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.

Top-predator carrion is scary: Fight-and-flight responses of wild boars to wolf carcasses.

Predation risk largely constrains prey behavior. However, whether predators may be scary also after death remains unexplored. Here, we describe the "fight-and-flight" responses of a prey, the wild boar (Sus scrofa), to carcasses of (a) its main predator, the gray wolf (Canis lupus) and (b) a carnivore that very rarely kills wild boars, the red fox (Vulpes vulpes), in the western Alps (Italy). We recorded the behavior of wild boars at 10 wolf and 9 fox carcass sites. We found eight "fight-and-flight" responses toward wolf carcasses, and none toward fox carcasses. Our results suggest that carnivore carcasses may indeed be scary; fear responses toward them are dependent on the species to which the carcass belongs; and animals approaching the carcasses are feared mainly when the latter are relatively fresh. This emphasizes the multiple and complex roles that carrion plays in the landscape of fear and opens exciting ecological, epidemiological, and evolutionary research avenues.

Predation impact on threatened spur-thighed tortoises by golden eagles when main prey is scarce.

A reduction in adult survival in long-living species may compromise population growth rates. The spur-thighed tortoise (Testudo graeca) is a long-lived reptile that is threatened by habitat loss and fragmentation. Golden eagles (Aquila chrysaetos), whose breeding habitats overlap that of tortoises, may predate them by dropping them onto rocks and breaking their carapaces. In SE Spain, the number of golden eagles has increased in the last decades and the abundance of their main prey (i.e., rabbits Oryctolagus cuniculus) has decreased. Our aims were to 1) describe the role of tortoises in golden eagles' diet, and 2) estimate the predation impact of golden eagles on tortoises in eagles' territories and in the regional tortoise population. We collected regurgitated pellets and prey remains under eagle nests and roosts, and obtained information on tortoise abundance and population structure and rabbit abundance. We found that tortoises were an alternative prey to rabbits, so that eagles shifted to the former where the latter were scarce. The average predation rate on tortoises was very low at the two studied scales. However, eagles showed a marked selection for adult female tortoises, which led the tortoise sex ratio to be biased towards males in those eagle territories with higher tortoise predation. Whether this may compromise the spur-thighed tortoise long-term population viability locally deserves further attention.

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.

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.

Smart carnivores think twice: Red fox delays scavenging on conspecific carcasses to reduce parasite risk.

The recent SARS-CoV-2 epidemic has highlighted the need to prevent emerging and re-emerging diseases, which means that we must approach the study of diseases from a One Health perspective. The study of pathogen transmission in wildlife is challenging, but it is unquestionably key to understand how epidemiological interactions occur at the wildlife-domestic-human interface. In this context, studying parasite avoidance behaviours may provide essential insights on parasite transmission, host-parasite coevolution, and energy flow through food-webs. However, the strategies of avoiding trophically transmitted parasites in mammalian carnivores have received little scientific attention. Here, we explore the behaviour of red foxes (Vulpes vulpes) and other mammalian carnivores at conspecific and heterospecific carnivore carcasses using videos recorded by camera traps. We aim to determine 1) the factors influencing the probability of foxes to practice cannibalism, and 2) whether the scavenging behaviour of foxes differ when facing conspecific vs. heterospecific carcasses. We found that red foxes were generally reluctant to consume mesocarnivore carrion, especially of conspecifics. When recorded, consumption by foxes was delayed several days (heterospecific carcasses) or weeks (conspecific carcasses) after carcass detection. Other mammalian scavengers showed a similar pattern. Also, meat-borne parasite transmission from wild carnivore carcasses to domestic dogs and cats was highly unlikely. Our findings challenge the widespread assumption that cannibalistic or intra-specific scavenging is a major transmission route for Trichinella spp. and other meat-borne parasites, especially for the red fox. Overall, our results suggest that the feeding decisions of scavengers are probably shaped by two main contrasting forces, namely the nutritional reward provided by carrion of phylogenetically similar species and the risk of acquiring meat-borne parasites shared with these species. This study illustrates how the detailed monitoring of carnivore behaviour is essential to assess the epidemiological role of these hosts in the maintenance and dispersion of parasites of public and animal health relevance.

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.

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.

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.

Tracking data and retrospective analyses of diet reveal the consequences of loss of marine subsidies for an obligate scavenger, the Andean condor.

Over the last century, marine mammals have been dramatically reduced in the world's oceans. We examined evidence that this change caused dietary and foraging pattern shifts of the Andean condor (Vultur gryphus) in Patagonia. We hypothesized that, after the decrease in marine mammals and the increase in human use of coastlines, condor diet changed to a more terrestrial diet, which in turn influenced their foraging patterns. We evaluated the diet by means of stable isotope analysis (δ13C, δ15N and δ34S) of current (last decade) and historical (1841-1933) feathers. We further evaluated the movement patterns of 23 condors using satellite tracking of individuals. Condors reduced their use of marine-derived prey in recent compared with historical times from 33 ± 13% to less than 8 ± 3% respectively; however, they still breed close to the coast. The average distance between the coast and nests was 62.5 km, but some nests were located close to the sea (less than 5 km). Therefore, some birds must travel up to 86 km from nesting sites, crossing over the mountain range to find food. The worldwide reduction in marine mammal carcasses, especially whales, may have major consequences on the foraging ecology of scavengers, as well as on the flux of marine inputs within terrestrial ecosystems.

From sport hunting to breeding success: Patterns of lead ammunition ingestion and its effects on an endangered raptor.

Lead is highly toxic for wildlife, with pernicious consequences especially in long-lived predators. The causes of lead ammunition ingestion in Bonelli's eagle (Aquila fasciata) and its effects on breeding success were studied in one of the most important populations of this endangered species in Europe. Regurgitated pellets belonging to different pairs from 2004 to 2014 were analyzed, both in the breeding (1363 pellets from 12 territories) and non-breeding (172 pellets from 9 territories) seasons. From these territories, 57 molted feathers to study lead contamination were analyzed, and breeding success was monitored for 41 breeding attempts. The occurrence of lead shots in pellets was detected using X-ray photographs. Pellets were also used to describe eagle diet. Lead shots in pellets were present in 83.3% of the territories. The frequency of occurrence of lead shots in pellets (2.81% in spring and 1.31% in autumn) was primarily related to the consumption of red-legged partridge in the breeding season (when partridges are hunted from blinds using calling lures), and secondarily to rabbit consumption in the non-breeding season (coinciding with the main hunting season). Thus, our results indicate that injured small-game were the main source of lead contamination in the Bonelli's eagle. For the first time for a raptor species, a positive relationship between the frequency of occurrence of lead shots in pellets and lead concentration in eagles' feathers has been documented. Lead concentration in feathers (mean±SD: 816±426µgkg-1, with no sex-related differences) was high for a species that rarely eats carrion or aquatic birds (the main prey-related lead source for raptors). This had negative effects on breeding success, which could jeopardize Bonelli's eagles in other European populations that are sustained by juvenile dispersal from the study population. Our work shows that some game modalities pose a potential threat to endangered raptors.