Carrion ecology in inland aquatic ecosystems: a systematic review.

Carrion ecology, i.e. the decomposition and recycling of dead animals, has traditionally been neglected as a key process in ecosystem functioning. Similarly, despite the large threats that inland aquatic ecosystems (hereafter, aquatic ecosystems) face, the scientific literature is still largely biased towards terrestrial ecosystems. However, there has been an increasing number of studies on carrion ecology in aquatic ecosystems in the last two decades, highlighting their key role in nutrient recirculation and disease control. Thus, a global assessment of the ecological role of scavengers and carrion in aquatic ecosystems is timely. Here, we systematically reviewed scientific articles on carrion ecology in aquatic ecosystems to describe current knowledge, identify research gaps, and promote future studies that will deepen our understanding in this field. We found 206 relevant studies, which were highly biased towards North America, especially in lotic ecosystems, covering short time periods, and overlooking seasonality, a crucial factor in scavenging dynamics. Despite the low number of studies on scavenger assemblages, we recorded 55 orders of invertebrates from 179 families, with Diptera and Coleoptera being the most frequent orders. For vertebrates, we recorded 114 species from 40 families, with birds and mammals being the most common. Our results emphasise the significance of scavengers in stabilising food webs and facilitating nutrient cycling within aquatic ecosystems. Studies were strongly biased towards the assessment of the ecosystem effects of carrion, particularly of salmon carcasses in North America. The second most common research topic was the foraging ecology of vertebrates, which was mostly evaluated through sporadic observations of carrion in the diet. Articles assessing scavenger assemblages were scarce, and only a limited number of these studies evaluated carrion consumption patterns, which serve as a proxy for the role of scavengers in the ecosystem. The ecological functions performed by carrion and scavengers in aquatic ecosystems were diverse. The main ecological functions were carrion as food source and the role of scavengers in nutrient cycling, which appeared in 52.4% (N = 108) and 46.1% (N = 95) of publications, respectively. Ecosystem threats associated with carrion ecology were also identified, the most common being water eutrophication and carrion as source of pathogens (2.4%; N = 5 each). Regarding the effects of carrion on ecosystems, we found studies spanning all ecosystem components (N = 85), from soil or the water column to terrestrial vertebrates, with a particular focus on aquatic invertebrates and fish. Most of these articles found positive effects of carrion on ecosystems (e.g. higher species richness, abundance or fitness; 84.7%; N = 72), while a minority found negative effects, changes in community composition, or even no effects. Enhancing our understanding of scavengers and carrion in aquatic ecosystems is crucial to assessing their current and future roles amidst global change, mainly for water-land nutrient transport, due to changes in the amount and speed of nutrient movement, and for disease control and impact mitigation, due to the predicted increase in occurrence and magnitude of mortality events in aquatic ecosystems.

Vulture culture: dietary specialization of an obligate scavenger.

Individual dietary variation has important ecological and evolutionary consequences. However, it has been overlooked in many taxa that are thought to have homogeneous diets. This is the case of vultures, considered merely as 'carrion eaters'. Given their high degree of sociality, vultures are an excellent model to investigate how inter-individual transmissible behaviours drive individual dietary variation. Here, we combine GPS-tracking and accelerometers with an exhaustive fieldwork campaign to identify the individual diet of 55 griffon vultures (Gyps fulvus) from two Spanish populations that partially overlap in their foraging areas. We found that individuals from the more humanized population consumed more anthropic resources (e.g. stabled livestock or rubbish), resulting in more homogeneous diets. By contrast, individuals from the wilder population consumed more wild ungulates, increasing their dietary variability. Between sexes, we found that males consumed anthropic resources more than females did. Interestingly, in the shared foraging area, vultures retained the dietary preference of their original population, highlighting a strong cultural component. Overall, these results expand the role of cultural traits in shaping key behaviours and call for the need of including cultural traits in Optimal Foraging models, especially in those species that strongly rely on social information while foraging.

Scavenging in the realm of senses: smell and vision drive recruitment at carcasses in Neotropical ecosystems.

Social information, acquired through the observation of other individuals, is especially relevant among species belonging to the same guild. The unpredictable and ephemeral nature of carrion implies that social mechanisms may be selected among scavenger species to facilitate carcass location and consumption. Here, we apply a survival-modelling strategy to data obtained through the placement and monitoring of carcasses in the field to analyse possible information transmission cascades within a Neotropical scavenger community. Our study highlights how the use of different senses (smell and sight) within this guild facilitates carcass location through the transmission of social information between species with different carrion foraging efficiencies. Vultures with a highly developed sense of smell play a key role in this process, as they are the first to arrive at the carcasses and their presence seems to serve as a visual cue for other species to locate the resource. Our study supports the local enhancement hypothesis within scavengers, whereby individuals locate carcasses by following foraging heterospecifics, also suggesting the importance of the sense of smell in the maintenance of the community structure.

Long-term demographic dynamics of a keystone scavenger disrupted by human-induced shifts in food availability.

Scavenging is a key ecological process controlling energy flow in ecosystems and providing valuable ecosystem services worldwide. As long-lived species, the demographic dynamics of vultures can be disrupted by spatiotemporal fluctuations in food availability, with dramatic impacts on their population viability and the ecosystem services provided. In Europe, the outbreak of bovine spongiform encephalopathy (BSE) in 2001 prompted a restrictive sanitary regulation banning the presence of livestock carcasses in the wild on a continental scale. In long-lived vertebrate species, the buffering hypothesis predicts that the demographic traits with the largest contribution to population growth rate should be less temporally variable. The BSE outbreak provides a unique opportunity to test for the impact of demographic buffering in a keystone scavenger suffering abrupt but transient food shortages. We studied the 42-year dynamics (1979-2020) of one of the world's largest breeding colonies of Eurasian griffon vultures (Gyps fulvus). We fitted an inverse Bayesian state-space model with density-dependent demographic rates to the time series of stage-structured abundances to investigate shifts in vital rates and population dynamics before, during, and after the implementation of a restrictive sanitary regulation. Prior to the BSE outbreak the dynamics was mainly driven by adult survival: 83% of temporal variance in abundance was explained by variability in this rate. Moreover, during this period the regulation of population size operated through density-dependent fecundity and subadult survival. However, after the onset of the European ban, a 1-month delay in average laying date, a drop in fecundity, and a reduction in the number of fledglings induced a transient increase in the impact of fledgling and subadult recruitment on dynamics. Although adult survival rate remained constantly high, as predicted by the buffering hypothesis, its relative impact on the temporal variance in abundance dropped to 71% during the sanitary regulation and to 54% after the ban was lifted. A significant increase in the relative impact of environmental stochasticity on dynamics was modeled after the BSE outbreak. These results provide empirical evidence on how abrupt environmental deterioration may induce dramatic demographic and dynamic changes in the populations of keystone scavengers, with far-reaching impacts on ecosystem functioning worldwide.

Avian scavengers' contributions to people: The cultural dimension of wildlife-based tourism.

Scavengers provide significant nature's contributions to people (NCP), including disease control through carcass removal, but their non-material NCP are rarely considered. For the first time, we assess the extent and value of the NCP provided by European avian scavengers through a scavenger-based tourism at Pyrenean supplementary feeding sites (SFS). Using a two-step cluster analysis, two different types of visitor were identified (specialist avian scavenger-watchers and generalist nature-lovers) at those SFS offering recreational experiences (n = 20, i.e. birdwatching, educational, or photographic activities). Most visitors (85%) perceived avian scavengers as beneficial NCP providers, associating this guild with non-material NCP (mostly supporting identities), followed by regulating and maintenance of options NCP (<1%). Our findings help to characterize the type of people who participate in scavenger related recreation and to identify and value their perceptions of avian scavengers. There has not been much previous research on positive human-wildlife interactions, even though ignoring people emotional bonds with nature can be perilous for biodiversity conservation.

The value of transhumance for biodiversity conservation: Vulture foraging in relation to livestock movements.

In recent decades, intensive techniques of livestock raising have flourished, which has largely replaced traditional farming practices such as transhumance. These changes may have affected scavengers' behaviour and ecology, as extensive livestock is a key source of carrion. This study evaluates the spatial responses of avian scavengers to the seasonal movements of transhumant herds in south-eastern Spain. We surveyed the abundance of avian scavengers and ungulates, and analysed the factors affecting the space use by 30 GPS-tracked griffon vultures (Gyps fulvus). Griffons' foraging activity increased in the pasturelands occupied by transhumant herds, which implied greater vulture abundance at the landscape level during the livestock season. In contrast, facultative scavengers were more abundant without transhumant livestock herds, and the abundance of wild ungulates did not change in relation to livestock presence. We conclude that fostering transhumance and other traditional farming systems, to the detriment of farming intensification, could favour vulture conservation.

Usually hated, sometimes loved: A review of wild ungulates' contributions to people.

Nature's contributions to people (NCP) may be both beneficial and detrimental to humans' quality of life. Since our origins, humans have been closely related to wild ungulates, which have traditionally played an outstanding role as a source of food or raw materials. Currently, wild ungulates are declining in some regions, but recovering in others throughout passive rewilding processes. This is reshaping human-ungulate interactions. Thus, adequately understanding the benefits and detriments associated with wild ungulate populations is necessary to promote human-ungulate co-existence. Here, we reviewed 575 articles (2000-2019) on human-wild ungulate interactions to identify key knowledge gaps on NCP associated with wild ungulates. Wild ungulate research was mainly distributed into seven research clusters focussing on: (1) silvicultural damage in Eurasia; (2) herbivory and natural vegetation; (3) conflicts in urban areas of North America; (4) agricultural damage in Mediterranean agro-ecosystems; (5) social research in Africa and Asia; (6) agricultural damage in North America; (7) research in natural American Northwest areas. Research mostly focused on detrimental NCP. However, the number of publications mentioning beneficial contributions increased after the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services conceptual framework was implemented. Human-ungulate interactions' research was biased towards the Global North and Cervidae, Suidae and Bovidae families. Regarding detrimental NCP, most publications referred to production damage (e.g. crops), followed by biodiversity damage, and material damage (e.g. traffic collisions). Regarding beneficial NCP, publications mainly highlighted non-material contributions (e.g. recreational hunting), followed by material NCP and regulating contributions (e.g. habitat creation). The main actions taken to manage wild ungulate populations were lethal control and using deterrents and barriers (e.g. fencing), which effectiveness was rarely assessed. Increasing research and awareness about beneficial NCP and effective management tools may help to improve the conservation of wild ungulates and the ecosystems they inhabit to facilitate people-ungulate co-existence in the Anthropocene.

Functional traits driving species role in the structure of terrestrial vertebrate scavenger networks.

Species assemblages often have a non-random nested organization, which in vertebrate scavenger (carrion-consuming) assemblages is thought to be driven by facilitation in competitive environments. However, not all scavenger species play the same role in maintaining assemblage structure, as some species are obligate scavengers (i.e., vultures) and others are facultative, scavenging opportunistically. We used a database with 177 vertebrate scavenger species from 53 assemblages in 22 countries across five continents to identify which functional traits of scavenger species are key to maintaining the scavenging network structure. We used network analyses to relate ten traits hypothesized to affect assemblage structure with the "role" of each species in the scavenging assemblage in which it appeared. We characterized the role of a species in terms of both the proportion of monitored carcasses on which that species scavenged, or scavenging breadth (i.e., the species "normalized degree"), and the role of that species in the nested structure of the assemblage (i.e., the species "paired nested degree"), therefore identifying possible facilitative interactions among species. We found that species with high olfactory acuity, social foragers, and obligate scavengers had the widest scavenging breadth. We also found that social foragers had a large paired nested degree in scavenger assemblages, probably because their presence is easier to detect by other species to signal carcass occurrence. Our study highlights differences in the functional roles of scavenger species and can be used to identify key species for targeted conservation to maintain the ecological function of scavenger assemblages.

Biases in the Detection of Intentionally Poisoned Animals: Public Health and Conservation Implications from a Field Experiment.

Intentional poisoning is a global wildlife problem and an overlooked risk factor for public health. Managing poisoning requires unbiased and high-quality data through wildlife monitoring protocols, which are largely lacking. We herein evaluated the biases associated with current monitoring programmes of wildlife poisoning in Spain. We compared the national poisoning database for the 1990-2015 period with information obtained from a field experiment during which we used camera-traps to detect the species that consumed non-poisoned baits. Our findings suggest that the detection rate of poisoned animals is species-dependent: Several animal groups (e.g., domestic mammalian carnivores and vultures) tended to be over-represented in the poisoning national database, while others (e.g., corvids and small mammals) were underrepresented. As revealed by the GLMM analyses, the probability of a given species being overrepresented was higher for heaviest, aerial, and cryptic species. In conclusion, we found that monitoring poisoned fauna based on heterogeneous sources may produce important biases in detection rates; thus, such information should be used with caution by managers and policy-makers. Our findings may guide to future search efforts aimed to reach a more comprehensive understanding of the intentional wildlife poisoning problem.

Rethinking megafauna.

Concern for megafauna is increasing among scientists and non-scientists. Many studies have emphasized that megafauna play prominent ecological roles and provide important ecosystem services to humanity. But, what precisely are 'megafauna'? Here, we critically assess the concept of megafauna and propose a goal-oriented framework for megafaunal research. First, we review definitions of megafauna and analyse associated terminology in the scientific literature. Second, we conduct a survey among ecologists and palaeontologists to assess the species traits used to identify and define megafauna. Our review indicates that definitions are highly dependent on the study ecosystem and research question, and primarily rely on ad hoc size-related criteria. Our survey suggests that body size is crucial, but not necessarily sufficient, for addressing the different applications of the term megafauna. Thus, after discussing the pros and cons of existing definitions, we propose an additional approach by defining two function-oriented megafaunal concepts: 'keystone megafauna' and 'functional megafauna', with its variant 'apex megafauna'. Assessing megafauna from a functional perspective could challenge the perception that there may not be a unifying definition of megafauna that can be applied to all eco-evolutionary narratives. In addition, using functional definitions of megafauna could be especially conducive to cross-disciplinary understanding and cooperation, improvement of conservation policy and practice, and strengthening of public perception. As megafaunal research advances, we encourage scientists to unambiguously define how they use the term 'megafauna' and to present the logic underpinning their definition.

Scientific priorities and shepherds' perceptions of ungulate's contributions to people in rewilding landscapes.

Nature's contributions to people (NCP) are all the contributions of living nature, both beneficial and detrimental, to the societies' life's quality. Ungulates play this dual role of providers of beneficial and detrimental NCP, as they are responsible of the supply of benefits (e.g. extractive experiences, habitat maintenance) and detriments (e.g. crops damage, traffic collisions). Our aim was to analyze the NCP provided by wild ungulates through examining the scientific priorities and the shepherds' perceptions in peninsular Spain. We reviewed scientific articles of NCP provided by ungulates in Spain and conducted questionnaires regarding NCP to shepherds in farming systems where domestic and wild ungulates cohabit. Then, we compared whether the scientific priorities match with those perceived by shepherds. Both stakeholders highlight more detrimental than beneficial NCP, although there are some mismatches between scientific priorities and shepherds' perceptions. Regarding detrimental NCP, soil alteration, silvicultural damage, human safety or traffic collision were included in scientific literature but not mentioned by shepherds. Contrarywise, shepherds mainly considered grazing competence and damage to animals (i.e. game species and livestock) as important detrimental NCP. Concerning beneficial NCP, whilst hunting was prominent in the publications, shepherds did not conceived it as an important beneficial contribution and considered the regulation of organisms (i.e. scavenging alternative prey) important benefits. These results can have twofold implications. The emphasis on detrimental NCP (studied and perceived) can reinforce the idea that ungulates can threaten humans rather than contribute to societies' wellbeing. The fact that research does not address the interests of shepherds can affect the social tolerance towards ungulates as the damages experienced or perceived by shepherds are not studied. Our results show the relevance of considering local knowledge held by shepherds and their perceptions, something highlighted by the NCP approach.

Avoidance of carnivore carcasses by vertebrate scavengers enables colonization by a diverse community of carrion insects.

Carrion resources sustain a complex and diverse community of both vertebrate and invertebrate scavengers, either obligate or facultative. However, although carrion ecology has received increasing scientific attention in recent years, our understanding of carrion partitioning in natural conditions is severely limited as most studies are restricted either to the vertebrate or the insect scavenger communities. Moreover, carnivore carcasses have been traditionally neglected as study model. Here, we provide the first data on the partitioning between vertebrate and invertebrate scavengers of medium-sized carnivore carcasses, red fox (Vulpes vulpes (Linnaeus)), in two mountainous Mediterranean areas of south-eastern Spain. Carcasses were visited by several mammalian and avian scavengers, but only one carcass was partially consumed by golden eagle Aquila chrysaetos (Linnaeus). These results provide additional support to the carnivore carrion-avoidance hypothesis, which suggests that mammalian carnivores avoid the consumption of carnivore carcasses to prevent disease transmission risk. In turn, the absence of vertebrate scavengers at carnivore carcasses enabled a diverse and well-structured successional community of insects to colonise the carcasses. The observed richness and abundance of the most frequent families was more influenced by the decomposition time than by the study area. Overall, our study encourages further research on carrion resource partitioning in natural conditions.

Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale.

Understanding the distribution of biodiversity across the Earth is one of the most challenging questions in biology. Much research has been directed at explaining the species latitudinal pattern showing that communities are richer in tropical areas; however, despite decades of research, a general consensus has not yet emerged. In addition, global biodiversity patterns are being rapidly altered by human activities. Here, we aim to describe large-scale patterns of species richness and diversity in terrestrial vertebrate scavenger (carrion-consuming) assemblages, which provide key ecosystem functions and services. We used a worldwide dataset comprising 43 sites, where vertebrate scavenger assemblages were identified using 2,485 carcasses monitored between 1991 and 2018. First, we evaluated how scavenger richness (number of species) and diversity (Shannon diversity index) varied among seasons (cold vs. warm, wet vs. dry). Then, we studied the potential effects of human impact and a set of macroecological variables related to climatic conditions on the scavenger assemblages. Vertebrate scavenger richness ranged from species-poor to species rich assemblages (4-30 species). Both scavenger richness and diversity also showed some seasonal variation. However, in general, climatic variables did not drive latitudinal patterns, as scavenger richness and diversity were not affected by temperature or rainfall. Rainfall seasonality slightly increased the number of species in the community, but its effect was weak. Instead, the human impact index included in our study was the main predictor of scavenger richness. Scavenger assemblages in highly human-impacted areas sustained the smallest number of scavenger species, suggesting human activity may be overriding other macroecological processes in shaping scavenger communities. Our results highlight the effect of human impact at a global scale. As species-rich assemblages tend to be more functional, we warn about possible reductions in ecosystem functions and the services provided by scavengers in human-dominated landscapes in the Anthropocene.

Shepherds' local knowledge and scientific data on the scavenging ecosystem service: Insights for conservation.

Integrating indigenous and local knowledge (ILK) and scientific knowledge (SK) in the evaluation of ecosystem services has been recommended by the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. We examined the similarities and contradictions between shepherds' ILK and SK on the scavenging service provided by vertebrates in Spain. We conducted 73 face-to-face surveys with shepherds to evaluate their ILK. We collected scientific information on 20 scavenger species by monitoring the consumption of 45 livestock carcasses with camera traps. We found a high consistency between ILK and SK regarding the provision of the scavenging service by vertebrates, which was also consistent over the range of shepherd ages and experience. Our findings support the importance of ILK held by shepherds to better understand and to collect information on the scavenging service, particularly at the species level. The integration of ILK and SK into the management strategies of scavengers can benefit the conservation of globally endangered scavengers and the ecosystem services they provide.

Probing into farmers' perceptions of a globally endangered ecosystem service provider.

Society's perception of ecosystem services is a key issue in conservation, particularly for endangered species providing services linked to human activities. Misperceptions may lead to wildlife-human conflicts with the risk of disappearance of the species involved. We contrasted farmers' perceptions with highly accurate quantitative data of an endangered vulture species, which provide ecosystem services. We combined surveys of 59 farmers with data from 48 GPS-tagged Canarian Egyptian vultures (Neophron percnopterus majorensis endemic to the Spanish Canary Islands) to disentangle factors influencing consistency between farmers' awareness of vulture occurrence on their properties and vulture behavior. Egyptian vultures were perceived as the main providers of scavenging services and the most beneficial avian scavenger. Consistency between farmers' perceptions (surveys) and vulture use of their farms (GPS data) was higher in the morning, in older males, and at farms with lower livestock numbers, located near vulture communal roosts, and visited more frequently by vultures. Our results underline the potential influence of modern livestock husbandry in disconnecting people from ecosystems, and how appreciation could be even lower for scarce or threatened ecosystem service providers.

Supplanting ecosystem services provided by scavengers raises greenhouse gas emissions.

Global warming due to human-induced increments in atmospheric concentrations of greenhouse gases (GHG) is one of the most debated topics among environmentalists and politicians worldwide. In this paper we assess a novel source of GHG emissions emerged following a controversial policy decision. After the outbreak of bovine spongiform encephalopathy in Europe, the sanitary regulation required that livestock carcasses were collected from farms and transformed or destroyed in authorised plants, contradicting not only the obligations of member states to conserve scavenger species but also generating unprecedented GHG emission. However, how much of this emission could be prevented in the return to traditional and natural scenario in which scavengers freely remove livestock carcasses is largely unknown. Here we show that, in Spain (home of 95% of European vultures), supplanting the natural removal of dead extensive livestock by scavengers with carcass collection and transport to intermediate and processing plants meant the emission of 77,344 metric tons of CO2 eq. to the atmosphere per year, in addition to annual payments of ca. $50 million to insurance companies. Thus, replacing the ecosystem services provided by scavengers has not only conservation costs, but also important and unnecessary environmental and economic costs.