OVERVIEW

Living reptiles display an immense diversity in morphological, physiological, behavioural and ecological traits. Indeed, ‘reptiles’ actually constitute a highly polyphyletic assemblage, encompassing four major lineages that diverged >200 million years ago. The extant taxa comprise 7390 species of squamates (lizards and snakes), 295 of turtles, 23 of crocodilians and 2 species of sphenodontians (the New Zealand tuatara) (Uetz, 2000). Correspondingly, the ways in which ecological divergence is manifested between the sexes, and the selective pressures and proximate mechanisms responsible for such divergence, take many forms. This chapter will outline the kinds of ecological traits known to differ between males and females in reptiles, and then explore the degree to which such differences are consistent with alternative hypotheses. Historically, conceptual models to predict and explain segregation between the sexes have been developed by workers with a primary focus on endothermic vertebrates, especially ungulates (see Chapters 2, 3, 9, 10, 11 and 19). Inevitably, the kinds of arguments that have been developed rely upon specific features of these organisms, so that attempts to interpret analogous sexual segregation phenomena in reptiles cannot be neatly subsumed within the same framework. However, the analogies in many cases are clear enough, and the framing of the models broad enough, that strong parallels can be drawn. Thus, we use the conceptual framework developed by ungulate biologists to categorize and investigate causal mechanisms for segregation between the sexes within reptile populations. We then propose a framework with which to analyse studies of sexual segregation.

INTRODUCTION

Adult males and females of many animal species differ in terms of the taxonomic range of food types they use, and/or the physical and chemical properties of the meals they ingest. Surprisingly, however, recognition and understanding of these differences has advanced slowly. For example, practitioners of wildlife production and conservation typically use total animal numbers for setting stocking rates, estimating area requirements, monitoring plant–animal interactions, etc., with no consideration of sex differences in feeding ecology. Yet the reason why textbooks on wildlife ecology and management (e.g. Caughley & Sinclair, 1994) seldom address sex differences is more the lack of conclusive published information than simple oversight. Hence, my purpose in writing this chapter will be served if it stimulates further research on this ecologically important topic.

My focus here is on sex differences in the foraging ecology of large mammalian herbivores (>5 kg), mostly because the principles underlying diet selection have been better studied in this group than in any other. It is obvious that substantial dietary differences will occur when male and female herbivores feed in separate plant communities, the possible reasons for which are discussed in Chapter 9. Here, however, I discuss sex differences in the consumption of plant material by large herbivores at the scale of the small patch, or feeding station (as defined by Senft et al., 1987).

OVERVIEW

Most research on sexual segregation has been focused on eutherian mammals, showing that this phenomenon is widely but unevenly distributed across eutherian taxa, and is particularly prevalent amongst ungulate species that are sexually dimorphic in body size and give birth highly synchronously. Marsupials comprise a clade of mammals that has undergone extensive radiation in parallel to that of eutherians in terms of morphology, ecology and behaviour. We would then expect sexual segregation to occur in some marsupials, as it does in some eutherians, and most likely in those marsupial species that exhibit sexual dimorphism in body size and give birth highly synchronously.

We reviewed the literature for evidence of sexual segregation in 23 species from three orders of extant Australian marsupials. These species were drawn from each family and sub-family within these orders, and from distinct life-history categories within one family. We collated the incidence and form of segregation, the degree of body size dimorphism and the degree of birth synchrony in each species. We predicted that if dimorphism and synchrony were associated with sexual segregation in marsupials, then segregation should occur predominantly in species that were dimorphic and/or highly synchronous, but not in species that were monomorphic and gave birth year-round. We also reviewed, in greater detail, the occurrence of sexual segregation in the genus Macropus, comprising the kangaroos and larger wallabies, since they are ecologically and behaviourally comparable to many ungulates.

OVERVIEW

Sexual segregation is fairly common in non-human primates, usually in the form of social segregation (Box 17.1). Spider monkeys (Ateles spp.) and chimpanzees (Pan troglodytes) have fission-fusion social systems in which individuals form temporary subgroups (parties) within socially bounded communities; social segregation is not complete, but single-sex parties are common, and males are more gregarious than females and associate predominantly with each other. Some nocturnal lemurs (e.g. grey mouse lemurs, Microcebus murinus: Radespiel et al., 2001a, b) and bushbabies (Galago spp., Galagoides spp., Otolemur spp.) forage solitarily, but form sleeping associations that consist mostly of females. Macaques (Macaca spp.) form cohesive mixed-sex groups, but maturing males in some species spend time alone or in peripheral all-male groups before joining mixed-sex groups. Habitat segregation is rare, although males may use larger home ranges than females (e.g. orangutans, Pongo pygmaeus: Singleton & van Schaik, 2001; chimpanzees: Hasegawa, 1990) or expand their ranges during mating seasons (e.g. grey mouse lemurs: Eberle & Kappeler, 2002).

However, most diurnal primates, even those that breed seasonally, form stable, cohesive groups in which males and females associate permanently. Even when some males are socially peripheral (e.g. squirrel monkeys, Saimiri spp.; see later), females associate permanently with others. Stable female groups without permanently associated males are known only in mandrills (Mandrillus sphinx; Abernethy et al., 2002).

OVERVIEW

Fish shoals have been fundamental in developing our understanding of the evolution of sociality (see Krause & Ruxton, 2002). They have been used in a range of laboratory and field studies, and have been particularly useful in investigating the adaptive significance of the phenotypic assortment of social groups (see Krause et al., 2000a for a review). In particular investigations on fish shoals have elucidated the mechanisms underlying assortment by body size (Krause et al., 2000b; Croft et al., 2003). However, in contrast to mammals (mainly ungulates) fish have largely been neglected from the literature on sexual segregation (see Sims et al., 2001a; Croft et al., 2004 for exceptions).

Sexual segregation is often associated with sex differences in body size (see Ruckstuhl & Neuhaus, 2000, 2002 for a review in ungulates – see also Chapter 10). In such cases, segregation by body size will automatically result in segregation by sex. Body size differences, however, are not restricted to sexual dimorphism but often found within the sexes as well. Thus, by understanding the mechanisms underlying body size assortment we may better understand a more general phenomenon that includes sexual segregation.

Group living is an important anti-predator strategy (Hamilton, 1971; Krause & Ruxton, 2002), consequently predation risk is a strong selective force influencing the composition of social groups. Initially, we examine the anti-predator benefits of the phenotypic and behavioural assortment of social groups in fish, paying particular attention to assortment by body length.

OVERVIEW

The importance of animal behaviour to the development of conservation strategies has received increased recognition in recent years. Behaviourists realize now that evolutionary studies rely on a diversity of species occurring in their natural habitats, whereas conservationists now recognize that animal behaviour plays a large role in ecological processes and, therefore, can have great implications for conservation. Several recent texts (Clemmons & Buchholz, 1997; Caro, 1998; Gosling & Sutherland, 2000; Festa-Bianchet & Apollonio, 2003) have been dedicated to this important union. Nonetheless, much remains to be learned about the specific ways by which animal behaviour influences populations, and how that knowledge can best be incorporated into effective conservation strategies (Shumway, 1999).

Sexual segregation is a behavioural and ecological phenomenon that can have great implications for wildlife conservation. A number of hypotheses have been proposed for explaining sexual segregation (Main et al., 1996; Ruckstuhl & Neuhaus, 2002; see general overview in Chapter 2). Understanding the causes of sexual segregation will provide further insight on the selective forces shaping animal behaviour and will lead to improved conservation strategies. Regardless of the mechanism(s) leading to sexual segregation, the outcome itself is an important issue that should be considered in conservation programmes. Indeed, the temporal and spatial groupings of males and females have implications for habitat management, population monitoring, research and management.

In this chapter, we review ways in which sexual segregation can influence effectiveness of conservation strategies.

In September 2002, we invited researchers to discuss their work, but also to consolidate our knowledge of sexual segregation in vertebrates, during a three-day workshop in the Zoology Department of the University of Cambridge. The book stems from this workshop, but is much more than a compilation of different research chapters. At that workshop we gave each author the task to integrate their knowledge of a particular system into the framework of sexual segregation. Many of the authors had not even previously worked on sexual segregation but, as you will see, they all did an excellent job in synthesizing information on sexual segregation and the ecology of the two sexes in different taxa. We're very fortunate to have been able to attract so many outstanding scientists who either contributed to the book itself or commented on the chapters. Our special thanks also go to Lotti and Hans Neuhaus who flew over from Switzerland to look after Anna May, so that we did not have to segregate for parental duties. We are also very grateful to the staff at Gonville and Caius College, Cambridge, who provided accommodation for the workshop; to the University of Cambridge, who provided us with tea and biscuits during tea breaks; and, in particular, we would like to thank the staff in the Zoology Department of Cambridge and all our colleagues who supported us in various stages during the writing and editing of this book.

OVERVIEW

As the chapters in this volume suggest, sexual segregation appears to be an important component in the social organization of many species. Indeed, some of the arguments made for sexual segregation among human children are similar to those made for sexual segregation in adults of other mammalian species (Ruckstuhl, 1998; Ruckstuhl & Neuhaus, 2002). For example, some authors suggest that male and female humans (Maccoby, 1998) and adult ungulates (Bon & Campan, 1996) segregate due to differences in behavioural ‘styles’. From this view, males interact with each other because their behaviour is physically vigorous and rough. Females, being more sedentary, avoid this sort of behaviour.

In this chapter we examine two hypotheses (‘energetics’ and social roles) proffered to explain the existence of social sexual segregation in human juveniles. This involves documenting what has been labelled ‘energetics’ (e.g. Ruckstuhl, 1998) or physical activity (e.g. Maccoby, 1998; Pellegrini et al., 1998), of the behaviours and social roles in male and female juveniles in humans. We will argue that segregation is based, ultimately, on male and female reproductive roles and can elegantly be explained by sexual selection theory (Darwin, 1871). As in most animals, human males experience more reproduction variation, relative to females (Trivers, 1971). This leads to males being the larger, more active and more competitive sex because they must compete with each other for access to mates. The social roles enacted correspond to reproductive roles and there are corresponding differences in levels of physical activity.

INTRODUCTION

Seals have a worldwide distribution ranging from the high Arctic, through the tropics, to the coast of the Antarctic continent. They occupy the higher positions in many of the world's marine food webs and are increasingly being used as model species to monitor the health of oceans worldwide (Jouventin & Weimerskirch, 1990a). Historically, knowledge of their biology was restricted to periods when they could be observed on land or ice but even this was limited to the more accessible species. Advances in animal-borne recording devices, such as satellite transmitters and time–depth recorders, have lead to a rapid increase in the understanding of seal behaviour (Boyd, 1993b). A few decades ago, any attempt to investigate sexual segregation would have been extremely limited in its scope. Even today, knowledge is skewed towards the more heavily studied species and we can only consider segregation in terms of large spatial scales or distinct behaviours. Information that is often taken for granted for terrestrial organisms, such as foraging locations and basic diet, is simply not known for many species of seal.

The Pinnipedia is a diverse suborder, represented by some 33–37 extant species spanning three families (Berta, 2002). This diversity, coupled with their global distribution, is reflected in a large range of life history strategies. They show the greatest range of sexual size dimorphism of any higher vertebrate group (Ralls & Mesnick, 2002). In some species males can be ten times heavier than females (Fig. 4.1), whereas females are slightly heavier in others (Table 4.1).

OVERVIEW

The two sibling species of giant petrels (northern Macronectes halli and the southern M. giganteus), the dominant scavengers of the sub-Antarctic and Antarctic environment, are one of the best examples of sexual segregation in avian foraging and feeding ecology. During breeding, males and females feed mainly on penguin and seal carrion, but females also feed extensively on marine prey such as cephalopods, fish and krill. Sexual differences in diet are reflected not only in analyses of regurgitations, but also in the isotopic composition of carbon and nitrogen, as well as in their heavy metal burdens. Direct observations and tracking of pelagic movements showed that males of both species usually forage closer to the breeding grounds, exploiting carcasses on beaches, whereas females show more pelagic habits. In consequence, foraging effort, foraging efficiency, predictability of resources exploited, optimum foraging time and activity budgets differ between sexes. During winter, however, studies on activity and pelagic movements suggest more similar feeding habits between sexes. Overall, differences in foraging and feeding ecology are probably related to the substantial sexual size dimorphism; males of both species are 16–35% heavier and have disproportionately larger bills than females. The importance of size in contest competition to access carrion may explain their large body size as well as the competitive exclusion of females from coastal habitats, reducing intraspecific competition for food. Ultimately, a differential exploitation of carrion probably increased sexual dimorphism not only in body size but also in the feeding structures such as bill size.