Collapse of the world’s largest herbivores

Introduction

Terrestrial mammalian herbivores, a group of ~4000 species, live in every major ecosystem on Earth except Antarctica. Here, we consider the 74 wild herbivore species with mean adult body masses ≥100 kg. These largest species represent four orders (Proboscidea, Primates, Cetartiodactyla, and Perissodactyla) and 11 families (Elephantidae, Rhinocerotidae, Hippopotamidae, Giraffidae, Bovidae, Camelidae, Tapiridae, Equidae, Cervidae, Suidae, and Hominidae). Most of these species are entirely herbivorous, but some are generalists (for example, Suidae). Herein, we provide the first comprehensive review that includes the endangerment status and key threats to the world’s largest herbivores (≥100 kg), the ecological consequences of their decline, and actions needed for their conservation. We review how the combined impacts of hunting, encroachment by humans and their livestock, and habitat loss could lead to the extinction of a suite of large herbivores relatively soon. By reviewing their ecological roles, we show how the loss of large herbivores can alter ecosystems, mostly to the detriment of other species, including humans, through the loss of ecological interactions and ecosystem services. We end by outlining future directions for research and conservation action to help diminish the imminent possibility of losing the remaining large herbivores from many ecosystems throughout the world.

Status

According to the International Union for the Conservation of Nature (IUCN), 44 of the 74 largest terrestrial herbivores (~60%) are listed as threatened with extinction (including 12 critically endangered or extinct in the wild), and 43 (~58%) have decreasing populations [(1); table S1]. Their current population sizes exhibit large differences among species, spanning over four orders of magnitude, with some populations estimated to comprise fewer than 100 individuals [for example, Javan rhinoceros (Rhinoceros sondaicus)], whereas a few others [for example, Eurasian elk/moose (Alces alces)] comprise more than 1 million individuals (table S1).

Most large herbivore species are found in Africa (n = 32), Southeast Asia (n = 19), India (n = 14), China (n = 14), and the rest of Asia (n = 19) (Fig. 1A). Fewer species are found in Europe (n = 7), Latin America (n = 5), and North America (n = 5) (fig. S1). Overall, 71 species occur in developing countries, whereas only 10 occur in developed countries. The highest number of threatened large herbivores occurs in Southeast Asia (n = 19, east of India and south of China), followed by Africa (n = 12), India (n = 9), China (n = 8), Latin America (n = 4), and Europe (n = 1) (Fig. 1B and fig. S1). Notably, all of the threatened species of large herbivores are found in developing countries, with the exception of European bison (Bison bonasus), with developed countries having already lost most of their large mammals in the ongoing megafauna extinction (2).

Ecoregions [n = 30, based on (3)] with the most-threatened large herbivore species (≥5) are found in southern Asia, throughout much of extreme Southeast Asia, as well as Ethiopia and Somalia of eastern Africa (Fig. 1B and tables S2 to S4). The ecoregions with seven threatened large herbivore species are the Himalayan subtropical broadleaf forests, the Sunda Shelf mangroves, and the peninsular Malaysian rain forests (table S4). Hunting for meat is the predominant threat in all ecoregions containing at least five threatened large herbivore species (table S2). These ecoregions fall mostly within the tropical and subtropical moist broadleaf forests biome (20 of 30 ecoregions), but biomes containing combinations of grasslands, shrublands, savannas, mangroves, or other forest types represent the other 10 ecoregions with at least five threatened large herbivore species (table S3).

All 10 large herbivore species within the families Elephantidae, Hippopotamidae, Hominidae, and Tapiridae are currently threatened (Fig. 2). The large herbivores of the families Suidae, Rhinocerotidae, Equidae, and Camelidae are also highly endangered, with 15 of 20 member species threatened (Fig. 2). Only eight terrestrial megafauna species (≥1000 kg) exist today as opposed to more than five times that number (~42) that were present in the late Pleistocene (4–6). The eight remaining species are split between Africa (African elephant, Loxodonta africana, hippopotamus, Hippopotamus amphibius, and the white and black rhinoceros, Ceratotherium simum and Diceros bicornis, respectively) and Southeast Asia (Asian elephant, Elephas maximus, and the Indian, Javan, and Sumatran rhinoceros, Rhinoceros unicornis, R. sondaicus, and Dicerorhinus sumatrensis, respectively). Of these, seven are threatened, including four critically endangered, and the white rhinoceros is nearly threatened with the current poaching crisis likely to alter its status downward in the near future. Ironically, this endangerment follows one of the greatest success stories in the history of modern conservation: the recovery of the southern white rhino (C. simum simum) from a single population of fewer than 100 individuals in the early 1900s to about 20,000 today [(7), table S1]. Even with the current crisis of rhinoceros poaching, this illustrates that, with sufficient protection, recovery is possible for relatively slow-breeding species that are highly prized by poachers.

Many of the largest herbivore species have ranges that are collapsing (8, 9). Estimates of range contractions have been made for 25 of the 74 species, and on average, these species currently occupy only 19% of their historical ranges (table S1). This is exemplified by the elephant, hippopotamus, and black rhinoceros, all of which now occupy just tiny fractions of their historical ranges in Africa (Fig. 3). Furthermore, many of these declining species are poorly known scientifically, and badly in need of basic ecological research. Scientific research effort, as measured by the number of published articles on each species, has been much greater for nonthreatened (\(\bar{X}\) = 296, SE_\(\bar{X}\) = 129) than threatened species (\(\bar{X}\) = 100, SE_\(\bar{X}\) = 33), and greater overall for species in developed countries (\(\bar{X}\) = 790, SE_\(\bar{X}\) = 376) than developing countries (\(\bar{X}\) = 172, SE_\(\bar{X}\) = 33). Indeed, those that have been most studied are primarily game species in wealthy countries, including red deer (Cervus elaphus), reindeer (Rangifer tarandus), and moose/Eurasian elk (A. alces) (fig. S2). In contrast, 18 of the large herbivore species from developing regions have been featured in fewer than 10 published articles each (fig. S2), which, in part, reflects negative or indifferent attitudes toward some species, or low levels of scientific funding, making it difficult to garner government and public support for scientific studies and conservation of these taxa (10). For example, although highly threatened, the six large-bodied species in the Suidae family are collectively represented by only 26 published articles (\(\bar{X}\) = 4 per species, range = 0 to 14) (table S5 and fig. S2).

Between 1996 and 2008, the conservation status of seven herbivore species ≥100 kg deteriorated, whereas only two species improved (table S1). By contrast, small herbivores are doing relatively well with just 16% of species below 5 kg in body mass classified as threatened (fig. S3). In contrast to the developing world, effective game laws and extirpation of large predators in developed countries of northern latitudes have frequently resulted in an overabundance of large herbivores. In the absence of wolves (Canis lupus) and other large carnivores, overabundant cervids can negatively impact biodiversity, stream morphology, carbon sequestration, and ecosystem function (11). Confining large herbivores within fixed boundaries can also lead to overabundance as with bison (Bison bison) in North America (12) and elephants in Africa (13).

Threats

The main threats to large herbivores are hunting, competition with livestock, and land-use change such as habitat loss, human encroachment, cultivation, and deforestation (Fig. 4 and fig. S4). Extensive overhunting for meat across much of the developing world is likely the most important factor in the decline of the largest terrestrial herbivores (14–17). Slow reproduction makes large herbivores particularly vulnerable to overhunting. The largest- and slowest-to-reproduce species typically vanish first, and as they disappear, hunters turn to smaller and more fecund species (14), a cascading process that has likely been repeated for thousands of years (6, 18, 19). In synergy with changes in land use, hunting for meat has increased in recent years due to human population growth, greater access to wildlands due to road building, use of modern firearms and wire snares, access to markets, and the rising demand for wild meat (14, 20). Wild meat harvests have been especially high in tropical forests, leading to vertebrate extirpations on large spatial scales, a process originally dubbed the “empty forest” syndrome (21). Annual consumption of wildlife meat was estimated to be 23,500 tons in Sarawak, Malaysia (22), and 89,000 tons in the Brazilian Amazon (23). Wild meat hunting also represents an increasing threat in African savannas, resulting in widespread declines in herbivore populations (17). Because wildlife populations outside of protected areas wane, hunters are shifting their attention more to populations in protected areas (17). Demand for wild meat is intensifying, supply is declining, and protected area management budgets for protecting wildlife from overhunting are often inadequate, particularly in developing nations. This creates a “perfect storm,” whereby overhunting often imparts catastrophic population declines (17). Between 1970 and 2005, large mammal populations in Africa’s protected areas decreased by about 59% (16). In part due to overhunting, current ungulate biomass was recently calculated to be only 21% of estimated potential ungulate biomass in Zambia’s national parks (24).

Hunting large herbivores for body parts is also driving down populations of some species, especially the iconic ones. Organized crime is facilitating a dramatic decline of elephants and rhinoceros in parts of Africa and southern Asia, reversing decades of conservation accomplishments. Poaching and illegal trade in elephant products are currently the top threats to elephants (25). Ivory poaching has surged in recent years, largely due to a rise in demand for and price of ivory in China (26). The number of forest elephants (L. africana cyclotis) in central Africa declined by 62% between 2002 and 2011 (25). Currently, 75% of elephant populations are declining and at risk of extirpation, and the range of elephants has drastically declined (26). More than 100,000 African elephants were poached during the 3-year period from 2010 to 2012 (26). This level of illegal kills represents 20% of the current estimated population size of 500,000 African elephants, and even populations of savanna (or bush) elephants (L. africana africana) are now declining (26). Poaching of rhinoceros for their horns has also soared in recent years because of its use in traditional Chinese medicine. The number of rhinoceros poached in South Africa grew by two orders of magnitude from 13 in 2007 to 668 in 2012 (27) and 1004 in 2013 (28). The situation is so desperate that an emergency intervention is planned in which large numbers of white rhinoceros will be translocated out of South Africa’s Kruger National Park and placed in potentially more secure areas (29). Furthermore, at least in part due to poaching, Africa’s western black rhinoceros (D. bicornis longipes) was declared extinct in 2011 (1). This slaughter is driven by the high retail price of rhinoceros horn, which exceeds, per unit weight, that of gold, diamonds, or cocaine (27). If accelerated poaching by organized crime syndicates continues, Africa’s rhinoceroses may become extinct in the wild within 20 years (27). Numerous species of other large herbivores are also hunted for their body parts, including hippopotamus for their ivory teeth, bovids for horns and skulls, equids for hides, tapirs for feet and hides, cervids for antlers, giraffids for hides, and gorillas for heads, hands, and feet (1). Large herbivores are more vulnerable than smaller herbivores to overharvesting through a combination of the generally higher value of larger bodies or their parts, and the slow life history of the larger herbivores. Together, these increase the likelihood of large herbivores being harvested and reduce their ability to recover from such harvests.

Livestock continues to encroach on land needed for wild grazers and browsers, particularly in developing countries where livestock production tripled between 1980 and 2002 (30). There are an estimated 3.6 billion ruminant livestock on Earth today, and about 25 million have been added to the planet every year (~2 million/month) for the last 50 years (31). This upsurge in livestock has resulted in more competition for grazing, a reduction in forage and water available to wild herbivores, a greater risk of disease transmission from domestic to wild species (32), and increased methane emissions (31). In central Asia, the expansion of goat grazing for cashmere wool production for international export has reduced habitats available to large herbivores with consequent impacts on their predators including snow leopards (Panthera uncia) (33). Livestock competition is also a significant threat to large herbivores elsewhere in Asia, with multiple species jeopardized by this threat in India (n = 7), China (n = 7), and Mongolia (n = 4) (fig. S4). Hybridization with domestic livestock varieties is also a serious problem for some wild species such as the Indian water buffalo (Bubalus arnee), Bactrian camel (Camelus ferus), wild yak (Bos mutus), Przewalski’s horse (Equus ferus), and several wild pig species (Sus spp.) in Southeast Asia (1). Ironically, in many pastoral settings in Africa, domestic livestock are abundant but not regularly consumed for subsistence, and are instead kept as a means of storing wealth, as a status symbol, or for consumption on special occasions (14). Livestock is a private good, and so, people invest significant energy to protect it, whereas wild herbivores are typically a public good, often resulting in weak incentives for their conservation and in many cases open access to the resource, both of which commonly result in overuse.

Habitat loss is a significant threat to large herbivores in parts of Latin America, Africa, and Southeast Asia (Fig. 4). The causes of this threat have important drivers originating in developed countries due to demand for agricultural and other products. Southeast Asia has the highest rate of deforestation among tropical regions, and if trends continue, Southeast Asia could lose 75% of its original forests and nearly half of its biodiversity by the end of this century (34). Habitat loss is typically asymmetrical with respect to quality, with remaining habitat generally being less productive. A similar trend is found in the tendency to create protected areas in steep, rocky, or dry terrain (35), trapping species of conservation concern in suboptimal habitats (36). Additionally, the greater area requirements of larger species make them unable to persist in smaller fragments of habitat, which may still support smaller herbivores. Their larger area requirement also makes larger species that persist in fragments increasingly susceptible to conservation challenges that affect small populations. This suggests a greater likelihood of extinction among the larger rather than smaller herbivores.

Other threats to large herbivores include human encroachment (including road building), cultivation of crops, and civil unrest, all of which contribute to population decline (Fig. 4). In the future, synergies among the factors discussed here will exacerbate the dangers to large herbivores, as is the case when increased hunting results from people being given access to fragmented, isolated forest remnants within previously extensive and less accessible areas (19). Beyond declines in abundance, the most threatened large herbivores are further imperiled by a loss of genetic diversity. The European bison, for instance, passed through a severe genetic bottleneck in the early 20th century and now suffers from balanoposthitis, a necrotic inflammation of the prepuce that inhibits breeding (37).

Consequences of large herbivore decline

Large herbivores shape the structure and function of landscapes and environments in which they occur (Fig. 5). They directly and indirectly affect other animal species throughout the food web, including their predators and smaller herbivores, and modify abiotic processes involving nutrient cycles, soil properties, fire regimes, and primary production. The roles of large herbivores thus cannot be taken over or compensated for by smaller herbivores. These effects of large herbivores on ecosystems are further discussed below.

Humans

The loss of large herbivores has direct effects on humans, especially for food security in developing regions. It is estimated that 1 billion people rely on wild meat for subsistence (15). Under a business-as-usual scenario, food security will continue to falter given that wild meat in African forests is expected to decline by more than 80% during the next 50 years (78). Moreover, charismatic large herbivores are important flagship fauna (Fig. 6) that draw many tourists to protected areas, especially when they are sympatric with large carnivores (79). Although the consistency of ecotourism can be interrupted by unpredictable events such as disease epidemics and civil unrest, a decline of large flagship species translates directly into reduced tourism (animal watching, photo and hunting safaris) and thereby a decline in trade balances and employment, particularly in rural parts of the developing world where most megaherbivores persist and poverty is common.

Future Directions

Saving the remaining threatened large herbivores will require concerted action. The world’s wealthier populations will need to provide the resources essential for ensuring the preservation of our global natural heritage of large herbivores. A sense of justice and development is essential to ensure that local populations can benefit fairly from large herbivore protection and thereby have a vested interest in it. The presence of a diversity of large charismatic species can yield financial benefits that flow to local communities (80). For example, with the African photo safari industry, the prospect of simply observing large carnivores, elephants, or rhinoceros can drive tourism revenue. The ultimate forces behind declining large mammal populations are a rising human population and increasing per capita resource consumption (Fig. 7). As is the case for the conservation of most taxa, programs that help to lower human birth rates in rapidly growing regions such as those that enhance educational and development opportunities, particularly for young women, are a high priority. However, the reality is that strategies for conserving herbivores in the context of high human population densities are likely to be increasingly important. Increasing levels of human carnivory are at the crux of the problem. Lowering human consumption of domestic ruminants could help conserve herbivore populations by reducing demand for rangeland forage, water, and feed crops. Reducing consumption of wild herbivores can also be effective, and enforced wildlife management such as via wildlife ranching has proven to be very successful at maintaining sustainably high harvests of wild meat while providing subsistence food resources to local people. The implementation of wildlife management strategies such as male-only harvests, age-specific harvests, and quotas has the potential to improve both conservation and food security if improved governance can allow for implementation of these strategies. In the near future, urgent action is needed to prevent the extinction of species with extremely low populations, especially those with limited captive populations (for example, Bactrian camel, rhinos, and suids). Decisive steps will be required to address key threats facing threatened large herbivores including, among others, the following.

Final thoughts

The wave of species extinctions that obliterated 80% of the Pleistocene megaherbivores (≥1000 kg) on planet Earth appears to be continuing today in Africa and Southeast Asia. The very recent extinctions of Africa’s western black rhinoceros and Vietnam’s Javan rhinoceros are sober reminders of this long-term trend (1, 90). Then as now, the Pleistocene extinctions were triggered in part by human hunters (2, 91). Solving the current poaching crisis, a sinister development of organized crime, will help but will likely be insufficient to stem, much less reverse, impending declines and future extinctions among the few remaining megafauna. Megafauna remain beset by long-standing and generally escalating threats due to land-use change and ongoing parochial poaching by locals. The situation for the 66 species of large herbivores having body masses of 100 to 1000 kg is not as dire as for those ≥1000 kg, but still ominous because 55% of these herbivores are currently threatened (fig. S3). Within this body mass range, hominid, tapirid, suid, and equid species are the most highly threatened families (Fig. 2). Some species may be slipping away even before they are discovered and described by science. Recently, two rare large herbivores were discovered: a fifth species of tapir, the kabomani tapir (Tapirus kabomani), in the Amazon (92) and a bovid, the saola (Pseudoryx nghetinhensis), in Southeast Asia (93). To jump-start protection for the saola, conservationists recently removed 27,000 snares from the forests of Vietnam and Laos (94).

The problem of large herbivore declines may not be solved by the current Convention on Biological Diversity target of protecting 17% of terrestrial land by 2020 (95). Given the substantial area requirements of large herbivores, 17% of land in isolated fragments is unlikely to provide sufficient protection to slow or reverse declines, particularly given that inadequate policing/funding can effectively reduce the size of protected areas (96). This is further exacerbated by the global tendency for protected areas to be in low-quality habitats (35), effectively reducing the densities, and hence numbers, that can be conserved in these areas (36).

The range contractions (fig. S6) and population declines of large herbivore species have ecological and evolutionary implications. Range contractions inevitably result from the loss of local populations, many of which are genetically distinct, thus representing a major and underappreciated pulse of biological extinction (97). Even if they survive in protected areas, many of these largest species might already be below the minimum numbers to be effective in generating ecological cascades (Fig. 5) or allowing evolutionary processes such as speciation (98). Furthermore, 11 of the 44 threatened species are on the Evolutionarily Distinct and Globally Endangered (EDGE) list due to their unique characteristics while being on the verge of extinction. These are the mountain, Asian, and Baird’s tapirs (Tapirus spp.), black, Javan, and Sumatran rhinoceros, Bactrian camel, Asian elephant (E. maximus), pigmy hippopotamus (Choeropsis liberiensis), African wild ass (Equus africanus), and western gorilla (99). Thousands of years ago, equids were among the most abundant large grazing animals of the grasslands and steppes of Africa, Asia, and the Americas, whereas today, after many of their populations have been decimated, five of the remaining seven species are threatened and at risk of extinction (1). These are the African wild ass, Asiatic wild ass (Equus hemionus), Przewalski’s horse, Grevy’s zebra (Equus grevyi), and mountain zebra (E. zebra).

Growing human populations, unsustainable hunting, high densities of livestock, and habitat loss have devastating consequences for large, long-lived, slow-breeding, and, therefore, vulnerable herbivore species, their ecosystems, and the services they provide. Large herbivores, and their associated ecological functions and services, have already largely been lost from much of the developed world. The scale and rate of large herbivore decline suggest that without radical intervention, large herbivores (and many smaller ones) will continue to disappear from numerous regions with enormous ecological, social, and economic costs. We have progressed well beyond the empty forest to early views of the “empty landscape” in desert, grassland, savanna, and forest ecosystems across much of planet Earth. Now is the time to act boldly, because without radical changes in these trends, the extinctions that eliminated most of the world’s largest herbivores 10,000 to 50,000 years ago will only have been postponed for these last few remaining giants.