Assessment of the exposure to heavy metals in Griffon vultures (Gyps fulvus) from the Iberian Peninsula

https://doi.org/10.1016/j.ecoenv.2014.12.016Get rights and content

Highlights

  • Cd and Hg were not detected in most of blood samples in Griffon vulture.

  • Pb was detected in all blood samples and most vultures exhibited subclinical exposure.

  • Vultures admitted at WRC do not reflect blood Pb levels of local populations.

Abstract

Griffon vultures (Gyps fulvus), by virtue of their position at the top of the food chain and as obligate scavengers, are at risk of accumulating and concentrating heavy metals in their tissues and may be more predisposed to their toxic effects. The aim of this study is to investigate heavy metal concentrations in Griffon vultures in Portugal and Catalonia, Spain and to determine if heavy metal concentrations in the blood of weak and/or injured Griffon vultures admitted to wildlife rehabilitation centres (WRC) reflect contamination profiles in the local, free-living and outwardly healthy population. Whole-blood samples taken from 121 Griffon vultures caught in the wild or admitted to WRC in Portugal and Catalonia, Spain were examined for cadmium (Cd), mercury (Hg) and lead (Pb) by inductively coupled plasma mass spectrometry (ICP-MS). Cd and Hg were not detected in most samples (98.3% and 95%, respectively), while Pb was detected in all birds in concentrations ranging between 4.97 and 300.23 µg/dl. Birds admitted to WRC had significantly lower Pb concentrations (24.15±15.07 and 25.98±18.04 µg/dl in Portugal and Catalonia, Spain, respectively) than animals caught in the wild (29.67±13.19 and 42.22±50.08 µg/dl in Portugal and Catalonia, Spain, respectively) (p<0.05). This may be explained by the fact that malnutrition was the main cause of admission of Griffon vultures to WRC, as ingestion has been described as the most significant pathway for Pb exposure in raptors. Therefore Griffon vultures admitted to WRC do not seem to be representative of the local, free-flying populations, so it remains necessary to continue catching when one intends to monitor Pb exposure in this species. The population of vultures captured in Catalonia, Spain showed the highest mean blood Pb concentration, perhaps due to the municipal rubbish dump located near the feeding station, with rubbish providing a significant fraction of their trophic needs. The ingestion of game meat with bullet fragments in carcasses or with Pb shots embedded in their flesh could also be the cause of the high blood Pb concentrations found in some vultures. The potential risk of Pb exposure in Griffon vulture populations must be given consideration, since most individuals evaluated had Pb concentrations between 20 and 100 µg/dl, which is considered to be subclinical exposure to Pb, and which is above the threshold level at which Pb can affect antioxidant system in this species (15 µg/dl).

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

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