Assessment of the exposure to heavy metals in Griffon vultures (Gyps fulvus) from the Iberian Peninsula
Introduction
Wild bird populations are susceptible to dangers derived from the environmental presence of toxic elements, especially those that are non-degradable and that in many occasions tend to concentrate through the food chain, such as heavy metals (Guitart et al., 1994). Cadmium (Cd), lead (Pb) and mercury (Hg) are the most dangerous metals, from environmental and toxicological standpoints, both for humans and for animals (Burger, 1995, Eisler, 1987, García-Fernández et al., 1996).
The toxic effects of the various heavy metals on birds have been documented. Pb can cause bird mortality or can indirectly affect populations through its effects on the food base, avian behaviour, reproductive success and immune response, depending on the dose (Burger, 1995). The use of Pb pellets for shooting has resulted in their release into the environment over many years, with serious repercussions for many bird-species populations, which have ingested them either directly or indirectly. Galliforms and doves probably ingest spent shot as grit, which is retained in their gizzards to aid digestion, while raptors are usually poisoned through ingesting pellets in dead or injured prey or in gut piles (Fisher et al., 2006, Guitart et al., 2010, Kendall et al., 1996). Diffuse environmental Pb contamination resulting from waste dumping, as well as mining and smelting activities, has also affected a wide range of bird species via the food chain (Blus et al., 1993, Buekers et al., 2009, Henny et al., 1994). There are few reports of Cd-induced injury to terrestrial wildlife in nature (Burger, 2008). In a laboratory setting, Cd can cause kidney toxicity, disrupted calcium metabolism, decreased food intake, decreased growth rate, altered avoidance behaviour, reduced egg production and thin egg shells (Burger, 2008, Furness, 1996). Mercury is considered to be very toxic for wild animals (Eisler, 1987) and has been shown to adversely affect birds particularly through its neurotoxicity and negative effects on reproduction. Some of those effects are neurobehavioral underdevelopment, induction of eggshell thinning and malformations, inhibition of egg production and embryotoxic effects (Evans et al., 1982, Heinz and Hoffman, 2003, Lundholm, 1995). Reproductive effects occur at lower doses than those required to produce other pathological effects (Scheuhammer, 1987, Thompson, 1996).
Vultures, by virtue of their position at the top of the food chain and their millenary dependence on human activities, which provide food resources through livestock management or hunting practices, are at risk of accumulating and concentrating heavy metals in their tissues and thus serve as sensitive indicators of the level of environmental contamination (Guitart et al., 1994, Moleón et al., 2014, Wyk et al., 2001). Several papers about metal concentrations in vultures have been published (Carpenter et al., 2003, Donázar et al., 2002, Gangoso et al., 2009, Hernández and Margalida, 2009, Pattee et al., 2006). However, few studies have monitored heavy metals in the blood of the Griffon vulture (Gyps fulvus) (Espín et al., 2014a, García-Fernández et al., 1995, García-Fernández et al., 2005, Shlosberg et al., 2012).
The Griffon vulture is a large bird of prey which is exclusively or near-exclusively a scavenger in its feeding habits as it feeds mainly on the muscles and viscera of ungulates. In the 20th century there was a proven widespread decline, mainly due to poisoned baits set for carnivores and in some areas a reduction in available food supplies, due to changes in livestock management and sanitary legislation (del Hoyo et al., 1994, Donázar et al., 2009, Iñigo and Atienza, 2007, Margalida, 2012, Margalida et al., 2010, Muzinic, 2007). When feeding on wild-game carcasses, free-ranging scavengers such as Griffon vultures are thus more predisposed to the ingestion of illegal poison baits intended to kill predators or the Pb particles stemming from ammunition used for hunting. Illegal poisoning is probably the most significant cause of non-natural mortality among large birds of prey (Lambertucci et al., 2010, Margalida, 2012, Margalida et al., 2013). The decline in food availability following the introduction of European Union (EU) regulations (Regulation CE 1774/2002) prohibiting the disposal of carcasses in the field-due to the outbreak of bovine spongiform encephalopathy (BSE) in 2001-had harmful effects on vulture populations. These effects included a halt in population growth, a decrease in breeding success and an apparent increase in mortality in younger age classes of vultures (Donázar et al., 2009; Margalida et al., 2010; Margalida and Colomer, 2012). What is more, behavioural changes and dietary shifts are also related to food shortages (Donázar et al., 2010, Margalida et al., 2011a, Margalida et al., 2014). The dietary range of the Griffon vulture has broadened and now includes significant amounts of wild rabbits (Oryctolagus cuniculus) and rubbish while there has also been an increase in the number of cases of vultures attacking and killing cattle (Donázar et al., 2010; Margalida et al., 2011a, Margalida et al., 2014). In Portugal the conservation status of the species is “near-threatened” (Catry et al., 2010), whereas in Spain the Griffon vulture is classified as “least concern”, due to a positive population trend in this country (del Moral, 2009).
In this report, we attempt to investigate the blood heavy metal (Cd, Pb and Hg) concentrations in Griffon vultures from different areas of Portugal and from Catalonia, Spain and also to determine if heavy metals in the blood of weak and/or injured Griffon vultures admitted to wildlife rehabilitation centres (WRC) reflect profiles of contamination in the local, free-living and outwardly healthy Griffon vulture population. Differences between sampling areas were also investigated.
Section snippets
Sample collection
Blood samples were taken by veterinarians by puncturing the radial or metatarsal vein from a total of 121 Griffon vultures, which came from catches (n=54) performed in Portugal and Spain and from animals referred to three different WRC in Portugal (n=47) and one in Catalonia, Spain (n=20) (Fig. 1).
All blood samples were stored in eppendorf tubes without anticoagulant at −20 °C until analysis.
Thirty Griffon vultures were caught in May of 2011 by means of a cage-trap at a feeding station placed
Results
Cd and Hg were not detected (N.D.) in 119 (98.3%) and 115 (95%), respectively of the total blood samples and, when detected, the blood concentrations were near the LOQ and were therefore excluded from statistical analysis. In contrast, Pb was detected in all blood samples: 41 Griffon vultures (33.9%) had Pb concentrations below 20 µg/dl; 79 (65.3%) had Pb concentrations between 20 and 100 µg/dl; and one vulture exhibited 300.23 µg/dl of Pb in blood, a concentration that is associated with clinical
Discussion
This is the first study involving the biomonitoring of heavy metals performed on vultures from Portugal and from the autonomous community of Catalonia, Spain. It is also the first study which compares blood Pb concentrations of weak and/or injured animals referred to wildlife rehabilitation centres against those of outwardly healthy animals caught in the wild.
It is known that blood concentrations of Cd, Hg and Pb are good indicators of contamination and can be considered appropriate indicators
Conclusion
In conclusion, the data from this study indicates the Griffon vultures (G. fulvus) were recently exposed to low levels of Hg and Cd and most of the studied birds exhibited subclinical exposure to Pb. However some individuals in the present study could be at risk of suffering sub-lethal effects related with Cd, Hg and Pb exposure.
The Pb levels found in the Griffon vultures from WRC and those caught in Portugal may be considered relatively low and normal for vultures sampled outside or in the
Acknowledgements
This study was supported by the fellowship SFRH/BD/62115/2009 provided by the Fundação para a Ciência e Tecnologia. Griffon vultures were captured within the Territorial Cooperation Programme Spain–France–Andorra (NECROPIR-EFA 130/09) and Innovation Against Poison Programme (LIFE09 NAT/ES/000533). Vultures were also admitted at four wildlife rehabilitation centres: Centro de Ecologia, Recuperação e Vigilância de Animais Selvagens – CERVAS; Centro de Recuperação e Investigação de Animais
References (58)
- et al.
Lead toxicity to wildlife: derivation of a critical blood concentration for wildlife monitoring based on literature data
Sci. Total Environ.
(2009) Assessment and management of risk to wildlife from cadmium
Sci. Total Environ.
(2008)- et al.
Sample collection guidelines for trace elements in blood and urine. IUPAC commission of toxicology
J. Trace Elem. Med. Biol.
(1996) - et al.
Conservation status and limiting factors in the endangered population of Egyptian vulture (Neophron percnopterus) in the Canary Islands
Biological Conservation
(2002) - et al.
Effects of heavy metals on biomarkers for oxidative stress in Griffon vulture (Gyps fulvus)
Environ. Res.
(2014) - et al.
Oxidative stress biomarkers in Eurasian eagle owls (Bubo bubo) in three different scenarios of heavy metal exposure
Environ. Res.
(2014) - et al.
A review of lead poisoning from ammunition sources in terrestrial birds
Biol. Conserv.
(2006) - et al.
Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources
Environ Pollut.
(2009) - et al.
Animal poisoning in Europe. Part 3: wildlife
Vet. J.
(2010) - et al.
Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population
Environ. Res.
(2009)
Use of dogs as indicators of metal exposure in rural and urban habitats in NW Spain
Sci. Total Environ.
Effects of methyl mercury at different dose regimes on eggshell formation and some biochemical characteristics of the eggshell gland mucosa of the domestic fowl
Comp. Biochem. Physiol. C. Pharmacol. Toxicol. Endocrinol.
Lead concentrations in birds of prey in Britain
Environ. Pollut.
The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review
Environ. Pollut.
Accumulation and effects of lead and cadmium on wood ducks near a mining and smelting complex in Idaho
Ecotoxicology
A risk assessment for lead in birds
J. Toxicol. Environ. Health
Experimental lead poisoning in turkey vultures (Cathartes aura)
J. Wildl. Dis.
Aves de Portugal, Ornitologia do território Continental
Handbook of the Birds of the World
El Buitre leonado en España
Too sanitary for vultures
Science
Dietary shifts in two vultures after the demise of supplementary feeding stations: consequences of the EU sanitary legislation
Eur. J. Wildl. Res.
Neurotoxicity of methylmercury in the pigeon
Neurotoxicology
Patterns and interpretation of mercury exposure in freshwater avian communities in northeastern north America
Ecotoxicology
Interpretation of tissue lead residues in birds other than waterfowl
Cadmium in birds
Raptor ecotoxicology in Spain: a review on persistent environmental contaminants
Ambio
Cited by (35)
A review of constraints and solutions for collecting raptor samples and contextual data for a European Raptor Biomonitoring Facility
2021, Science of the Total EnvironmentIntegrating active and passive monitoring to assess sublethal effects and mortality from lead poisoning in birds of prey
2021, Science of the Total EnvironmentCitation Excerpt :In other studies around the world, the prevalence of exposure to Pb (>20 μg/dL) in large eagles (genera Aquila and Haliaeetus) was between 4.5 and 65% depending on age, time of the year or hunting intensity (Langner et al., 2015; Herring et al., 2020; Slabe et al., 2020), and in vultures was between 6.7 and 91% (García-Fernández et al., 2005; Mateo-Tomás et al., 2016; Herring et al., 2018; van den Heever et al., 2019). Here we have found a high prevalence in the Eurasian griffon vulture (73.7%), although within the range observed in other studies with this species in Spain (25–91%) (García-Fernández et al., 2005; Espín et al., 2014; Carneiro et al., 2015; Mateo-Tomás et al., 2016). The results of blood Pb concentrations in Eurasian griffon deserve a specific comment because it is well above the rest of the species.
Blood and bone lead levels in South Africa's Gyps vultures: Risk to nest-bound chicks and comparison with other avian taxa
2019, Science of the Total EnvironmentWhat do we know about lead contamination in wild vultures and condors? A review of decades of research
2019, Science of the Total EnvironmentAssessment of the exposure to heavy metals and arsenic in captive and free-living black kites (Milvus migrans) nesting in Portugal
2018, Ecotoxicology and Environmental SafetyCitation Excerpt :The measurement of metal concentrations in blood is a good indicator of recent exposure and for this reason it has been increasingly used in wildlife programs as a monitoring unit in the measurement of the current contamination and of short-term variation in contamination levels (Benito et al., 1999; Kahle and Becker, 1999; Evers et al., 2005). There are few biomonitoring studies of metals with raptors in Portugal (Palma et al., 2005; Lourenço et al., 2011; Carneiro et al., 2014, 2015, 2016). Therefore, this study was conducted to determine if the habitat of black kites in Portugal is contaminated by heavy metals and As.