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

Carrion Availability in Space and Time

Introduction Availability of carrion to scavengers is a central issue in carrion ecology and management, and is crucial for understanding the evolution of scavenging behaviour. Compared to live animals, their carcasses are relatively unpredictable in space and time in natural conditions, with a few exceptions (see below, especially Sect. “Carrion Exchange at the Terrestrial-Aquatic Interface”). Carrion is also an ephemeral food resource due to the action of a plethora of consumers, from microorganisms to large vertebrates, as well as to desiccation (i.e., loss of water content; DeVault et al. 2003; Beasley et al. 2012; Barton et al. 2013; Moleón et al. 2014). With a focus on vertebrate carcasses, here we give an overview of (a) the causes that produce carrion, (b) the rate of carrion production, (c) the factors affecting carrion quality, and (d) the distribution of carrion in space and time, both in terrestrial and aquatic environments (including their interface). In this chapter, we will focus on naturally produced carrion, whereas non-natural causes of animal mortality are described in chapter “Human-Mediated Carrion: Effects on Ecological Processes”. However, throughout this chapter we also refer to extensive livestock carrion, because in the absence of strong restrictions such as those imposed in the European Community after the bovine spongiform encephalopathy crisis (Donázar et al. 2009; Margalida et al. 2010), the spatiotemporal availability of carrion of extensive livestock and wild ungulates is similar

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.JM was supported by a Basque Government predoctoral grant (PRE_2018_2_0112), ZMR, LNA and EA by contracts co-funded by the Generalitat Valenciana and the European Social Fund (ESF) (APOSTD/2019/016, ACIF/2019/056 and APOSTD/2021/028 respectively). MM, JMPG and ESG were funded by MCIN/AEI/10.13039/501100011033, by ‘European Union NextGenerationEU/PRTR’, ERDF ‘A way of making Europe’ and by ESF ‘Investing in your future’ (grant numbers RYC-2015-19231, IJC-2019-038968, TED2021-130890B-C21, PID2021-128952NB-I00 and RYC-2019-027216-I). ESG was also partially funded by the HORIZONMSCA-2021-SE-0 action number: 101086387, ‘REMARKABLE’ project. ZMR and DRG were also funded by the Junta de Andalucía (POSTDOC_21_00353 and PREDOC_00262). RPR was co-funded by the ESF and Plan Propio I+D+i UCLM

Laying the Foundations for a Human-Predator Conflict Solution: Assessing the Impact of Bonelli's Eagle on Rabbits and Partridges

BACKGROUND: Predation may potentially lead to negative effects on both prey (directly via predators) and predators (indirectly via human persecution). Predation pressure studies are, therefore, of major interest in the fields of theoretical knowledge and conservation of prey or predator species, with wide ramifications and profound implications in human-wildlife conflicts. However, detailed works on this issue in highly valuable--in conservation terms--Mediterranean ecosystems are virtually absent. This paper explores the predator-hunting conflict by examining a paradigmatic, Mediterranean-wide (endangered) predator-two prey (small game) system. METHODOLOGY/PRINCIPAL FINDINGS: We estimated the predation impact ('kill rate' and 'predation rate', i.e., number of prey and proportion of the prey population eaten, respectively) of Bonelli's eagle Aquila fasciata on rabbit Oryctolagus cuniculus and red-legged partridge Alectoris rufa populations in two seasons (the eagle's breeding and non-breeding periods, 100 days each) in SE Spain. The mean estimated kill rate by the seven eagle reproductive units in the study area was c. 304 rabbits and c. 262 partridges in the breeding season, and c. 237 rabbits and c. 121 partridges in the non-breeding period. This resulted in very low predation rates (range: 0.3-2.5%) for both prey and seasons. CONCLUSIONS/SIGNIFICANCE: The potential role of Bonelli's eagles as a limiting factor for rabbits and partridges at the population scale was very poor. The conflict between game profitability and conservation interest of either prey or predators is apparently very localised, and eagles, quarry species and game interests seem compatible in most of the study area. Currently, both the persecution and negative perception of Bonelli's eagle (the 'partridge-eating eagle' in Spanish) have a null theoretical basis in most of this area

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

Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature.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.CRUE-CSICSpringer Natur

From local monitoring to a broad‐scale viability assessment: a case study for the Bonelli's Eagle in western Europe

Population viability analysis (PVA) has become a basic tool of current conservation practice. However, if not accounted for properly, the uncertainties inherent to PVA predictions can decrease the reliability of this type of analysis. In the present study, we performed a PVA of the whole western European population (France, Portugal, and Spain) of the endangered Bonelli's Eagle (Aquila fasciata), in which we thoroughly explored the consequences of uncertainty in population processes and parameters on PVA predictions. First, we estimated key vital rates (survival, fertility, recruitment, and dispersal rates) using monitoring, ringing, and bibliographic data from the period 1990-2009 from 12 populations found throughout the studied geographic range. Second, we evaluated the uncertainty about model structure (i.e., the assumed processes that govern individual fates and population dynamics) by comparing the observed growth rates of the studied populations with model predictions for the same period. Third, using the model structures suggested in the previous step, we assessed the viability of both the local populations and the overall population. Finally, we analyzed the effects of model and parameter uncertainty on PVA predictions. Our results strongly support the idea that all local populations in western Europe belong to a single, spatially structured population operating as a source-sink system, whereby the populations in the south of the Iberian Peninsula act as sources and, thanks to dispersal, sustain all other local populations, which would otherwise decline. Predictions regarding population dynamics varied considerably, and models assuming more constrained dispersal predicted more pessimistic population trends than models assuming greater dispersal. Model predictions accounting for parameter uncertainty revealed a marked increase in the risk of population declines over the next 50 years. Sensitivity analyses indicated that adult and pre‐adult survival are the chief vital rates regulating these populations, and thus, the conservation efforts aimed at improving these survival rates should be strengthened in order to guarantee the long‐term viability of the European populations of this endangered species. Overall, the study provides a framework for the implementation of multi‐site PVAs and highlights the importance of dispersal processes in shaping the population dynamics of long‐lived birds distributed across heterogeneous landscapes

An Emerging Infectious Disease Triggering Large-Scale Hyperpredation

Hyperpredation refers to an enhanced predation pressure on a secondary prey due to either an increase in the abundance of a predator population or a sudden drop in the abundance of the main prey. This scarcely documented mechanism has been previously studied in scenarios in which the introduction of a feral prey caused overexploitation of native prey. Here we provide evidence of a previously unreported link between Emergent Infectious Diseases (EIDs) and hyperpredation on a predator-prey community. We show how a viral outbreak caused the population collapse of a host prey at a large spatial scale, which subsequently promoted higher-than-normal predation intensity on a second prey from shared predators. Thus, the disease left a population dynamic fingerprint both in the primary host prey, through direct mortality from the disease, and indirectly in the secondary prey, through hyperpredation. This resulted in synchronized prey population dynamics at a large spatio-temporal scale. We therefore provide evidence for a novel mechanism by which EIDs can disrupt a predator-prey interaction from the individual behavior to the population dynamics. This mechanism can pose a further threat to biodiversity through the human-aided disruption of ecological interactions at large spatial and temporal scales.MM and JASZ were partially supported by a project of the Spanish Ministerio de Educación y Ciencia (reference CGL-2006-10689/BOS)

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. We conducted a systematic review on human-carnivore relations in the American West covering studies between 2000 and 2018. We first 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. We found similarities among Arizona, California, Utah, and New Mexico according to how coexistence, tolerance, services and conflicts are addressed in literature. We identified percentage of federal/private land, carnivore family, social actors, and management actions, as factors explaining how coexistence, tolerance, conflicts and services are addressed in literature. We provide a roadmap to foster tolerance towards carnivores and successful coexistence strategies in the American West based on four main domains, (1)the dual role of carnivores as providers of both beneficial and detrimental contributions to people, (2)social-ecological factors underpinning the provision of beneficial and detrimental contributions, (3)the inclusion of diverse actors, and (4) cross-state collaborative management

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

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

Network Structure of Vertebrate Scavenger Assemblages at the Global Scale: Drivers and Ecosystem Functioning Implications

The organization of ecological assemblages has important implications for ecosystem functioning, but little is known about how scavenger communities organize at the global scale. Here, we test four hypotheses on the factors affecting the network structure of terrestrial vertebrate scavenger assemblages and its implications on ecosystem functioning. We expect scavenger assemblages to be more nested (i.e. structured): 1) in species‐rich and productive regions, as nestedness has been linked to high competition for carrion resources, and 2) regions with low human impact, because the most efficient carrion consumers that promote nestedness are large vertebrate scavengers, which are especially sensitive to human persecution. 3) We also expect climatic conditions to affect assemblage structure, because some scavenger assemblages have been shown to be more nested in colder months. Finally, 4) we expect more organized assemblages to be more efficient in the consumption of the resource. We first analyzed the relationship between the nestedness of the scavenger assemblages and climatic variables (i.e. temperature, precipitation, temperature variability and precipitation variability), ecosystem productivity and biomass (i.e. NDVI) and degree of human impact (i.e. human footprint) using 53 study sites in 22 countries across five continents. Then, we related structure (i.e. nestedness) with its function (i.e. carrion consumption rate). We found a more nested structure for scavenger assemblages in regions with higher NDVI values and lower human footprint. Moreover, more organized assemblages were more efficient in the consumption of carrion. However, our results did not support the prediction that the structure of the scavenger assemblages is directly related to climate. Our findings suggest that the nested structure of vertebrate scavenger assemblages affects its functionality and is driven by anthropogenic disturbance and ecosystem productivity worldwide. Disarray of scavenger assemblage structure by anthropogenic disturbance may lead to decreases in functionality of the terrestrial ecosystems via loss of key species and trophic facilitation processes