Figure \(\PageIndex{1}\): A male Bornean orangutan (Pongo pygmaeus). This species’ large size and close genetic relatedness to humans often make them appealing to the public, categorizing them as a “charismatic species.” Such charismatic animals may garner more resources for conservation. In species like the Critically Endangered Bornean orangutan, whose habitat is highly threatened, this attention can be crucial to their survival (Ancrenaz et al. 2016).
Hunting represents one of the most critical threats to primates (Figure B.7). Bushmeat, which is the meat of wild animals, has historically been a staple diet in many societies. However, human population growth and economic development have increased the commercialization of bushmeat hunting, thereby increasing its impact (Estrada et al. 2017). The increased availability and use of shotguns has also dramatically increased the volume of carcasses that hunters capture (Cronin et al. 2015). Across 89 markets in Nigeria and Cameroon, John Fa and colleagues (2015) calculated that almost 150,000 primate carcasses (from at least 16 different species) were sold annually. In one market on the Liberia/Ivory Coast border, Ryan Covey and Scott McGraw (2014) estimated that the carcasses of nearly 9,500 primates (from at least nine different species) were sold per year, resulting in an almost 3% annual reduction in the local primate population.
Not all primates are hunted specifically for food. Biomedical researchers use primates as models for understanding human biology and as test subjects for the development of vaccines, drugs, and hormones (Conaway 2011). Many of these experiments require large numbers of primates; therefore biomedical facilities often require a continuous supply of primates. To support the international demand for biomedical research test subjects, rhesus macaques (Macaca mulatta) in northern and central India experienced a 90% decline in populations over a 28-year period, from 1959 to 1986 (Southwick and Siddiqi 1988). Between 2007 and 2008, a single biomedical laboratory purchased roughly 4,000 nocturnal monkeys for over 100,000 USD through a network of 43 traders across Brazil, Colombia, and Peru (Maldonado et al. 2009).
Figure \(\PageIndex{2}\): A female gelada (Theropithecus gelada) with a snare around its neck in central Ethiopia. Many rural hunters prefer to hunt using snare traps, which can be easily constructed and offer a more affordable and accessible alternative to firearms (Noss 1998; Tumusiime et al. 2010). Snare traps are constructed out of wire nooses anchored to trees or the ground. Snares are designed to tighten around prey as they struggle to free themselves. Though larger primates are sometimes able to detach snares from their anchored positions, the snare often remains wrapped around the affected body part and can result in loss of circulation, infection, and mutilation (Yersin et al. 2017).
Aside from biomedical research, captured primates are both legally and illegally sold to pet owners, zoos, tourist centers, and circuses. In Peru, it is estimated that, as recently as 2015, hundreds of thousands of primates are illegally traded every year, comparable to levels of trade prior to a 1973 national ban on primate exportation (Shanee et al. 2017). Once captured, primates may spend over a week in transit from a rural village to a coastal market. To make the transportation of primates more manageable, common trafficking strategies include sedation, asphyxiation, electrocution, and the removal of teeth. As these conditions severely affect the health of the trafficked primates, many perish during the journey while others die within the hands of authorities. Out of the 77 greater slow lorises (Nycticebus coucang) confiscated from a single wildlife trader in Indonesia, 22 died from either trauma or from the severity of their wounds (Fuller et al. 2018). Even when primates are successfully confiscated from wildlife traders, it is not uncommon for authorities to either resell or gift these animals to friends and family (Shanee et al. 2017).
To help curb illegal trafficking of animals, the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) was established in 1973 and ratified in 1975. Under this treaty, the 183 participating countries work together to both regulate the international trade of wildlife and to prevent the overexploitation of wild populations. While only some primates are listed as endangered or threatened under the Endangered Species Act (ESA), all primates are listed under CITES. According to the CITES database, more than 450,000 live primates were traded over the past 15 years (CITES n.d.). However, as the CITES database only includes information formally reported by each country, the real number of primates involved is likely to be much higher.
Habitat Loss, Fragmentation, and Degradation
The geographic distribution of many primate species has been severely limited by habitat loss. A recent analysis showed human demands for agricultural land threaten 76% of primate species, followed by demands for logging (60%) and livestock farming (31%) (Estrada et al. 2017). Habitat loss is not new and has affected the distribution of some primate species for thousands of years. Since the Bronze Age, for example, increases in human land use throughout China have been associated with corresponding decreases in suitable habitats for golden snub-nosed monkeys (Rhinopithecus roxellana) (Wang et al. 2014). However, our ever-growing need for food, water, and other natural resources has drastically decreased primate habitats globally (Figure B.8). From 2000 to 2013, roughly 220,000 km2 of tropical forest have been completely deforested in the Brazilian Amazon alone (Tyukavina et al. 2017). Since the start of oil palm development in Indonesia’s Ketapang District in 1994, over 65% of habitats without government protection have been allocated to the oil palm industry (Carlson et al. 2012). Even within protected areas, primate habitats are rapidly declining. In South Asia, 36% of surveyed protected areas had more than half of their habitat modified for human use, many of which experienced near-total habitat transformation (Clark et al. 2013). One of these protected areas, the Borajan Reserve Forest in India, saw a more than two-thirds reduction in suitable habitat within a three-year period, resulting in severe population declines for five primate species (Srivastava et al. 2001).
Figure \(\PageIndex{3}\) Cattle graze in a newly formed papaya plantation, which was once forested land in Montagne des Français, Madagascar. Forests are cleared throughout the tropics for both large-scale commercial agricultural as well as for subsistence farming. Conversion for agricultural expansion alone accounts for nearly 75% of all tropical deforestation (Hosonuma et al. 2012). While some primates may still be able to utilize these agricultural matrix environments for foraging and resting, it may put them in danger because of potential heightened human-wildlife conflict.
Habitat fragmentation compounds the effects of habitat loss. Whereas habitat loss reduces the total area in which primates can survive, habitat fragmentation divides large, contiguous primate habitats into smaller isolated patches (Figure B.9). The construction of road networks cutting through savannas, forests, and other primate habitats is a key driver of this fragmentation. Within the next half-century, over 25,000,000 kmof new roads are expected to be built, many of which in developing nations through primate habitats (Laurance et al. 2014). By fragmenting habitats, it becomes increasingly challenging for primates (particularly arboreal primates) to disperse between isolated habitat patches. While only 0.1% of black-and-white snub-nosed monkey (Rhinopithecus bieti) habitat was lost to the construction of China National Highway 214, movement between habitat patches on either side of the highway was reduced by over 20% (Clauzel et al. 2015). In the long run, habitat fragmentation can force primate populations into genetic bottlenecks, which occur when populations become so small that genetic diversity in them is severely reduced. In the forest fragments of Manaus, Brazil, groups of pied tamarins (Sanguinus bicolor) that historically formed one biological population were found to harbor only a subset of the genetic diversity previously exhibited in the region (Farias et al. 2015). Furthermore, primates living in fragments with scarce resources experience elevated levels of stress, which can also have long-term consequences on the health of individuals and populations (Rimbach et al. 2014).
Figure \(\PageIndex{}\) Forest cleared for cattle ranching in the province of Manabí, Ecuador. Cattle ranching is currently the main driver of deforestation in South American countries (Steinweg et al. 2016). Landholders clear and burn primary forests to convert them into cattle pastures, and when yield begins to decline, they typically move to another old-growth forest and the cycle begins again. Not surprisingly, tropical forests are disappearing faster than any other biome (Aide et al. 2013; Wright 2005). Halting deforestation through community-based conservation programs is one of the main objectives of many non-governmental organizations, such as Proyecto Washu in Ecuador.Figure \(\PageIndex{}\) An industrial-sized truck leaves the Montagne des Français region in Madagascar, with dozens of bags of charcoal in tow to be delivered to a nearby town. Much of sub-Saharan Africa still relies on charcoal and other fuelwoods as a main source of energy for cooking and heating. Fuelwood collection and charcoal production are the main proximate drivers of forest degradation throughout Africa (Hosonuma et al. 2012). Degradation and forest loss can lead to a suite of harmful effects for primates living in these regions.
Aside from habitat loss, other drivers of habitat degradation may affect primate populations. For example, streams can carry toxic chemicals used for agriculture into local habitats where they are either directly or indirectly consumed by primates. In Uganda, chimpanzees (Pan troglodytes) living within the Sebitoli Forest have been spotted with facial and limb deformities that are suspected of being related to their exposure to pesticides and herbicides used by local tea farmers (Krief et al. 2017). Additionally, invasive species that outcompete native species and alter habitats can affect primate behaviors. In Madagascar, southern bamboo lemurs (Hapalemur meridionalis) spent less time feeding in forests dominated by invasive Melaleuca trees (Melaleuca quinquenervia) than in forests without these trees (Eppley et al. 2015). Lastly, the use of fuelwood and charcoal is still widely used throughout sub-Saharan Africa as a means to produce heat and energy for cooking (Figure B.10).
Climate Change
Current State
Climate change is one of the most devastating threats facing primates because it compounds preexisting threats, such as habitat degradation and fragmentation. In a little over a century, the earth has seen temperatures rise by 0.85ºC globally, with each decade being warmer than the last (IPCC Climate Change 2014). The resulting changes that occur, many of which are just beginning to be documented, can be unpredictable and cause a range of consequences for biodiversity. Increasingly frequent regional droughts, especially in the Southern Hemisphere, not only affect resource abundance but also create a cascade of other ecosystem disturbances that contribute to increased carbon dioxide production (Zhao and Running 2010). In Kibale National Park, Uganda, Jessica Rothman and colleagues (2015) found that the increasing carbon dioxide levels associated with climate change decreased the nutritional value of leaves, an important food resource for many primates.
Climate change is associated with volatile and unpredictable weather patterns. El Niño Southern Oscillation events (ENSO) influence weather patterns across the globe. Although ENSO events have been occurring for thousands of years, climate change is causing them to occur more frequently and with greater intensity (Wiederholt and Post 2010). The warm air and unpredictable rains that come with an ENSO event can negatively affect food resource abundance. Primates whose diets include high quantities of fruit experience the effects of fruit shortages most strongly (Campos et al. 2015). Madagascar, a primate hot spot and country with high levels of anthropogenic disturbance, is a prime example of how the increased intensity and frequency of climatic events such as ENSO can have consequences for primates (Figure B.11). Amy Dunham and colleagues (2008) found that even the folivorous Milne-Edwards’ sifaka (Propithecus edwarsi), found within Ranomafana National Park in southeastern Madagascar, would experience severely reduced populations within three generations if ENSO events continued at the current frequency.
Figure \(\PageIndex{}\) An old-growth tree is uprooted after Cyclone Enawo made landfall in northeast Madagascar in March 2017. Ocean surface temperatures are increasing as a result of anthropogenic climate change, which may cause stronger tropical storms. These storms often result in dramatic alterations to ecosystems, changing vegetation composition by damaging trunks and branches of trees (Dinsmore et al. 2018). These changes in habitat structure can in turn have repercussions for primates living in these regions, driving them to alter feeding, moving, and reproductive patterns.
Rapidly changing climate also causes other extreme weather events in primate areas. Due to climate change, hurricanes and cyclones are occurring more frequently. Several studies have looked at the effects on primate populations before and after hurricanes (e.g., Ratsimbazafy 2006; Schaffner et al. 2012; Zimmerman and Kovich 2007). A population of howler monkeys in Belize (Alouatta pigra) experienced population reduction and reduced reproduction after a hurricane hit. This response lasted more than three years (Behie and Pavelka 2005; Pavelka and Chapman 2006). However, not all primates are as vulnerable to the effects of major storms. In Kirindy Mitea National Park in western Madagascar, Verreaux’s sifakas (Propithecus verreauxi) did not suffer reduced population or reproduction, despite a reduction in their food supply following a cyclone (Lewis and Rakontondranaivo 2011). The different responses of these species to catastrophic events is likely related to differences in their behavioral flexibility, such as adjusting the types of foods consumed and the amount of time spent resting, feeding, moving, and socializing by each species (Strier 2017) and evolutionary adaptability (Wright 1999).
Large-Scale Change
On a large scale, the deleterious effects of climate change can make primates’ current environments inhospitable. Most primates are adapted to live in tropical environments and many have specialized diets. Climate change alters the flowering and fruiting seasons of many plants, requiring a great deal of dietary flexibility from the organisms that rely on their production (Anderson et al. 2012). Many primates are not capable of this adjustment and would need to shift their habitat range to cope. Unfortunately, habitat loss and fragmentation make these range shifts impossible for many species without human assistance in the form of translocations. Primates have relatively slow life-histories, often producing only one offspring at a time, and their extended juvenile period results in slow evolutionary adaptation to change (Campos et al. 2017). To cope with the large-scale effects of climate change, primates must rely on behavioral flexibility and aid from humans. Primates are projected to have some of the most restricted ranges due to climate change (Schloss et al. 2012), forcing them to utilize a variety of possible, non-preferred habitats
Small-Scale Change
On a small or local scale, the effects of climate change are more fine-tuned and can differ depending on the species. For example, spider monkeys (Ateles geoffroyi yucatanensis) exhibited behavioral plasticity after two hurricanes hit Mexico, spending more time resting, feeding on leaves, and in smaller subgroups than they did before the hurricanes (Schaffner et al. 2012). Critically endangered species, such as the northern sportive lemur (Lepilemur septentrionalis), are more vulnerable to catastrophic weather events because in small populations the loss of just a few individuals can have major impacts (Figure B.12) (Dinsmore et al. 2016). Species that are not threatened or that have large, intact ranges are not likely to be greatly affected by localized climatic conditions, but they may nonetheless experience local devastation and even extinction (Strier 2017).
Figure \(\PageIndex{}\) A northern sportive lemur (Lepilemur septentrionalis) rests in a tree at Montagne des Français, Madagascar. A Critically Endangered species, the nocturnal northern sportive lemur is estimated to have a population of only ~50 individuals that are restricted to one forest fragment in northern Madagascar. For small populations like the northern sportive lemur, the impacts of climate change can be exacerbated. However, non-governmental organizations, such as Madagascar Biodiversity Partnership (MBP), work with species like the northern sportive lemur to increase their populations and minimize such impacts. MBP has been working at Montagne des Français to monitor northern sportive lemurs and initiate reforestation efforts since 2012.
Disease
Disease is especially intertwined with climate change and has increasingly become a critical threat to primates (Nunn and Altizer 2006). Shifting temperatures, unpredictable precipitation, crowding in fragmented habitats, and increased human contact can contribute to increased disease transmission among primates (Nunn and Gillespie 2016). Mosquito populations, which are vectors of diseases that affect humans and nonhuman primates like Zika virus, yellow fever, and malaria, often thrive in this type of environment and have expanded in recent years (Lafferty 2009). Disease outbreaks have the potential to severely reduce primate populations. In 2016 and 2017, a large yellow fever outbreak devastated several populations of the brown howler monkey (Alouatta guariba) endemic to the Atlantic forest of Brazil (Fernandes et al. 2017). Ebola outbreaks have similarly diminished populations of African apes; in 2003 and 2004, an outbreak killed up to 5,000 endangered western gorillas (Gorilla gorilla) (Bermejo et al. 2006) and severely reduced populations of chimpanzees (Pan troglodytes) (Leroy et al. 2004) in Gabon and the Republic of Congo.
Human encroachment into primate habitats as a result of agricultural expansion, resource extraction, or even through irresponsible eco-tourism or research practices can introduce novel pathogens into both human and nonhuman primate populations (Strier 2017). Due to our close shared lineage, many diseases are communicable between humans and primates, such as Ebola, HIV, tuberculosis, herpes, and other common ailments. Close contact and primate handling are often the most direct ways in which these diseases are transmitted. However, poor hygiene practices, improper waste disposal, and primate provisioning contribute to disease susceptibility in primates (Wallis and Lee 1999). For example, two groups of olive baboons (Papio cynocephalus anubis) living in the Masai Mara Game Reserve in Kenya contracted tuberculosis from foraging at contaminated garbage dumps near the tourist lodge (Tarara et al. 1985). Similarly, in Gombe National Park, Tanzania, there is evidence that contact with humans and their domesticated animals in nearby villages caused an outbreak of polio in chimpanzees (Pan troglodytes) (Williams et al. 2008). Transmission of diseases through increased human contact can have devastating effects on primate populations that have not built any resistance (Laurance 2015).
Extinction Vortex
Figure \(\PageIndex{}\) A model of the extinction vortex. The extinction vortex shows the threats and pressures that work simultaneously to threaten populations. These pressures are often exacerbated by the compounding effects they have on each other. Once a population has entered the vortex, this cascade of events can prevent recovery, resulting in extinction.
The many threats facing primates that we have listed here are completely interrelated. As such, they tend to interact with one another, creating what is known as an extinction vortex (Figure B.13; Gilpin and Soulé 1986). Habitat fragmentation and loss, hunting, climate change, and disease compound to reduce primate populations at a greater rate than when acting alone. Small populations living in isolated fragments of habitat are disconnected from the rest of their species and are therefore more vulnerable to inbreeding effects. Daniel Brito and colleagues (2008) found that many populations of the critically endangered northern muriqui (Brachyteles hypoxanthus) residing in the remaining fragments of the Atlantic Forest would experience genetic decay with possibility of extinction over the next 50 generations if management practices were not put into place. Slow life histories resulting in long interbirth intervals push many species of primates farther into the extinction vortex. Shifting demographics can have dire consequences for primates, thrusting them into a cycle that is hard to break once entered. With the continued presence of threats, many species have a difficult time recovering (Brook et al. 2008; Strier 2011a).
Figure \(\PageIndex{1}\): A male Bornean orangutan (Pongo pygmaeus). This species’ large size and close genetic relatedness to humans often make them appealing to the public, categorizing them as a “charismatic species.” Such charismatic animals may garner more resources for conservation. In species like the Critically Endangered Bornean orangutan, whose habitat is highly threatened, this attention can be crucial to their survival (Ancrenaz et al. 2016).
Figure \(\PageIndex{2}\): A female gelada (Theropithecus gelada) with a snare around its neck in central Ethiopia. Many rural hunters prefer to hunt using snare traps, which can be easily constructed and offer a more affordable and accessible alternative to firearms (Noss 1998; Tumusiime et al. 2010). Snare traps are constructed out of wire nooses anchored to trees or the ground. Snares are designed to tighten around prey as they struggle to free themselves. Though larger primates are sometimes able to detach snares from their anchored positions, the snare often remains wrapped around the affected body part and can result in loss of circulation, infection, and mutilation (Yersin et al. 2017).
Figure \(\PageIndex{3}\) Cattle graze in a newly formed papaya plantation, which was once forested land in Montagne des Français, Madagascar. Forests are cleared throughout the tropics for both large-scale commercial agricultural as well as for subsistence farming. Conversion for agricultural expansion alone accounts for nearly 75% of all tropical deforestation (Hosonuma et al. 2012). While some primates may still be able to utilize these agricultural matrix environments for foraging and resting, it may put them in danger because of potential heightened human-wildlife conflict.