have a major impact on these animals' biology and behavior. The primary goal of this chapter is to discuss how differences in overall fruit availability and fallback foods play a central role in shaping energetic and reproductive responses of the great apes, and then to examine the implications of this for hominin evolution.

A review of the literature reveals that relatively few studies present quantitative data on changes in diet or energetics over time. Descriptions are more likely to be statements about how diet or behavior changes in response to fluctuations in food availability.

Introduction

Primates live in habitats in which food abundance and other resources fluctuate over time, usually on a seasonal basis, and space. This variation affects the lives of primates in many ways, from behavioral ecology to reproduction (see Chapters 3 and 11). In this chapter, we explore how environmental and behavioral seasonality affect sexual dimorphism.

Sexual dimorphism in body and canine size among primates generally is viewed as primarily a consequence of sexual selection operating through the mechanism of male–male competition for mates (Leutenegger & Kelly 1977; Clutton-Brock et al. 1977; Kay et al. 1988; Plavcan & van Schaik 1992, 1997; Ford 1994; Lindenfors & Tullberg 1998) and modified by female choice for male traits (Plavcan 2004). Sexual dimorphism can be affected by environmental seasonality in two independent ways (see Fig. 14.1): first through the indirect impact of seasonality on the potential for mate monopolization (Mitani et al. 1996a; Nunn 1999; Pereira et al. 2000), and second through the direct impact of seasonality on male and female body size (Albrecht 1978; Turner et al. 1997). In the first case, phenological or climatic seasonality brings about the simultaneous presence of multiple cycling females due to reproductive seasonality and also may favor larger female group size. These effects in turn should affect the number of males present in a group, and patterns of male–male competition and resulting reproductive skew – in other words, several aspects of social organization and the mating system, all of which are tied to sexual dimorphism.

Introduction

Seasonality refers to recurrent fluctuations that tend to have a period of one year. Seasonality in climate is a basic consequence of the tilt of the Earth's axis relative to its orbital plane (e.g. Pianka 1994). As a result, the position of the zenithal Sun (when it is directly overhead) varies through the year. It is directly overhead at 23.5° S on December 22 (winter solstice, in northern hemisphere terminology), then marches north, reaching the Equator on March 21 (equinox), moving on to the summer solstice on June 22 at 23.5° N, where it turns south again, passing the Equator on September 23 (another equinox) toward the winter solstice. The Sun's march affects not only sunshine but also other aspects of climate, such as windiness and rainfall. Hence, seasonality is felt around the globe.

This book is about the impact of seasonality on the lives of primates. Members of the order Primates are confined largely to the tropics, where they occupy a broad range of terrestrial habitats, although 90% of species live in tropical forest (Mittermeier 1988). Hence, our focus will be on seasonality in the tropics. In this region, seasonal variation in temperature is limited: temperature fluctuations over the 24-hour day exceed the range of monthly means and frosts are extremely rare (MacArthur 1972). Likewise, variation in day length, although present everywhere except right on the Equator, is limited. However, seasonal variations in rainfall and sunshine characterize all tropical habitats.

Introduction

Human hunting strategies, like those of many non-human primates, vary seasonally with fluctuations in prey abundance, encounter rates, and profitability (Winterhalder 1981; Smith 1991). Temporality in resource supply has profound social effects as well, and some of the earliest studies of hunter–gatherers emphasized the impact of seasonality on settlement size, mobility, general economic organization, and even property rights, religion, family structure, and the sexual division of labor (Mauss & Beuchat 1906; Thomson 1936). For Mauss and Beuchat (1906), seasonality meant temperature: they suggested that Inuit families were organized very differently in the summer than in the winter as a result of the nature of changes in foraging opportunities. For Thomson (1936), seasonality meant rainfall, commenting that the effect of distinct wet and dry seasons in northern Australia might lead one to think that they were observing two different “tribes” of people. Anthropological interest in seasonality and its effects on human social organization has waned since then, frustrated by an inability to find correlations between seasonality and human behavior. Our goal in this chapter is to explore the utility of two approaches to understanding the relationship between seasonality and social behavior. One attempts to use comparative ecological data across groups to explain differences in aspects of social and economic behavior such as mobility and land tenure decisions; the other examines how different individuals within a group may respond differently to resource seasonality.

Introduction

Primates obtain most of their food from plants (Oates 1987), but some species are well known for their predatory behavior. Chimpanzees (Pan troglodytes) were the first non-human primates observed to hunt and eat meat in the wild (Goodall 1963). Subsequent field observations of baboons (Papio spp.) and capuchin monkeys (Cebus capucinus) have shown them to be proficient hunters (Harding 1973, 1975; Strum 1975, 1981; Hausfater 1976; Fedigan 1990; Perry & Rose 1994; Rose 1997, 2001). Given seasonal variations in primate feeding patterns (see Chapter 3), it is not surprising that primate predators display temporal variation in their tendencies to hunt. Studies of primate hunting seasonality generate considerable ecological and ethological interest and take on additional significance because of their potential to shed light on the evolution of meat-eating by early hominids (see Chapters 17 and 19). Systematic attempts to describe seasonal variation in hunting activity by non-human primates and efforts to identify its causal factors, however, have not been made.

In this chapter, we provide an overview of seasonal variation in primate predatory behavior. We focus on chimpanzees, baboons, and capuchin monkeys, three species for which sufficient observations exist to make comparisons. We begin by reviewing data on temporal variation in hunting frequency and success by each species. We proceed to discuss the factors that appear to affect this variation. Here, we consider several ecological factors that have been hypothesized to affect temporal variation in hunting (Table 8.1).

Introduction

It is well established that most primate populations show at least some seasonality in the frequency of births (Lancaster & Lee 1965; Lindburg 1987; Di Bitetti & Janson 2000). There are two major questions concerning this seasonality: (i) what determines the narrowness of the peak (if there is one)?, and (ii) what determines when the peak occurs? Because these two questions deal with distinct kinds of hypotheses and data analyses, we will treat them separately. In this chapter, we attempt to cover the background, current hypotheses, and observed patterns for each topic by analyzing quantitative birth data on 70 wild populations of primates; there are many more data sets on captive primates, but we do not deal with those here. To streamline the presentation, the details of how we acquired the data set and performed statistical analyses are given in Appendix 11.1. We conclude with a brief summary of the results and implications for primate responses to seasonal variation in general.

Before discussing adaptive hypotheses for birth seasonality, it is important to distinguish seasonality from synchrony. The patterns and causes of these two phenomena are distinct. High seasonality in births necessarily will produce a high level of synchrony, but the reverse is not true. Births can be synchronized within a group but less synchronized between groups. Factors that favor or cause within-group synchrony of births, such as predation on infants (Boinski 1987) and infanticide (Butynski 1982), may show little seasonality and thus may not select for high population-wide seasonality of births (Di Bitetti & Janson 2000).

Introduction

The order Primates is one of the few mammalian orders that are confined largely to the tropics (Richard 1985): only a few cercopithecines are found outside the tropics. Thus, the great majority of primate species live in tropical forests and woodlands, with a small minority inhabiting the open savanna.

Our aim here is to explore phenology, the production of young leaves (“flush”), flowers, and fruit, of woody plants in these prime primate habitats to seek useful generalizations for the primate ecologist. Despite the remarkable variability in phenological activity patterns of individual species (e.g. Newstrom et al. 1994; Sakai et al. 1999), there is enough between-species synchrony to distinguish clear patterns in tropical phenology that should be helpful to predict the responses of non-specialist primate consumers to fluctuations in food availability. This chapter should thus provide a general backdrop for the more detailed studies of the responses of primate consumers to changes in the availability of their various food items presented in subsequent chapters.

Specifically, we present the results of a meta-analysis of studies of phenology of plant communities of tropical forests and woodlands, many of them produced by primatologists in the course of their fieldwork. We explore the extent to which we can distinguish clear relationships between phenology and the timing of climatic events, the extent to which climatic seasonality is translated into phenological seasonality, and the temporal relationship between the fluctuations in availability of flush and ripe fruit. We also explore interannual variation in phenology.