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.

Introduction

The emergence and spread of savannas in Africa during the past five million years is often cited as a major factor in hominid evolution. Tropical savannas are different from forests in having less rainfall, which is strongly seasonal and often very unpredictable, even within seasons (Bourliere & Hadley 1983; Solbrig 1996). Human ancestors are thought to have moved into savannas as a response to cooling and drying climates, and the exigencies of the savanna environment – including the marked seasonal changes in plant food availability – are often cited as key selective pressures shaping the hominid lineage (see reviews and references in Foley [1987, 1993], Potts [1998a, 1998b], Klein [1999], and Chapters 4, 5, and 17). This scenario invites a careful examination of responses to seasonality in extant savanna-dwelling primates.

Like most vertebrates, the large majority of primate species exhibit reproductive seasonality that reflects the seasonality of their habitats (see review in Chapter 11). Indeed, among savanna-dwelling primates, there are only two exceptions to the rule of seasonal reproduction: humans and baboons (genus Papio). This shared characteristic – the ability to reproduce throughout the year in seasonal environments – may be related to the extraordinary success of these two genera. While only humans (and their commensals) have spread across the globe, baboons have achieved a nearly continental distribution in Africa.

Introduction

In this chapter, we examine the extent to which environmental seasonality and, hence, phenological seasonality affect aspects of primate communities. Two aspects of community structure are especially interesting in this context: (i) community composition and, hence, species richness, trophic distribution, and size distribution, and (ii) community biomass. Over the past few decades, there have been several major efforts to identify the factors responsible for the variation in these features of primate communities (Bourlière 1985; Terborgh & van Schaik 1987; Fleagle et al. 1999; Stevenson 2001). Surprisingly, however, few general conclusions have emerged. There may be several reasons for this lack of success, although at this stage we will have to take an empirical approach.

The general question of how seasonality affects communities can be broken down into two parts. First, we can ask what factors affect the presence of a species at any given site and, hence, more broadly, what factors affect the distributional range of a species. This question about the determinants of species richness and geographical patterns in diversity has spawned a large literature (Huston 1994; Rosenzweig 1995). If biogeographic, i.e. historical, factors are kept constant, then there is an approximately linear relationship between productivity, from the perspective of the taxon under consideration, and local species richness or alpha-diversity, at least for animal consumers such as primates (Ganzhorn et al. 1997; Kay et al. 1997).

Introduction

Seasonal variation in the frequency of births is a nearly universal phenomenon in human populations (Cowgill 1965; Lam & Miron 1991; Bronson 1995). Indeed, the absence of birth seasonality in any particular population can be considered a remarkable observation (Brewis et al. 1996; Pascual et al. 2000). However, the broad prevalence of human birth seasonality does not imply simple causation. Several mechanisms have been proposed to account for the seasonality of births in different specific cases, and most investigators acknowledge that multiple causes are almost certainly involved. Nevertheless, some of the causes of human birth seasonality are likely to have deeper roots in our biology as hominoid primates than others. It will not be possible to review all the hypotheses that have been put forth or to survey the extensive empirical literature on human birth seasonality in this chapter. Rather, the purpose of this chapter is to discuss some of the major hypothesized causes of human birth seasonality in a way that highlights their relevance to the evolutionary ecology of our species and their relationship to the ecology of other primates.

The major hypotheses regarding human birth seasonality can be grouped under three headings: seasonality due to social factors that influence the frequency of intercourse; seasonality due to climatological factors that directly affect human fecundity; and seasonality due to energetic factors that principally affect female fecundity. The first group of hypotheses does not necessarily posit any change in reproductive physiology underlying human birth seasonality, placing primary emphasis on behavior.

Introduction: types of seasonality

Primates, like other mammals, exhibit varying patterns of reproductive seasonality, spanning the continuum from sharply delineated seasonal periods of mating and births to absolute non-seasonality, where mating and births are distributed broadly throughout the year. Both more qualitative reviews (Lancaster & Lee 1965; Lindberg 1987; Whitten & Brockman 2001) and recent quantitative reviews (Di Bitetti & Janson 2000) (see also Chapter 11) show that seasonal birth distributions are the norm rather than the exception for primates, particularly for species residing at higher latitudes, where food resources undergo pronounced annual seasonal fluctuations (see Chapter 11). Seasonal variation in the frequency of births is also a fairly common phenomenon in human populations (see Chapter 13), although its adaptive significance may have been more pronounced in earlier hominins than in contemporary humans. However, while documentation of the temporal patterning of reproduction and its regulation in primates have advanced steadily over the past few decades, we are a long way from having the detailed interspecific comparisons needed to answer the ultimate question, “Why be seasonal, and if so, how?”

Answers to this question invariably center on how resources are used and are allocated in support of reproductive effort (Drent & Daan 1980; Stearns 1989, 1992) under differing environmental regimes. In seasonal environments, we expect that it is in a female's best interest to align the costliest portion of her reproductive cycle with seasonal food peaks, so that she can acquire the essential resources to compensate for peaks in energy expenditure, thereby enhancing her overall fitness (Sadleir 1969).

Introduction

The current geographic distribution of primates is confined largely to tropical and subtropical regions, where they have colonized a variety of habitats. The majority of primate taxa inhabit tropical forests with little annual fluctuation in environmental conditions. Some species, however, live in habitats characterized by pronounced seasonal fluctuations in climate and or resource availability. These primates tend to live at relatively high latitudes or altitudes, or both. Primates in such seasonal habitats provide an opportunity to identify behavioral and physiological adaptations that enable them to cope with fluctuating environmental conditions. Furthermore, it is interesting to ask whether and how schedules of growth and reproduction are adapted to maximize individual reproductive success under such seasonal conditions, because they may have to be traded off against maintenance requirements during the lean part of the year.

Primates living in seasonal environments exhibit a number of specific behavioral, ecological, and physiological adaptations. For example, during the climatically and or energetically most stressful time of year, they may reduce energy expenditure, e.g. by reducing overall activity, and many have scheduled periods of growth and infant weaning to coincide with seasons of relative abundance. Behavioral and physiological mechanisms of thermoregulation play especially important roles in maintaining homeostasis in seasonally stressed primates. These mechanisms are importantly influenced by circadian activity patterns because diurnal and nocturnal animals are exposed to fundamentally different constraints and options in this respect.

Introduction

To sustain animal populations, an adequate supply of consumable resources is essential. Effects of insufficient resources are well documented in primate populations in the form of reduced rates of fecundity, growth, and survival (Altmann et al. 1977; Hamilton 1985; Gould et al. 1999). Weight loss (Goldizen et al. 1988) and mortality peak during periods of low food availability on an annual (Milton 1980) or interannual basis (Foster 1982; Wright et al. 1999). Food availability relative to consumer requirements has been estimated as seasonally deficient in some (Smythe et al. 1982; Terborgh 1986; Janson & Emmons 1990) but not all (Coehlo et al. 1976) cases. Identifying food-limiting periods generally involves comparisons between estimates of food supply and animal requirements, which in turn require estimates of population density, biomass, energy intake, and metabolic rate. Field techniques measuring doubly labeled water (Nagy & Milton 1979; Williams et al. 1997) and products of fat metabolism in urine samples (Knott 1998) (see also Chapter 12) are highly informative in determining whether consumers are operating at a negative energy balance. The great majority of studies, however, rely on phenological monitoring to suggest periods of food scarcity for vertebrate consumers.

Phenological monitoring has revealed spatial and temporal variation in the availability of ripe fruits and young leaves in practically all forests studied (see reviews by van Schaik et al. [1993], [Fenner 1998], [Jordano [2000], and van Schaik & Pfannes [Chapter 2 of this book]).

Introduction

The importance of high ambient temperatures and intense solar radiation for the evolution of hominids in open savanna habitats has been the subject of considerable interest. A series of studies has considered the thermoregulatory advantages related to bipedalism (Wheeler 1991), loss of functional body hair (Wheeler 1992a), body size (Wheeler 1992b), physique (Wheeler 1993), and shade-seeking behavior (Wheeler 1994a). Furthermore, these papers have generated considerable debate (Porter 1993; Chaplin et al. 1994; Wheeler 1994b; do Amaral 1996; Wheeler 1996). It is surprising, therefore, that the importance of the thermoregulation in primate behavioral ecology has received comparatively little attention, with the body of former work focusing on other ecological factors such as food availability (Stelzner 1988). Nevertheless, a number of studies have reported primates to alter their activity schedules in response to thermoregulatory needs (baboons, Papio spp. [Stolz & Saayman 1970]; gelada, Theropithecus gelada [Iwamoto & Dunbar 1983]; pigtail macaques, Macaca nemestrina [Bernstein 1972]; sooty mangabeys, Cercocebus atys [Bernstein 1976]; chimpanzees, Pan troglodytes [Wrangham 1977]; gorillas, Gorilla gorilla [Fossey & Harcourt 1977]). However, in most cases, these studies have invoked post-hoc thermoregulatory interpretations, and few have examined explicitly the importance of the thermal environment under natural conditions.

The most detailed studies of thermoregulation in wild primates have been conducted on baboons (e.g. Stelzner & Hausfater [1986], Stelzner [1988], Brain & Mitchell [1999], Pochron [2000], and Hill [2005]).