Assessing the applicability of stable isotope analysis to determine the contribution of landfills to vultures’ diet

Human activities cause changes to occur in the environment that affect resource availability for wildlife. The increase in the human population of cities has led to a rise in the amount of waste deposited in landfills, installations that have become a new food resource for both pest and threatened species such as vultures. In this study we used stable isotope analysis (SIA) and conventional identification of food remains from Egyptian Vultures (Neophron percnopterus) to assess the applicability of SIA as a new tool for determining the composition of the diets of vultures, a group of avian scavengers that is threatened worldwide. We focused on an expanding Egyptian Vulture population in NE Iberian Peninsula to determine the part played by landfills and livestock in the diet of these species, and aimed to reduce the biases associated with conventional ways of identifying food remains. We compared proportions of diet composition obtained with isotope mixing models and conventional analysis for five main prey. The greatest agreement between the two methods was in the categories ‘landfills’ and ‘birds’ and the greatest differences between the results from the two methods were in the categories ‘livestock’, ‘carnivores’ and ‘wild herbivores’. Despite uncertainty associated to SIA, our results showed that stable isotope analysis can help to distinguish between animals that rely on waste and so present enriched levels of δ 13C than those that feed on the countryside. Indeed, a high proportion of food derived from landfills (nearly 50%) was detected in some breeding pairs. Furthermore we performed GLMM analyses that showed that high values of δ 13C in Egyptian Vulture feathers (a proxy of feeding in landfills) are related with high levels of humanization of territories. This method has the potential to be applied to other threatened vulture species for which there is a lack of information regarding resources they are consuming, being especially important as the main causes of vultures decline worldwide are related to the consumption and availability of food resources.

[1]  T. Kuiken,et al.  One Health approach to use of veterinary pharmaceuticals , 2014, Science.

[2]  Boyan Milchev,et al.  Diet of the Egyptian vulture (Neophron percnopterus) after livestock reduction in Eastern Bulgaria , 2012 .

[3]  M. Carrete,et al.  Large scale risk-assessment of wind-farms on population viability of a globally endangered long-lived raptor , 2009 .

[4]  M. Delibes,et al.  Stable isotope evidence for Turkey Vulture reliance on food subsidies from the sea , 2016 .

[5]  M. Attalla,et al.  N-Nitrosopiperazines form at high pH in post-combustion capture solutions containing piperazine: a low-energy collisional behaviour study. , 2010, Rapid communications in mass spectrometry : RCM.

[6]  M. Carrete,et al.  Habitat, human pressure, and social behavior: Partialling out factors affecting large-scale territory extinction in an endangered vulture , 2007 .

[7]  Richard Inger,et al.  Best practices for use of stable isotope mixing models in food-web studies , 2014 .

[8]  J. Real,et al.  Using Stable Isotopes To Determine Dietary Patterns In Bonelli's Eagle (Aquila fasciata) Nestlings , 2011 .

[9]  W. Bouten,et al.  Feathered Detectives: Real-Time GPS Tracking of Scavenging Gulls Pinpoints Illegal Waste Dumping , 2016, PloS one.

[10]  Potrava supa mrchožravého.  Food of the Egyptian Vulture ( Neophron percnopterus ) in Biscay , 2005 .

[11]  S. Carpenter,et al.  Global Consequences of Land Use , 2005, Science.

[12]  S. Oppel,et al.  No short-term effect of closing a rubbish dump on reproductive parameters of an Egyptian Vulture population in Turkey , 2017, Bird Conservation International.

[13]  N. Funel,et al.  Mutational Profiling of Kinases in Human Tumours of Pancreatic Origin Identifies Candidate Cancer Genes in Ductal and Ampulla of Vater Carcinomas , 2010, PloS one.

[14]  P. López‐López,et al.  Food predictability determines space use of endangered vultures: implications for management of supplementary feeding. , 2014, Ecological applications : a publication of the Ecological Society of America.

[15]  Ecology of a population of subsidized predators : Common ravens in the central Mojave Desert , California , 2006 .

[16]  A. Angerbjörn,et al.  Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes , 2005, Oecologia.

[17]  S. Agustí,et al.  Determination of fluoroquinolone antibiotic residues in the plasma of Eurasian griffon vultures (Gyps fulvus) in Spain. , 2016, The Science of the total environment.

[18]  M. Conroy,et al.  Analysis and Management of Animal Populations , 2002 .

[19]  L. Wassenaar,et al.  Stable nitrogen isotopes in waterfowl feathers reflect agricultural land use in western Canada. , 2001, Environmental science & technology.

[20]  R. Furness,et al.  Assessing the diet of great skuas, Catharacta skua, using five different techniques , 2002, Polar Biology.

[21]  Paola Laiolo,et al.  Consequences of pastoral abandonment for the structure and diversity of the alpine avifauna , 2004 .

[22]  S. Kark,et al.  Abrupt spatial and numerical responses of overabundant foxes to a reduction in anthropogenic resources , 2010 .

[23]  P. Aymerich,et al.  Identifying key demographic parameters for the viability of a growing population of the endangered Egyptian Vulture Neophron percnopterus , 2015, Bird Conservation International.

[24]  Andrew E. Derocher,et al.  Stable isotope mixing models fail to estimate the diet of an avian predator , 2017, The Auk.

[25]  P. Oliveira,et al.  Assessment of the exposure to heavy metals in Griffon vultures (Gyps fulvus) from the Iberian Peninsula. , 2015, Ecotoxicology and environmental safety.

[26]  J. Donázar,et al.  ROOST-TREE CHARACTERISTICS FOOD HABITS AND SEASONAL ABUNDANCE OF ROOSTING EGYPTIAN VULTURES IN NORTHERN SPAIN , 1990 .

[27]  M. Carrete,et al.  Dietary shifts in two vultures after the demise of supplementary feeding stations: consequences of the EU sanitary legislation , 2010, European Journal of Wildlife Research.

[28]  J. L. Pretus,et al.  Landfills determine the distribution of an expanding breeding population of the endangered Egyptian Vulture Neophron percnopterus , 2017 .

[29]  Robert G. Clark,et al.  Assessing Avian Diets Using Stable Isotopes II: Factors Influencing Diet-Tissue Fractionation , 1992 .

[30]  Richard Inger,et al.  Source Partitioning Using Stable Isotopes: Coping with Too Much Variation , 2010, PloS one.

[31]  S. Oppel,et al.  Diet is not related to productivity but to territory occupancy in a declining population of Egyptian Vultures Neophron percnopterus , 2015, Bird Conservation International.

[32]  M. Carrete,et al.  Action on multiple fronts, illegal poisoning and wind farm planning, is required to reverse the decline of the Egyptian vulture in southern Spain , 2015 .

[33]  Aleem Ahmed Khan,et al.  Diclofenac residues as the cause of vulture population decline in Pakistan , 2004, Nature.

[34]  Mike S. Fowler,et al.  Ecological and evolutionary implications of food subsidies from humans. , 2013, Ecology letters.

[35]  C. Guillou,et al.  Stable isotopes to discriminate lambs fed herbage or concentrate both obtained from C(3) plants. , 2008, Rapid communications in mass spectrometry : RCM.

[36]  A. Margalida,et al.  Biases in Studying the Diet of the Bearded Vulture , 2007 .

[37]  P. Mundy,et al.  The Vultures of Africa , 1992 .

[38]  T. Tatoni,et al.  Effects of anthropogenic food resources on yellow-legged gull colony size on Mediterranean islands , 2007, Population Ecology.

[39]  M. Virani,et al.  Another Continental Vulture Crisis: Africa's Vultures Collapsing toward Extinction , 2016 .

[40]  I. González-Martín,et al.  Use of isotope analysis to characterize meat fromIberian-breed swine. , 1999, Meat science.

[41]  E. Piasentier,et al.  Stable isotope ratio analysis for authentication of lamb meat. , 2003, Meat science.

[42]  J. Donázar,et al.  Reinventing mutualism between humans and wild fauna: insights from vultures as ecosystem services providers , 2013 .

[43]  T. Tatoni,et al.  Is the yellow-legged gull a superabundantbird species in the Mediterranean? Impacton fauna and flora, conservation measuresand research priorities , 1998, Biodiversity & Conservation.

[44]  Thomas Guillerme,et al.  SIDER: AN R PACKAGE FOR PREDICTING TROPHIC DISCRIMINATION FACTORS OF CONSUMERS BASED ON THEIR ECOLOGY AND PHYLOGENETIC RELATEDNESS , 2018 .

[45]  I. Casa-Resino,et al.  Breeding near a landfill may influence blood metals (Cd, Pb, Hg, Fe, Zn) and metalloids (Se, As) in white stork (Ciconia ciconia) nestlings , 2014, Ecotoxicology.

[46]  S. Bearhop,et al.  Multi-Scale Effects of Nestling Diet on Breeding Performance in a Terrestrial Top Predator Inferred from Stable Isotope Analysis , 2014, PloS one.

[47]  Lluís Jover,et al.  Feeding ecology of yellow-legged gulls Larus michahellis in the western Mediterranean: a comparative assessment using conventional and isotopic methods , 2009 .

[48]  D. Froese,et al.  Stable Carbon Isotope Compositions of Eastern Beringian Grasses and Sedges: Investigating Their Potential as Paleoenvironmental Indicators , 2007 .

[49]  Antoni Margalida,et al.  Factors influencing the breeding density of Bearded Vultures, Egyptian Vultures and Eurasian Griffon Vultures in Catalonia (NE Spain): management implications , 2007, Animal Biodiversity and Conservation.

[50]  Rafael Heredia,et al.  Diet and food preferences of the endangered Bearded Vulture Gypaetus barbatus: a basis for their conservation: Diet and food preferences in the Bearded Vulture , 2009 .

[51]  J. Zabala,et al.  Effect of human activities on Egyptian vulture breeding success , 2008 .

[52]  A. Margalida,et al.  Poison-related mortality effects in the endangered Egyptian vulture (Neophron percnopterus) population in Spain , 2009, European Journal of Wildlife Research.

[53]  M. Carrete,et al.  Too sanitary for vultures. , 2009, Science.

[54]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[55]  W. Trivelpiece,et al.  Integrating Stomach Content and Stable Isotope Analyses to Quantify the Diets of Pygoscelid Penguins , 2011, PloS one.

[56]  Helen M. Regan,et al.  Effects of wind farms and food scarcity on a large scavenging bird species following an epidemic of bovine spongiform encephalopathy , 2012 .

[57]  S. Kelly,et al.  Verifying the geographical origin of beef: The application of multi-element isotope and trace element analysis , 2008 .

[58]  S. Delacroix,et al.  The Responses of Medical General Practitioners to Unreasonable Patient Demand for Antibiotics - A Study of Medical Ethics Using Immersive Virtual Reality , 2016, PloS one.

[59]  G. Tavecchia,et al.  Population control of an overabundant species achieved through consecutive anthropogenic perturbations. , 2015, Ecological applications : a publication of the Ecological Society of America.

[60]  M. Carrete,et al.  Testing the Goodness of Supplementary Feeding to Enhance Population Viability in an Endangered Vulture , 2008, PloS one.

[61]  L. Boitani,et al.  Home range, activity and movements of a wolf pack in central Italy , 1997 .

[62]  Antonio Gasbarrini,et al.  Incidence of DAA failure and the clinical impact of retreatment in real-life patients treated in the advanced stage of liver disease: Interim evaluations from the PITER network , 2017, PloS one.

[63]  A. Martına,et al.  Use of a garbage dump by some mammal species in the Majella massif (Abruzzo, Italy) , 1997 .

[64]  R. Green,et al.  Toxicity of diclofenac to Gyps vultures , 2006, Biology Letters.

[65]  P. Danieli,et al.  Stable isotopes in tissues discriminate the diet of free-living wild boar from different areas of central Italy , 2017, PloS one.

[66]  Olaf Schmidt,et al.  Inferring the origin and dietary history of beef from C, N and S stable isotope ratio analysis , 2005 .

[67]  H. Förstel,et al.  Stable isotope variation as a tool to trace the authenticity of beef , 2004, Analytical and bioanalytical chemistry.

[68]  E. Kellogg,et al.  A global database of C4 photosynthesis in grasses. , 2014, The New phytologist.

[69]  J. Donázar,et al.  Long‐term relationship between diet breadth and breeding success in a declining population of Egyptian Vultures Neophron percnopterus , 2012 .

[70]  K. Hobson,et al.  Assessing Avian Diets Using Stable Isotopes I: Turnover of 13C in Tissues , 1992 .

[71]  E. Piasentier,et al.  Multielement (H, C, N, O, S) stable isotope characteristics of lamb meat from different Italian regions. , 2009, Rapid communications in mass spectrometry : RCM.

[72]  R. Koenig.  Vulture Research Soars as the Scavengers' Numbers Decline , 2006, Science.

[73]  R. Risebrough,et al.  Pleistocene to recent dietary shifts in California condors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[74]  C. Voigt,et al.  Spatial, seasonal and individual variation in the diet of White-tailed Eagles Haliaeetus albicilla assessed using stable isotope ratios , 2016 .

[75]  J. Tella,et al.  Traditional farming and key foraging habitats for chough Pyrrhocorax pyrrhocorax conservation in a Spanish pseudosteppe landscape , 1998 .

[76]  Richard Inger,et al.  Comparing pellet and stable isotope analyses of nestling Bonelli's Eagle Aquila fasciata diet , 2014 .

[77]  A. Powell,et al.  Evaluating gull diets: a comparison of conventional methods and stable isotope analysis , 2011 .

[78]  Joan Real.  Biases in diet study methods in the Bonelli's eagle , 1996 .

[79]  F. Monahan,et al.  Multielement isotope analysis of bovine muscle for determination of international geographical origin of meat. , 2011, Journal of agricultural and food chemistry.

[80]  J. Donázar,et al.  Foraging habitat selection, land-use changes and population decline in the lesser kestrel Falco naumanni , 1993 .

[81]  Daniel Oro,et al.  Short-term effects of culling on the ecology and population dynamics of the yellow-legged gull , 2000 .

[82]  Aurélien Besnard,et al.  Relative contribution of local demography and immigration in the recovery of a geographically-isolated population of the endangered Egyptian vulture , 2015 .