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

M.M. was supported by a research contract Ramon y Cajal from the MINECO (RYC-2015-19231) . This study was partly funded by the Spanish Ministry of Economy, Industry and Competitiveness and EU ERDF funds through the project CGL2017-89905-R.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.MINECO RYC-2015-19231Spanish Ministry of Economy, Industry and CompetitivenessEuropean Commission CGL2017-89905-

Non-trophic functions of carcasses: from death to the nest

Peer reviewe

Past, present and future of the ecosystem services provided by cetacean carcasses

This study was supported by the Spanish Ministry of Economy, Industry and Competitiveness and EU ERDF funds through the projects CGL2015-66966-C2-1-2-R and CGL2017-89905-R. M.M. was supported by a research contract Ramon y Cajal from the MINECO (RYC-2015-19231) , and A.CA. by a contract Juan de la Cierva Incorporacion (IJCI-2014-20744; Spanish Ministry of Economy and Competitiveness, Spain) and a PostDoc contract Programa Vicent Mut of Govern Balear, Spain (PD/039/2017) . NS was supported by the Bekker programme of the Polish National Agency for Academic Exchange (NAWA) . Acknowledgements of specific institutions and people sharing their valuable strandings database is in Table B3.Ecosystem services associated with cetacean strandings have been altered by humans through exploitation of wild populations during the whaling era and more recently by regulations on carcass management and disposal to abide by environmental health requirements. Here, we systematically review the scientific literature and gather data on cetacean strandings worldwide to: 1) identify the ecosystem services provided by stranded cetacean carcasses in the past and present; 2) estimate the density of cetacean strandings currently occurring in selected coastal areas around the globe, and analyse its association with human population density and regulations; and 3) identify and discuss the regulations and methods concerned with whale carcass disposal in specific regions of the world. Our literature review revealed that stranded cetacean carcasses have provided a rich and varied array of provisioning, regulating, cultural, and supporting ecosystem services to ancient and modern civilisations worldwide. Also, we found that the current density of stranded carcasses (mean: 0.090 strandings . year(-1). km(-1); range: 0.001-0.978) and the disposal methods widely varied across the studied regions and countries. In addition, neither human population density nor the existence of regulations were good predictors of stranding densities. Finally, we provide recommendations for the future management of stranded cetacean carcasses, by identifying those disposal methods that minimize costs and maximize ecosystem functions and services. In particular, we encourage natural decomposition in situ whenever possible; otherwise, the present coastal management strategies could be improved by including zoning, seasonal use limitation and educational outreach depending upon the local scenario. Overall, further socio-ecological research is strongly needed to guide stranded cetacean carcass management towards enhancing the net benefits that humans and ecosystems gain from carcasses, especially considering that coastal areas become more populated, new disposal regulations are approved, and cetacean populations are recovering - and thus strandings may become more frequent.Spanish Government EU ERDF funds CGL2015-66966-C2-1-2-R CGL2017-89905-Rresearch contract Ramon y Cajal from the MINECO RYC-2015-19231 contract Juan de la Cierva Incorporacion (Spanish Ministry of Economy and Competitiveness, Spain) IJCI-2014-20744PostDoc contract Programa Vicent Mut of Govern Balear, Spain PD/039/2017Polish National Agency for Academic Exchange (NAWA

Human-carnivore relations: conflicts, tolerance and coexistence in the American West

Carnivore and humans live in proximity due to carnivore recovery efforts and ongoing human encroachment into carnivore habitats globally. The American West is a region that uniquely exemplifies these human-carnivore dynamics, however, it is unclear how the research community here integrates social and ecological factors to examine human-carnivore relations. Therefore, strategies promoting human-carnivore coexistence are urgently needed.Weconducted a systematic review on human-carnivore relations in the American West covering studies between 2000 and 2018. Wefirst characterized human-carnivore relations across states of the American West. Second, we analyzed similarities and dissimilarities across states in terms of coexistence, tolerance, number of ecosystem services and conflicts mentioned in literature. Third, we used Bayesian modeling to quantify the effect of social and ecological factors influencing the scientific interest on coexistence, tolerance, ecosystem services and conflicts. Results revealed some underlying biases in humancarnivore relations research. Colorado and Montana were the states where the highest proportion of studies were conducted with bears and wolves the most studied species. Non-lethal management was the most common strategy to mitigate conflicts. Overall, conflicts with carnivores were much more frequently mentioned than benefits.Wefound similarities among Arizona, California, Utah, and New Mexico according to how coexistence, tolerance, services and conflicts are addressed in literature.MEG was supported by a research contract from Sistema Nacional de Garantía Juvenil co-funded by the Social European Fund and the Junta de Andalucía, Spain (PID_UAL_2018/001). AJC, NHC, and JMRM were funded by the NSF Idaho EPSCoR Program under award number IIA-1301792 and OIA‐1757324. MM and AFM were supported by Ramón y Cajal research contracts from the MINECO (RYC-2015- 19231 and RYC-2016-21114, respectively), ZMR by a postdoctoral contract from the Generalitat Valenciana (APOSTD/2019/016) and ACA by a postdoctoral contract of Programa Viçent Mut of Govern Balear, Spain (PD/039/2017)

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

This study was funded by MCIN/AEI/10.13039/501100011033 and “ERDF A way of making Europe” through project PID2021- 128952NB-I00. DRG was funded by a predoctoral grant from the Junta de Andalucía (PREDOC_00262). MM was partly sup- ported by a research contract Ramón y Cajal from the MINECO (RYC-2015-19231)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 car- nivore 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.Junta de Andalucia PREDOC_00262Ministry of Science and Innovation, Spain (MICINN) Instituto de Salud Carlos III Spanish Government PID2021-128952NB-I00RYC-2015-1923

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.Ministry of Science and Innovation, Spain (MICINN)Spanish Government CGL2012-33536 CGL2015-64144 FPU1700633European Commission CGL2012-33536 CGL2015-64144MCIN/AEI PID2019-105682RA-I00Regional Valencian Government AICO/2021/145 APOSTD/2020/090Ramon y Cajal research contract from MINECO RYC-2015-19231European Union-Next Generation EU in the Maria Zambrano Program ZAMBRANO 21-2

The Role of Carrion in the Landscapes of Fear and Disgust: A Review and Prospects

Animal behavior is greatly shaped by the ‘landscape of fear’, induced by predation risk, and the equivalent ‘landscape of disgust’, induced by parasitism or infection risk. However, the role that carrion may play in these landscapes of peril has been largely overlooked. Here, we aim to emphasize that animal carcasses likely represent ubiquitous hotspots for both predation and infection risk, thus being an outstanding paradigm of how predation and parasitism pressures can concur in space and time. By conducting a literature review, we highlight the manifold inter- and intraspecific interactions linked to carrion via predation and parasitism risks, which may affect not only scavengers, but also non-scavengers. However, we identified major knowledge gaps, as reviewed articles were highly biased towards fear, terrestrial environments, vertebrates, and behavioral responses. Based on the reviewed literature, we provide a conceptual framework on the main fearand disgust-based interaction pathways associated with carrion resources. This framework may be used to formulate predictions about how the landscape of fear and disgust around carcasses might influence animals’ individual behavior and ecological processes, from population to ecosystem functioning. We encourage ecologists, evolutionary biologists, epidemiologists, forensic scientists, and conservation biologists to explore the promising research avenues associated with the scary and disgusting facets of carrion. Acknowledging the multiple trophic and non-trophic interactions among dead and live animals, including both herbivores and carnivores, will notably improve our understanding of the overlapping pressures that shape the landscape of fear and disgust.Ramón y Cajal from the MINECO RYC-2015-19231Spanish Ministry of Economy, Industry and CompetitivenessEU ERDF funds CGL2015-66966-C2-1-2-R CGL2017-89905-

The underestimated role of carrion in vertebrates' diet studies

Aim: Despite the increasing scientific evidence on the importance of carrion in the ecology and evolution of many vertebrates, scavenging is still barely considered in diet studies. Here, we draw attention to how scientific literature has underestimated the role of vertebrates as scavengers, identifying the ecological traits that characterize those species whose role as scavengers could have gone especially unnoticed. Location: Global. Time Period: 1938–2022. Major Taxa Studied: Terrestrial vertebrate scavengers. Methods: We analysed and compared (a) the largest database available on scavenging patterns by carrion-consuming vertebrates, (b) 908 diet studies about 156 scavenger species and (c) one of the most complete databases on bird and mammal diets (Elton Traits database). For each of these 156 species, we calculated their scavenging degree (i.e. proportion of carcases where the species is detected consuming carrion) as a proxy for carrion consumption, and related their ecological traits with the probability of being identified as scavengers in diet studies and in the Elton Traits database. Results: More than half of the species identified as scavengers at monitored carcasses were not assigned carrion as food source in their diet studies nor in the Elton Traits database. Using a subset of study sites, we found a direct relationship between a species' scavenging degree and its rate of carrion biomass removal. In addition, scavenger species, which were classified as non-predators and mammals had a lower probability of being identified as scavengers in diet studies and in the Elton Traits database, respectively. Main Conclusions: Our results clearly indicate an underestimation of the role of scavenging in vertebrate food webs. Given that detritus recycling is fundamental to ecosystem functioning, we encourage further recognition and investigation of the role of carrion as a food resource for vertebrates, especially for non-predator species and mammals with higher scavenging degree.Junta de Andalucia POSTDOC_21_00353 PREDOC_00262Eusko Jaurlaritza PRE_2018_2_0112Center for Forestry Research & Experimentation (CIEF) ACIF/2019/056 APOSTD/2019/016 APOSTD/2021/028HORIZON EUROPE Marie Sklodowska-Curie Actions 101086387Instituto de Salud Carlos III Spanish Government IJC-2019-038968 PID2021-128952NB-I00 RYC-2015-19231 RYC-2019-027216-I TED2021-130890B-C2

Conserving outside protected areas: edge effects and avian electrocutions on the periphery of Special Protection Areas

Electrocution on power lines is one of the principal problems facing raptors and other mediumand large-sized birds at the global scale. The recent European-based Spanish state legislation on avian electrocutions has focused on Special Protection Areas (SPA). Here we evaluate whether this policy has been successful, using the Community of Valencia, Spain, as a regional model. We compiled a database of 400 electrocution events from information on electrocuted birds taken into Wildlife Recovery Centres and incidents registered by the main local power company during the last decade. A small proportion (c.18%) of electrocution casualties occurred within SPA boundaries but the 5 km wide belt immediately surrounding the SPAs produced more than three times the number of avian electrocutions (c.60% of the total recorded). This was probably caused by higher densities of both power lines and susceptible birds, and higher use of the pylons for perching and roosting in the areas surrounding the SPAs. We therefore conclude that the focus on preventative measures being applied within SPAs is inefficient and that action should be targeted in these peripheral areas. Our results illustrate a classic problem of an edge effect associated with a protected area, where external human influences directly affect the persistence of protected species within reserves. Equally, they support the idea that management strategies within parks cannot be independent of the human activities surrounding them

Thelazia callipaeda as a potential new threat to european wildcats: insights from an eco-epidemiological study

Global warming and displacement of vectors and wild and domestic hosts by humans greatly change host-parasite interactions and parasite transmission rates. Thelazia callipaeda Railliet and Henry, 1910 (Spirurida: Thelaziidae) is a zoonotic parasite rapidly colonizing Europe from its Asian native range. This nematode is vectored by Phortica flies and may cause ocular disorders, such as keratitis and corneal ulcers, in wild mammals, dogs, cats and humans. With the aim of detecting possible threats for the European wildcat (Felis silvestris) in one of its last Mediterranean strongholds, we initiated in 2017 a long-term monitoring program in Sierra Arana (southeastern Spain), which includes exploring its epidemiological and spatial relationships with domestic cats (Felis catus). During routine medical check-ups, we detected ocular nematodes in 3 of 17 (17.6%) wildcats and 1 of 23 (4.3%) domestic cats tested, confirmed to be T. callipaeda by microscopic and molecular analyses. This nematode species was first detected in the study area in 2021. To our knowledge, this is the first case of infection in wildcats in Spain. Through telemetry, we detected little spatial overlap between the home ranges of wildcats and domestic cats, which seems to be sufficient to facilitate the inter-specific transmission of T. callipaeda. Our findings suggest that this pathogen could be a new threat to the wildcat, a locally endangered wild felid. Further ecoepidemiological monitoring and sanitary control of domestic cats will be strongly needed, especially given the ongoing global warming scenario