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An Introduction to Primate Conservation. Edited by Serge A. Wich and Andrew J. Marshall. © Oxford University Press 2016. Published 2016 by Oxford University Press.

The last systematic treatment of primate con-servation, Cowlishaw and Dunbar’s widely read Primate Conservation Biology, was published a decade and a half ago (2000). At that time, 200 to 230 species of primates were recognized (Groves 1993), 31% of which were classified as threatened by the International Union for the Conservation of Nature (IUCN) (Baillie and Groombridge 1996). Since then, both the number of primate species recognized (479) and the proportion classified as threatened (48%) have risen sharply (Mittermeier et al. 2013). The increase in the number of threat-ened taxa is due to a variety of threats, especially important among these being hunting and the loss, fragmentation, and degradation of primate habitats

1.1 Introduction

Primate conservation is a discipline that aims to develop the scientific understanding necessary to implement actions that will ensure long-term pres-ervation of non-human primates and their habitats (Cowlishaw and Dunbar 2000). Interest in primate conservation has grown substantially in recent dec-ades, reflected in substantial increases in the num-bers of publications related to the topic (Figure 1.1). There are likely many reasons for this increase, including the growing threats to primates and an increased awareness of their biological, intellectual, economic, and ecological importance (Marshall and Wich, Chapter 2, this volume).

CHAPTER 1

An introduction to primate conservationSerge Wich and Andrew J. Marshall

Copyright: conservationdrones.org.

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OUP-FIRST UNCORRECTED PROOF, March 8, 2016

2 A N I N T R O D U C T I O N TO P R I M AT E C O N S E R VAT I O N

known primate fossils (Smith. 2006). Although hu-mans are primates, in this book, we use the term ‘primate’ to refer only to non-human primates.

The primate order is commonly divided into ei-ther Prosimians and Anthropoids (Fleagle 2013) or Strepsirhines and Haplorhines (e.g. Disotell 2008). The difference between these classifications de-pends on whether gradistic or phyletic information is used and as a result the position of the tarsiers differs (Figure 1.2). Traditionally, Tarsioidea were classified together with Lemuroidea (lemurs) and Lorisoidea (lorises) in the suborder Prosimii, but recent taxonomies based on phylogenetic related-ness have classified the tarsiers with the traditional members of the suborder Anthropoidea (Ceboidea, Cercopithecoidea, and Hominoidea) to form the new suborder Haplorhinii. Modern taxonomies typically follow this classification, with the lemurs and lorises grouped in Strepsirhinii and the mon-keys, apes, and tarsiers forming Haplorhinii. The IUCN currently recognizes 16 primate families, 77 genera, 479 species, and 681 taxa (Mittermeier et al. 2013). They occur mainly in the tropical and subtropical areas of South America, Africa, and Asia (Figure 1.3).

(Bennett et al. 2002; Fa et al. 2005; Hansen et al. 2008; DeFries et al. 2010; FAO 2010; Meijaard et al. 2011; Wich et al. 2012; Hansen et al. 2013). While only one primate species is thought to have gone extinct over this period (Procolobus badius waldroni; McGraw and Oates (2007)), the threats to most primate popula-tions are increasing and the survival of many pop-ulations and several species is severely in doubt (Mittermeier et al. 2013). In this edited volume we provide an overview of the current state of primate conservation, incorporating much of the informa-tion on primate behaviour, ecology, species distri-bution, conservation challenges, and conservation solutions that has emerged in the time since pub-lication Cowlishaw and Dunbar’s influential book.

1.2 The primate order

Primates are an order of mammals. Recent analyses of molecular data indicate that primates diverged from other placental mammals roughly 75.8 million years ago (Steiper and Seiffert 2012). This date is considerably more recent than previous estimates (Tavaré et al. 2002) and comports more closely with the estimated divergence time based on the earliest

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Figure 1.1 The number of scientific publications on primate conservation published annually from 1970 to 2012. Data reflect the number of publications returned using a keyword search in Scopus (http://www.scopus.com) for publications that contained both the keywords ‘primate’ and ‘conservation’ in each year. The data search was conducted on 11 November 2013.

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A N I N T R O D U C T I O N TO P R I M AT E C O N S E R VAT I O N 3

have an opposable big toe that allows them to use their feet as hands (Stanford et al. 2013). Most pri-mates are also characterized by having flattened nails instead of claws or hooves, but in the family Callitrichidae these have evolved into claw-like nails on all digits except the big toe, presumably as an adaptation to their diet and arboreal lifestyle (Garber et al. 1996). Primates also have forward- facing eyes with overlapping fields of view, permit-ting stereoscopic vision that, often in combination with their grasping hands, is thought to have ini-tially evolved as an adaptation to ancestral life in the trees (Elliot Smith 1924), catching small prey (Cartmill 1992), foraging on small objects in an ar-boreal environment (Sussman 1991), or avoiding predation by snakes (Isbell 2009).

Primates exhibit tremendous variation in size from male gorillas (Gorilla sp.) that can weigh over 200 kg (Harcourt et al. 1981) to mouse lemurs (Microcebus berthae) that can weigh as little as 30 g (Dammhahn and Kappeler 2005). There is no single trait that unambiguously distinguishes primates from other mammals; instead they are generally identified by a shared suite of characteristic traits (Stanford et al. 2013). Primates have a fairly gener-alized mammalian body plan, with the exception of distinct anatomical adaptations for specialized locomotion (Fleagle 2013). Primates also generally exhibit opposable thumbs, which permit precision grasp and sensitive tactile manipulation—although in some strepsirrhines this trait is less fully devel-oped. In contrast to humans, other primates also

Taxonomic overview

Primates

Tarsioidea

Tarsiidae Cebidae

Ceboidea

Haplorhines

Cercopithecoidea Hominoidea

HylobatidaePonginaeHomininae

Cercophithecidae

Colobinae

AnthropoidsProsimians

Cercopithecinae

Strepsirhines

Lorisoidea

LorisidaeGalagonidae

Lemuroidea

LemuridaeCheirogalidaeDaubentoniidaeIndriidae

Figure 1.2 Overview of primate taxonomy illustrating the two alternative classification systems. Under one system the Tarsioidea are grouped with Ceboidea, Cercopithecoidea, and Hominoidea as Haplorhines (and Lemuroidea and Lorisoidea comprise the Strepsirhines); under the other Tarsioidea are grouped with Lemuroidea and Lorisoidea as Prosimians while the Ceboidea, Cercopithecoidea, and Hominoidea comprise the Anthropoids. After Stanford et al. 2013.

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Primates also have unusual life histories. Com-pared to other mammals, primates in general have slower life histories, living longer, maturing more slowly, and producing smaller numbers of off-spring (Charnov and Berrigan 1993). Proposed explanations for the slow life history exhibited by primates include their relatively large brains (Har-vey et al. 1987), social complexity (Dunbar and Shultz 2007), cooperative breeding (van Schaik et al. 2012), arboreality (Shattuck and Williams 2010), and low levels of daily energy expenditure (Pontzer et al. 2014).

Most primate species live in permanent groups with complex social interactions (Mitani et al. 2012). These groups can be as large as a few hundred at the sleeping sites of gelada baboons or very small as in the case of one-male, multi-female groups of some langur species. There are, however, notable exceptions such as orang-utans (Pongo sp.) that do not live in permanent groups (Wich et al. 2009) and primate species that live in pairs (Palombit 1996). There are also species that exhibit fission–fusion

Most primate species consume a diverse diet, which is reflected in their rather unspecialized teeth compared to other mammals, although varia-tion in dental characteristics such as incisor length, structure of molars, and enamel thickness has been linked to diet (Swindler 2002; Lucas 2004), particu-larly the components of the diet that are most dif-ficult to process (Rosenberger 1992; Marshall and Wrangham 2007). In the past it was argued that all primates could be distinguished from other mam-mals due to their possession of a small part of the inner ear called the petrosal bulla (Szalay Freder-ick and Eric 1979), but it is now unclear whether the earliest primates possessed this trait (MacPhee et al. 1983). Another anatomical feature that has been of considerable interest is the bony postorbital bar that completely or almost completely encloses the eyes of primates, but is absent in most other mammals (Fleagle 2013). The function of this trait is under considerable debate, but a recent hy-pothesis suggests that it protects the eye from the mechanical strains of chewing (Heesy 2005).

Primate distribution

Figure 1.3 Global primate distribution. Based on the IUCN Red List Primate Distribution Layer: http://www.iucnredlist.org.

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1.3 Threats to primates

A key goal of primate conservation is to determine and quantify the nature and magnitude of threats to primates. Below we note the most widely discussed threats to primates, most of which are considered in greater detail in subsequent chapters.

1.3.1 Habitat loss

There are three main threats to primate habitats: (1) total loss of habitat (e.g. due to clear cut logging or conversion to agriculture); (2) degradation of habi-tat (e.g. due to logging or mining); and (3) fragmen-tation of habitat (e.g. due to loss of surrounding habitat or roads). Habitat loss is the most severe of these because it reduces the total amount of suitable habitat available to a species and often results in the loss of all individuals contained in the destroyed habitat patch. Habitat loss is straightforward to quantify in the field because it is a complete replace-ment of natural vegetation by something else (e.g. agriculture, timber plantations, roads, houses). De-spite this, assessments of habitat loss from satellites can be more complex because some mature timber plantations are difficult to distinguish from forest (Hansen et al. 2013). Forests in the tropics, with the exception of Brazil, are declining at faster rates in recent years (Hansen et al. 2013); a worrying trend because most primates disappear once their habitat is cleared (e.g. chimpanzees; Campbell et al. (2008)).

1.3.2 Habitat degradation

Habitat degradation most often occurs due to legal or illegal logging. The effects of such degradation on primates differ greatly, depending on the species, logging intensity, the methods used, and the time since degradation (Johns and Skorupa 1987; Thomas 1991; Peres 1993; Chapman et al. 2000; Cowlishaw et al. 2009; Husson et al. 2009). An important unan-swered question for research on primate survival in altered habitats is whether primates can survive in areas that are under continuous, albeit well-managed logging, or whether a period of recovery between logging bouts is required (Chapman et al. 2000; An-crenaz et al. 2010). Although the effects of habitat deg-radation on primates have been studied for decades

social systems (Pan spp., Ateles spp.) where indi-viduals reside in a large community but spend their time in smaller subgroups that frequently change in composition as individuals move among them. The evolution of group living in primates is typically considered to have been shaped by food distribution, feeding competition, predation, and infanticide (Wrangham 1980; Schaik 1983; Schaik and Hooff 1983; Sterck et al. 1997). Socio- ecological models aim to explain the diversity of primate social systems on the basis of those factors (Kappeler and van Schaik 2002). Although these models have shed light on many aspects of primate socio-ecology, they have yet to explain the full range of variation seen in extant primates (Kappeler and van Schaik 2002; Clutton‐Brock and Janson 2012). In addition, while typical socio-ecological models imply great flexibil-ity in sociality in response to ecological conditions, there is clearly substantial phylogenetic inertia in primate social systems as well (Schultz et al. 2011).

Although some primate species are found in colder areas in countries like China, Nepal, and Ja-pan, most species live in warmer tropical climates (Figure 1.3). Within the tropics, primates occupy a large variety of habitat types that range from tropi-cal evergreen rainforests to arid savannahs. Within forests, primates can often be found at all heights, with some species being exclusively arboreal and others almost exclusively terrestrial. In contrast to many other mammals, the majority of primate spe-cies are active during the day (diurnal), although there are a substantial number of primate species that are active at night (nocturnal) and some that are active around dawn or dusk (crepuscular).

Most primate species consume a broad diet that consists mostly of fruit, leaves, flowers, and other vegetative materials. Often protein-rich foods such as insects, and occasionally meat, are also added. Perhaps the most well-known primate meat eaters are the chimpanzees, who hunt colobus monkeys on a regular basis in many populations (Boesch 1994; Stanford 1996; Watts and Mitani 2002). Other pri-mates, such as mandrills, have also been observed catching duikers (Kudo and Mitani 1985), while orang-utans have been witnessed to feed on a small nocturnal primate, the slow loris (Nyctecebus cou-cang) (Utami and van Hooff 1997; Hardu et al. 2012). Some primates also feed on gum from trees.

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collection of live primates for trade often entails kill-ing of other individuals, especially mothers (Malone et al. 2002; Shepherd et al. 2004; Nijman et al. 2011; Stiles et al. 2013). Although the trade in live primates is difficult to quantify, estimates are that tens if not hundreds of thousands of primates are caught for the pet trade per year (Nijman et al. 2011).

1.3.6 Disease

The threat of disease to primates is perhaps best understood in the African great apes. It is well documented that the Ebola virus has decimated gorilla and chimpanzee populations in Gabon and Congo (Walsh et al. 2003; Bermejo et al. 2006). In ad-dition, the increasing contact between humans and great apes through hunting, encroachment into ape habitat, research, and tourism has led to numer-ous cases where primates have been negatively affected by diseases acquired from humans (Wal-lis and Lee 1999). Recent research on chimpanzees in Ivory Coast has unequivocally established that disease can directly spread from humans to apes (Koendgen et al. 2008).

1.3.7 Climate change

There is increasing concern that climate change will negatively affect primates, through altering their time budgets, changing their food supplies, or re-ducing their habitats (Lehmann et al. 2010; Gregory et al. 2012). There has to date been little research con-ducted on the potential impact of climate change on primates, and the effects of climate change are unlikely to be easy to predict. This is partly due our limited understanding of the nature and rates of change in key factors such as food species dis-tribution and phenology, primate species’ dispersal abilities, and inter-specific interactions. In addition, potential interactions among these factors, and the adaptive potential of primate species to a changing climate, are virtually unknown (Marshall and Wich, Chapter 18, this volume).

1.3.8 Roads

The global road network is expanding rapidly as a result of increased demand for natural resources

and knowledge continues to accrue, we have yet to develop a predictive model of primate persistence under varying logging intensities.

1.3.3 Habitat fragmentation

The effect of habitat fragmentation on primate sur-vival depends on a variety of factors, including fragment size, species’ home range size and diet, inter-patch distance, and the nature of the matrix in which the habitat fragments are embedded (Chi-arello 1999; Michalski and Peres 2005; Boyle and Smith 2010; Meijaard et al. 2010).

1.3.4 Drivers of habitat loss, fragmentation, and degradation

A main cause of habitat loss and fragmentation is conversion to agricultural lands (Gibbs et al. 2010). During the 1980s and the 1990s more than 55% of new agricultural land in the tropics was created by replacing primary forest, while another 28% came from conversion of logged forests (Gibbs et al. 2010). Other proximate drivers of habitat loss, fragmentation, and degradation are wood extrac-tion and infrastructure development (Geist and Lambin 2002). Ultimate drivers of deforestation include economic factors such as the demand for timber; institutional factors related to land-use poli-cies; and demographic factors such as population growth (Geist and Lambin 2002). A recent analysis of the drivers of tropical deforestation showed that it is driven by urban population growth and urban and international demands for agricultural prod-ucts; perhaps somewhat counterintuitively, rural population growth was not associated with defor-estation (DeFries et al. 2010).

1.3.5 Hunting

Hunting occurs both within forests, when people hunt primates for either their own consumption or for trade, and at the interface between forests and agricultural lands, when primates raid crops (Peres 2001; Fa and Brown 2009; Meijaard et al. 2011). For many species hunting is not sustainable and can lead to local extinctions (Fa and Brown 2009). Killing also often occurs in the context of the pet trade because

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et al. 2005) and approximately 12% of the Earth’s terrestrial surface area carries some level of pro-tected status (Gaveau et al., Chapter 12, this vol-ume). Researchers have conducted various studies to evaluate the effectiveness of protected areas at preventing wildlife habitat loss, degradation, and fragmentation (Gaveau et al., Chapter 12, this vol-ume; DeFries et al. 2005; Andam et al. 2008; Joppa et al. 2008; Nagendra 2008; Newmark 2008; Joppa and Pfaff 2009). The conclusions of these studies differ, at least in part due to the use of different ana-lytical approaches. In addition, broad conclusions are unlikely to be appropriate because conditions, threats, opportunities, resources, and implementa-tion differ widely across protected areas. A recent large-scale study found that only half of the pro-tected areas assessed protected biodiversity well (Laurance et al. 2012). There is an ongoing debate over why protected areas might not be as efficient as we might wish. Part of this debate focuses on the management of protected areas and the issue of whether strictly protected areas that exclude local community participation are more effective than methods in which local communities have a more participatory role in management (Bruner et al. 2001; Wilshusen et al. 2002; Hayes 2006; Hansen and DeFries 2007). Other aspects of this debate focus on how protected area management plans should interact with larger scale landscape conservation strategies for multi-use landscapes (Meijaard, Chapter 13, this volume).

1.4.2 Law enforcement

A recurrent structural problem for primate conser-vation is the lack of appropriate law enforcement in many of the countries that primates inhabit (Struh-saker et al. 2005; Fischer 2008; Tranquilli et al. 2012). A recent Africa-wide review showed that law en-forcement is the best predictor of ape persistence in resource management areas (Tranquilli et al. 2012). Law enforcement is necessary to prevent illegal habitat conversion in protected areas or lands where alteration is prohibited (e.g. steep areas in Indone-sia; Wich et al. (2011)). It is also required to reduce the intense, illegal hunting of many primate popu-lations (Fa and Tagg, Chapter 9, this volume; Stiles et al. 2013). Although improving law enforcement is

and arable land. Although the importance of this infrastructure for human health and development is clear, it is raising many problems of great concern to conservationists. Roads facilitate access for hunt-ers and loggers, reduce forest cover, fragment pri-mate habitats, and kill wildlife through collisions with vehicles (Laurance and Balmford 2013; Caro et al. 2014). Road construction is therefore likely to limit primate distribution and reduce primate population density (Laurance et al. 2008; Gaveau et al. 2009; Laurance et al. 2009). There is thus an ur-gent need for careful planning so that future roads will not be established in areas that are important for conservation (Laurance and Balmford 2013; Laurance et al. 2013). In addition, greater consulta-tion between infrastructure developers and natural resource managers, a case-by-case examination of each proposed road, effective enforcement of traffic speed and volume, and the development of policies that make international development aid condi-tional upon appropriate assessments of the long-term costs of road development are also required (Caro et al. 2014).

1.4 Approaches to primate conservation

Given the magnitude and multitude of threats it is easy to despair for the persistence of primate populations; the challenges are great and the avail-able resources are scant. Nevertheless, primate conservationists have successfully protected pri-mate populations, sometimes despite apparently insurmountable hurdles (McNeilage 1996; Gray et al. 2013). Successes tend to be the result of a com-bination of multiple strategies and tactics and a careful tailoring of conservation approaches to the particular conditions and challenges on the ground. Below we briefly highlight some of the major cur-rent approaches to primate conservation. This is not meant to be an exhaustive list, rather we highlight some that are well represented in the literature or are novel and might be promising for the future.

1.4.1 Protected areas

Conservation efforts for primates and biodiversity have traditionally focused on the establishment of protected areas (Terborgh et al. 2002; Chape

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Chapter 7), primate trade (Nijman and Healey, Chapter 8), hunting (Fa and Tagg, Chapter 9), infectious diseases (Nunn and Gillespie, Chap-ter 10), and climate change (Korstjens and Hillyer, Chapter 11). The third section considers solutions to primate conservation challenges from sev-eral perspectives: protected areas (Gaveau et al., Chapter 12), landscape mosaics (Meijaard, Chap-ter 13), human–primate conflict (Humle and Hill, Chapter 14), reintroduction (Beck, Chapter 15), ecosystem services (Garcia-Ulloa and Koh, Chap-ter 16), and evidence-based conservation (Tran-quilli, Chapter 17). We conclude the book with a consideration of some future directions for pri-mate conservation research (Marshall and Wich, Chapter 18).

Acknowledgements

We thank Guy Cowlishaw for reviewing the chapter.

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1.4.3 Payments for ecosystem services

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1.5 Overview of the book

The chapters in this book are grouped into three sections: (1) background and conceptual issues, (2) threats, and (3) solutions. In the first section, the authors consider why we should conserve pri-mates (Marshall and Wich, Chapter 2), summarize the conservation status of primates (Cotton et al., Chapter 3), discuss species concepts and their relevance to conservation (Groves, Chapter 4), re-view primate conservation genetics (Salgado-Lynn et al., Chapter 5) and describe primate abundance and distributions (Campbell et al., Chapter 6). The second section includes discussion of threats from habitat destruction and degradation (Irwin,

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