Marcos Moleón

Surveying carnivores at large spatial scales: a comparison of four broad-applied methods

Reliable methods to estimate species richness are very important to managers and conservationists because they provide key data to make the right decisions in conservation programmes. In the case of carnivore mammals, traditional methods, such as direct count censuses, are not useful since these animals are usually scarce, elusive and nocturnal. Difficulties in carnivore sampling are compounded when monitoring programmes are developed at large spatial scales, where high economic costs and field efforts are necessary to achieve reliable richness or abundance estimates. These problems have highlighted the need to find more effective carnivore survey methods, especially in regions with high rates of landscape change, such as the Mediterranean basin. The present study, performed in a typical Mediterranean area, was the first in Europe to test simultaneously the relative efficiencies of four broad-applied sampling methods to detect carnivore species at large spatial scales. Sign surveys based on scat detection, scent stations, camera-trapping and live-trapping were investigated. We compared efficiencies using biological parameters and by considering both the logistic and economic costs of each method. Overall, scent stations and sign surveys were the most efficient methods both in economic and logistic terms. In addition, the use of scent stations may be necessary to detect species rarely detected by scats. Detailed and extensive training programmes for conducting sign surveys and scent stations may overcome perceived problems thus enhancing the widespread use of both methods. Our results are applicable not only to other Mediterranean areas, but also to other habitats and regions of the world. More research into the suitability of these and other methods in relation to different landscapes, seasons and species is required.

Inter‐specific interactions linking predation and scavenging in terrestrial vertebrate assemblages

Predation and scavenging have been classically understood as independent processes, with predator–prey interactions and scavenger–carrion relationships occurring separately. However, the mere recognition that most predators also scavenge at variable rates, which has been traditionally ignored in food‐web and community ecology, leads to a number of emergent interaction routes linking predation and scavenging. The general goal of this review is to draw attention to the main inter‐specific interactions connecting predators (particularly, large mammalian carnivores), their live prey (mainly ungulates), vultures and carrion production in terrestrial assemblages of vertebrates. Overall, we report an intricate network of both direct (competition, facilitation) and indirect (hyperpredation, hypopredation) processes, and provide a conceptual framework for the future development of this promising topic in ecological, evolutionary and biodiversity conservation research. The classic view that scavenging does not affect the population dynamics of consumed organisms is questioned, as multiple indirect top‐down effects emerge when considering carrion and its facultative consumption by predators as fundamental and dynamic components of food webs. Stimulating although challenging research opportunities arise from the study of the interactions among living and detrital or non‐living resource pools in food webs.

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 Bonellis 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.

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.

Roles of raptors in a changing world: from flagships to providers of key ecosystem services

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.

Predator–prey relationships in a Mediterranean vertebrate system: Bonelli’s eagles, rabbits and partridges

Summary. Birds of prey have been, in comparison to other avian groups, an uncommon study model, mainly due to the limitations imposed by their conservative life strategy (low population density and turnover). Nonetheless, they have attracted a strong interest from the point of view of conservation biology because many populations have been close to extinction and because of their recognised role in ecosystems as top predators and scavengers and as flagship species. Today, after more than a century of persecution, and with the exception of some vultures still very much affected by illegal poisoning, many populations of birds of prey have experienced significant recoveries in many regions of Spain and the European Mediterranean. These changes pose new challenges when addressing the conservation of raptors in the coming decades. On this basis, and from a preferentially Mediterranean perspective, we have focused our attention on the need of describing and quantifying the role of these birds as providers of both regulating (rodent pest control and removal of livestock carcasses) and cultural ecosystem services. Moreover, we revisited persisting conflicts with human interests (predation of game species) and call attention to the emergence of new conflicts with a strong social and media component such as the predation on live cattle by vultures. Also, the rampant humanization of the environment determines the need for new solutions to the growing, yet scarcely explored, problem of accidents in new infrastructures such as mortality in wind farms. Finally, we explored in depth the ecological response of birds of prey to large-scale habitat changes such as urbanisation and abandonment of marginal lands that are also expected to increase in the near future. We urgently need more scientific knowledge to provide adequate responses to the challenge of keeping healthy populations of avian predators and scavengers in a rapidly changing world.

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

How predators impact on prey population dynamics is still an unsolved issue for most wild predator–prey communities. When considering vertebrates, important concerns constrain a comprehensive understanding of the functioning of predator–prey relationships worldwide; e.g. studies simultaneously quantifying ‘functional’ and ‘numerical responses’ (i.e., the ‘total response’) are rare. The functional, the numerical, and the resulting total response (i.e., how the predator per capita intake, the population of predators and the total of prey eaten by the total predators vary with prey densities) are fundamental as they reveal the predator’s ability to regulate prey population dynamics. Here, we used a multi-spatio-temporal scale approach to simultaneously explore the functional and numerical responses of a territorial predator (Bonelli’s eagle Hieraaetus fasciatus) to its two main prey species (the rabbit Oryctolagus cuniculus and the red-legged partridge Alectoris rufa) during the breeding period in a Mediterranean system of south Spain. Bonelli’s eagle responded functionally, but not numerically, to rabbit/partridge density changes. Type II, non-regulatory, functional responses (typical of specialist predators) offered the best fitting models for both prey. In the absence of a numerical response, Bonelli’s eagle role as a regulating factor of rabbit and partridge populations seems to be weak in our study area. Simple (prey density-dependent) functional response models may well describe the short-term variation in a territorial predator’s consumption rate in complex ecosystems.

Multi-Scale Effects of Nestling Diet on Breeding Performance in a Terrestrial Top Predator Inferred from Stable Isotope Analysis

Summary 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.

Pollutant accumulation patterns in nestlings of an avian top predator: biochemical and metabolic effects

Inter-individual diet variation within populations is likely to have important ecological and evolutionary implications. The diet-fitness relationships at the individual level and the emerging population processes are, however, poorly understood for most avian predators inhabiting complex terrestrial ecosystems. In this study, we use an isotopic approach to assess the trophic ecology of nestlings in a long-lived raptor, the Bonelli’s eagle Aquila fasciata, and investigate whether nestling dietary breath and main prey consumption can affect the species’ reproductive performance at two spatial scales: territories within populations and populations over a large geographic area. At the territory level, those breeding pairs whose nestlings consumed similar diets to the overall population (i.e. moderate consumption of preferred prey, but complemented by alternative prey categories) or those disproportionally consuming preferred prey were more likely to fledge two chicks. An increase in the diet diversity, however, related negatively with productivity. The age and replacements of breeding pair members had also an influence on productivity, with more fledglings associated to adult pairs with few replacements, as expected in long-lived species. At the population level, mean productivity was higher in those population-years with lower dietary breadth and higher diet similarity among territories, which was related to an overall higher consumption of preferred prey. Thus, we revealed a correspondence in diet-fitness relationships at two spatial scales: territories and populations. We suggest that stable isotope analyses may be a powerful tool to monitor the diet of terrestrial avian predators on large spatio-temporal scales, which could serve to detect potential changes in the availability of those prey on which predators depend for breeding. We encourage ecologists and evolutionary and conservation biologists concerned with the multi-scale fitness consequences of inter-individual variation in resource use to employ similar stable isotope-based approaches, which can be successfully applied to complex ecosystems such as the Mediterranean.