



Of the nearly 600 species and subspecies of primates living today approximately half are in danger of extinction; an estimate that has increased alarmingly over the preceding decade (Mittermeier et al. 2009). In fact, one subspecies in West Africa, Miss Waldron's red colobus (Procolobus badius waldronae), may already be extinct (Oates et al. 2000, but see McGraw 2005). Furthermore, the number of recognized serious threats to primate survival has increased over the last decade. A decade ago, while disease was recognized as an important area of study, it was not considered a factor that could threaten primate populations with local extinction. In contrast, today there are a number of well documented cases of dramatic primate population declines caused by disease (e.g., Bermejo et al. 2006) and it is considered a vital factor in conservation planning, particularly for those populations that are in danger of contracting diseases from exposure to humans (e.g., ape ecotourism). Similarly, in the last decade, climate change has gone from something largely ignored by many countries to a phenomenon of grave concern. Here we review the current major threats to primate populations (habitat loss, disease, bushmeat hunting, and climate change), consider how perceptions of these threats have changed, and reflect on whether the situation is hopelessly grave (the cup half empty) or there are reasons for optimism (the cup is half full).

Habitat Loss

In 2010, the Food and Agriculture Organization of the United Nations (FAO) estimated that 16 million ha/year of forest was lost globally in the 1990s (FAO 2010); approximately 12.5 million ha/year were lost in countries with primate populations, an area greater than the state of Mississippi, or just smaller than Greece (Chapman & Peres 2001). Based on global estimates of primate densities this would have resulted in the loss of 32 million primates/year (Chapman & Peres 2001). In contrast, in the last decade, the rate of deforestation has decreased globally to approximately 13 million ha/year and reforestation and natural expansion of forests in some countries significantly reduced the net loss of forest (FAO 2010). The net loss in forested area from 2000 to 2010 was estimated at 5.2 million ha per year, down from 8.3 million ha/year in the preceding decade. Some of the increased rate of reforestation can be attributed to declining human fertility rates and an increasing urbanization trend that is occurring in many developing countries (Jacob et al. 2008, Wright & Muller-Landau 2006). These factors have resulted in the decreased demand and even abandonment of agricultural lands in many parts of the world. Changes in human demographic patterns and forest cover vary dramatically depending on what region of the world one is considering (Figure 1), and these parameters provide both a means of predicting future forest loss — or gain — and are an important element in conservation planning at a local level. A detailed example of this is found in the Rio Cuale watershed in the state of Jalisco, Mexico (Figure 2). Interviews and analysis of demographic data of the residents revealed that the lack of high schools and job opportunities in the rural areas encouraged migration of the youth to the nearby city of Puerto Vallarta; a tourist center with greater economic opportunities (Bauche 2007, Jacob et al. 2008). This migration left areas un-used and tropical forests regenerated.



Figure 1 An example of the tropical deforestation that occurs in Central Africa. © 2012 Courtesy of Melissa Remis. All rights reserved.



Figure 2 (Top) The annual rate of forest loss in different regions of the world between 1990 and 2000, and between 2000 and 2010 (FAO 2010), and (Bottom) the annual rate of change of the area of forest designated primarily for conservation of biodiversity in different regions of the world between 1990 and 2000, and between 2000 and 2010 (FAO 2010). © 2012 All rights reserved.



Figure 3 Increase in forested areas in the Rio Cuale Watershed, Jalisco, Mexico, from 1979 (a) to 2002 (b) Forest in green, agricultural land in yellow. © 2012 Adapted from Jacob et al. 2008. All rights reserved.

Although slowing rates of habitat loss are an encouraging sign for primate conservation, deforestation is still occurring at an alarming rate, and strong efforts must be made to promote forest conservation and regeneration. We state this both because of the direct impact of any habitat loss on primate populations and because of how it indirectly affect primates by interacting with other drivers of populations change. For example, deforestation and other land use changes are estimated to have released 150 billion metric tonnes of carbon into the atmosphere since 1850, approximately one fifth of the total carbon in the atmosphere (Houghton 2003). Currently, deforestation accounts for approximately 18% of global carbon emissions, which is the third largest source of emissions (IPCC 2007, Keith et al. 2009), and it is this carbon dioxide that is one of the main drivers of climate changes. Climate change is predicted to have strong negative effects on some primate species (see below).

Disease

The sudden appearance of diseases like swine flu in humans and wildlife, the devastating impacts that diseases like Ebola have had on both human and wildlife communities, and the immense social and economic costs created by viruses like HIV, underscore our need to understand the ecology of infectious diseases. Given that monkeys and apes often share diseases with humans — due in part to their shared evolutionary history — understanding the ecology of infectious diseases in non-human primates is of paramount importance for both primate conservation and public health. This is well illustrated by outbreaks of the Ebola virus, which trace their origins to zoonotic transmissions from local apes (Leroy et al. 2004). The most dramatic illustration of the potential impact of disease on primates is the documented declines in endangered great ape populations. For example, throughout the Congo Basin there have been reports of gorilla and chimpanzee populations being decimated, with documented declines of affected populations being as high as 80 to 99% (Bermejo et al. 2006, Huijbregts et al. 2003).

As recently as the 1980s the dominant perspective on the treatment and prevention of infectious diseases was one of optimism (Cohen 2000), and immunization and antibiotics were considered adequate for combating infectious diseases. In fact, the eradication of smallpox in 1979 led to the hope that, through collective global action, most major diseases could be eradicated (Fenner 1983). This optimism was shattered by the increased prevalence of antibiotic resistant bacteria and the emergence of diseases such as Ebola, HIV, multi-drug-resistant tuberculosis, malaria, and enterohemmorhagic E. coli, and extreme difficulty in eradicating diseases globally despite massive efforts. Diseases are now viewed as being a serious threat to primate and human populations, and a consideration of how environmental change may promote contact between humans and non-human primates, and increase the possibility of sharing infectious diseases, is now paramount to both conservation and human health planning (Bonnell et al. 2010). Furthermore, the realization has been made that disease outbreaks can be promoted by anthropogenic changes to the environment, such as logging (Gillespie et al. 2005) and climate change (Chapman et al. 2010), which is cause for additional concern.

Bushmeat Hunting

While hunting has likely been a major driver of primate population declines for many decades, it was not until the early 1990s that academics and conservation biologists started to realize how devastating an impact hunting was having on the local abundance of some primate species. For example, a market survey in two cities in Equatorial Guinea, West Africa, with a combined human population size of 107,000, recorded 4,222 primate carcasses on sale over 424 days (Fa et al. 1995). Peres (1990) documented that a single family of rubber tappers in a remote forest site of the Brazilian Amazon killed more than 200 woolly monkeys (Lagothrix lagotricha), 100 spider monkeys (Ateles paniscus), and 80 howler monkeys (Alouatta seniculus) over 18 months. Estimates suggest that the annual wild meat harvest is 23,500 tonnes in Sarawak, Malaysia, 67 to 164 thousand tonnes in the Brazilian Amazon, and 1 to 3.4 million tonnes in Central Africa (Milner-Gullard et al. 2003). The estimate from Central Africa is approximately six times the maximum sustainable rate of harvest (Milner-Gullard et al. 2003). The trade and consumption of bushmeat is often incorrectly perceived as being a local issue, with the meat being consumed only by people within the region. This perception is false — bushmeat trade is a large international business. For example, it is estimated that approximately five tonnes of bushmeat is smuggled in personal baggage through Paris Charles de Gaulle airport every week (Chaber et al. 2010). This weight in bushmeat is equivalent to moving approximately 570 cows through this airport a year.

Since the bushmeat trade is not just a local issue, there are great opportunities to coordinate advances in both development and conservation. When bushmeat is not consumed locally it requires transportation, which often takes the form of loading carcasses onto logging trucks. This provides the unique opportunity for governments and conservation agencies to develop strategies when road systems are being developed or logging concessions assigned, which minimize adverse effects on forest wildlife (Wilkie 2000).



Figure 4 An example of bushmeat hunting in the Brazilian Amazon. © 2012 Courtesy of Carlos Peres. All rights reserved.

Climate Change

The Earth's climate has warmed by ~0.6°C over the past 100 years, and some estimates suggest that the climate could warm by 6°C this century (IPPC 2001, Walther et al. 2002). There is a great deal of concern voiced about potential impacts of climate change on primate populations and their tropical environments, but actual data that can be brought to bear on the effects of climate change are very scarce. However, Dunbar (1998) projected how gelada baboons (Theropithecus gelada) would respond to climate warming and suggested that the lower altitudinal limit of the species would rise by approximately 500 m for every 2°C increase in global mean temperature; as a result the land area available would effectively halve and become more fragmented. A 7°C rise in temperature would be sufficient to reduce the species' population size from its current size of approximately 250,000 to about 5,000 geladas on a few isolated mountain peaks where their long-term survival would be unlikely.

As well as direct effects of climate change on primate populations, primates may be affected by either the loss of particular plant species or changes in the leafing, flowering, and fruiting patterns of plant communities. Through a series of computer modelling exercises, McClean et al. (2005) studied the impact of projected climate change on the distribution of 5,197 African plant species. For 81–97% of these species, areas of suitable climate are projected to decrease in size and/or shift in location, many to higher altitudes, and 25–41% of species will lose all their area by 2085. The models suggest dramatic changes in the forest that extend from Guinea in West Africa all the way to the Rwenzori Mountains on the east side of the Democratic Republic of Congo, which today encompasses some of the most extensive blocks of remaining forest in Africa.

Changes in the climate will also interact with other drivers determining primate population sizes. Human medical professionals have recently become concerned as to whether global warming will cause increased rates of infectious diseases and, with their wealth of clinical data, are well ahead of primate ecologists at documenting trends. For example, connections between weather and disease are well established, and many diseases occur during certain seasons or erupt in association with unseasonable conditions. For example, in sub-Saharan Africa, meningococcal meningitis epidemics erupt during the hot dry season and subside soon after the onset of the rains (Patz et al. 1996). In the United States, 68% of waterborne disease outbreaks were preceded by precipitation events above the 80% percentile (Hunter 2003). Similar links between environment and diseases likely exist for primates, suggesting climate change may change how current diseases affect primate populations as well.

Future Directions

It is obvious that many primates are endangered by human actions and that great effort needs to be placed in conserving the forests they inhabit. However, we believe that there is reason to be optimistic as the rate of forest loss is declining, a great deal is now known about primate diseases, and programs to decrease the bushmeat industry are being successfully implemented (Wilkie1992). This optimism should not make us reduce our efforts; rather this knowledge of the threats offers great opportunities for scientists to make significant contributions to primate conservation. In many respects, the research done over the last few decades has laid out very clear objectives that can be met to promote primate conservation; for example, by offering people sustainable alternatives to the bushmeat trade, reducing deforestation and promoting reforestation, developing parks, and making protocols for reducing the risk of disease transmission between people and primates, and reducing carbon emissions to curb climate change. Certainly there are many questions that now need to be addressed to make primate conservation a reality. These include: What will direct depopulated areas into a process of ecological recovery or into plantation economies? How can conservation gains be made from declining rural populations in a socially responsible way? What are effective measures to reduce the transmission of diseases among people and non-human primates? How is it possible to reduce the national and international trade in bushmeat? And, how will climate change impact specific regions and primate species? All of these questions provide the foundation upon which to build research programs that will make a difference and provide the information needed to construct informed conservation/management plans.