Global decline of apex scavengers threatens human health

Significance

Each year, zoonotic diseases kill millions of people, with pathogens in carrion (dead animal matter) contributing to this crisis. Scavenging animals mitigate this disease risk by consuming carrion. However, our analysis of 1,376 vertebrate scavenger species reveals that more than a third of them are threatened or declining in abundance. Due to human activities, apex (large or specialized) scavengers are particularly struggling, while mesoscavengers (small or opportunistic) are thriving. Even with increasing mesoscavengers, the loss of apex scavengers leads to more uneaten carrion, potentially proliferating zoonotic pathogen loads. The growing number of mesoscavengers, particularly those carrying diseases such as rabies, may further threaten human health. Therefore, addressing the threats to apex scavengers is critical to improving global health.

Abstract

Vertebrate scavengers play a critical role in ecosystem functioning worldwide. Through the cascading effects of their ecological role, scavengers can also alleviate the burden of zoonotic diseases on people. This importance to human health fuels a growing need to understand how vertebrate scavengers and their ecosystem services are faring globally in the Anthropocene. We reviewed the conservation status of 1,376 vertebrate scavenging species and examined the implications for human health. We uncovered that 36% of these species are threatened or decreasing in population abundance and that apex (large-bodied or obligate) scavengers are disproportionately imperiled. In contrast, mesoscavengers (small-bodied or facultative) are thriving from anthropogenic food subsidies and ecological release. We posit that this global shift in scavenger community structure increases carrion persistence enabling zoonotic pathogens to propagate. Our analysis also indicates that the release of mesoscavengers is associated with reservoir host proliferation, potentially further exacerbating human disease burdens. Urgently tackling the key threats to scavengers—intensive livestock production, land use change, wildlife trade, and the interactions among them—is critical to securing the long-term public health benefits of the world’s diverse scavenger communities.

Zoonotic diseases impose crippling burdens on human health, with 56 zoonoses annually contributing to 2.5 billion morbidities and 2.7 million deaths (1). Spillovers of zoonoses from animal hosts into human populations are mediated by contact between people and wildlife. Of particular concern are zoonotic pathogens in carrion, which serves as a resource-rich breeding ground for pathogens (2). These pathogens can then infect people, through close contact, dissemination by vectors, or contamination of food, soil, and water (3–6). Engineered solutions such as intensive carcass removal, incineration, and burial can reduce the health risks posed by carrion (5). However, such interventions are expensive and labor-intensive, particularly for low-income regions where communicable disease burdens are greatest (7). However, the natural world offers its own solution to managing carcass waste: scavenging species that consume carrion, thereby potentially limiting the proliferation of pathogens. In the Anthropocene, some scavengers coexist and thrive alongside people, while human activities also imperil the survival of other scavenging species (2). To test these seemingly contrasting patterns among scavengers and their consequences for humans, we review a) the global diversity and distribution of wild vertebrate scavengers, b) their ecosystem services, c) their conservation status, d) the determinants of their conservation status, and e) the consequences for public health.

Scavengers Are Diverse and Ubiquitous

Vertebrate scavengers are phylogenetically, geographically, and functionally diverse. All vertebrate predators likely scavenge to varying extents. Even some herbivores, such as American bison (Bison bison), elk (Cervus canadensis), and Mediterranean parrotfish (Sparisoma cretense), consume carrion (5, 8, 9). Scavenging is emerging as a more prevalent and consequential behavior across species than previously believed (though aberrant scavenging by herbivores may not necessarily affect ecosystem functioning). In consideration of the ubiquity of scavenging and our focus on the effects of scavenging on human health, our review therefore focuses on 1,376 wild vertebrate species that: a) have been reliably recorded to consume carrion, b) may have some impact on human health through scavenging, and c) are included in the International Union for Conservation of Nature (IUCN) Red List (10). Data sources are listed in the SI Appendix. Over 200 taxonomic families are represented in our compiled scavenger list, though 52% of species belong to just 5% of families (ordered by family with most to least scavenging species): Soricidae (shrews), Accipitridae (raptors), Cricetidae (cricetid rodents), Corvidae (corvids), Laridae (gulls), Canidae (canids), Sciuridae (squirrels), Didelphidae (opossums), Mustelidae (mustelids), and Myxinidae (hagfish). In contrast to the ten families dominating this list, 100 families are only represented by a single species. For example, hammer-headed bats (Hypsignathus monstrosus), observed to feed on discarded poultry carcasses (11), were the only Old World fruit bat species included. Finally, while our list of scavengers seeks to capture well-observed scavenging species that are most likely to affect human health, we recognize that the spectacular diversity of scavengers may extend well beyond the species discussed here.

Scavenging species are not only phylogenetically diverse but also ubiquitous globally (Fig. 1). Freshwater and terrestrial scavenger richness is highest in Asia, Africa, and North America, while marine scavenger richness is highest in the North Atlantic, Indian, and North Pacific Oceans. According to the IUCN’s habitats classification scheme, tropical forests, shrublands, and agricultural lands host the greatest richness of freshwater and terrestrial scavengers. Similarly, the neritic, intertidal, and epipelagic zones host the greatest richness of marine scavengers. Despite the considerable global richness of scavengers in tropical forests, observed scavenger richness does not conform to the traditional latitudinal diversity gradient (Fig. 1) (12). Several factors, beyond sampling biases, may contribute to the relatively lower scavenger richness observed at local scales in tropical forests. First, vertebrate scavengers primarily use olfactory and visual cues to detect carrion, and densely forested landscapes may conceal carrion from visual detection (13, 14). Second, invertebrates decompose carrion at faster rates at higher temperatures, potentially subjecting vertebrate scavengers to further competition in the tropics (15, 16). Additionally, the higher pathogen diversity in the tropics may expose vertebrate scavengers to greater disease risk, thereby discouraging carrion consumption (17, 18).

Fig. 1.

Vertebrate scavengers are geographically and phylogenetically diverse. Colors on the map indicate species richness. Icons of species provide examples of scavenging vertebrate species. The ranges of these 1,363 scavenging species were sourced from five datasets (10, 19–22).

Given this phylogenetic and geographic diversity, vertebrate scavengers are also expected to exhibit remarkable variation in their adaptations to carrion consumption. Obligate scavengers exclusively use carrion as a food source and have consequently evolved specific behaviors, morphologies, and physiologies for this demanding foraging strategy (5). These adaptations include large body sizes to endure significant periods of carrion scarcity, soaring flight to minimize energetic costs of searching for carrion, and enhanced immune systems capable of responding to pathogens and toxins in carrion. As such, only some vulture species are considered true obligate scavengers, given that carrion constitutes 100% of their diets (23). Using this classification, obligate scavengers comprise 1% of all scavengers listed here. A further 50% of species are considered facultative scavengers, though the biomass of carrion in their diet considerably varies (23). The dependence on carrion for the remaining 49% of scavenging species is undescribed, though the majority are likely facultative scavengers, except for 20 hagfish species. Deep-sea hagfish can quickly detect carrion from even dilute chemical cues and can endure starvation for at least nine months by lowering their metabolic rates (24). This functional diversity highlights the adaptations that scavengers have evolved to exploit carrion across environments.

Scavengers Provide Sanitation and Disease Control Benefits

Vertebrate scavengers provide several benefits to humanity (Fig. 2). First, scavengers consuming carrion are recognized as natural waste managers. Scavenging efficiency among vertebrates is surprisingly high, with 75% of all available carcasses partly or fully consumed by scavengers across the Americas and Europe (25). In low-income countries, waste management systems exhaust a fifth of municipal budgets, while collecting less than 40% of all waste (26). In these high-cost-low-benefit contexts, scavengers stand out by removing impressive volumes of waste. For example, spotted hyenas (Crocuta crocuta) annually consumed 200 tons of livestock carcass waste in Mekelle, Ethiopia (27), where poor waste management is considered the most severe public service issue (28). Even in urban areas of high-income countries, scavengers remove 63 to 72% of all carcass biomass (29). Furthermore, in agricultural settings, waste production is almost fivefold that in urban areas (26), and yet, even here, scavengers have met this demand for waste removal. In Spain, vultures have historically removed dead livestock and annually saved farmers up to USD 67 million in costs incurred by collecting and transporting of carcasses to processing plants (30). At the continental level, these benefits are immensely large: Turkey vultures (Cathartes aura) across the Americas annually remove 1.5 million tons of waste, saving almost USD 1 billion in removal costs (31). By removing organic waste, vertebrate scavengers sanitize environments and partially address a growing global waste management crisis. Due to poor waste disposal facilities, at least three billion people continue to dump organic waste openly (32). Therefore, significant progress is still required to meet the United Nations’ 2030 Sustainable Development Goal 6 target of providing adequate and equitable waste management systems to all. Through the consumption of carrion, vertebrate scavengers contribute to this target, particularly in settings with limited infrastructure to collect, transport, and process waste.

Fig. 2.

Scavengers provide benefits to humanity globally. Color of circles represents different benefits. Size of circles represents the spatial scale of benefit quantification. All valuations of services are annualized and rounded. All economic valuations are converted to USD using exchange rates from each respective article’s time of submission and adjusted for inflation through August 2023. Please refer to the cited articles for precise valuations including uncertainty values (4, 27, 31, 33–44).

A downstream benefit of carrion removal by scavengers is disease control. Carrion provides a conducive environment for pathogens to proliferate (2). These pathogens then infect people through close contact, contamination of food and water, and vector transmission (3–6). By consuming carrion quickly and completely, vertebrate scavengers repress the environmental source, and consequently, the spread of infectious diseases. For example, scavenging by periurban spotted hyenas in Mekelle, Ethiopia, annually prevents five anthrax and bovine tuberculosis spillover events from close contacts between infected carcasses and people (27). This mitigation of close contacts between pathogen sources and people is particularly important for the 15 to 20 million people worldwide who earn a living by salvaging recyclable and valuable items from dump sites and landfills (45). Working in these conditions often exposes people to potentially infected animal carcasses and imposes substantial health burdens (46).

Scavengers also reduce contamination of water by carrion. Carcasses discarded in water bodies deplete dissolved oxygen levels and increase fecal coliforms (47). Following a country-wide collapse of vulture populations in India, dissolved oxygen in water dropped up to 12% while fecal coliforms doubled (33). In Australian wetlands, turtle consumption of carrion is associated with quicker recovery of dissolved oxygen in water to baseline levels (34). This evidence underscores the role of scavengers in controlling pathogenic contamination in water.

Experimental evidence also indicates that scavengers control vector-borne diseases. In Sabah, Malaysia, vertebrate scavengers limited carrion persistence, which consequently decreased Salmonella spp. and Shiga toxin-producing Escherichia coli abundance on flies collected above the carcasses (4). Carrion consumption, which reduces carcass size, also likely reduces the abundance of flies around carcasses (48). These decreases in both bacterial loads on vectors and abundances of vectors are associated with fewer people presenting diarrheal diseases (49, 50). Given these disease-control benefits, vertebrate scavengers contribute to the 2030 Sustainable Development Goal 3 target of ending communicable disease epidemics. Importantly, in the context of environmental justice, these disease control services are particularly valuable in low-income countries where communicable diseases account for 36% of all deaths, compared to the 5% of all deaths in high-income countries (7).

Beyond human health, scavengers also benefit livestock health and production. In Mekelle, spotted hyena scavenging annually prevented 140 anthrax and bovine tuberculosis transmission events from infected carcasses to livestock (27). In Wyoming, USA, canid and eagle scavenging of elk (Cervus canadensis) fetuses, a source of brucellosis, halved the proportion of elk interacting with these fetuses (35). This potential reduction in brucellosis spread within the elk reservoir may limit spillover to livestock. Scavenging also likely reduces direct livestock interaction with elk fetuses. These improvements to livestock health have downstream benefits for human health, further highlighting the mechanisms by which scavengers can protect human well-being (51). Overall, given their global distribution, scavengers likely deliver these economic and health benefits to many of the world’s 200 to 500 million pastoralists (52).

Scavengers also provide other services to humanity, including greenhouse gas emission reductions. Globally, 22 vulture species prevent carrion from naturally decomposing and producing 11 million metric tons of carbon dioxide equivalent annually (36). Furthermore, while we largely focus on their sanitation and disease control benefits here, vertebrate scavengers also support wildlife-based tourism industries, contribute to cultural identities, and enrich spiritual connections with nature (53).

Apex Scavengers Are Declining, While Mesoscavengers Are Thriving

Analysis of the conservation status of scavengers reveals that certain species are critically declining, while others are thriving in the Anthropocene. The IUCN deems 18% (17 to 23%; these bounds capture uncertainty from species considered Data Deficient) of scavenging species as threatened (listed as Vulnerable, Endangered, or Critically Endangered). This figure is consistent with the 18% of all vertebrate species considered as threatened (Fig. 3A) (10). More concerningly, 42% (30 to 59%) of scavenging species are experiencing declines in population size, while only 12% are experiencing increases (Fig. 3B). Large marine scavengers, such as requiem (family Carcharhinidae) and sleeper sharks (family Somniosidae), are among the worst affected, with the 98% loss of the global oceanic whitetip shark (Carcharhinus longimanus) population as a paradigm of this decline (54). Similarly, nine scavenging albatrosses, petrels, and shearwaters are considered threatened, suggesting that declining marine scavengers are not limited to below the ocean’s surface. The threat of extirpations and extinctions is also pronounced in other bird species, such as New World vultures, raptors (order Accipitriformes), and storks. Among mammals, those at most risk tend to be large species, such as bears, felids, hyenas, and pigs; however, some smaller mammals such as cricetids, marsupial carnivores, and shrews are also facing a similar risk. While declines in these avian and mammalian scavengers have been previously documented, reptilian scavengers have largely been overlooked (55, 56). Over 60% of scavenging iguanids, pond turtles, and tortoises evaluated here are identified as threatened by the IUCN, and these taxa therefore join large marine scavengers as the most severely declining taxa.

Fig. 3.

Some scavengers are critically declining, while others are thriving. (A) Distributions of IUCN Red List categories for all five major groups of vertebrates, and (B) population trends for scavengers in each vertebrate taxon. (C) Mean Red List category and population trend of scavengers in each taxonomic family. Using the latest IUCN assessments available, each species was assigned numeric values to represent their Red List category (from Critically Endangered = 1 to Least Concern = 5) and population trend (from decreasing = 1 to increasing = 3). Points have been jittered to avoid overplotting. Size of point indicates the relative number of scavenging species in each family (ranging from 1 to 127 species). Furthermore, green points indicate the top 10% of families experiencing improvement in Red List category over time (using previously published IUCN assessments, where available), while red points indicate the top 10% of families experiencing declines in Red List category over time.

In contrast to these significant declines, some scavengers are thriving in the Anthropocene. For example, 94% of scavenging corvids, falcons, gulls, herons, tits, and woodpeckers are nonthreatened, as well as all scavenging alligators, colubrids, and skinks. Among the 16 scavenging amphibians assessed here, only the Red Hills Salamander (Phaeognathus hubrichti) is classified as threatened. Fish succeeding in the Anthropocene include wrasses, righteye flounders, and short-nosed chimeras, while successful scavenging mammalian taxa include canids, murids, opossums, raccoons, and squirrels. Importantly, these patterns of declining and thriving families may not necessarily apply to all species within the aforementioned families. For example, among canids, large species such as African wild dogs (Lycaon pictus), dholes (Cuon alpinus), Ethiopian wolves (Canis simensis), and red wolves (Canis rufus) do not enjoy the same nonthreatened status as many of their smaller relatives. Equally, while many pigs are on the decline, wild boar (Sus scrofa) and bushpigs (Potamochoerus larvatus) are thriving.

Although both declining and thriving taxa are considerably diverse, two patterns differentiate the losers from the winners of the Anthropocene (Fig. 3C). First, threatened scavengers are larger in body mass than nonthreatened scavengers (Fig. 4A). This phenomenon is consistent with size-differential defaunation, which is observed among vertebrates broadly and is particularly pronounced among predators (57). In such cases, the decline of apex predators often facilitates the rise of mesopredators (58). Second, obligate scavengers, who specialize in carrion consumption, are disproportionately more threatened than facultative scavengers (Fig. 4B). Obligate scavengers are also disproportionately more threatened than scavengers with unknown scavenging dependence, most of which are likely facultative scavengers (Fig. 4B). This trend reflects a more widespread pattern observed across numerous ecological contexts: the turnover of specialist species in favor of generalists (59, 60).

Fig. 4.

Apex (large and obligate) scavengers are more threatened. (A) Body mass distributions, calculated by density estimation, of threatened and nonthreatened scavengers indicate size-differential defaunation. Median mass of species is indicated for all three conservation status categories. * indicates Holm–Bonferroni corrected P < 0.001 in two-sample Kolmogorov–Smirnov tests (P value approximated due to presence of ties). (B) Red List category proportions of obligate and facultative scavengers indicate loss of specialists. * indicates Holm–Bonferroni corrected P < 0.001 in Fisher’s exact tests, where P values are simulated by 1,000,000 Monte Carlo simulations.

Both large and obligate scavengers are functionally dominant, and we generally refer to these as apex scavengers here (61). These species consume more carrion per capita than smaller, less efficient scavengers, known as mesoscavengers. Importantly, these functional dominance relationships are context-dependent, since a mesoscavenger species in one area could be an apex scavenger in another. However, for simplicity and due to the global scope of this study, we follow the simplified aforementioned definitions of apex scavengers and mesoscavengers. Therefore, our analysis reveals that the Anthropocene is witnessing a global turnover of apex scavengers in favor of mesoscavengers. These changes to scavenger communities mirror those experienced by biodiversity more broadly (57, 61).

Humans Are Driving Changes to Scavenger Communities

The losers and winners of scavenger communities in the Anthropocene are largely determined by their capacity to adapt to humans. Declining scavengers confront multiple, often synergistic, threats from human activities, making adaptation a formidable challenge. While the sheer geographic and phylogenetic diversity of scavenging species results in a broad spectrum of threats, IUCN assessments reveal that almost 50% of scavenging species are significantly impacted by just three human activities: wildlife trade, land use change, and intensive livestock production (10). Below, we outline how these activities also disproportionately affect apex scavengers, thereby contributing to the global shift toward mesoscavengers.

Wildlife trade and overexploitation are particularly concerning, with hunting activity affecting 25% of scavenging species and causing more severe declines than most other threats. Apex scavengers in particular are exposed to heightened risk, as hunters preferentially target large animals for consumption and trade (62). Incidental killings are equally concerning for these large and obligate scavengers. For example, in Africa’s Kavango-Zambezi Transfrontier Conservation Area, wire snares, which typically target mammalian herbivores for bushmeat, have killed 5% of lion (Panthera leo) populations and up to 13% of spotted hyena populations (63). The hunting of prey species also has consequential effects on scavengers: The extinction of Australian and North American vultures is partly attributed to the hunting-induced megafaunal collapse (64–66). These threats of targeted and incidental killings by humans also pervade marine habitats (Fig. 5A). Here, marine apex scavengers, such as sharks, continue to face increasing extinction risk due to fishing pressure (67).

Fig. 5.

Scavengers in human-dominated landscapes are thriving, while scavengers in natural habitats face a multitude of threats. (A) Nonmetric multidimensional scaling (NMDS) of marine (in blue) and nonmarine habitats (in green) based on the threats that their scavengers confront, using Bray–Curtis dissimilarity (stress = 0.047). (B) NMDS of freshwater (in blue) and terrestrial habitats (in green) based on the threats that their scavengers confront, using Bray–Curtis dissimilarity (stress = 0.074). This NMDS excludes marine habitats and habitats with fewer than 40 scavenging species (caves, introduced vegetation, other, and unknown habitats) from the analysis. In (A and B), arrows indicate gradient of impact of threats. Therefore, habitat points close to arrow tips (representing threats) indicate that scavengers in those habitats are strongly affected by those threats. Only key threats to scavengers in marine habitats are labeled in (A), as these habitats are excluded in the analysis in (B). Threats in bold indicate threats associated with the three key human activities affecting scavengers (intensive livestock production, land use change, and wildlife trade). Both (A and B) exclude gathering plants and geological events as threats from the analyses, as fewer than 40 scavenging species are facing these threats. (C) Mean Red List category and population trend of scavengers in each habitat. Using the latest IUCN assessments available, each species was assigned numeric values to represent their Red List category (from Critically Endangered = 1 to Least Concern = 5) and population trend (from decreasing = 1 to increasing = 3). Red and black points on the enlarged plot indicate human-dominated and natural habitats, respectively. The size of point indicates relative number of scavenging species in each habitat. Habitat importance was calculated as the percentage of species that require the given habitat within their life cycle (e.g., for breeding or food) (10).

Land use change is also a daunting threat to scavengers. Land use change is expected to increase particularly in East Africa, eastern United States, and southeastern Europe over the next 50 y (68); these regions also host high scavenging species richness (Fig. 1). Natural habitats closely associated with land use change include boreal and tropical forests, savannas, and tropical grasslands (Fig. 5B); these habitats collectively host almost 60% of scavenging species, and the IUCN regard these habitats as important for the survival of over a third of these species. Moreover, land use change affects scavengers of all sizes: Apex scavengers, such as large canids and felids, have lost up to 98% of their historic ranges, while IUCN assessments suggest that many small, understudied scavengers, such as cricetids and shrews, are also vulnerable to such changes (10, 56). However, habitat fragmentation driven by land use change disproportionately affects large species requiring expansive contiguous areas (69). Additionally, land use change can increase access to wildlife for hunters, a synergy of threats that consequently leads to size-differential effects on biodiversity loss (70, 71).

Livestock production can also motivate the persecution of scavengers, especially when facultative scavengers depredate on livestock (72). Obligate scavengers can also inadvertently become victims caught in crossfires, as poisoned carcasses targeting mammalian predators have contributed to 62 to 95% declines in vulture populations across Africa (73). Similarly, Gyps vulture populations in India have dropped by more than 95% due to poisoning from diclofenac residue, a toxic veterinary drug found in livestock carcasses (73). These observed vulture declines can occur even if less than 1% of livestock carcasses were contaminated with diclofenac (74).

While these activities are disproportionately harming apex scavengers, mesoscavengers are profiting from the reduction in competition over carrion. Referred to as the “mesoscavenger release hypothesis,” this turnover of species has received empirical support globally (61, 75). For example, in Tasmania, Australia, the severe disease-induced population declines in Tasmanian devils (Sarcophilus harrisii), an apex scavenger, are associated with the doubling of forest raven (Corvus tasmanicus) numbers (76). In Spain, vulture absence is associated with a threefold increase in red fox (Vulpes vulpes) density (77). Along with reduced competition over carrion, the loss of large facultative scavengers has released mesoscavengers from top–down control. Across several US national parks, coyotes (Canis latrans) have thrived under low wolf (Canis lupus) presence (58, 78–80). Even across oceans in Australia, New Zealand, North America, and South Africa, the overfishing of large sharks has allowed smaller scavengers, such as dogfishes, to thrive (81). Thus, the human-driven declines of apex scavengers are generally benefitting mesoscavengers globally.

Reduced competition over carrion and limited top–down effects from the loss of apex scavengers are not the only mechanisms driving the success of mesoscavengers. Perhaps most importantly, thriving scavengers appear to tolerate, and even capitalize on, human presence. Humans discard considerable quantities of meat-based food, which then become available for consumption by vertebrate scavengers (82). These food subsidies are annually estimated as nine million tons of fishery discards (83) and 72 million tons of discarded livestock meat (84, 85). Significantly smaller quantities of hunting remains are also made available by wildlife hunters (75). Collectively, these anthropogenic food subsidies are nonnegligible for terrestrial scavengers: Comparatively, wild terrestrial mammal biomass is estimated at 22 million tons, and only a fraction of this biomass will be made available as carrion annually (82, 86). Although some apex scavengers may also benefit from anthropogenic food, mesoscavengers appear to be particularly adept at exploiting these subsidies (87). For example, small- and medium-sized canids, such as coyotes, golden jackals (Canis aureus), and red foxes, have experienced notable population booms with increasing availability of anthropogenic food subsidies (88–90). Among gull species, anthropogenic food subsidies are associated with better body conditions, larger clutch sizes, larger egg sizes, higher fledging survival, greater hatchling success, and population growths (91–93). Notably, corvids and gulls, along with some other facultative avian scavengers, are thriving not only relative to obligate avian scavengers but also relative to avian nonscavengers (55). This underscores the extent to which these birds have adapted to the challenges and opportunities of the Anthropocene.

However, the greatest beneficiaries of food subsidies are likely rodents, particularly murids. Due to anthropogenic food subsidies, murids, such as black (Rattus rattus) and Norway (Rattus norvegicus) rats, have higher growth rates in urban areas than those in rural areas (94–96). This anthropogenic food can even buffer rats against environmental fluctuations, allowing them to sustain high growth rates even in low primary productivity years (97). Examples such as these indicate that scavengers that are adapted to human presence and can exploit anthropogenic food subsidies are largely found in, or even preferentially choose to inhabit, human-dominated habitats. Furthermore, when scavenging species are grouped by their habitats, scavengers in human-dominated habitats are less threatened and increasing in population, relative to scavengers in natural habitats (Fig. 5C) (98). This finding further substantiates the claim that the losers and winners of the Anthropocene are largely driven by their ability to tolerate people: Scavengers in decline, such as apex scavengers, are threatened by human activities, while thriving scavengers, typically mesoscavengers, benefit from competition and top–down release, while also profiting from anthropogenic food subsidies.

Decline of Apex Scavengers Imperils Benefits

The sanitation and disease control services provided by scavengers are now in jeopardy due to the replacement of apex scavengers with mesoscavengers in the Anthropocene (Fig. 6). At face value, we initially expected growing mesoscavenger populations to compensate for loss in ecosystem functioning from apex scavenger decline. However, the available empirical evidence indicates otherwise. For example, carcass decomposition by mammalian scavengers was almost threefold slower in the absence of vultures in Kenya (99). Similarly, full consumption of carcasses by coyotes, wild boars, and Virginia opossums (Didelphis virginiana) plunged by 90% in the absence of vultures in South Carolina, USA (100). Declines in Australian apex scavengers, such as Tasmanian devils and yellow-spotted monitors (Varanus panoptes), have similarly increased carrion persistence, despite increases in mesoscavengers (76, 101, 102). Overall, while some mesoscavengers deliver sizeable carrion removal services (41), they often cannot functionally replace apex scavengers.

Fig. 6.

Decline of apex scavengers increases risk of disease spillover. Intensive livestock production, land use change, wildlife trade, and their synergies directly exacerbate zoonotic spillover by increasing human–wildlife contact (103, 104). As highlighted in yellow, these three human activities are also driving global shifts in scavenger communities. The decline of apex scavengers is both reducing carrion removal and releasing mesoscavengers associated with disease, ultimately exacerbating disease burdens in humans (33).

Although mesoscavengers compete with apex scavengers for carrion, they also benefit by using apex scavengers to find and access carrion. In Poland, canid and corvid mesoscavengers could only feed on European bison (Bison bonasus) carcasses after wolves had pierced open the carcass skin. Even after the initial perforation, wolf scavenging progressively increased access to other parts of the carcasses, such that mesoscavenger feeding activity was higher after wolf feeding bouts (105). Vultures are known to provide similar carcass dismemberment benefits to mesoscavengers, and several scavenger species also capitalize on the vulture’s adaptations to detect carrion quickly (106). In Kenya, black-backed jackals (Canis mesomelas) found carrion twice as quickly when following vultures (107). Given this facilitation of mesoscavengers by apex scavengers, more carrion will likely persist, and for longer, in the absence of apex scavengers (100). Pathogens will likely proliferate, leading to more zoonoses in people (Fig. 6). The most notable example of scavenger declines driving public health crises comes from India: In districts with high habitat suitability for vultures, all-cause human death rates jumped by 4.7% following the collapse of vulture populations (33). Loss of species diversity generally leads to poorer ecosystem functioning (108, 109), and the same appears to be true for vertebrate scavengers and their services. Corroboration of this relationship clearly warrants further experimental work.

Beyond the potential diminished sanitation and disease control services, the rise of mesoscavengers may also threaten human health by an even more insidious mechanism. Some of the Anthropocene’s thriving mesoscavengers are notorious disease reservoir hosts, capable of transmitting zoonotic diseases unrelated to carrion (Fig. 6). During the 1990s vulture collapse in India, free-ranging dogs (Canis familiaris) were released from competition over carrion and proliferated by 4 to 7 million. The cascading impacts on human health were seismic: From 1992 to 2006, 39 million additional dog bites and 48,000 additional rabies-associated deaths were estimated. The annual economic burden of these additional bites and deaths exceeded USD 2.7 billion (42). This replacement of vultures by dogs is not unique to South Asia. In Addis Ababa, Ethiopia, dog detections more than doubled following a 73% decline in Gyps vultures (110). In Zimbabwe, dogs increasingly replaced vultures as the dominant scavengers as human activity intensified across a spatial gradient (111). The global collapse of apex scavengers and increases in anthropogenic food subsidies may have profited many of the 750 million free-ranging dogs worldwide (112, 113). Due to their role in echinococcosis, leishmaniasis, and rabies transmission, free-ranging dogs may consequently be imposing increasingly large burdens on human health and economy (114, 115).

The replacement of apex scavengers with dogs is increasingly gaining recognition, and analogous changes favoring other disease-associated mesoscavengers also appear to be occurring. Globally, murids, such as house mice (Mus musculus) and rats (Rattus spp.), are thriving, with potential repercussions for the spread of zoonotic diseases (116). For example, leptospirosis outbreaks have increased over the last 50 y, now globally affecting over a million people annually (117). Its disease burden is particularly pronounced in the Caribbean, East Africa, Oceania, and Southeast Asia. Here, farming, forestry, and hunting activities attract people closer to food, soil, and water contaminated with Leptospira bacteria from rodent urine (118). On islands, murids dominate scavenger communities and are likely important disease reservoirs. Because islands typically lack diverse terrestrial mammalian communities, these rodents can proliferate by exploiting unoccupied niches and exacerbate disease burdens (119). For example, murids in New Zealand may contribute to the unusually high incidence of cryptosporidiosis, a diarrheal disease, by contaminating food and water with Cryptosporidium parasites found in their excrement (120, 121). Rodents also host ectoparasitic arthropods, thereby amplifying the diseases carried by these vectors. In the western United States, thriving western gray squirrel (Sciurus griseus) populations coexisting with people are the primary reservoir hosts of Lyme disease (122). This may indicate that these squirrels, among others (123), are a potentially overlooked, yet important, source of Lyme disease. Beyond rodents, wild boars are important sources of zoonotic infections for consumers of wild boar meat. In Europe, hepatitis E infections are common among wild boars, and consumption of wild boar meat in Japan has caused hepatitis E-related deaths (124). Similarly, brucellosis is known to spread among wild boars and spill over to hunters in Europe and North America.

Finally, the potential effects on humanity from the loss of aquatic apex scavengers requires further investigation. Carrion persistence in freshwater ecosystems increases nutrient concentrations and causes cyanobacterial blooms (34). Toxins from these blooms may poison people and impose economic losses through fishery and tourism closures (125). Additionally, in marine ecosystems, carrion can create hypoxic environments. This risk is currently limited by the abundance of oceanic vertebrate scavengers who quickly consume much of the available carrion (126). However, with marine apex scavengers rapidly declining, increasing bacterial decomposition and invertebrate scavenging of carrion may locally deoxygenate waters, with conceivable cascading effects on ecosystem and human health. Predicted shifts in scavenger communities such as these demand further study, given their potential implications for human health.

Although carrion consumption is typically expected to reduce pathogens, scavengers may also spread zoonotic diseases from carrion. Scavengers can carry pathogens acquired from carrion on their bodies, dispersing these pathogens through their movements. Moreover, certain pathogens ingested with carrion remain infectious even after passing through a scavenger’s digestive system and are subsequently dispersed through feces (127–129). By opening carcasses and releasing infectious materials within carcasses, scavengers may also contribute to localized environmental contamination. However, in the case of apex scavengers, these intuitive expectations are challenged by experimental evidence. For example, anthrax spore density in soils around anthrax-positive carcasses appeared unaffected by vertebrate scavengers (130). Indeed, rapid removal of infected carcasses by apex scavengers may mitigate sporulation. In India, wildlife scientists have linked the collapse of vultures with unusual surges of anthrax-related deaths in humans (131). In contrast, facultative scavengers are associated with anthrax spread (132). The role of scavengers in disease transmission certainly warrants further study, though the growing body of research currently supports two postulations. First, the species identity and natural history of scavengers largely determine whether their scavenging habits limit or spread pathogens (2, 5). Second, apex scavengers are likely net limiters of zoonotic disease transmission.

Human Health Is Contingent on Tackling Three Key Human Activities

The decline of apex scavengers is an increasing threat to human health. Increased carrion persistence may foster more pathogens, while the rise of mesoscavengers may exacerbate disease burdens from noncarrion sources. These repercussions for public health ultimately stem from three human activities: intensive livestock production, land use change, wildlife trade—and the interactions among them. Beyond threatening scavengers and their disease control services, these three human activities also mediate zoonotic spillover more directly by increasing human–wildlife contact (103, 104). Therefore, addressing these human activities has additive benefits for human health and contributes to enhancing nature’s contributions to people, Target 11 of the Kunming-Montreal Global Biodiversity Network. Encouragingly, interventions to tackle these human activities have yielded promising results for scavenger conservation thus far. For example, in response to vulture population collapses, India has banned the use of the toxic drug, diclofenac, in livestock production. Five years after the ban, the rapid decline of white-rumped vultures (Gyps bengalensis) reversed, with populations now slowly recovering (133). Similarly, many landowners neighboring Kenya’s Maasai Mara National Park have limited land use change on their properties by forming wildlife conservancies. This habitat protection has benefited large scavenging carnivores, with lion densities in some conservancies even exceeding those within the adjoining national park (134, 135). Equally, the ratification of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) in 1975 heralded efforts to regulate rampant wildlife trade. Crocodilian scavengers in particular have spectacularly recovered following the CITES prohibition of commercial trade in wild-sourced skins (136). Replicating conservation successes such as these are imperative to alleviating disease burdens, particularly in drafting policies to mitigate environmental injustices in low-income and rural areas. In the face of escalating global health challenges, protecting apex scavengers is critical to securing a healthier future for all of humanity.

Materials and Methods

To systematically compile a list of scavenging vertebrate species, we used four datasets of species feeding habits (23, 137–139) and observation notes from Herpetological Review. We also conducted a targeted search on Google Scholar using the terms “scaveng*,” “carrion,” “carcass,” and “discard” with taxon names to address gaps for taxa underrepresented in existing datasets due to limited ecological knowledge. Each species in the list was subsequently searched on Google with the terms “scavenge” or “carrion” to exclude aberrant scavengers unlikely to impact ecosystem function. Species were retained in the list if at least two sources, including the original, from the first 20 search results confirmed reliable scavenging behavior.

Taxonomic classifications, IUCN Red List categories, population trends, threats, and habitats for each species were obtained from the IUCN Red List of Threatened Species Version 2023-1 (10). Body masses were sourced from AmphiBIO, AVONET, EltonTraits 1.0, Encyclopedia of Life, PanTHERIA, and Slavenko et al. (2016) (23, 138, 140–144). Species ranges were derived from BirdLife International Version 2022-2, Global Assessment of Reptile Distributions 1.7, IUCN Red List, Lumbierres et al. (2022), and Rabosky et al. (2018) (10, 19–22). Further details on the use of these data sources are provided in the SI Appendix.

Supplementary Material

Appendix 01 (PDF)

Data, Materials, and Software Availability

List of scavenging species, and simplifications of IUCN habitats and threats data have been deposited in Figshare are available at ref. 145. Further information on data availability is provided in the SI Appendix.