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When we started considering the idea to write this book on lemurs’ behaviour in 2010 we thought of making reference to the relatively few experimental studies on lemur cognition in the introduction, mentioning them as a promising novel branch of investigation for strepsirrhines. But over the past few years the research on the subject has blossomed and many articles have been published on scientific journals, converting the lemur cognition domain in one of the most flourishing fields of investigation of primatology, anthropology and comparative psychology. We realised, then, that we could not dismiss cognitive studies with a couple of paragraphs in the introductory section and we decided to reserve the final chapter to the topic, which probably better than others points towards unexplored lemur potentials and future directions for a more comprehensive understanding of the primate world. In the following pages we try to provide the reader with the basic elements that we think are necessary to understand what is going on when lemurs are tested on cognitive tasks. We suggest that the reader uses this chapter for orientation, as a sort of compass to navigate through the different aspects of lemur cognition. If it is of interest, we invite the reader to consult the original papers to gather further details on the experimental apparatuses and procedures. Manipulative lemurs? Maybe In her 1966 Science article, Alison Jolly observed that ‘some prosimians, the social lemurs, have evolved the usual primate type of society and social learning without the capacity to manipulate objects as monkeys do. It thus seems likely that the rudiments of primate society preceded the growth of primate intelligence, made it possible, and determined its nature’. As primatological studies have advanced, some evidence of tool manipulation ability, a possible precursor of tool use, has been found in lemurs (for a review see Fichtel and Kappeler, 2010; Schilling, 2013). Only few incidents of spontaneous object manipulation have been observed in the wild. The aye-aye ( Daubentonia madagascariensis; Figure 9.1) is known for using the probing middle finger for tapping, and extracting nectar, kernels and insects embedded in trees or branches; it can also use the fourth finger for tasks requiring strength, scooping action and deep access (Lhota et al., 2008).

If we understand particular exchanges as being the result of a particular social system…it may become clear why exchange is a powerful metaphor for social relationships and their transformation. Sitta von Reden, 1998 Biological (or pseudo-cultural?) market It is well known that both Darwin and Wallace were influenced by the work of the economist and demographist Thomas Malthus ( An Essay on the Principle of Population , published in 1797) while elaborating their theories on evolution. Probably, the mechanisms underlying the economic system are the outcome of an evolutionary process, which has acted on the biological system and reflects on our behaviour. The analogy between economical and biological systems is not limited to this example. In biology, as well as in economics and politics, power is a key concept for understanding asymmetric relationships between subjects (Dahl, 1957). Distributive power, derived from Russell's definition of social power (1938), focuses upon who has got the power over whom. It can originate from coercion, when an individual can force another to do something, or from leverage, when the use of force is not possible. Specifically, coercive power depends on fear, suppression of free choice and/or use of threat, for its existence. It is normally based on an imbalance of social, psychological and physical power between individuals. Examples of this kind of power are theft with violence to obtain valuable goods (Matsueda et al. , 2006), bullying to aggressively impose domination over others (Rayner and Hoel, 1997) and rape (Thornhill and Thornhill, 1983; Emery-Thompson, 2009; Muller and Wrangham, 2009). Human, gorilla, chimpanzee and orangutan males perform sexual coercion over females to obtain forced copulations (Goetz and Shackelford, 2006; Muller and Wrangham, 2009). Wild orangutans provide one of the most dramatic examples of this phenomenon. It has been reported that in this species ‘most copulations by subadult males and nearly half of all copulations by adult males occur after the female's fierce resistance has been overcome through violent restraint’ (Smuts and Smuts, 1993, p. 6). Sexual coercion is also present in many other animals spanning invertebrates and mammals. It is worth mentioning, among others, that scorpion flies (Thornhill, 1980), guppies (Head and Brooks, 2006), salamanders (Ethan et al. , 2006), snakes (Shine and Mason, 2005), mallards (Barash, 1977), bottlenose dolphins (Scott et al. , 2005), and a huge variety of non-human primates (Smuts and Smuts, 1993) force their mates into sex.

Introduction The use of the small cheirogaleid, the gray mouse lemur ( Microcebus murinus , which will be referred to as “mouse lemur” throughout this chapter), for laboratory studies of the brain and cognitive aging began in the early 1990s (Bons et al ., 1991, 1994; Picq, 1992, 1993; Mestre and Bons, 1993). In the decades that followed, several research groups have become interested in M. murinus and carried out routine assessment of cognitive capacities on various behavioral tasks (see present review). Therefore, the mouse lemur represents an exception among the prosimians, which were largely ignored for a long time by researchers studying cognition. Indeed, when consulting a textbook, such as Primate Cognition (Tomasello and Call, 1997), the following type of remark is commonly encountered: “as usual, we know little about cognitive skills of prosimians …”. In fact, there was a longstanding lack of interest regarding the investigation of cognitive functions in prosimians, which resulted from two major ideas. First, prosimians were generally thought to be untrainable, as they were considered to be nervous, easily distracted, and non-cooperative (Wilkerson and Rumbaugh, 1979). Early attempts to work with these animals were very disappointing. For example, it was reported that “when removed from the home cage, lemurs grew hysterical, lorisoids sulked, and both refused to work” (Jolly, 1964b). Second, prosimians were believed to be less intelligent when compared to other primates. It was claimed that “Old and New World monkeys' intelligence outdistanced that of other mammals, including the prosimian primates” (Jolly, 1966). Two major explanations were proposed to explain the modest cognitive capacity of prosimians. First of all, it was suggested that they have found an ecological niche in which intelligence is not required (i.e., a niche with reduced opportunities for competition between species) (Andrew, 1962; Jolly, 1966). Second, they have been described as primitive, representing “surviving approximations of those ancestral primate forms from whose core components the higher primates evolved” (Wilkerson and Rumbaugh, 1979). Indeed, according to the view of Le Gros Clark (1959), the primate order is composed of a series of forms that are successive approximations of the evolutionary antecedents of man (characterized by high cognitive abilities), with prosimians at the bottom of the scale.

Introduction Ectoparasites of terrestrial mammals include several groups of insects (lice, fleas, louse flies, and others) and arachnids (mites and ticks) that inhabit the host skin or pelage and have morphological adaptations for this habitat and for host attachment. A diverse assemblage of blood-feeding flies including mosquitoes, sandflies, black flies, biting midges, horse and deer flies and certain muscoid flies have very short-term associations with mammals (only during feeding) and do not have adaptations for living on hosts; these flies will not be discussed in detail in this chapter. Ectoparasites are a diverse component of the Malagasy fauna, and have the potential to impact the health and well-being of their hosts. Because lemurs provide a biotic environment and ecosystem for their ectoparasites, an understanding of lemur ecology can directly include lemur ectoparasite ecology; similarly, an understanding of lemur ectoparasites can provide further information on the health and evolutionary history of their hosts. Unfortunately, there has been no coordinated research effort to investigate these parasites, and most of the research has been directed only at the description of new taxa. Consequently, very little is known about the relationships between cheirogaleid lemurs and their ectoparasites; however, there is great potential for the ecological and systematic relationships between these parasites and their hosts to be revealed. Ectoparasites include lice (Phthiraptera), fleas (Siphonaptera), louse flies (Diptera), true bugs (Hemiptera), and ticks and mites (Arachnida: Acari). Most mites known to biologists are free-living, predaceous or plant-feeders, but there is a very diverse subgroup that includes parasites of animals. In contrast, all ticks are parasites, feeding primarily on the blood of their hosts and acting as vectors for numerous infectious pathogens. Sucking lice are dorsoventrally flattened, feed exclusively on the blood of their hosts and also spend every stage (eggs, three nymphal instars and adults) of their life cycle on the host. Members of the Siphonaptera (fleas) are bilaterally flattened, wingless insects that feed solely on the blood of birds and mammals. A few members of the Hemiptera (true bugs) are important blood-feeders and, in the neotropical region, some are vectors of a zoonotic protozoan parasite.

Heterothermy in lemurs – flexibility is key All dwarf lemurs ( Cheirogaleus ) of Madagascar are obligate hibernators in their natural environments (Petter, 1962, 1978; Petter et al. , 1977; Hladik et al ., 1980; Petter-Rousseaux et al ., 1980; Wright and Martin, 1995; Dausmann, 2008, 2014). Hibernation is an actively suppressed metabolic state of endothermic species to overcome predictable, usually seasonal, metabolic energy and water crises. It is typified by dramatically reduced bodily functions and expressed by lowered metabolic rates and core body temperature (T b ), prolonged pauses between breaths, and lowered heart rates (Carey et al ., 2003; Geiser, 2004; Heldmaier et al ., 2004). This strategy is especially advantageous for small species, due to the allometric relationship between metabolism and body size (higher mass-specific metabolic rates and greater heat losses over their relatively larger surface areas; Heldmaier et al ., 2004; White and Seymour, 2005). The energy needed to sustain vital functions during hibernation is stored as fat deposits or food caches at the end of the active season. Although the ultimate aim – decreasing energy and water demands drastically by using hibernation to survive the harsh conditions of the Malagasy winter – is the same for all Cheirogaleus species, proximate modi operandi differ notably between species inhabiting different habitats. Biomes in Madagascar can roughly be divided between western dry forests and eastern rainforests (Dufils, 2003). Degree of seasonality (i.e., changes in occurrence and intensity of rainfall, and variation in ambient temperature, T a ) and resource predictability differ markedly between these two regions due to a combination of geographic history (mountains as physical barriers running north to south along central Madagascar), wind systems, and oceanic currents (Donque, 1972; Dufils, 2003; Jury, 2003). In addition, altitudinal gradients also influence environmental conditions and are important in explaining geographic distributions of certain taxa (Raxworthy and Nussbaum, 1994). These differences in environmental conditions not only shape Malagasy taxonomy, but also influence species’ physiological processes. In lemurs, heterothermy has so far only been confirmed in the Cheirogaleidae, a family of rather small, omnivorous, night-active species. Within this family, individuals have proven flexible in regard to their use and patterns of heterothermy, even within populations inhabiting the same forest areas, or within individuals between different years, depending on environmental seasonality (mainly changes in temperature and precipitation), unpredictability of environmental factors, and individual body condition (Dausmann, 2008, 2014).

Introduction - Malagasy habitats undergo vast seasonal changes in temperature and rainfall regimes, which in turn strongly infl uence the biology and life history of their inhabitants (Wright, 1999 ). The western dry deciduous forests show a yearly alternation between a distinct dry season and a hot and humid rainy season (Jury, 2003 ). Correspondingly, the phenology of dry forest trees – i.e., the availability of leaves, fl owers and fruits – changes substantially over the course of a year (Sorg and Rohner, 1996 ; Thoren et al ., 2011 ). As a result, plant food resources are not available evenly throughout the yearly cycle, and a relatively resource-poor dry season can be distinguished from a relatively resource-rich rainy season (Hladik et al ., 1980 ). The length of both seasons varies across Madagascar due to a geographical gradient in minimal temperatures and annual rainfall . Adaptive responses of lemurs to this environmental seasonality include seasonal changes in general activity (Schmid and Kappeler, 1998 ; Wright, 1999 ; Dausmann et al ., 2004 ), shelter usage pattern (Ramanankirahina et al ., 2012 ), body mass (Hladik et al ., 1980 ; Schmid and Kappeler, 1998 ; Atsalis, 1999 ; Randrianambinina et al ., 2003 ), reproduction (Hladik et al ., 1980 ; Wright, 1999 ), and feeding regime (Hladik et al ., 1980 ; Thoren et al ., 2011 ). It is known, for example, that diademed sifakas ( Propithecus diadema ) shift their diet from fruits and seeds to non-fruit foods, such as leaves and fl owers, and decrease food ingestion and general feeding time during the dry season (Irwin et al ., 2014 ). This ability to fl exibly change behavior or resource usage patterns in view of certain environmental changes is the result of adaptive plasticity (Nussey et al ., 2007 ). Adaptive plasticity in seasonal feeding regimes can be expected to be highest in omnivorous species that can, in principle, switch between different sources of energy and protein by consuming different food plant species or varying the proportion of animal prey in the diet. Moreover, omnivores can consume different parts, such as fruits and gum s, of the same food plant species according to the availability of these items.

The dwarf and mouse lemurs of Madagascar are two very species-rich lemur genera, yet there is a relative paucity of information on this primate family in published literature. In this first ever treatment of the Cheirogaleidae, international experts are brought together to review and integrate our current knowledge of the behaviour, physiology, ecology, genetics and biogeography of these species. A wide range of direct and indirect research methods that are currently used to study these cryptic nocturnal solitary foragers are described. By uniting often disparate research on captive and free-ranging taxa and synthesising recent methodological advances, this book provides new insights that will encourage further studies of this fascinating primate family. This synthesis will provide an incentive for more integrative studies of the Cheirogaleidae in captivity and in the wild, enabling the impacts of deforestation and other factors to be identified and directions for future conservation efforts to be established.

INTRODUCTION Fieldworkers are often unaware of the value of making accurate records of their study animals' morphology. External morphology includes measurements, observations of glandular activity and detailed description of the pelage; internal morphology may include skull and postcranial measurements, recording of suture closure, epiphyseal fusion, dental eruption and wear, and observations on the gut. All these observations will yield information on taxonomy, age–sex class (Table 9.1), reproductive status, individual variation, growth, development, sexual dimorphism and so on. It may also be interesting to look at individuals' behaviour in the light of their external differences: does facial coloration correlate with behaviour in mandrills ( Mandrillus sphinx ), does flange development correlate with behaviour in orangutans ( Pongo spp.), and so on? Measurements may be made either on dead specimens, or on living animals when they are captured (Chapter 7) and, preferably, anaesthetized (Chapter 8). Valuable descriptive information, other than measurements, can be gathered from simple observations, or from photographs (Chapter 17). On occasion, measurements can even be made in this way. For example, Markham and Groves (1990) cite a personal communication from Herman Rijksen of how he weighed four wild orangutans (worth repeating here because it is such a wonderful example of lateral thinking) ‘… by “measuring” the bending arc of particular branches when supporting the full weight of the animal and hoisting up buckets of sand to match the same arc’.

Preface Part I. Introduction: 1. Seasonality in primate ecology, reproduction, and life history: an overview Carel P. van Schaik and Diane K. Brockman Part II. Seasonal Habitats: 2. Tropical climates and phenology: a primate perspective Carel P. van Schaik and Kristina Pfannes Part III. Seasonality and Behavioural Ecology: 3. The influence of seasonality on primate diet and ranging Claire Hemingway and Nora Bynum 4. Seasonality in predation risk: varying activity periods in lemurs and other primates Michele Rasmussen 5. Physiological adaptations to seasonality in nocturnal primates Jutta Schmid and Peter Kappeler 6. Seasonality and long-term change in a savannah environment Susan C. Alberts, Jeanne Altmann, Julie A Hollister-Smith, Raphael S. Mututua, Serah N. Sayialel, Philip M. Muruthi and Kinyua Warutere 7. Day length seasonality and the thermal environment Russell Hill 8. Seasonality in hunting by nonhuman primates John C. Mitani and David P. Watts 9. Human hunting seasonality Rebecca Bliege-Bird and Douglas W. Bird Part IV. Seasonality, Reproduction, and Social Organisation: 10. Seasonality and reproductive function Diane K. Brockman and Carel P. van Schaik 11. Seasonality of primate births in relation to climate Charles Janson and Jennifer Verdolin 12. Energetic responses to food availability in the great apes: implications for hominin evolution Cheryl D. Knott 13. Human birth seasonality Peter T. Ellison, Claudia R. Valeggia and Diana S. Sherry 14. Seasonality, social organisation, and sexual dimorphism in primates J. Michael Plavcan, Carel P. van Schaik and W. Scott McGraw Part V. Seasonality and Community Ecology: 15. Seasonality and primate communities Carel P. van Schaik, Richard Madden and Jorg U. Ganzhorn 16. Primate diversity and environmental seasonality in historical perspective Nina G. Jablonski Part VI. Seasonality and Human Evolution: 17. Tropical and temperate seasonal influences on human evolution Kaye Reed and Jennifer L. Fish 18. Orbital controls on seasonality John D. Kingston 19. What do studies of primate seasonality tell us about human evolution? Diane K. Brockman.

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 In a variety of mammals and a few birds, newly immigrated or newly dominant males are known to attack and kill dependent infants (Hausfater & Hrdy, 1984; Parmigiani & vom Saal, 1994; van Schaik & Janson, 2000). Hrdy (1974) was the first to suggest that this bizarre behaviour was the product of sexual selection: by killing infants they did not sire, these males advanced the timing of the mother's next oestrus and, owing to their new social position, would have a reasonable probability of siring this female's next infant. Infanticide would therefore be one of the most dramatic expressions of sexual conflict (Smuts & Smuts, 1993; Gowaty, 1997, this volume). Although this interpretation, and indeed the phenomenon itself, has been hotly debated for decades (e.g. Dolhinow, 1977; Boggess, 1984; Bartlett et al ., 1993; Sussman et al ., 1995), on balance, this hypothesis provides a far better fit with the observations on primates than any of the alternatives (cf. van Schaik, 2000a). First, several detailed studies showed that the males never attacked or killed their own offspring (Borries et al ., 1999; Soltis et al ., 2000), in accordance with the more anecdotal information compiled from all directly observed cases of infanticide in the wild (van Schaik, 2000a). Second, several large-scale studies have estimated that the time gained by the infanticidal male amounts to 25 per cent, 26 per cent and 32 per cent of the mean interbirth interval (Crockett & Sekulic, 1984; Sommer, 1994; Borries, 1997).