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Modelling the effects of sanitary policies on European vulture conservation

Modelling the effects of sanitary policies on European vulture conservation Modelling the effects of sanitary policies on European vulture conservation SUBJECT AREAS: 1 a ` 2 Antoni Margalida &M Angels Colomer BIODIVERSITY COMPUTATIONAL BIOLOGY AND BIOINFORMATICS Division of Conservation Biology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse, 6, 3012, Bern, Switzerland, Department of Mathematics, University of Lleida, Av. Alcalde Rovira Roure, 191, 25198, Lleida, Spain. ZOOLOGY ANIMAL BEHAVIOUR Biodiversity losses are increasing as a consequence of negative anthropogenic effects on ecosystem dynamics. However, the magnitude and complexity of these effects may still be greatly underestimated. Received Most Old World vultures have experienced rapid population declines in recent years. In Europe, their immediate conservation depends on changes in health regulations affecting the availability of food provided 6 June 2012 by domestic carcasses. Information is lacking on the effects of a hypothetical food shortage on the Accepted population dynamics of vultures, and is necessary to assess the potential impacts of policy decisions on 1 October 2012 future changes in biodiversity and ecosystem services. A novel computational model (P-systems) was used to model these effects, forecasting a rapid decline in the Eurasian griffon vulture (Gyps fulvus). By contrast, Published vulture species with greater plasticity in their dietary range appeared less sensitive to declining food 18 October 2012 availability. This study extends our understanding of vulture ecosystem services, which have social and economic implications. Correspondence and uring the last decade, the relationship between biodiversity and ecosystem function has emerged as an requests for materials important issue due to the strong connection between the ecological mechanisms that maintain biodi- 1–3 should be addressed to D versity in a community and their ecological consequences for ecosystem function . However, few eco- A.M. (antoni. system service assessment approaches have direct utility in political, social and ecological decision-making. Ecosystem services are natural processes that benefit humans, with birds contributing to four of the service types margalida@iee.unibe. (provisioning, regulating, cultural, and supporting services) recognised by the UN Millennium Ecosystem ch) 4–6 Assessment . Avian scavengers are part of the detrital food web of ecosystems and they provide the important ecological service of recycling carrion biomass to prevent the accumulation of dead biomass, thereby contributing to waste removal, disease regulation, and nutrient cycling . At the start of the 21st century, European avian scavenger communities were one of the few exceptions to the 8–12 global decline in Old World avian scavenger birds . Asian and, to a lesser degree African, vulture populations 8–12 declined as a consequence of ingestion of veterinary drugs and due to illegal poisoning . On the contrary, European vulture populations maintained or increased their numbers . However, the detection of variant (vCJD) and new variant (nvCJD) Creutzfeldt-Jakob disease in humans, which was acquired from cattle infected by bovine spongiform encephalopathy (BSE), led to sanitary legislation (Regulation CE 1774/2002) that greatly restricted the use of animal by-products that were not intended for human consumption. Thus, all carcasses of domestic animals had to be collected from farms and transformed or destroyed in authorised plants, although only 80% of domestic carcasses are currently recovered by specialised companies . In Spain, since 2006 supplementary feeding points for vultures, supplied by intensive farming, have also greatly diminished (280%) as a consequence of sanitary regulations . The disparity between sanitary and environmental policies, i.e., to eliminate corpses 3,15,16 versus to conserve scavenger species , led to several European dispositions that regulated the use of animal by- 13,16 products as food for necrophagous birds . Revised regulations on the use of animal by-products that are not intended for human consumption were made by the end of 2011 and they will be applied during 2012 . However, there has been no assessment of food availability or of the effects of different trophic scenarios on the population dynamics of European vultures. Recently, as a consequence of food shortages, several demographic warning signals have been documented, including a halt in population growth, decreased breeding success, and an apparent increase in mortality among younger age classes . However, empirical analyses of the relationships between vulture population dynamics and food availability have only assessed the role of wild ungulates . Modelling the effects of sanitary laws on population trends may provide evidence that can inform the design of policies that are compatible with vulture conservation. Multi-agent models are necessary for modelling population dynamics relative to demographic parameters and food availability such as P Systems, which is a SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 1 www.nature.com/scientificreports include the carrying capacity, suitable areas with potential for re- colonisation, or the benefits of supplying supplementary feeding sites. The present study used P systems to test the effects of variable levels of food availability over 21 years, on the population viability and conservation of four European vultures (the Eurasian griffon vulture Gyps fulvus, the Egyptian vulture Neophron percnopterus and the cinereous vulture Aegypius monachus considered as meat- eaters and the bearded vulture Gypaetus barbatus, considered a specialized bone-eater) as a consequence of sanitary regulations (see Methods). Taking into account a well-studied region in northern Spain (with 10 subareas) inhabited by the four European vulture species, we model the effects of available domestic carcasses (testing four initial scenarios of 100%, 50%, 25%, and 0% of domestic car- casses available in the field and separating meat and bone remains available as a consequence of the different dietary habits between meat and bone consumers) on their population dynamics. The 100% scenario represents conditions before the outbreak of BSE (,2002) while the 0%–25% scenarios represent the current condi- tions, depending on the area considered, as food limitations progres- sively worsened between 2006 and 2012. Future changes to the sanitary legislation may modify the availability of domestic carcasses and will probably progressively increase food availability, shifting conditions from 0–25% to 50% and expected to ultimately reach pre-outbreak conditions (100% of domestic carcasses available). Spain contains the most important European vulture populations (approximately 95% of their total numbers) and the results may have particularly important conservation applications in the assessment of their ecosystem services, the function of supplementary feeding sites, the carrying capacity, or the feeding resources available in an ecosystem during future reintroduction projects. The hypothetical effects of sanitary restrictions on vulture conservation were esti- mated and this method provides a computational tool that could be applied in other countries. Results Temporal and spatial food availability in different management scenarios. Meat was predicted to be the major factor limiting the survival of avian scavengers during winter and summer (Figure 1). In the breeding season (winter), the available food was predicted to be insufficient to cover energetic requirements in two areas with half the domestic carcasses available (PJ and AU), which increased to three (also AR) with a quarter of the domestic carrion available (current situation) and six (also PJ, N and S) without domestic carcasses Figure 1 | Spatial and temporal estimate of the difference between the available (with insufficient bone biomass in N). In the summer biomass estimated by the model and the energetic requirements for the scenario, food availability was predicted to be higher due to current avian scavenger population standardized by surface unit transhumance. However, the food available was also predicted to (expressed in calories per km ) in the ecosystem, for each of 10 be insufficient in one area (PJ) with half the domestic carcasses, municipalities in Catalonia, Northern Spain, according to the four increasing to three areas (also AR and AU) with a quarter of the scenarios of food availability considered (100%, 50%, 25% and 0% of food domestic carrion available to vultures and five (also N and S) provided by domestic ungulates). without domestic carcasses. From a population perspective, these three areas (AR, PJ and AU) were the most important for the avian computational modelling paradigm that was inspired by the func- scavenger guild because the areas with a quarter of the domestic 21,22 tioning of cells working in parallel . This technique was applied carcasses available contain 59% of the bearded vulture population, recently in several approaches to modelling the dynamics of scav- 56% of Egyptian vultures, 71% of griffon vultures, and 100% of 19,23,24 enger species . However, these studies did not consider future cinereous vultures in the study area. trends in vulture populations under different trophic scenarios. They also failed to take into account the temporal distribution of feeding Population dynamics in different management scenarios. The po- resources in different breeding seasons (i.e., winter vs. summer) and pulation trends of bearded, Egyptian and cinereous vultures were the spatial scale of areas where the resources were homogenously dis- predicted to increase in relation to the current situation and were tributed. This theoretical approach is valid, but the results obtained similar across the four scenarios considered (bearded vulture: F 5 3,83 are limited from an ecological viewpoint because the models failed 2.61, P 5 0.057; Egyptian vulture: F 5 0.12, P 5 0.95; cinereous 3,83 to detect spatial changes in species distributions or temporal limita- vulture: F 5 0.71, P 5 0.55, Figure 2) except for the griffon 3,83 tions in food availability. Managers and conservationists require vulture, for which significant differences were found (F 5 3,83 more detailed data to accurately determine parameters for optimis- 117.54, P 5 0.0001). The model predicted differences in the ing investment in the management of resources. These parameters groups formed with 50% and 100% of domestic carcasses available SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 2 www.nature.com/scientificreports movement of animals between neighbouring areas (Figure 3). It was predicted that most individuals would not colonize new areas, so the population balance of the species in each area was not predicted to be affected (a trend similar to the 100% scenario) and only some indi- viduals could colonize unoccupied areas such as VA and C. The growth trend with 50% domestic carcass availability is similar to 100% availability during the first 12 years. After this time, the food resources in the receiving areas (VA, C, B and N) were predicted to be insufficient for all pairs such that there is a significant decrease in griffon vulture populations in areas AR, PJ and AU and population stability only occurred with an increase in the biomass provided by wild ungulate populations. Benefits of vulture ecological services. On average, the Spanish vul- ture populations were estimated to remove 133.6–200.5 t of bones and 5,550.7–8,326 t of meat each year. Th e corresponding economic savings of natural carrion removal were estimated at a minimum of 907,679– 1,488,719 EUR, while vulture populations throughout the entire European Union may contribute an annual cost reduction of 972,915– 1,595,715 EUR. The animal biomass consumed by avian scavengers and removed from the ecosystem in the study area (assuming 50–75% of the diet is based on domestic ungulates) was estimated at 4.236– .38 t of bones and 176.73–265.10 t of meat. This constituted annual bene- fits estimated at 28,900–47,400 EUR for farmers and authorities. Discussion Sudden changes in the availability of food may cause changes in the population dynamics of species . The current study highlights the consequences of different levels of food availability on the population dynamics of an avian scavenger guild, indicating the halt and sub- sequent decline in population growth of the most meat-dependent species, i.e., the griffon vulture. The model predicted meat biomass to be the major limiting factor whereas the dietary plasticity of the other species allowed them to avoid declining population trends, as did their specific dietary habits (small animals for the Egyptian vul- ture and bones for the bearded vulture) and low densities. From a conservation perspective, these results suggest that the population growth of the most endangered species (Egyptian, cinereous, and bearded vultures) will continue in the current scenario, despite san- 13,16 itary legislation that limits food resources , given that a quarter of domestic ungulates are available in the ecosystem. However, this trend may be reversed by an increased effect of non-natural mortality Figure 2 | Predicted population trends for the four avian scavengers in when considering the effects of factors, such as illegal poisoning or 27–31 the study area, for each of the four scenarios tested, expressed as the lead poisoning, on breeding success and survival . These problems percentage of domestic ungulate carcasses available in the ecosystem. currently affect the threatened bearded vulture and they appear to Note the different y-axis scales. have stabilised their populations via non-natural mortality effects on adult survival . In addition, given the difficult nature of assessing the compared to the 25% and 0% scenarios (Duncan’s test, P , 0.05). numbers and age structure of the non-breeding population for mod- With a quarter of domestic carcasses available, a 14% reduction in the elling demographic trends and movements, and because these indi- griffon vulture population was forecast during the first year, after viduals mainly feed at supplementary feeding sites , our model only which their numbers were expected to become stable. In contrast, considered the immature population (chicks reared). Thus, we can without domestic carcasses (0% scenario) a sudden decrease is ex- consider our model conservative because a portion of available food pected with a reduction of 80% in griffon vulture populations, could benefit other non-breeding individuals. stabilizing at around 200–250 pairs. However, no global differences In recent years, the Spanish griffon vulture population has experi- were found between 100% and 50% domestic carcass availability (P enced decreases in their breeding parameters and changes in the 5 0.44), although the model indicated that statistically significant spatial distribution of the breeding and non-breeding population, differences would be detected after the 12th year (F 5 603.60, P while there have also been increases in their number of aggressive 1,268 , 0.0001) when there would be a reduction in the population growth interactions with live livestock and an increase in the mortality of 18,33 of griffon vultures. their young . By contrast, other species have increased their popula- 27,30 Assuming the network movements estimated in the study area tions, although illegal poisoning has affected some subpopulations . (Figure 3), the predicted response of griffon vulture populations to It is speculated that these changes were due to food shortages, the different scenarios studied is shown in Figure 4. With 25% or 0% although no empirical evidence is presented to support this hypo- of domestic carcasses available, a significant reduction of the popu- thesis. For the first time, the current study suggests that food limita- lation was forecasted in all study areas. The decrease was especially tions mainly affect griffon vultures. According to the model, vultures important in populated areas (AR, PJ and AU). A decrease of 50% in might respond to food shortages by shifting their spatial distribu- the contributions of domestic carcasses was predicted to promote tion leading to population decline (in the case of the 0% and 25% SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 3 www.nature.com/scientificreports Figure 3 | (a) Possible avian scavenger foraging movements between areas, when there is a lack ofresources. The continuous lines are the possible movements of the bearded vulture (Gypaetus barbatus), Egyptian vulture (Neophron percnopterus), and cinereous vulture (Aegypius monachus). The dashed line represents the Eurasian griffon vulture (Gyps fulvus). (b) Distribution of the ten areas considered in the study: VA: Val d’Aran; AR:Alta Ribagorc¸a; PJ: Pallars Jussa`; PS: Pallars Sobira`; AU: Alt Urgell; C: Cerdanya; R: Ripolle`s; B: Bergueda`; S: Solsone`s; N: Noguera. A, F, and PPO correspond to peripheral areas (alternative environments in the model) in which the population might obtain alternative food resources outside of the study area (see more details in Methods). scenarios) and these effects could accelerate in coming years if food closely resembling actual ecosystems, thereby preventing behaviou- 19,34,36,37 limitations continue. These regressive scenarios suggested by the ral changes or any negative effects on population dynamics . model do not imply an increase in mortality. Instead, individuals were Based on the carrying capacity and the population trend observed, predicted to abandon the ecosystem to search for suitable alternative supplementary feeding programs appear to be unnecessary in areas where food and breeding sites are available, when food resources hypothetical scenarios where half and 100% of domestic carcasses are insufficient and the carrying capacity at small spatial scales are available. The latter scenario corresponds to that present in the approaches the maximum levels. From an ecological perspective, grif- period before the establishment of sanitary regulations (progressively fon vultures are the dominant species of the avian scavenger guild in a applied since 2006), which could be representative of most Medi- competitive scenario because they can monopolise resources to the terranean populations that are characterised by widespread grazing 14 19,38 detriment of other species . This suggests that the provision of sup- and the food resources provided by wild ungulates . Thus, this plementary feeding sites as a stopgap measure to meet food deficits study should be taken into account by managers and conservationists would mainly favour this species. However, other ecological effects on if the sanitary legislation is amended in the future. In fact, the pres- the ecosystem of a population decline are unknown and the conse- ence of carcasses in the field as a consequence of extensive grazing is quences may be a new concern for managers and policy-makers .The considered to be the most useful and economic method of managing 13,17 ecological services provided by vultures have an important role and avian scavenger populations . This is an important issue for man- the regular use of feeding stations by these species could reduce eco- agers and policy-makers because solutions to the management of 18,25,35 logical service provision in terms of scavenging . In addition, the European vulture populations are based on an assumption that role of griffon vultures as facilitator species preparing carrion for other food shortages due to sanitary regulations should be compensated facultative and obligate scavengers is unknown but may have cascade for with supplementary feeding sites. This management approach effects within the ecosystem. may have detrimental consequences because a patchy distribution of A more advisable management measure would be to reduce the resources can artificially modify the habitat quality, with subsequent 36,39 amount of food provided at large feeding stations and promote negative effects on population dynamics . Thus, the carrying the creation of smaller sites that simulate a trophic scenario by more capacity should be regulated by feeding resources provided in the SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 4 www.nature.com/scientificreports Figure 4 | Predicted population trend of the Eurasian griffon vulture in the different areas, according the four scenarios of domestic carcasses available. The population increase in several areas in which the species is initially absent (VA and C) or of low densities is a consequence of spatial changes related with food shortages or maximum carrying capacity. ecosystem despite the long tradition in several countries of artificial reintroduction projects, thereby allowing managers to improve the food handling via supplementary feeding sites . However, the sens- success rate of reintroductions. This is particularly important for itivity of some species (several threatened) in terms of demographic avian scavengers because they are highly dependent on carrion 29,40,41 parameters, such as adult survival due to the presence of non- resources, the availability of which can be modified by humans by natural mortality factors (mainly illegal poisoning) , could increase direct management, e.g., hunting of wild ungulates, the sanitary mortality rates and destabilise populations. Given that supplement- legislation for domestic ungulates, or the establishment of a network of supplementary feeding sites. Given the global decline affecting Old ary feeding increases pre-adult survival , this method may continue to favour the most endangered species, especially if the quantity World vultures , the availability of robust tools can help managers to 43,44 supplied is reduced and its unpredictability is increased. optimise the investment of economic resources and to identify the most appropriate conservation measures. The results of this study are relevant to future reintroduction and conservation projects. Our model is capable of identifying the spatial and temporal distribution of feeding resources, thereby facilitating Methods the planning and optimisation of the most appropriate management Model building and assumptions. Using a Population Dynamic P System (see approach, including supplementary feeding activities, to support Supplementary Information) we defined a model allowing the study of the ecosystem dynamics in a zone subdivided into 10 areas inhabited by four avian scavengers whose the most food-poor areas where necessary. The application of this diet depends on the food provided by the carcasses of wild and domestic ungulates. model to reintroduction projects demonstrates that calculations of 19,24 For the validation of the model , we used census data obtained in the study area food availability can provide guidelines when establishing the car- 24,25 between 1994 and 2008 taking into account the inter-annual variation in rying capacity to optimise economic investment. In the case of avian demographic parameters and density-dependent effects affecting the population scavengers, food availability studies can identify problems prior to trends observed. SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 5 www.nature.com/scientificreports Besides natural and non-natural mortality, the model assumes that an ungulate dies when it lacks physical space as a consequence of its carrying capacity. In the case of avian scavengers, if a species has insufficient resources it moves to nearby areas. It returns to the starting point if there are food limitations but no space limitations. An individual colonises a new area if insufficient space is available. Scavengers can choose from more than one destination if they need to move, and they select one randomly. If the alternative area selected lacks resources, this random sampling continues until resources are found, leaving the ecosystem if resources are not found. If there is an avian scavenger who lacks sufficient resources after carrying out the rules of feeding and controlling for the maximum density of each species, it will move to another environment, running the feeding process and/or density previously unrealized for this animal. If space is not a limiting factor, they will return to the source environment or otherwise colonize a new area. When defining the model, a directed network-graph of avian scavenger movement is specified (Figure 3). The avian scavengers move to search for food in the peripheral areas (A, F, PPO) when feeding resources in the regular home ranges are insufficient. For the foraging areas, we consider the maximum linear foraging movement from the nest for the griffon vulture to be 90 km, 40 km for the bearded vulture, 15 km for the Egyptian vulture and 60 km for the cinereous vulture (A.M. unpubl. data). The model takes into account that each species takes advantage of the resources close to their nesting area and widens the radius of their movements as they deplete. The amount of meat and bones consumed by scavengers depends on the season. The excess meat disappears from the ecosystem at the end of each period (summer or winter). The model assumes that 20% of the unconsumed bones remain available in the ecosystem, because bones can be preserved for up to 10 times longer than meat . Populations of animals will generally grow exponentially if they have sufficient resources, although this growth is restricted due to limitations in physical space, which supports the maximum carrying capacity used in the model (Table S1). The objective of the final module is to restore the initial configuration to restart the loop. Running the model requires some initial parameters, so these are entered before returning an output. The evolution rules used by the model are run for each individual and they are Figure 5 | Scheme of the model. The model takes into account two executed simultaneously for all individuals. Thus, the system operates in parallel, periods (summer and winter) and the basic processes of reproduction, which means there can be competition when animals of the same or different species mortality, and feeding. The scavenger birds forage in others areas when share resources. The values of the parameters used in the model were derived from the 19,24 insufficient resources are available (i.e., they move). If food is scarce, the bibliography . The running model is detailed in Supplementary Information. animals take the food and return to their initial area. They change territory Management scenarios. Several possible scenarios were modelled by testing the if space is scarce. The carrying capacity of each area is limited and it is impact of different food availability regimes to elucidate their potential effects on necessary to control the number of animals present. Before repeating the population projections over time. Four initial scenarios were considered that depended loop, it is necessary to restore the initial configuration. Two executions of a on the hypothetical biomass provided by domestic ungulates. Thus, the 100% scenario 13,16 represented the ecosystem function prior to the application of sanitary regulations loop are equivalent to the passage of one year in the ecosystem. where all domestic and wild ungulate carcasses were available to the avian scavenger guild. The 50% scenario represented a scenario where only half of the hypothetical food The model consists of a loop with six modules (Figure 5). One year in the ecosystem resources provided by domestic carcasses were available. The 25% scenario might involves running the loop twice, i.e., once for the summer period (four months) and reflect a scenario that is similar to the current situation because approximately 80% of once for the winter season (eight months). The model starts with the run of the carcasses are recovered and destroyed by specialist companies. Finally, the 0% scenario reproduction module. The species are modelled with only one reproductive period simulates an ecosystem where food is provided only by wild ungulates. each year. While the population of wild animals is a dynamic system conditioned by First, the biomass was calculated provided for each subzone by subtracting the environmental and ecological factors, domestic animals are controlled by humans megacalories available from the energetic requirements of the avian scavengers such that there are significant fluctuations in the population between the summer and inhabiting each subzone. This provided a picture of the surplus or constraints on food winter as a consequence of transhumant movements. availability from a spatial perspective. Second, the population trend was simulated In the reproduction module, all breeding age females can reproduce successfully in with consideration for the demographic parameters of hypothetical growth in each a probabilistic way. After the application of reproduction rules, the mortality module species (see Supplementary Information) and the availability of biomass provided by is carried out; there are two possible causes of death, i.e., natural mortality (e.g., the different scenarios plus the biomass provided by wild ungulates and feeding senescence or accidents) and non-natural mortality (e.g., hunting or illegal poison- stations. Data used for the a posteriori statistical analyses were obtained by using the ing). In most ungulate species (except wild boar), hunting practices are focused on model to simulate the population dynamics (21 years and a total of 50 replicates) in a males, producing variations in the sex-ratio. The model takes into account temporal probabilistic manner, which reflected the random behaviour of the natural situation. and sex-ratio mortality variations influencing population growth and the biomass provided. In the following module the model takes into account whether food and Quantifying carrion removal vs. vulture ecological services. To estimate the carrying capacity are sufficient in the environment occupied to maintain their potential biomass that avian scavengers can remove from the ecosystem, the annual presence. energetic requirements of each individual and species were determined based on their 48,56,57 For each vulture species we obtained parameters on breeding, demography and standard metabolism , and then multiplied by the number of individuals present energetic requirements according to their metabolism (Supplementary Information in the ecosystem. It was estimated that 50–75% of the diet of avian scavengers was Table S2), mortality and the biomass that dead wild ungulates provided in the field, composed of domestic ungulate remains, which was based on the animal biomass separating bone and meat remains in accordance with the different dietary habits of range (its natural removal from the ecosystem). To compare the results, this estimate the species . The diet of avian scavengers is complemented by external inputs of the ecological services provided by the Spanish vulture population was added to the through supplementary feeding sites and in smaller quantities by other small species total for the European population . The cost of removing this carrion for farmers and 19,24,46–49 such as birds, reptiles and small mammals and micromammals . Available authorities was calculated as the cost for the removal and transport of each ton of grass biomass is enough to cover the energetic requirements of wild and domestic carrion: an average of 89 EUR, and the cost of disposal in authorised plants, 76.3 50,51 58 ungulates and has not been considered as a limiting factor. EUR . This allowed the economic estimate of the ecological services performed by With respect to the interspecific hierarchies in the access and exploitation of avian scavengers to be compared with the cost of carrion removal. carrion, we consider that Egyptian and cinereous vultures are the first species to access the carrion and griffon and bearded vultures the last (A.M. unpubl. data). Statistical analyses. Normality of the data was confirmed using the Kolmogorov– Intraspecific age hierarchies are not differentiated in access to food, since the Smirnov test, before a one-way ANOVA to compare the annual population trend of 52–54 behavioral patterns observed at feeding sites may differ from the random avian scavengers obtained in different management scenarios. This analysis took into distribution of food in the wild. account the animal biomass as a dependent variable while the species were factors. When resources are limited, they are distributed randomly according to the When ANOVA tests were significant, a further test of homogeneity was performed number of individuals of each species competing for the same type of food and using Duncan’s test to identify inter-group differences. according to the amount of resources they need. The model also takes into account the presence of a non-breeding population (Table S2) consisting of fledglings produced by the breeding population. These are counted individually and when they reach 1. Loreau, M., Naeem, S. & Inchausti, P. Biodiversity and ecosystem functioning: breeding maturity, two individuals become a breeding pair occupying a new territory. synthesis and perspectives, Oxford University Press, 2002. SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 6 www.nature.com/scientificreports 2. Loreau, M. Linking biodiversity and ecosystems: towards a unifying ecological 37. Dupont, H, Mihoub, J. B., Bobbe, S. & Sarrazin, F. Modelling the consequences of theory. Philos. Trans. R. Soc. B 36, 49–60 (2010). farmer’s carcass disposal practices on scavengers’ ecological service. J. Appl. Ecol. 3. Naeem, S. et al. Biodiversity, ecosystem functioning and human wellbeing: an 49, 404–411 (2012). ecological and economic perspective, Oxford University Press, 2009. 38. Olea, P. & Mateo-Toma´ s, P. The role of traditional farming practices in ecosystem 4. Sekercioglu, C. H., Daily, G. C. & Ehrlich, P. R. Ecoystem consequences of bird conservation: the case of transhumance and vultures. Biol. Conserv. 142, declines. Proc. Ntl. Acad. Sci. USA 101, 18042–18047 (2004). 1844–1853 (2009). 5. Whelan, C. J., Wenny, D. G. & Marquis, R. J. Ecosystem services provided by birds. 39. Robb, G. N., McDonald, R. A., Chamberlain, D. E. & Bearhop, S. Food for thought: Ann. New York Acad. Sci. 1134, 25–60 (2008). supplementary feeding as a driver of ecological change in avian populations. 6. Wenny, D. G. et al. The need to quantify ecosystem services provided by birds. Front. Ecol. Environ. 6, 476–484 (2008). Auk 128, 1–14 (2011). 40. Le Gouar, P. et al. Roles of survival and dispersal in reintroduction success of 7. DeVault, T. L., Rhodes, O. E. & Shivik, J. A. Scavenging by vertebrates: behavioral, Griffon vulture (Gyps fulvus). Ecol. Appl. 18, 859–872 (2008). ecological, and evolutionary perspectives on an important energy transfer 41. Grande, J. M. et al. Survival in a long-lived territorial migrant: effects of life-history pathway in terrestrial ecosystems. Oikos 102, 225–234 (2003). traits and ecological conditions in wintering and breeding areas. Oikos 118, 8. Oaks, L. et al. Diclofenac residues as the cause of vulture population declines in 580–590 (2009). Pakistan. Nature 427, 630–633 (2004). 42. Margalida, A. Poison baits and funding cuts: a deadly mix. Science (In press). 9. Green, R. E. et al. Diclofenac poisoning as a cause of vulture population declines 43. Sutherland, W. J. & Freckleton, R. P. Making predictive ecology more relevant to across the Indian subcontinent. J. Appl. Ecol. 41, 793–800 (2004). policy makers and practitioners. Philos. Trans.R. Soc. B 367, 322–330 (2012). 10. Thiollay, J. M. Raptor declines in West Africa: comparisons between protected, 44. Wilson, H. B., Joseph, L. N., Moore, A. L. & Possingham, H. P. When should we buffer and cultivated areas. Oryx 41, 322–329 (2007). save the most endangered species? Ecol. Lett. 14, 886–890 (2011). 11. Naidoo,V., Wolker,K., Cuthbert, R.&Duncan, N. Veterinarydiclofenacthreatens 45. Cardona, M. et al. A P-System based model of an ecosystem of some scavenger Africa’s endangered vulture species. Regul. Toxicol. Pharm. 53, 205–208 (2009). birds. Lect. Notes Comput. Sc. 5957, 182–195 (2010). 12. Virani, M. Z., Kendall, C., Njoroge, P. & Thomsett, S. Major declines in the 46. Dona´ zar, J. A. The Iberian Vultures. Biology and Conservation, J.M. Reyero Editor, abundance of vultures and other scavenging raptors in and around the Masai Mara ecosystem, Kenya. Biol. Conserv. 144, 746–752 (2011). 47. Margalida, A., Bertran, J. & Heredia, R. Diet and food preferences of the ´ ´ 13. Donazar, J. A., Margalida, A., Carrete, M. & Sanchez-Zapata, J. A. Too sanitary for endangered Bearded vulture Gypaetus barbatus: a basis for their conservation. Ibis vultures. Science 326, 664 (2009). 151, 235–243 (2009). ´ ´ 14. Cortes-Avizanda, A., Carrete, M. & Donazar, J. A. Managing supplementary 48. Margalida, A. et al. Long-term relationship between diet and breeding success in a feeding for avian scavengers: guidelines for optimal design using ecological declining population of Egyptian Vulture. Neophron percnopterus Ibis 154, criteria. Biol. Conserv. 143, 1707–1715 (2010). 184–188 (2012). 15. Tella, J. L. Action is needed now, or BSE crisis could wipe out endangered bird of ´ ´ 49. Donazar, J. A., Cortes-Avizanda, A. & Carrete, M. Dietary shifts in two vultures prey. Nature 410, 408 (2001). after the demise of supplementary feeding stations: consequences of the EU 16. Margalida, A., Dona´ zar, J. A., Carrete, M. & Sa´ nchez-Zapata, J. A. Sanitary versus sanitary legislation. Eur.J. Wildl. Res. 56, 613–621 (2010). environmental policies: fitting together two pieces of the puzzle of European 50. Fillat, F. Gestio´ n semi-extensiva de prados y pastos europeos ricos en especies: vulture conservation. J. Appl. Ecol. 47, 931–935 (2010). caso particular de los Pirineos espan˜ oles. Pastos 33, 171–215 (2006). 17. Margalida, A., Carrete, M., Sa´ nchez-Zapata, J. A. & Dona´ zar, J. A. Good news for 51. Garc´ı a-Martı´ nez, A., Olaizola, A. & Bermue´ s, A. Trajectories of evolution and European vultures. Science 335, 284 (2012). drivers of change in European mountain cattle farming systems. Animal 3, 18. Dona´ zar, J. A, Margalida, A. & Campio´ n, D. Vultures, feeding stations and sanitary 152–165 (2009). legislation: a conflict and its consequences from the perspective of conservation 52. Bose, M. & Sarrazin, F. Competitive behaviour and feeding rate in a reintroduced biology. Sociedad de Ciencias Aranzadi 2009. population of Griffon Vultures . Gyps fulvus Ibis 149, 490–501 (2007). 19. Margalida, A.,Colomer,M.A.&Sanuy, D. Canwildungulatecarcassesprovide 53. Bose,M., Duriez,O.&Sarrazin F. 2012 Intra-specific competition in foraging griffon enough biomass to maintain avian scavenger populations? An empirical assessment vultures:1.The dynamics of feedingingroups. Bird Study 59, 182–192 (2012). using a bio-inspired computational model. PLoS One 6, e20248 (2011). 54. Duriez, O., Herman, S. & Sarrazin, F. 2012 Intra-specific competition in foraging 20. Bousquet, F. C. & Le Page, C. Multi-agent simulations and ecosystem griffon vultures: 2. the influence of supplementary feeding management. Bird management: a review. Ecol. Model. 176, 313–332 (2004). Study 59, 193–206 (2012). 21. Pa˘un, G. Computing with membranes. J. Comp. Syst. Sci. 61, 108–143 (1998). 55. Houston, D. C. & Copsey, J. A. Bone digestion and intestinal morphology of the 22. Pa˘un, G., Rozenberg, G. & Salomaa, A. The Oxford Handbook of Membrane Bearded Vulture. J. Raptor Res. 28, 73–78 (1994). Computing, Oxford University Press, 2010. 56. Prinzinger et al. Energy metabolism and body temperature in the Griffon Vulture 23. Cardona, M. et al. Modelling ecosystems using P Systems: The Bearded Vulture, a (Gyps fulvus) with comparative data on the Hooded Vulture (Necrosyrtes case study. Lect. Notes Comput. Sc. 5391, 137–156 (2009). monachus) and the White-backed Vulture (Gyps africanus). J. Ornithol.143, 24. Colomer, M. A., Margalida, A., Sanuy, D. & Pe´ rez-Jime´ nez, M. J. A bio-inspired 456–467, (2002) computing model as a new tool for modeling ecosystems: the avian scavengers as a 57. King, J. R. & Farner, D. S. Energy metabolism, thermoregulation and body case study. Ecol. Model. 222, 33–47 (2011). temperature. In, Marshall, J. A. (Ed.) Biology and comparative physiology of birds 25. Dupont, H., Mihoub, J. B., Becu, N. & Sarrazin, F. Modelling interactions between Vol. II New York: Academic Press, pp. 215–288, 1961. scavenger behaviour and farming practices: Impacts on scavenger population and 58. Boumellasa, H. Rapaces ne´ crophages: concilier conservation de l’espe` ce et ecosystem service efficiency. Ecol. Model. 222, 982–992 (2011). minimisation des de´ penses, vers un reinforcement du lien Agriculture- 26. Ostfeld, R. S. & Keesing, F. Pulsed resources and community dynamics of Environment. University Paris X 2004. consumers in terrestrial ecosystems. Trends Ecol. Evol. 15, 232–237 (2000). 27. Herna´ ndez, M. & Margalida, A. Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus)populationinSpain. Ecotoxicology 7, 264–272 (2008). 28. Gangoso, L. et al. Long-term effects of lead poisoning on bone mineralization in Acknowledgements vultures exposed to ammunition sources. Environ. Pollut. 157, 569–574 (2009). We gratefully acknowledge the Natural Computing Group at Sevilla University for their 29. Oro, D. et al. Testing the goodness of supplementary feeding to enhance help with the design of the simulator. AM was supported by the Departament d’Agricultura, population viability in an endangered vulture. PLoS One 3, e4084 (2008). Ramaderia, Pesca i Medi Natural of Generalitat de Catalunya and Ministerio de Medio 30. Herna´ ndez, M. & Margalida, A. Poison-related mortality effects in the endangered Ambiente. Egyptian Vulture (Neophron percnopterus) population in Spain: conservation measures. Eur. J. Wildl. Res. 55, 415–423 (2009). 31. Herna´ ndez, M. & Margalida, A. Assessing the risk of lead exposure for the Author contributions conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) A.M. and M.A.C. designed the experiment, collected all the data, performed analysis of the population. Environ. Res. 109, 837–842 (2009). data, and wrote the manuscript. Both the authors discussed the results and commented on ´ ´ 32. Margalida, A., Oro, D., Cortes-Avizanda, A., Heredia, R. & Donazar, J. A. the manuscript. Misleading population estimates: biases and consistency of visual surveys and matrix modelling in the endangered Bearded Vulture. PLoS One 6, e26784 (2011). 33. Margalida, A., Campio´ n, D. & Dona´ zar, J. A. European vultures’ altered Additional information Supplementary information accompanies this paper at http://www.nature.com/ behaviour. Nature 480, 457 (2011). 34. Olson, Z. J., Beasley, J. C., DeVault, T. L. & Rhodes, E. jr. Scavenger community scientificreports response to the removal of a dominant scavenger. Oikos 121, 77–84 (2011). Competing financial interests: The authors declare no competing financial interests. 35. Deygout, C., Sarrazin, F., Gault, A. & Bessa-Gomes, C. Modeling the impact of License: This work is licensed under a Creative Commons feeding stations on vulture scavenging service efficiency. Ecol. Model. 220, Attribution-NonCommercial-NoDerivative Works 3.0 Unported License. To view a copy 1826–1835 (2009). of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/ 36. Carrete, M., Dona´ zar, J. A. & Margalida, A. Density-dependent productivity depression in Pyrenean Bearded Vultures: implications for conservation. How to cite this article: Margalida, A. & Colomer, M.A. Modelling the effects of sanitary Ecol.Appl. 16, 1674–1682 (2006). policies on European vulture conservation. Sci. Rep. 2, 753; DOI:10.1038/srep00753 (2012). SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 7 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Scientific Reports Springer Journals

Modelling the effects of sanitary policies on European vulture conservation

Scientific Reports , Volume 2 (1) – Oct 18, 2012

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Springer Journals
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Copyright © 2012 by The Author(s)
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Science, Humanities and Social Sciences, multidisciplinary; Science, Humanities and Social Sciences, multidisciplinary; Science, multidisciplinary
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Abstract

Modelling the effects of sanitary policies on European vulture conservation SUBJECT AREAS: 1 a ` 2 Antoni Margalida &M Angels Colomer BIODIVERSITY COMPUTATIONAL BIOLOGY AND BIOINFORMATICS Division of Conservation Biology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse, 6, 3012, Bern, Switzerland, Department of Mathematics, University of Lleida, Av. Alcalde Rovira Roure, 191, 25198, Lleida, Spain. ZOOLOGY ANIMAL BEHAVIOUR Biodiversity losses are increasing as a consequence of negative anthropogenic effects on ecosystem dynamics. However, the magnitude and complexity of these effects may still be greatly underestimated. Received Most Old World vultures have experienced rapid population declines in recent years. In Europe, their immediate conservation depends on changes in health regulations affecting the availability of food provided 6 June 2012 by domestic carcasses. Information is lacking on the effects of a hypothetical food shortage on the Accepted population dynamics of vultures, and is necessary to assess the potential impacts of policy decisions on 1 October 2012 future changes in biodiversity and ecosystem services. A novel computational model (P-systems) was used to model these effects, forecasting a rapid decline in the Eurasian griffon vulture (Gyps fulvus). By contrast, Published vulture species with greater plasticity in their dietary range appeared less sensitive to declining food 18 October 2012 availability. This study extends our understanding of vulture ecosystem services, which have social and economic implications. Correspondence and uring the last decade, the relationship between biodiversity and ecosystem function has emerged as an requests for materials important issue due to the strong connection between the ecological mechanisms that maintain biodi- 1–3 should be addressed to D versity in a community and their ecological consequences for ecosystem function . However, few eco- A.M. (antoni. system service assessment approaches have direct utility in political, social and ecological decision-making. Ecosystem services are natural processes that benefit humans, with birds contributing to four of the service types margalida@iee.unibe. (provisioning, regulating, cultural, and supporting services) recognised by the UN Millennium Ecosystem ch) 4–6 Assessment . Avian scavengers are part of the detrital food web of ecosystems and they provide the important ecological service of recycling carrion biomass to prevent the accumulation of dead biomass, thereby contributing to waste removal, disease regulation, and nutrient cycling . At the start of the 21st century, European avian scavenger communities were one of the few exceptions to the 8–12 global decline in Old World avian scavenger birds . Asian and, to a lesser degree African, vulture populations 8–12 declined as a consequence of ingestion of veterinary drugs and due to illegal poisoning . On the contrary, European vulture populations maintained or increased their numbers . However, the detection of variant (vCJD) and new variant (nvCJD) Creutzfeldt-Jakob disease in humans, which was acquired from cattle infected by bovine spongiform encephalopathy (BSE), led to sanitary legislation (Regulation CE 1774/2002) that greatly restricted the use of animal by-products that were not intended for human consumption. Thus, all carcasses of domestic animals had to be collected from farms and transformed or destroyed in authorised plants, although only 80% of domestic carcasses are currently recovered by specialised companies . In Spain, since 2006 supplementary feeding points for vultures, supplied by intensive farming, have also greatly diminished (280%) as a consequence of sanitary regulations . The disparity between sanitary and environmental policies, i.e., to eliminate corpses 3,15,16 versus to conserve scavenger species , led to several European dispositions that regulated the use of animal by- 13,16 products as food for necrophagous birds . Revised regulations on the use of animal by-products that are not intended for human consumption were made by the end of 2011 and they will be applied during 2012 . However, there has been no assessment of food availability or of the effects of different trophic scenarios on the population dynamics of European vultures. Recently, as a consequence of food shortages, several demographic warning signals have been documented, including a halt in population growth, decreased breeding success, and an apparent increase in mortality among younger age classes . However, empirical analyses of the relationships between vulture population dynamics and food availability have only assessed the role of wild ungulates . Modelling the effects of sanitary laws on population trends may provide evidence that can inform the design of policies that are compatible with vulture conservation. Multi-agent models are necessary for modelling population dynamics relative to demographic parameters and food availability such as P Systems, which is a SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 1 www.nature.com/scientificreports include the carrying capacity, suitable areas with potential for re- colonisation, or the benefits of supplying supplementary feeding sites. The present study used P systems to test the effects of variable levels of food availability over 21 years, on the population viability and conservation of four European vultures (the Eurasian griffon vulture Gyps fulvus, the Egyptian vulture Neophron percnopterus and the cinereous vulture Aegypius monachus considered as meat- eaters and the bearded vulture Gypaetus barbatus, considered a specialized bone-eater) as a consequence of sanitary regulations (see Methods). Taking into account a well-studied region in northern Spain (with 10 subareas) inhabited by the four European vulture species, we model the effects of available domestic carcasses (testing four initial scenarios of 100%, 50%, 25%, and 0% of domestic car- casses available in the field and separating meat and bone remains available as a consequence of the different dietary habits between meat and bone consumers) on their population dynamics. The 100% scenario represents conditions before the outbreak of BSE (,2002) while the 0%–25% scenarios represent the current condi- tions, depending on the area considered, as food limitations progres- sively worsened between 2006 and 2012. Future changes to the sanitary legislation may modify the availability of domestic carcasses and will probably progressively increase food availability, shifting conditions from 0–25% to 50% and expected to ultimately reach pre-outbreak conditions (100% of domestic carcasses available). Spain contains the most important European vulture populations (approximately 95% of their total numbers) and the results may have particularly important conservation applications in the assessment of their ecosystem services, the function of supplementary feeding sites, the carrying capacity, or the feeding resources available in an ecosystem during future reintroduction projects. The hypothetical effects of sanitary restrictions on vulture conservation were esti- mated and this method provides a computational tool that could be applied in other countries. Results Temporal and spatial food availability in different management scenarios. Meat was predicted to be the major factor limiting the survival of avian scavengers during winter and summer (Figure 1). In the breeding season (winter), the available food was predicted to be insufficient to cover energetic requirements in two areas with half the domestic carcasses available (PJ and AU), which increased to three (also AR) with a quarter of the domestic carrion available (current situation) and six (also PJ, N and S) without domestic carcasses Figure 1 | Spatial and temporal estimate of the difference between the available (with insufficient bone biomass in N). In the summer biomass estimated by the model and the energetic requirements for the scenario, food availability was predicted to be higher due to current avian scavenger population standardized by surface unit transhumance. However, the food available was also predicted to (expressed in calories per km ) in the ecosystem, for each of 10 be insufficient in one area (PJ) with half the domestic carcasses, municipalities in Catalonia, Northern Spain, according to the four increasing to three areas (also AR and AU) with a quarter of the scenarios of food availability considered (100%, 50%, 25% and 0% of food domestic carrion available to vultures and five (also N and S) provided by domestic ungulates). without domestic carcasses. From a population perspective, these three areas (AR, PJ and AU) were the most important for the avian computational modelling paradigm that was inspired by the func- scavenger guild because the areas with a quarter of the domestic 21,22 tioning of cells working in parallel . This technique was applied carcasses available contain 59% of the bearded vulture population, recently in several approaches to modelling the dynamics of scav- 56% of Egyptian vultures, 71% of griffon vultures, and 100% of 19,23,24 enger species . However, these studies did not consider future cinereous vultures in the study area. trends in vulture populations under different trophic scenarios. They also failed to take into account the temporal distribution of feeding Population dynamics in different management scenarios. The po- resources in different breeding seasons (i.e., winter vs. summer) and pulation trends of bearded, Egyptian and cinereous vultures were the spatial scale of areas where the resources were homogenously dis- predicted to increase in relation to the current situation and were tributed. This theoretical approach is valid, but the results obtained similar across the four scenarios considered (bearded vulture: F 5 3,83 are limited from an ecological viewpoint because the models failed 2.61, P 5 0.057; Egyptian vulture: F 5 0.12, P 5 0.95; cinereous 3,83 to detect spatial changes in species distributions or temporal limita- vulture: F 5 0.71, P 5 0.55, Figure 2) except for the griffon 3,83 tions in food availability. Managers and conservationists require vulture, for which significant differences were found (F 5 3,83 more detailed data to accurately determine parameters for optimis- 117.54, P 5 0.0001). The model predicted differences in the ing investment in the management of resources. These parameters groups formed with 50% and 100% of domestic carcasses available SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 2 www.nature.com/scientificreports movement of animals between neighbouring areas (Figure 3). It was predicted that most individuals would not colonize new areas, so the population balance of the species in each area was not predicted to be affected (a trend similar to the 100% scenario) and only some indi- viduals could colonize unoccupied areas such as VA and C. The growth trend with 50% domestic carcass availability is similar to 100% availability during the first 12 years. After this time, the food resources in the receiving areas (VA, C, B and N) were predicted to be insufficient for all pairs such that there is a significant decrease in griffon vulture populations in areas AR, PJ and AU and population stability only occurred with an increase in the biomass provided by wild ungulate populations. Benefits of vulture ecological services. On average, the Spanish vul- ture populations were estimated to remove 133.6–200.5 t of bones and 5,550.7–8,326 t of meat each year. Th e corresponding economic savings of natural carrion removal were estimated at a minimum of 907,679– 1,488,719 EUR, while vulture populations throughout the entire European Union may contribute an annual cost reduction of 972,915– 1,595,715 EUR. The animal biomass consumed by avian scavengers and removed from the ecosystem in the study area (assuming 50–75% of the diet is based on domestic ungulates) was estimated at 4.236– .38 t of bones and 176.73–265.10 t of meat. This constituted annual bene- fits estimated at 28,900–47,400 EUR for farmers and authorities. Discussion Sudden changes in the availability of food may cause changes in the population dynamics of species . The current study highlights the consequences of different levels of food availability on the population dynamics of an avian scavenger guild, indicating the halt and sub- sequent decline in population growth of the most meat-dependent species, i.e., the griffon vulture. The model predicted meat biomass to be the major limiting factor whereas the dietary plasticity of the other species allowed them to avoid declining population trends, as did their specific dietary habits (small animals for the Egyptian vul- ture and bones for the bearded vulture) and low densities. From a conservation perspective, these results suggest that the population growth of the most endangered species (Egyptian, cinereous, and bearded vultures) will continue in the current scenario, despite san- 13,16 itary legislation that limits food resources , given that a quarter of domestic ungulates are available in the ecosystem. However, this trend may be reversed by an increased effect of non-natural mortality Figure 2 | Predicted population trends for the four avian scavengers in when considering the effects of factors, such as illegal poisoning or 27–31 the study area, for each of the four scenarios tested, expressed as the lead poisoning, on breeding success and survival . These problems percentage of domestic ungulate carcasses available in the ecosystem. currently affect the threatened bearded vulture and they appear to Note the different y-axis scales. have stabilised their populations via non-natural mortality effects on adult survival . In addition, given the difficult nature of assessing the compared to the 25% and 0% scenarios (Duncan’s test, P , 0.05). numbers and age structure of the non-breeding population for mod- With a quarter of domestic carcasses available, a 14% reduction in the elling demographic trends and movements, and because these indi- griffon vulture population was forecast during the first year, after viduals mainly feed at supplementary feeding sites , our model only which their numbers were expected to become stable. In contrast, considered the immature population (chicks reared). Thus, we can without domestic carcasses (0% scenario) a sudden decrease is ex- consider our model conservative because a portion of available food pected with a reduction of 80% in griffon vulture populations, could benefit other non-breeding individuals. stabilizing at around 200–250 pairs. However, no global differences In recent years, the Spanish griffon vulture population has experi- were found between 100% and 50% domestic carcass availability (P enced decreases in their breeding parameters and changes in the 5 0.44), although the model indicated that statistically significant spatial distribution of the breeding and non-breeding population, differences would be detected after the 12th year (F 5 603.60, P while there have also been increases in their number of aggressive 1,268 , 0.0001) when there would be a reduction in the population growth interactions with live livestock and an increase in the mortality of 18,33 of griffon vultures. their young . By contrast, other species have increased their popula- 27,30 Assuming the network movements estimated in the study area tions, although illegal poisoning has affected some subpopulations . (Figure 3), the predicted response of griffon vulture populations to It is speculated that these changes were due to food shortages, the different scenarios studied is shown in Figure 4. With 25% or 0% although no empirical evidence is presented to support this hypo- of domestic carcasses available, a significant reduction of the popu- thesis. For the first time, the current study suggests that food limita- lation was forecasted in all study areas. The decrease was especially tions mainly affect griffon vultures. According to the model, vultures important in populated areas (AR, PJ and AU). A decrease of 50% in might respond to food shortages by shifting their spatial distribu- the contributions of domestic carcasses was predicted to promote tion leading to population decline (in the case of the 0% and 25% SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 3 www.nature.com/scientificreports Figure 3 | (a) Possible avian scavenger foraging movements between areas, when there is a lack ofresources. The continuous lines are the possible movements of the bearded vulture (Gypaetus barbatus), Egyptian vulture (Neophron percnopterus), and cinereous vulture (Aegypius monachus). The dashed line represents the Eurasian griffon vulture (Gyps fulvus). (b) Distribution of the ten areas considered in the study: VA: Val d’Aran; AR:Alta Ribagorc¸a; PJ: Pallars Jussa`; PS: Pallars Sobira`; AU: Alt Urgell; C: Cerdanya; R: Ripolle`s; B: Bergueda`; S: Solsone`s; N: Noguera. A, F, and PPO correspond to peripheral areas (alternative environments in the model) in which the population might obtain alternative food resources outside of the study area (see more details in Methods). scenarios) and these effects could accelerate in coming years if food closely resembling actual ecosystems, thereby preventing behaviou- 19,34,36,37 limitations continue. These regressive scenarios suggested by the ral changes or any negative effects on population dynamics . model do not imply an increase in mortality. Instead, individuals were Based on the carrying capacity and the population trend observed, predicted to abandon the ecosystem to search for suitable alternative supplementary feeding programs appear to be unnecessary in areas where food and breeding sites are available, when food resources hypothetical scenarios where half and 100% of domestic carcasses are insufficient and the carrying capacity at small spatial scales are available. The latter scenario corresponds to that present in the approaches the maximum levels. From an ecological perspective, grif- period before the establishment of sanitary regulations (progressively fon vultures are the dominant species of the avian scavenger guild in a applied since 2006), which could be representative of most Medi- competitive scenario because they can monopolise resources to the terranean populations that are characterised by widespread grazing 14 19,38 detriment of other species . This suggests that the provision of sup- and the food resources provided by wild ungulates . Thus, this plementary feeding sites as a stopgap measure to meet food deficits study should be taken into account by managers and conservationists would mainly favour this species. However, other ecological effects on if the sanitary legislation is amended in the future. In fact, the pres- the ecosystem of a population decline are unknown and the conse- ence of carcasses in the field as a consequence of extensive grazing is quences may be a new concern for managers and policy-makers .The considered to be the most useful and economic method of managing 13,17 ecological services provided by vultures have an important role and avian scavenger populations . This is an important issue for man- the regular use of feeding stations by these species could reduce eco- agers and policy-makers because solutions to the management of 18,25,35 logical service provision in terms of scavenging . In addition, the European vulture populations are based on an assumption that role of griffon vultures as facilitator species preparing carrion for other food shortages due to sanitary regulations should be compensated facultative and obligate scavengers is unknown but may have cascade for with supplementary feeding sites. This management approach effects within the ecosystem. may have detrimental consequences because a patchy distribution of A more advisable management measure would be to reduce the resources can artificially modify the habitat quality, with subsequent 36,39 amount of food provided at large feeding stations and promote negative effects on population dynamics . Thus, the carrying the creation of smaller sites that simulate a trophic scenario by more capacity should be regulated by feeding resources provided in the SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 4 www.nature.com/scientificreports Figure 4 | Predicted population trend of the Eurasian griffon vulture in the different areas, according the four scenarios of domestic carcasses available. The population increase in several areas in which the species is initially absent (VA and C) or of low densities is a consequence of spatial changes related with food shortages or maximum carrying capacity. ecosystem despite the long tradition in several countries of artificial reintroduction projects, thereby allowing managers to improve the food handling via supplementary feeding sites . However, the sens- success rate of reintroductions. This is particularly important for itivity of some species (several threatened) in terms of demographic avian scavengers because they are highly dependent on carrion 29,40,41 parameters, such as adult survival due to the presence of non- resources, the availability of which can be modified by humans by natural mortality factors (mainly illegal poisoning) , could increase direct management, e.g., hunting of wild ungulates, the sanitary mortality rates and destabilise populations. Given that supplement- legislation for domestic ungulates, or the establishment of a network of supplementary feeding sites. Given the global decline affecting Old ary feeding increases pre-adult survival , this method may continue to favour the most endangered species, especially if the quantity World vultures , the availability of robust tools can help managers to 43,44 supplied is reduced and its unpredictability is increased. optimise the investment of economic resources and to identify the most appropriate conservation measures. The results of this study are relevant to future reintroduction and conservation projects. Our model is capable of identifying the spatial and temporal distribution of feeding resources, thereby facilitating Methods the planning and optimisation of the most appropriate management Model building and assumptions. Using a Population Dynamic P System (see approach, including supplementary feeding activities, to support Supplementary Information) we defined a model allowing the study of the ecosystem dynamics in a zone subdivided into 10 areas inhabited by four avian scavengers whose the most food-poor areas where necessary. The application of this diet depends on the food provided by the carcasses of wild and domestic ungulates. model to reintroduction projects demonstrates that calculations of 19,24 For the validation of the model , we used census data obtained in the study area food availability can provide guidelines when establishing the car- 24,25 between 1994 and 2008 taking into account the inter-annual variation in rying capacity to optimise economic investment. In the case of avian demographic parameters and density-dependent effects affecting the population scavengers, food availability studies can identify problems prior to trends observed. SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 5 www.nature.com/scientificreports Besides natural and non-natural mortality, the model assumes that an ungulate dies when it lacks physical space as a consequence of its carrying capacity. In the case of avian scavengers, if a species has insufficient resources it moves to nearby areas. It returns to the starting point if there are food limitations but no space limitations. An individual colonises a new area if insufficient space is available. Scavengers can choose from more than one destination if they need to move, and they select one randomly. If the alternative area selected lacks resources, this random sampling continues until resources are found, leaving the ecosystem if resources are not found. If there is an avian scavenger who lacks sufficient resources after carrying out the rules of feeding and controlling for the maximum density of each species, it will move to another environment, running the feeding process and/or density previously unrealized for this animal. If space is not a limiting factor, they will return to the source environment or otherwise colonize a new area. When defining the model, a directed network-graph of avian scavenger movement is specified (Figure 3). The avian scavengers move to search for food in the peripheral areas (A, F, PPO) when feeding resources in the regular home ranges are insufficient. For the foraging areas, we consider the maximum linear foraging movement from the nest for the griffon vulture to be 90 km, 40 km for the bearded vulture, 15 km for the Egyptian vulture and 60 km for the cinereous vulture (A.M. unpubl. data). The model takes into account that each species takes advantage of the resources close to their nesting area and widens the radius of their movements as they deplete. The amount of meat and bones consumed by scavengers depends on the season. The excess meat disappears from the ecosystem at the end of each period (summer or winter). The model assumes that 20% of the unconsumed bones remain available in the ecosystem, because bones can be preserved for up to 10 times longer than meat . Populations of animals will generally grow exponentially if they have sufficient resources, although this growth is restricted due to limitations in physical space, which supports the maximum carrying capacity used in the model (Table S1). The objective of the final module is to restore the initial configuration to restart the loop. Running the model requires some initial parameters, so these are entered before returning an output. The evolution rules used by the model are run for each individual and they are Figure 5 | Scheme of the model. The model takes into account two executed simultaneously for all individuals. Thus, the system operates in parallel, periods (summer and winter) and the basic processes of reproduction, which means there can be competition when animals of the same or different species mortality, and feeding. The scavenger birds forage in others areas when share resources. The values of the parameters used in the model were derived from the 19,24 insufficient resources are available (i.e., they move). If food is scarce, the bibliography . The running model is detailed in Supplementary Information. animals take the food and return to their initial area. They change territory Management scenarios. Several possible scenarios were modelled by testing the if space is scarce. The carrying capacity of each area is limited and it is impact of different food availability regimes to elucidate their potential effects on necessary to control the number of animals present. Before repeating the population projections over time. Four initial scenarios were considered that depended loop, it is necessary to restore the initial configuration. Two executions of a on the hypothetical biomass provided by domestic ungulates. Thus, the 100% scenario 13,16 represented the ecosystem function prior to the application of sanitary regulations loop are equivalent to the passage of one year in the ecosystem. where all domestic and wild ungulate carcasses were available to the avian scavenger guild. The 50% scenario represented a scenario where only half of the hypothetical food The model consists of a loop with six modules (Figure 5). One year in the ecosystem resources provided by domestic carcasses were available. The 25% scenario might involves running the loop twice, i.e., once for the summer period (four months) and reflect a scenario that is similar to the current situation because approximately 80% of once for the winter season (eight months). The model starts with the run of the carcasses are recovered and destroyed by specialist companies. Finally, the 0% scenario reproduction module. The species are modelled with only one reproductive period simulates an ecosystem where food is provided only by wild ungulates. each year. While the population of wild animals is a dynamic system conditioned by First, the biomass was calculated provided for each subzone by subtracting the environmental and ecological factors, domestic animals are controlled by humans megacalories available from the energetic requirements of the avian scavengers such that there are significant fluctuations in the population between the summer and inhabiting each subzone. This provided a picture of the surplus or constraints on food winter as a consequence of transhumant movements. availability from a spatial perspective. Second, the population trend was simulated In the reproduction module, all breeding age females can reproduce successfully in with consideration for the demographic parameters of hypothetical growth in each a probabilistic way. After the application of reproduction rules, the mortality module species (see Supplementary Information) and the availability of biomass provided by is carried out; there are two possible causes of death, i.e., natural mortality (e.g., the different scenarios plus the biomass provided by wild ungulates and feeding senescence or accidents) and non-natural mortality (e.g., hunting or illegal poison- stations. Data used for the a posteriori statistical analyses were obtained by using the ing). In most ungulate species (except wild boar), hunting practices are focused on model to simulate the population dynamics (21 years and a total of 50 replicates) in a males, producing variations in the sex-ratio. The model takes into account temporal probabilistic manner, which reflected the random behaviour of the natural situation. and sex-ratio mortality variations influencing population growth and the biomass provided. In the following module the model takes into account whether food and Quantifying carrion removal vs. vulture ecological services. To estimate the carrying capacity are sufficient in the environment occupied to maintain their potential biomass that avian scavengers can remove from the ecosystem, the annual presence. energetic requirements of each individual and species were determined based on their 48,56,57 For each vulture species we obtained parameters on breeding, demography and standard metabolism , and then multiplied by the number of individuals present energetic requirements according to their metabolism (Supplementary Information in the ecosystem. It was estimated that 50–75% of the diet of avian scavengers was Table S2), mortality and the biomass that dead wild ungulates provided in the field, composed of domestic ungulate remains, which was based on the animal biomass separating bone and meat remains in accordance with the different dietary habits of range (its natural removal from the ecosystem). To compare the results, this estimate the species . The diet of avian scavengers is complemented by external inputs of the ecological services provided by the Spanish vulture population was added to the through supplementary feeding sites and in smaller quantities by other small species total for the European population . The cost of removing this carrion for farmers and 19,24,46–49 such as birds, reptiles and small mammals and micromammals . Available authorities was calculated as the cost for the removal and transport of each ton of grass biomass is enough to cover the energetic requirements of wild and domestic carrion: an average of 89 EUR, and the cost of disposal in authorised plants, 76.3 50,51 58 ungulates and has not been considered as a limiting factor. EUR . This allowed the economic estimate of the ecological services performed by With respect to the interspecific hierarchies in the access and exploitation of avian scavengers to be compared with the cost of carrion removal. carrion, we consider that Egyptian and cinereous vultures are the first species to access the carrion and griffon and bearded vultures the last (A.M. unpubl. data). Statistical analyses. Normality of the data was confirmed using the Kolmogorov– Intraspecific age hierarchies are not differentiated in access to food, since the Smirnov test, before a one-way ANOVA to compare the annual population trend of 52–54 behavioral patterns observed at feeding sites may differ from the random avian scavengers obtained in different management scenarios. This analysis took into distribution of food in the wild. account the animal biomass as a dependent variable while the species were factors. When resources are limited, they are distributed randomly according to the When ANOVA tests were significant, a further test of homogeneity was performed number of individuals of each species competing for the same type of food and using Duncan’s test to identify inter-group differences. according to the amount of resources they need. The model also takes into account the presence of a non-breeding population (Table S2) consisting of fledglings produced by the breeding population. These are counted individually and when they reach 1. Loreau, M., Naeem, S. & Inchausti, P. Biodiversity and ecosystem functioning: breeding maturity, two individuals become a breeding pair occupying a new territory. synthesis and perspectives, Oxford University Press, 2002. SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 6 www.nature.com/scientificreports 2. Loreau, M. Linking biodiversity and ecosystems: towards a unifying ecological 37. Dupont, H, Mihoub, J. B., Bobbe, S. & Sarrazin, F. Modelling the consequences of theory. Philos. Trans. R. Soc. B 36, 49–60 (2010). farmer’s carcass disposal practices on scavengers’ ecological service. J. Appl. Ecol. 3. Naeem, S. et al. Biodiversity, ecosystem functioning and human wellbeing: an 49, 404–411 (2012). ecological and economic perspective, Oxford University Press, 2009. 38. Olea, P. & Mateo-Toma´ s, P. The role of traditional farming practices in ecosystem 4. Sekercioglu, C. H., Daily, G. C. & Ehrlich, P. R. Ecoystem consequences of bird conservation: the case of transhumance and vultures. Biol. Conserv. 142, declines. Proc. Ntl. Acad. Sci. USA 101, 18042–18047 (2004). 1844–1853 (2009). 5. Whelan, C. J., Wenny, D. G. & Marquis, R. J. Ecosystem services provided by birds. 39. Robb, G. N., McDonald, R. A., Chamberlain, D. E. & Bearhop, S. Food for thought: Ann. New York Acad. Sci. 1134, 25–60 (2008). supplementary feeding as a driver of ecological change in avian populations. 6. Wenny, D. G. et al. The need to quantify ecosystem services provided by birds. Front. Ecol. Environ. 6, 476–484 (2008). Auk 128, 1–14 (2011). 40. Le Gouar, P. et al. Roles of survival and dispersal in reintroduction success of 7. DeVault, T. L., Rhodes, O. E. & Shivik, J. A. Scavenging by vertebrates: behavioral, Griffon vulture (Gyps fulvus). Ecol. Appl. 18, 859–872 (2008). ecological, and evolutionary perspectives on an important energy transfer 41. Grande, J. M. et al. Survival in a long-lived territorial migrant: effects of life-history pathway in terrestrial ecosystems. Oikos 102, 225–234 (2003). traits and ecological conditions in wintering and breeding areas. Oikos 118, 8. Oaks, L. et al. Diclofenac residues as the cause of vulture population declines in 580–590 (2009). Pakistan. Nature 427, 630–633 (2004). 42. Margalida, A. Poison baits and funding cuts: a deadly mix. Science (In press). 9. Green, R. E. et al. Diclofenac poisoning as a cause of vulture population declines 43. Sutherland, W. J. & Freckleton, R. P. Making predictive ecology more relevant to across the Indian subcontinent. J. Appl. Ecol. 41, 793–800 (2004). policy makers and practitioners. Philos. Trans.R. Soc. B 367, 322–330 (2012). 10. Thiollay, J. M. Raptor declines in West Africa: comparisons between protected, 44. Wilson, H. B., Joseph, L. N., Moore, A. L. & Possingham, H. P. When should we buffer and cultivated areas. Oryx 41, 322–329 (2007). save the most endangered species? Ecol. Lett. 14, 886–890 (2011). 11. Naidoo,V., Wolker,K., Cuthbert, R.&Duncan, N. Veterinarydiclofenacthreatens 45. Cardona, M. et al. A P-System based model of an ecosystem of some scavenger Africa’s endangered vulture species. Regul. Toxicol. Pharm. 53, 205–208 (2009). birds. Lect. Notes Comput. Sc. 5957, 182–195 (2010). 12. Virani, M. Z., Kendall, C., Njoroge, P. & Thomsett, S. Major declines in the 46. Dona´ zar, J. A. The Iberian Vultures. Biology and Conservation, J.M. Reyero Editor, abundance of vultures and other scavenging raptors in and around the Masai Mara ecosystem, Kenya. Biol. Conserv. 144, 746–752 (2011). 47. Margalida, A., Bertran, J. & Heredia, R. Diet and food preferences of the ´ ´ 13. Donazar, J. A., Margalida, A., Carrete, M. & Sanchez-Zapata, J. A. Too sanitary for endangered Bearded vulture Gypaetus barbatus: a basis for their conservation. Ibis vultures. Science 326, 664 (2009). 151, 235–243 (2009). ´ ´ 14. Cortes-Avizanda, A., Carrete, M. & Donazar, J. A. Managing supplementary 48. Margalida, A. et al. Long-term relationship between diet and breeding success in a feeding for avian scavengers: guidelines for optimal design using ecological declining population of Egyptian Vulture. Neophron percnopterus Ibis 154, criteria. Biol. Conserv. 143, 1707–1715 (2010). 184–188 (2012). 15. Tella, J. L. Action is needed now, or BSE crisis could wipe out endangered bird of ´ ´ 49. Donazar, J. A., Cortes-Avizanda, A. & Carrete, M. Dietary shifts in two vultures prey. Nature 410, 408 (2001). after the demise of supplementary feeding stations: consequences of the EU 16. Margalida, A., Dona´ zar, J. A., Carrete, M. & Sa´ nchez-Zapata, J. A. Sanitary versus sanitary legislation. Eur.J. Wildl. Res. 56, 613–621 (2010). environmental policies: fitting together two pieces of the puzzle of European 50. Fillat, F. Gestio´ n semi-extensiva de prados y pastos europeos ricos en especies: vulture conservation. J. Appl. Ecol. 47, 931–935 (2010). caso particular de los Pirineos espan˜ oles. Pastos 33, 171–215 (2006). 17. Margalida, A., Carrete, M., Sa´ nchez-Zapata, J. A. & Dona´ zar, J. A. Good news for 51. Garc´ı a-Martı´ nez, A., Olaizola, A. & Bermue´ s, A. Trajectories of evolution and European vultures. Science 335, 284 (2012). drivers of change in European mountain cattle farming systems. Animal 3, 18. Dona´ zar, J. A, Margalida, A. & Campio´ n, D. Vultures, feeding stations and sanitary 152–165 (2009). legislation: a conflict and its consequences from the perspective of conservation 52. Bose, M. & Sarrazin, F. Competitive behaviour and feeding rate in a reintroduced biology. Sociedad de Ciencias Aranzadi 2009. population of Griffon Vultures . Gyps fulvus Ibis 149, 490–501 (2007). 19. Margalida, A.,Colomer,M.A.&Sanuy, D. Canwildungulatecarcassesprovide 53. Bose,M., Duriez,O.&Sarrazin F. 2012 Intra-specific competition in foraging griffon enough biomass to maintain avian scavenger populations? An empirical assessment vultures:1.The dynamics of feedingingroups. Bird Study 59, 182–192 (2012). using a bio-inspired computational model. PLoS One 6, e20248 (2011). 54. Duriez, O., Herman, S. & Sarrazin, F. 2012 Intra-specific competition in foraging 20. Bousquet, F. C. & Le Page, C. Multi-agent simulations and ecosystem griffon vultures: 2. the influence of supplementary feeding management. Bird management: a review. Ecol. Model. 176, 313–332 (2004). Study 59, 193–206 (2012). 21. Pa˘un, G. Computing with membranes. J. Comp. Syst. Sci. 61, 108–143 (1998). 55. Houston, D. C. & Copsey, J. A. Bone digestion and intestinal morphology of the 22. Pa˘un, G., Rozenberg, G. & Salomaa, A. The Oxford Handbook of Membrane Bearded Vulture. J. Raptor Res. 28, 73–78 (1994). Computing, Oxford University Press, 2010. 56. Prinzinger et al. Energy metabolism and body temperature in the Griffon Vulture 23. Cardona, M. et al. Modelling ecosystems using P Systems: The Bearded Vulture, a (Gyps fulvus) with comparative data on the Hooded Vulture (Necrosyrtes case study. Lect. Notes Comput. Sc. 5391, 137–156 (2009). monachus) and the White-backed Vulture (Gyps africanus). J. Ornithol.143, 24. Colomer, M. A., Margalida, A., Sanuy, D. & Pe´ rez-Jime´ nez, M. J. A bio-inspired 456–467, (2002) computing model as a new tool for modeling ecosystems: the avian scavengers as a 57. King, J. R. & Farner, D. S. Energy metabolism, thermoregulation and body case study. Ecol. Model. 222, 33–47 (2011). temperature. In, Marshall, J. A. (Ed.) Biology and comparative physiology of birds 25. Dupont, H., Mihoub, J. B., Becu, N. & Sarrazin, F. Modelling interactions between Vol. II New York: Academic Press, pp. 215–288, 1961. scavenger behaviour and farming practices: Impacts on scavenger population and 58. Boumellasa, H. Rapaces ne´ crophages: concilier conservation de l’espe` ce et ecosystem service efficiency. Ecol. Model. 222, 982–992 (2011). minimisation des de´ penses, vers un reinforcement du lien Agriculture- 26. Ostfeld, R. S. & Keesing, F. Pulsed resources and community dynamics of Environment. University Paris X 2004. consumers in terrestrial ecosystems. Trends Ecol. Evol. 15, 232–237 (2000). 27. Herna´ ndez, M. & Margalida, A. Pesticide abuse in Europe: effects on the Cinereous vulture (Aegypius monachus)populationinSpain. Ecotoxicology 7, 264–272 (2008). 28. Gangoso, L. et al. Long-term effects of lead poisoning on bone mineralization in Acknowledgements vultures exposed to ammunition sources. Environ. Pollut. 157, 569–574 (2009). We gratefully acknowledge the Natural Computing Group at Sevilla University for their 29. Oro, D. et al. Testing the goodness of supplementary feeding to enhance help with the design of the simulator. AM was supported by the Departament d’Agricultura, population viability in an endangered vulture. PLoS One 3, e4084 (2008). Ramaderia, Pesca i Medi Natural of Generalitat de Catalunya and Ministerio de Medio 30. Herna´ ndez, M. & Margalida, A. Poison-related mortality effects in the endangered Ambiente. Egyptian Vulture (Neophron percnopterus) population in Spain: conservation measures. Eur. J. Wildl. Res. 55, 415–423 (2009). 31. Herna´ ndez, M. & Margalida, A. Assessing the risk of lead exposure for the Author contributions conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) A.M. and M.A.C. designed the experiment, collected all the data, performed analysis of the population. Environ. Res. 109, 837–842 (2009). data, and wrote the manuscript. Both the authors discussed the results and commented on ´ ´ 32. Margalida, A., Oro, D., Cortes-Avizanda, A., Heredia, R. & Donazar, J. A. the manuscript. Misleading population estimates: biases and consistency of visual surveys and matrix modelling in the endangered Bearded Vulture. PLoS One 6, e26784 (2011). 33. Margalida, A., Campio´ n, D. & Dona´ zar, J. A. European vultures’ altered Additional information Supplementary information accompanies this paper at http://www.nature.com/ behaviour. Nature 480, 457 (2011). 34. Olson, Z. J., Beasley, J. C., DeVault, T. L. & Rhodes, E. jr. Scavenger community scientificreports response to the removal of a dominant scavenger. Oikos 121, 77–84 (2011). Competing financial interests: The authors declare no competing financial interests. 35. Deygout, C., Sarrazin, F., Gault, A. & Bessa-Gomes, C. Modeling the impact of License: This work is licensed under a Creative Commons feeding stations on vulture scavenging service efficiency. Ecol. Model. 220, Attribution-NonCommercial-NoDerivative Works 3.0 Unported License. To view a copy 1826–1835 (2009). of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/ 36. Carrete, M., Dona´ zar, J. A. & Margalida, A. Density-dependent productivity depression in Pyrenean Bearded Vultures: implications for conservation. How to cite this article: Margalida, A. & Colomer, M.A. Modelling the effects of sanitary Ecol.Appl. 16, 1674–1682 (2006). policies on European vulture conservation. Sci. Rep. 2, 753; DOI:10.1038/srep00753 (2012). SCIENTIFIC REPORTS | 2 : 753 | DOI: 10.1038/srep00753 7

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Published: Oct 18, 2012

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