Ecosystem services and scavengersecological and socio-cultural assessment

  1. Morales Reyes, Zebensui
Supervised by:
  1. José Antonio Sánchez Zapata Director
  2. Marcos Moleón Paiz Co-director

Defence university: Universidad Miguel Hernández de Elche

Fecha de defensa: 25 June 2018

  1. Fernando Hiraldo Cano Chair
  2. Andrés Giménez Casalduero Secretary
  3. Elisa Oteros Rozas Committee member
  4. Joan Real Ortí Committee member
  5. Nuria Selva Committee member

Type: Thesis


The relationship between biodiversity and ecosystem functioning in supporting human well-being through the provision of ecosystem services is broadly recognized. In recent decades, there has been an increase in the research on the crucial role of carrion and scavengers in ecosystem functioning. Vertebrate scavengers are providers of multiple ecosystem services such as nutrient cycling, disease and pest control, and recreational services such as ecotourism. Nevertheless, obligate scavengers (i.e., vultures) and many large facultative scavengers (e.g., apex predators) constitute one of the most threatened functional group worldwide. Interestingly, Spain still holds a relatively healthy population of vultures and a wide array of facultative scavengers. Thus, Spain becomes one of the main responsibles for the conservation of European scavengers. This thesis focuses on the ecosystem services provided by vertebrate scavengers in Spain from a social-ecological perspective. Specifically, this thesis aims: i) to review the state of the art on the research on carrion, scavenging and associated ecosystem functions and services, social perceptions and attitudes toward scavengers, as well as indigenous and local knowledge (ILK) on carrion and scavenging (Chapter 1); ii) to spatially quantify the greenhouse gases (GHG) emitted by supplanting the natural removal of livestock carcasses by scavengers through the artificial carcass collection and transport from extensive farms to processing plants (Chapter 2); iii) assess the conservation and environmental consequences of the protection areas for the feeding of necrophagous species of European interest (PAFs) in Spain (Chapter 3); iv) to examine farmer perceptions of the ecosystem services provided by scavenging vertebrates in Spain (Chapter 4); v) to evaluate the similarities and contradictions between ILK and scientific knowledge (SK) regarding the scavenging service provided by vertebrates in extensive livestock farming systems (Chapter 5); and vi) to discuss the main results of the previous chapters, with special emphasis on the conservation implications and future perspectives (Chapter 6). Chapter 1 presents an overview of the main research topics addressed through the rest of the thesis. This introductory chapter revealed that the ecosystem function and services provided by scavengers have been scarcely studied until very recently. Moreover, research on social perceptions and attitudes towards scavengers, as well as indigenous and local knowledge on carrion and scavenging, remains virtually unexplored. In Chapter 2, we assessed the novel source of GHG emissions emerged following the implementation of a controversial European sanitary regulation (EC 1774/2002). After the mad cow crisis in Europe, the sanitary regulation required the collection of livestock carcasses from farms and their transformation or destruction in authorized plants. This situation had not only negative impacts on the conservation of scavengers but it also generated an unprecedented source of GHG emissions through the artificial elimination of livestock carcasses. To spatially calculate the GHG emissions, first, peninsular Spain was divided into 10 x 10 km UTM grids and the carcasses biomass generated per year was estimated for each grid. Second, we calculated the distance covered by trucks in the transport of carcasses from the center of each grid to intermediate and/or processing plants. Third, the GHG emissions associated with the transport of livestock carcasses were estimated according to the Intergovernmental Panel on Climate Change (IPCC) methodology. In addition, information from the National Biodiversity Inventory was used to analyze the relationship between the estimated GHG emissions with the distance from the center of each grid to the nearest breeding site of the four Spanish species of vultures, and with vulture richness per grid. Results showed that 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 equivalent to the atmosphere per year, in addition to annual payments of ca. $50 million to insurance companies. Paradoxically, the areas with the highest levels of GHG emissions coincided with areas holding the highest densities of vultures. Thus, findings from this chapter support the return to a traditional and natural scenario in which scavengers freely remove livestock carcasses. In Chapter 3, the network of protection areas for the feeding of necrophagous species of European interest (PAFs) was evaluated. In Europe, in an attempt to mitigate the negative impacts of the abovementioned, restrictive sanitary regulation (EC 1774/2002), a new regulation was approved (EC 142/2011) to allow farmers to leave the carcasses of extensive livestock within PAFs. To evaluate the Spanish PAFs network, first, all the Spanish autonomous communities were contacted to gather information about the characteristics of the PAFs. Second, we calculated the extensive livestock carrion biomass available inside PAFs. Third, data from the National Biodiversity Inventory were used to quantify the percentage of breeding distribution of the targeted and non-targeted scavenger species as well as the threatened and non-threatened species falling within PAFs. Fourth, we calculated the overlap between PAFs and the home range of 71 GPS-tracked vultures of four species, determining the use of the different administrative units by individuals and populations. Additionally, published studies on the home range of GPS-marked vultures in Spain were reviewed. Fifth, the potential savings in GHG emissions associated with the transport of livestock carcasses in relation to the pre-PAF scenario were estimated. The results displayed that the majority of the autonomous communities established PAFs in their territories, although the design criteria were variable. The extensive livestock carrion biomass potentially available for scavengers within PAFs was 33,474 tons per year, which represented 35% of the annual extensive livestock biomass generated in peninsular Spain. The breeding distribution of the targeted species was better represented within PAFs than that of the non-targeted species. Similarly, breeding distribution of threatened species was better represented than the one of non-threatened species. The overlap between PAFs and the home range of GPS-tracked vulture populations ranged between 63% and 100%, whereas at the individual level, it ranged between 21% and 100%. The home area of these and other populations of GPS-marked vultures in peninsular Spain covered 3–14 autonomous communities and 1–4 countries. At the individual level, vultures used an average of 3.4 autonomous communities and 1.5 countries. The implementation of the PAF network implied a potential reduction of ca. 44% of GHG emissions compared to the previous scenario. Thus, the implementation of PAFs was potentially an important improvement compared to the previous scenario. However, the new regulation could be improved by considering the overall distribution of additional scavenger species and by supra-regional and supra-national coordination and management. In Chapter 4, the farmer perceptions about the ecosystem services provided by vertebrate scavenger in Spain were assessed. To do this, 276 face-to-face surveys with farmers in 7 large extensive livestock systems were conducted. The findings indicated that the scavenging service (i.e., carrion consumption) was perceived by farmers as the most important service provided by scavengers. Interestingly, a "Dr. Jekyll and Mr. Hyde" paradox was detected, since the same species and species within the same guild can be dually perceived as beneficial or harmful depending on their consideration as primarily as scavengers or predators, respectively. Vultures were perceived by farmers as the most beneficial taxonomic group, followed by other raptors, non-raptor birds, and mammals. Farmers perceived the importance of scavengers as providers of ecosystem services when species had a more restricted distribution and their populations were perceived as declining. By contrast, farmers perceived that the provision of scavenging services increased with broader scavenger distributions. Moreover, in the scavenger communities with higher functional diversity, farmers perceived a higher capacity of the scavenger guild to provide ecosystem services. Farmers performing traditional livestock practices such as transhumance and the abandonment of livestock carcasses in the field had higher knowledge on scavengers and positive perception of them. In contrast, farmers having a higher livestock numbers, whether there were any attacks on livestock by scavengers, and having carcass removal insurance in the past, showed more negative perceptions of scavengers. In general, results from this chapter support the implementation of conservation policies in Europe that favor traditional extensive farming systems and strengthen the link between farmers and scavengers. In Chapter 5, we examined the similarities and contradictions between shepherds’ ILK and SK on the scavenging service provided by the vertebrate scavengers in Spain. To do so, 73 face-to-face surveys with livestock farmers of 2 extensive livestock systems were conducted. In addition, we carried out the monitoring of the consumption of 45 livestock carcasses by scavengers with camera traps. The level of consistency between the two knowledge systems was evaluated for three categories of shepherds’ age and experience and at different levels of ecological organization (i.e., species and community). Overall, a high consistency between ILK and SK was found, particularly at the species level, which was also consistent over the range of shepherd ages and experience. At the species level, the scavengers’ occurrence at carcasses observed by shepherds was highly correlated with the occurrence calculated from camera traps in both study areas. Likewise, the shepherds’ consideration of each species as provider of the scavenging service and the carrion biomass consumed by the species calculated from camera traps were also highly related in both study areas. At the community level, no differences were found between ILK and SK regarding the mean detection time of carcasses by scavengers, whereas there were differences in the mean consumption time of carcasses, being lower for ILK than the calculated with trap cameras. In general, these results support the integration of ILK and SK into the management strategies of vertebrate scavengers. Finally, Chapter 6 discusses the main results obtained in the previous chapters, including conservation and policy implications, limitations and caveats, and future perspectives. Overall, through addressing some important gaps regarding carrion, scavenging and associated ecosystem services, as well as social perceptions and ILK on vertebrate scavengers in Spain from a social-ecological perspective, this thesis emphasizes the need to i) link sanitary and environmental policies, ii) support the implementation of policies that favor traditional extensive farming systems, and iii) integrate ILK and SK into the conservation strategies of vertebrate scavengers.