Hunting, Poaching, and Wildlife Trade
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 (Estrada et al. 2017). The availability and use of shotguns has also dramatically increased the quantity of carcasses that hunters capture (Cronin et al. 2015). A study in the Ivory Coast indicated that primates are preferentially targeted for bushmeat hunting by economically reliant hunters, as primate meat is more likely to be sold in markets compared to smaller species (such as rodents), possibly due to its demand as a luxury product for those in nearby urban environments (Bachman et al. 2020). 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. 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, Nijman, and Bearder 2009). Although the use of apes in biomedical research has been severely reduced and/or banned in many countries, such as Austria, New Zealand, the United Kingdom, and the United States (Aguilera, Perez Gomez, and DeGrazia 2021), the use of other primates to study disease transmission, incubation, vaccine effectiveness, and similar topics is still ongoing and has recently been widespread in studying SARS-CoV-2 (Corbett et al. 2020; Lu et al. 2020; Stammes et al. 2021).
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, Mendoza, and Shanee 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, authorities sometimes resell or gift these animals to friends and family (Shanee, Mendoza, and Shanee 2017).
A growing concern of primate conservationists is the use of social media to convey harmful images of primates. People posting on social media sites, such as Instagram, TikTok, Facebook, and YouTube, who show videos and photos of primates dressed in human clothing, tourists engaging with primates while traveling, and “funny” or “cute” photos of primates as pets, may not realize the negative impact their posts can have. The sharing of this content, coupled with comments expressing the desire to own the subject as a pet, can motivate further harvesting of these species from the wild (Clarke et al. 2019; Norconk et al. 2019). After a video depicting a pygmy slow loris (Nycticebus pygmaeus) being “tickled” went viral in 2009, and another depicting a slow loris eating rice went viral in 2012, international confiscations of slow lorises increased (Nekaris et al. 2013).
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.
Disease has become a critical threat to human and nonhuman primates alike (Nunn and Altizer 2006). Shifting temperatures, unpredictable precipitation, crowding in fragmented habitats, and more frequent human contact can contribute to increased disease transmission among primates (Nunn and Gillespie 2016). Mosquito populations often thrive in this environment and are vectors of diseases that affect both humans and primates, such asZika virus, yellow fever, and malaria (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 monkeys (Alouatta guariba) and other species in the Atlantic forest of Brazil (Fernandes et al. 2017; Strier et al. 2017; Possamai et al. 2022). 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 ecotourism or research practices can introduce novel pathogens into both human and 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 (e.g. providing food resources to primates) 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). Recently with the proliferation of social media, tourists are coming into close contact with charismatic primate species, such as orangutans, in an effort to capture engaging photographs. Such close contact with varied populations is yet another driver for possible increased disease transmission (Molyneaux et al. 2021). Transmission of diseases through increased human contact can have devastating effects on primate populations that have not built any resistance (Laurance 2015).
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 biological resources threaten 81% of primate species, followed by demands for agricultural land (80%) and residential and commercial development (32%; see Fernández et al. 2022). Habitat loss is not new and has affected the distribution of some primate species, including golden snub-nosed monkeys (Rhinopithecus roxellana), for thousands of years (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). Habitat loss can lead to increased human-primate conflict. After a 2004 tsunami destroyed large areas of natural habitat on India’s Nicobar Islands, local farmers witnessed increased crop raiding by long-tailed macaques (Macaca fascicularis; Velankar et al. 2016). In Saudi Arabia, expanding cities and improper waste disposal practices contributed to the formation of unusually large urban troops of Hamadryas baboons (Papio hamadryas) that are less fearful of humans than troops surveyed in rural areas (Biquand et al. 1994). 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). In a protected area in northern Madagascar that houses the last remaining population of the critically endangered Northern sportive lemur (Lepilemur septentrionalis), forest cover was reduced from 76% to 24% in a 60-year time frame (Dinsmore et al. 2021a).
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 km of new roads are expected to be built, many of which will be located 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 (Sanguins 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).
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, fuelwood and charcoal are still widely used throughout sub-Saharan Africa to produce heat and energy for cooking. Heavy reliance on these resources can result in degradation of primate habitat, fragmentation, and overall forest loss (Figure B.10).
The ramifications of climate change, many of which are just beginning to be documented, can be unpredictable and cause a range of consequences for biodiversity, compounding preexisting threats facing primates, as each decade is warmer than the last (IPCC 2022). On a large scale, the deleterious effects of climate change can make primates’ current environments inhospitable. Additionally, climate change alters the flowering and fruiting seasons of many plants, requiring 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. Arboreal primates have already been observed to shift the utilization of their habitats due to climate change, especially by spending more time on the ground (Eppley et al. 2022). Unfortunately, habitat loss and fragmentation make these range shifts impossible for many species without human assistance in the form of translocations. Compounding this, primates have relatively slow life-histories, often producing only one offspring at a time, and their extended juvenile period results in minimal evolutionary adaptation to change (Campos et al. 2017; Bernard and Marshall 2020). Primates are projected to have some of the most restricted ranges due to climate change (Schloss, Nuñez, and Lawler 2012), forcing them to utilize a variety of possible, nonpreferred habitats.
Rapidly changing climate also causes other extreme weather events in primate areas. Due to climate change, hurricanes and cyclones are increasing in severity. On a small or local scale, these stochastic environmental events are more fine-tuned and the severity can differ depending on the primate species, which can directly impact populations or their habitats (Figure B.11). For example, spider monkeys (Ateles geoffroyi yucatanensis) were not severely affected after two hurricanes hit Mexico but still exhibited behavioral plasticity by spending more time resting, feeding on leaves, and gathering in smaller subgroups than they did before the hurricanes (Schaffner et al. 2012). Some species, such as the critically endangered northern sportive lemur (Lepilemur septentrionalis), which has an estimated population of ~87 individuals, exhibited behavioral plasticity after a Category 4 cyclone (Figure B.12; Bailey et al. 2020; Dinsmore et al. 2021b). However, stochastic weather events can still severely impact the species by causing the direct death of individuals in an already-small population, reducing overall population totals and genetic diversity (Dinsmore et al. 2021b). 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).
Dig Deeper: The COVID-19 Pandemic
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes COVID-19, was first recorded in December of 2019 and has infected millions of people since then. Although humans have been the primary focus during this global pandemic, other animals, such as minks, cats, fruit bats, and nonhuman primates can also be infected (Oude Munnink et al. 2021). Human-to-animal transmission of diseases like COVID-19 is a process most commonly known as “zooanthroponosis” or “reverse zoonosis” (Messenger, Barnes, and Gray 2014). For example, in January 2021, western lowland gorillas at the San Diego Zoo in California were confirmed to have contracted SARS-CoV-2 (USDA 2021).
Apart from the direct risks that respiratory viruses bring to nonhuman primates, the COVID-19 pandemic also brought economic crisis and limited human presence in conservation areas.The reduction in human mobility due to the pandemic is being referred to as “anthropause”—a term coined to represent the temporary diminishment of the human footprint. However, this reduction in movement halted conservation action on the ground, potentially increasing poaching and the wildlife trade by people who rely more heavily on natural resources due to global market stress (Rutz et al. 2020). Given the interactions among the multiple consequences of the COVID-19 pandemic, many scientists fear that increased poaching pressure could push some primates, especially the great apes, closer to extinction (Casal and Singer 2021).
Dig Deeper: Extinction Vortex
The many threats facing primates that we have listed here are interrelated: as they interact with one another, they create 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 any one factor acts 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 the possibility of extinction over the next 50 generations if management practices are not put into place. Slow life histories resulting in long interbirth intervals push many primate species 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).