In addition to their inherent value for primatology as such, results from field studies of primate behaviour and ecology have made numerous significant contributions to discussions of human evolution. In an entirely different direction, they have also become increasingly important for conservation biology. Primates typically inhabit tropical or subtropical forests, and their relatively high profile makes them prominent indicator species for the rapidly advancing process of deforestation that is a central problem for conservation generally. Reliable data on primate behaviour and ecology accordingly constitute one of the tools used in modern biology as increasing resources are devoted to the battle against extinction. Field studies have progressively expanded to cover the entire order Primates to varying degrees, yielding an impressive wealth of data.

Despite this veritable explosion in primate field studies, however, relatively little attention has been devoted to synthetic publications dealing with methodological issues. Apart from an early guide produced in Washington by the Subcommittee on Conservation of Natural Populations (1981), which focussed on ecological aspects and has now been out of print for some considerable time, there is no single published source for even a basic set of methods required for primate field studies. One is reminded of the lament made by Cain (1959) with respect to a similar failing that once afflicted taxonomy: ‘Is it not extraordinary that young taxonomists are trained like performing monkeys, almost wholly by imitation, and that only in the rarest cases are they given any instruction in taxonomic theory?

INTRODUCTION

A population study of a wild primate typically involves a considerable investment of time and resources (i.e. money, equipment, labour) and it is vital to ensure that such effort is well targeted. When designing your study, a key issue is whether your study objectives genuinely demand an absolute estimate of the population density from either a census (a total count) or a survey (in which density is estimated from statistically valid samples), or whether less information will suffice. Relative estimates of density using data from methods such as ‘catch-per-unit effort’ from trapping or systematic searching do not provide absolute densities but, as long as the sampling methods and other conditions are standardised, can allow reliable comparisons between locations and monitoring of population change over time. Population indices are based on indirect indicators, such as the density of faeces or other characteristic signs, that can be correlated with population density. Such methods may be a more practical alternative to searching for secretive, hard-to-find animals.

In practice, no population survey or census is completely bias free and many studies may find that a reliable relative population estimate or index is more achievable than a reliable absolute estimate of the population size (Bibby et al., 1992; Greenwood, 1996; Krebs, 1999). There is a trade-off between the depth of the data gathered and the number of replicate samples that can be obtained.

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 orang-utans (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, anaesthetised (Chapter 8). Valuable descriptive information, other than measurements, can be gathered from simple observations, or from photographs (Chapter 16). On occasion, measurements can even be made in this way. For example, Markham & Groves (1990) cite a personal communication from Herman Rijksen of how he weighed four wild orang-utans (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’.

INTRODUCTION

Ornithologists have been exploring the possibilities and methodology of tape-recording and archiving animal sounds for many decades. Primatologists, however, have only recently become aware that tape-recordings of primate sound may be just as valuable as traditional scientific specimens such as skins or skeletons, and should be preserved for posterity. Audio recordings should be fully documented, archived and curated to ensure proper care and accessibility. As natural populations disappear, sound archives will become increasingly important.

This article describes how to tape-record non-human primate vocalisations. It provides information on the advantages and disadvantages of various types of equipment, and gives tips for better recordings of primate vocalisations, both in the field and in the zoo. Ornithologists have to deal with very similar problems, and their introductory texts are recommended for further study (e.g. Budney & Grotke, 1997; Kroodsma et al., 1996; see also ‘Internet sites with review texts on recording nature sounds’ at the end of this chapter). Methods and equipment required for sound analysis are not included, as information on that topic has been presented elsewhere (Charif et al., 1995; Hopp et al., 1998).

As a rule, prices for sound equipment go up over the years. Prices for equipment discussed below should only be used as very rough estimates. Retailers' prices differ widely and comparing prices over the Internet before buying is recommended.

WHY NON-INVASIVE?

Until recently, genetic studies of wild non-human primate populations (henceforth called primates in this chapter) have lagged behind those of other groups of animals studied by ecologists and evolutionary biologists. During the 1980s when, for example, avian, carnivore and hymenopteran molecular studies dominated the pages of high profile journals, primate studies were notable by their absence, and, to date, with a few exceptions, this remains the case. Two reasons underlie this imbalance.

First, primate populations do not provide the necessary replicates, sample sizes and relatively simple structures of many other groups. Social systems are often complex, generation times are long and habituated groups are extremely precious commodities. Molecular ecological methods were not always able to answer the questions that primatologists wanted to ask.

Secondly, obtaining genetic material before the advent of faecal and hair genotyping was logistically and ethically almost impossible for many populations, especially in groups where habituation over many years might have been severely affected by a large-scale, invasive sampling programme. Such problems particularly prevented many of the long-term studies that characterise primatology from taking up the challenge of adding a genetic dimension, even though there was potentially a great deal of new information to be gained. Non-invasive genetic analysis using new, high precision, molecular tools is therefore an extremely important development in primatology. However, it remains extremely difficult, time-consuming, expensive and prone to error.

INTRODUCTION

Although the past two decades have seen a revolution in many aspects of field biology due to advances in radio-tracking and telemetry, including the development of satellite and Global Positioning System (GPS) technology, these techniques have been applied less to primates than to other orders of mammals or to vertebrates in general (Casperd, 1992). A comprehensive account of animal tagging, or even of radio-tagging, would warrant a book in itself, but here we aim to draw the attention of primatologists to the advances in this family of techniques. We review a number of important studies of primates that have used them, and introduce the practicalities involved. The reader considering the use of these techniques should advance no further without exploring the wider, and vast, literature associated with radio-tracking other mammals. General reviews of radio-tracking are presented in Amlaner & Macdonald (1980), Kenward (2001), and Millspaugh & Marzluff (2001) (see ‘List of suppliers and useful Internet sites’ at the end of this chapter).

The term ‘radio-tracking’ is correctly applied only to the use of radio-transmitters and receivers to record location information. Traditionally, most field biologists have used VHF (very high frequency) or UHF (ultra high frequency) radio-tracking transmitters, but recently there has been a rapid growth in satellite tracking systems and associated technology (Chapter 4). ‘Biotelemetry’ is, strictly, the remote measurement of biological, particularly physiological, data (e.g. heart rate, blood pressure, body temperature, brain wave activity) (Amlaner, 1978; Chapter 18).

INTRODUCTION

Terrestrial animals live in an environment that undergoes regular variations, ultimately induced by the geophysical conditions prevailing in our solar/earth system. Solar radiation and gravity, in combination with the earth's rotation around its inclined axis and its orbit around the sun, and the moon's revolution around earth, produce marked diurnal, seasonal and lunar as well as tidal periodicities in important physical environmental factors, such as light intensity, ambient temperature, humidity, precipitation, day and night length, and duration of twilight. As a consequence of these periodicities being superimposed on one another, many relevant biotic environmental factors, such as food availability and predator pressure, as well as social contact, communication and competition with conspecifics, and intra- and interspecific competition for food may also vary diurnally, seasonally, lunar periodically or tidally. In this way each animal's environment has a highly complex time structure, is highly repetitive in time and thus highly predictive. Reliable predictivity provides a good substrate for genetically fixed adaptations. Hence, in addition to other general or specific physiological, ecological and/or behavioural adaptations, animals have also evolved endogenous diurnal (circadian), annual (circannual), lunar (circalunar) and/or tidal (circatidal) rhythms.

In non-human primates (in the following referred to only as primates), adaptation to the time structure in their physical and biotic environment is restricted mainly to the development of a circadian timing system involved in the regulation of the pronounced daily (circadian) organisation of physiology and behaviour.

In the early days of expeditions, a naturalist's field equipment consisted of little more than a gun, the means to preserve specimens, and luggage bearers. Later on, field primatologists relied on pencil and paper, binoculars, a compass and, if they were studying nocturnal species, a torch. More recently, a shift in emphasis towards integration of methods has led to collaboration between laboratory and field researchers working on wild primates. Technological advances have presented fieldworkers with the opportunity to collect more sophisticated data, store samples for later laboratory analysis, analyse samples in the field and collect information remotely. This has led to an increase in data concerning (for example): population and group structure; growth, development and physiology; and the application of non-invasive techniques for DNA analyses and hormonal assays. Ecological methods and techniques available for monitoring primate habitats have also improved, with the application of remote sensing, mapping (Global Positioning System, GPS), and data integration (Geographical Information Systems, GIS). These methods open up possibilities for collecting new information on previously studied populations, and a means for collecting data on species that, for example, cannot be habituated for behavioural observations. However, these technological advances come at a time when 64% of primate species are under threat and insufficient data are available to assess the status of a further 11% of species (2000 IUCN Redlist of threatened species).

INTRODUCTION

There are many reasons to capture your study animals, including marking or radio-collaring individuals (Chapter 10), taking morphological measurements (Chapter 9) and biological sampling (Chapters 1 and 8). For small nocturnal primates, trapping may be the only way to gather data for density estimates (Chapter 6). Furthermore, it is essential for the determination of spatial distribution and social interactions of individuals, as the most effective method uses direct observation of radio-tagged animals (Sterling et al., 2000). Historically, studies in which wild, larger-bodied non-human primates (hereafter called primates in this chapter) are habituated for long-term observation have rarely included capture, perhaps because researchers have been understandably wary of its effects on subsequent behaviour and habituation. However, our survey (Jolly & Phillips-Conroy, 1993; C. J. Jolly and J. E. Phillips-Conroy, unpublished data) of more than 120 studies that combined observation with capture, and which involved about 65 primate species, showed that a careful capture–release programme using trapping will not cause a previously habituated population to change its behaviour towards human observers, and will not be associated with excess mortality or serious injury. Changes in ranging habits caused by baiting and trapping will be temporary at worst, and basic social organisation and structure will not be affected. The survey also showed that trapping has been used most often to catch diurnal–terrestrial and nocturnal–arboreal species. Diurnal–arboreal primates (apart from callitrichines) have generally been captured by darting (Chapter 8), a bias that seems unjustified.

INTRODUCTION

Field endocrinology can be considered as the application of non-invasive methodologies to examine behavioural–endocrine interactions in primates living in natural conditions and social settings. In bringing together laboratory and field-based research methods, the discipline is providing new and exciting opportunities for developing a more integrated approach to studies of primate behavioural ecology (in this chapter ‘primate’ implies non-human primate).

Traditionally, field studies have relied mainly on visual measures, such as behaviour and/or morphology. Although this has generated a great deal of essential information, its limitation is that interpretation of the meaning of an observation is often based on assumptions concerning the physiological context in which it was made. The availability of non-invasive methodologies, based on measurement of hormones in either urine or faeces, now provides us with quantitative measures (of physiological status) by which the significance of these observational field data can be gauged. In turn, this greatly facilitates the testing of hypotheses concerning the adaptive significance of behavioural traits or mating systems and is helping to provide new insights into reproductive processes in an evolutionary context. For a comprehensive review of the topic of field endocrinology and its application to studies in primatology, readers should consult Whitten et al. (1998a).

INTRODUCTION

Field biologists adopted the term habituation from physiology, as the relatively persistent waning of a response as a result of repeated stimulation that is not followed by any kind of reinforcement (Thorpe, 1963). Repeated neutral contacts between non-human primates (hereafter called primates in this chapter) and humans can lead to a reduction in fear, and ultimately to the ignoring of an observer. The techniques and processes involved have only rarely been described (e.g. Schaller, 1963; Kummer, 1995), as habituation has generally been viewed as a means to an end (Tutin & Fernandez, 1991). The few studies that have quantified primate behaviour in relation to habituators describe the process with African great apes (Grieser Johns, 1996; van Krunkelsven et al., 1999; Blom et al., 2001). As we become increasingly aware of the potential effects of observer presence on primate behaviour, and especially the potential risks of close proximity with humans, it behoves us to measure as much as possible about the habituation process.

Many behavioural responses are taxon specific, and these should be taken into account when one is trying to habituate human-naïve wild primates. Between us we have had experience with a wide range of wild primates, ranging in size from marmosets (Callithrix spp.) to gorillas (Gorilla spp.), from South America, Africa, Madagascar and Asia, which, together with discussions with colleagues, we have used to make this chapter as broadly applicable as possible.

INTRODUCTION

Geographical Information Systems (GIS) and the Global Positioning System (GPS) are powerful tools that enable ecologists to acquire, store, analyse and display spatial ecological data (Dominy & Duncan, 2001), whereas remote sensing can provide information unobtainable by traditional methods. Although there has been an exponential rise in the use of this technology-based synergism for spatial analyses, mapping and modelling in the ecological and plant sciences (Du Puy & Moat, 1998; Dale, 1999; Wadsworth & Treweek, 1999), there have been few, fully integrative applications by primatologists (but see Table 4.1). Applications relevant to primatologists include: vegetation classification and mapping; forest fragmentation assessment; biomass estimation; population viability analyses; animal censusing; habitat sensitivity/vulnerability mapping and analysis; location and delimitation of protected areas; radio-tracking/foraging patterns and cost–distance analyses; and nesting pattern analysis.

In remote areas, where species and habitat information is limited, predictive modelling within a GIS can be a useful precursor to fieldwork (Lenton et al., 2000), and integrating remotely sensed imagery can enhance such models. This is particularly useful in areas such as Central Africa where political instability and boundary conflicts may significantly influence fieldwork decisions: satellite sensors can safely gather data across national boundaries. The use of remotely sensed imagery is particularly appropriate if suitable maps are not available.

INTRODUCTION

Habitat characteristics represent the matrix for the evolution of morphological, physiological and behavioural adaptations and life history traits of animals. These include bottom-up factors (such as distribution and abundance of food) and top-down constraints (such as protection from predators). The role of different habitat components in the survival and reproduction of individuals is of prime interest and is relevant for evolutionary understanding as well as for primate conservation. So far, this has been studied by linking habitat characteristics with phenotypic traits of animals, assuming that these traits represent adaptation to a given habitat constraint. However, we should bear in mind that the characteristics we observe today may represent adaptations to constraints that acted in the past (the Epaminondas effect, named after the little boy who always did the right thing for the previous situation; or, in evolutionary terminology, animals are tracking fitness optima by trying to climb the sides of shifting adaptive peaks (Cody, 1974). However, testing hypotheses based on these ‘ghosts of past constraints’ has so far been impossible.

The present chapter focuses on the description of the vegetation of forest habitats as the biotic matrix for the evolution of life history traits.

BEFORE YOU START

Any statistical analysis requires quantitative measurements of habitat and animal characteristics. Most habitats are extremely complex and there are many features that can be measured, spending endless time and money, without measuring the right variable.

INTRODUCTION

This guide is designed to provide a light-hearted, yet serious, list of suggestions for improving your comfort and safety in isolated tropical locations where the facilities may be relatively basic. We hope that it will also be useful for research and travel under less arduous conditions. It has been written as both a checklist and a set of instructions, gleaned from conversations with a wide variety of fieldworkers over a number of years and through personal experience. We end with a few wise sayings relating to the environment – to keep you going in times of adversity.

A

1. Adaptors. Check what sort of electrical sockets to expect at your destination and take the right adaptors.

2. Ant-proof socks. Have you ever had the problem of army ants invading your trousers so that you have to get undressed to pull them out of your skin? Just in case you do, tuck in your trouser bottoms and use Gortex¯ over-socks. Ants are unable to negotiate the smooth material and never make it to your nether regions. These socks also keep your feet dry, since water can only pass out. Not very glamorous, but at least you can feel smug while your companions disrobe in a hurry or suffer from rotting feet.

B

1. Bags. Hip bags of various kinds are invaluable, and cloth bags/shoe bags of different sizes and colours can help to store things and enable you to find them quickly at the bottom of a rucksack. Large polythene bags will keep things dry and double as laundry bags (see also Zip-lock or self-seal bags).

2. […]

INTRODUCTION

Over the past decades, economic, political and social forces in the developing world have brought about deforestation on a massive scale, depleting the remaining natural habitats of wild nonhuman primates (NHPs). Squeezed into ever smaller domains surrounded by human society, NHPs are coming into increasingly regular contact with humans. Poaching and habitat destruction are recognised dangers to NHP populations in the wild. In contrast, the potentially devastating threat posed by human-to-NHP disease transmission in wild NHP populations is under-appreciated and not well studied (see also Chapter 8). We believe that effective programmes for the conservation of wild NHP populations must acknowledge the interrelation of habitat destruction, bushmeat hunting and human-to-NHP disease transmission.

Pathogens endemic to humans have the capacity to devastate NHP populations. This phenomenon has been observed repeatedly in laboratory settings, where epidemics of endemic human diseases such as influenza, tuberculosis, chicken pox and measles can cause mortality rates greater than 90% among NHPs, including animals newly captured from the wild (Padovan & Cantrell, 1986; Mansfield & King, 1998). If endemic human pathogens can cause such profound destruction among captive NHPs, it follows that we should explore the threat that human contact poses to wild NHPs.

INTRODUCTION

Chapter 12 introduced dietary analysis and discussed physical aspects of potential foods as they might influence feeding behaviour. Here, we deal with chemical aspects of potential foods. Attempts to explain the influence of chemical factors on primate nutrition, and the dietary factors that promote or deter the uptake of nutrients, are limited by our understanding of how the primate gut operates. We are still not sure what the optimal dietary requirements are for humans (Challem, 1999). Research is developing both on theoretical (e.g. Jumars, 2000a, b) and practical levels (Minekus et al., 1999), but the effective rate of uptake is not simply a question of enzymatic action. The quantity of plant fibre that a primate ingests is a major influence on the rate of passage of food through the gut and thus digestibility. A variable gut population of micro-organisms and parasites also play a large positive or negative role, as do specialisations in the stomach or large intestine. The situation is even less clear when it comes to chemical compounds that act as feeding deterrents, toxins or anti-nutritional factors. These have largely been bred or processed out of the agricultural products on which humans feed, so they have received relatively little attention in food science. Currently, these chemicals are assessed by crude measures, such as total phenolics, which, of necessity, ignore the wide range of variation within each class of chemicals in the nature and intensity of the biological effect.

INTRODUCTION

The study of how animals apportion their time and energy (energetics) can provide much insight into physiology, ecology and evolution (Bartholomew, 1982; Schmidt-Nielsen, 1997). Body temperature has a profound effect on the ability of animals to function effectively. Since all animals generate heat internally to some extent, energetics is closely linked to the problem of heat management and thermoregulation. For example, homeothermic or ‘warm-blooded’ animals (birds and mammals) must produce a great amount of heat in order to maintain a high and constant body temperature in cold as well as in warm surroundings (Schmidt-Nielsen, 1997). Moreover, natural environments can be extremely variable in their thermal attributes and consequently animals show behavioural and physiological adaptations that enable them to cope with these external gradients.

In recent years, there has been a tremendous increase in methodologies and techniques applicable to studies of energy expenditure and thermoregulation. This is particularly true for the study of daily energy requirements and body temperature rhythms of wild animals behaving normally in their natural habitats. In this contribution, I therefore review methods for the study of energetics and mechanisms of temperature regulation in primates (although these can generally be applied to almost all mammalian species). I also briefly mention other possibilities for physiological measurements. All procedures described here require capture of the study animals, and some require invasive surgical intervention. They therefore raise ethical questions when dealing with wild animals and/or endangered species, and require governmental permits and authorisation.

INTRODUCTION

Arthropods, along with other invertebrates, make up 95% of the global fauna, with 1.5 million described species and at least a further 6 million that remain undescribed. These organisms, which include insects, arachnids and myriapods, play a significant role in the life histories of a range of primate species, not least in their diet. Body size plays an important part in determining the degree of insectivory (Kay, 1984); however, an example of insect eating can be found within all lineages of the primate phylogeny. Prosimians have long been described as insectivores, some having morphological adaptations for insect feeding (e.g. the extractive finger of the aye-aye, Daubentonia madagascariensis) and others adopting behaviours such as aerial snatching (e.g. galagos, Galago demidovii), or stalking specific arthropod prey (e.g. angwantibos, Arctocebus calabarensis) (Charles-Dominique, 1974). Some Loridae, like the potto (Perodicticus potto), have evolved specialised diets in which the arthropod prey emit distasteful chemicals (e.g. formic acid from ants: Crematogaster spp.) or have the potential to inject venom (e.g. large scolopendrid centipede: Spirostreptus spp.) (Charles-Dominique, 1974). Chimpanzees (Pan troglodytes) use tools to help to eat insects such as bees (Apis spp.), and the honey they produce (Tutin & Fernandez, 1992). Even folivores that appear to be entirely vegetarian inadvertently eat thousands of insects a day (e.g. mountain gorillas, Gorilla gorilla beringei, and langurs, Semnopithecus entellus).