Ecological and spatial factors drive intra- and interspecific variation in exposure of subarctic predatory bird nestlings to persistent organic pollutants
Introduction
Being lipophilic and highly resistant to chemical and biological degradation, persistent organic pollutants (POPs) are of concern for the health of ecosystems because of three reasons. Firstly, POPs associate with organic matter, in particular lipids, and therefore potentially bioaccumulate in biological tissues and biomagnify through food chains (Borgå et al., 2012). As a consequence, wildlife feeding at the top of the food chain may bioaccumulate POPs to levels that disrupt immune, endocrine and reproductive systems (Letcher et al., 2010, Sonne, 2010). Secondly, ecosystems are currently still exposed to legacy POPs (Helander et al., 2008, Johansson et al., 2011), even though legal mitigation has been undertaken decades ago (Betts, 2008, Porta and Zumeta, 2002). Thirdly, POPs are subject to long-range atmospheric and hydrologic transport (Lohmann et al., 2007, Möller et al., 2011), rendering anthropogenic pollution with POPs a major environmental threat also to Arctic ecosystems (AMAP, 2011, UNEP/AMAP, 2011).
Arctic populations living at their northernmost distribution are supposedly subject to already high natural stress. Any additional stress from POP exposure may therefore synergistically inflict detrimental health effects (Boonstra, 2004). In order to study POP exposure and its effects, predatory birds are both conceptually (Burger and Gochfeld, 2001) and effectively (Chen and Hale, 2010) valuable sentinels. Recently, Sonne et al., 2010, Sonne et al., 2012 investigated relationships between POP concentrations and clinical–chemical parameters in blood plasma of predatory bird nestlings in northern Norway. Both negative relationships with total bilirubin, glucose, and alanine aminotransferase, and positive relationships with cholesterol, albumin, urea and alkaline phosphatase, suggested that liver, kidney and bone endocrinology and metabolism may have been impacted. This indication of disturbed homeostatic functioning underlines the relevance of the present study.
As often found when assessing wildlife exposure (e.g. Letcher et al., 2010), significant intra- and interspecific variation in POP exposure was recently found in predatory bird nestlings from northern Norway (Eulaers et al., 2011a). It is however unclear which biological variables gave rise to the observed variation. While environmental physico-chemical properties are of importance to determine POP exposure in lower trophic species, dietary accumulation is expected to be the major POP exposure pathway in predatory birds (Ruus et al., 2002). Therefore, the analysis of feeding ecology, by means of carbon and nitrogen stable isotopes (SIs), may be of particular interest in exposure assessment studies (Jardine et al., 2006). The ratio of heavier 15N to lighter 14N stable isotopes (δ15N) typically increases throughout the food chain (Boecklen et al., 2011, Jardine et al., 2006) due to the preferential deamination of light amine groups during de- and transamination processes (Macko et al., 1986). The ratio of stable carbon isotopes (δ13C) depicts the food chain origin of the diet, e.g. by discrimination between 13C-depleted terrestrial ecosystems compared to enriched marine ones (Boecklen et al., 2011, Jardine et al., 2006).
Recent studies on terrestrial passerines, such as Light-vented Bulbul (Pycnonotus sinensis), Long-tailed Shrike (Lanius schach) and Oriental Magpie-robin (Copsychus saularis; Sun et al., 2012), and marine top predators, such as Bald Eagle (Haliaeetus leucocephalus; Elliott et al., 2009) and Herring Gull (Larus argentatus; Sørmo et al., 2011), have related variation in dietary ecology, through analysis of carbon and nitrogen SIs, to variation in POP exposure. Until now, however, it has not been investigated whether and how dietary ecology independently, or in combination with other biological or spatial factors, may influence intra- and interspecific POP exposure in predatory birds. In addition, SI half-lives in the tissues used in above-mentioned studies (≤ 18 days for blood plasma, liver and muscle; Boecklen et al., 2011) are much shorter than average POP half-lives (≤ 400 days; Fisk et al., 2001), and may have possibly resulted in less accurate associations.
In the present study, we performed a large-scale field sampling of fully-grown predatory bird nestlings, targeted at maximising ecological (dietary carbon source and trophic level) and spatial variation (local habitat and regional nest location), while minimising confounding biological factors, such as migration, age and reproductive status. During three breeding seasons (2008–2010), we sampled body feathers from nestlings of three ecologically distinct predatory bird species in subarctic Norway: Northern Goshawk (Accipiter gentilis), White-tailed Eagle (Haliaeetus albicilla) and Golden Eagle (Aquila chrysaetos). To the best of our knowledge, the present study performs for the first time the combined analysis of nestling body feathers for POPs and SIs, thus integrating the SI incorporation and POP accumulation over the larger part of the nestling stage: body feather growth is initiated at day 27 and is still ongoing at day 60 upon sampling (Golden Eagle observations; Watson, 2010). We aimed to investigate whether and how ecological (dietary carbon source, trophic level), biological (sex, body condition) and spatial factors (local habitat) independently, or in combination, influenced intraspecific variation in nestling exposure to polychlorinated biphenyl 153 (CB 153), dichlorodiphenyldichloroethylene (p,p′-DDE), polybrominated diphenyl ether 47 (BDE 47) and hexachlorobenzene (HCB). In addition, we aimed at investigating how the feeding ecology (dietary carbon source, trophic level) and regional nest location may have influenced interspecific exposure.
Section snippets
Field sampling
The sampling area (68.46–70.59 °N; 15.62–26.10 °E) was situated within the two northernmost counties of Norway, Troms and Finnmark (Fig. 1; Table 1). During the breeding seasons in 2008, 2009 and 2010, we have sampled nestlings from three predatory bird species, each resident in a typical ecosystem in subarctic Norway: White-tailed Eagle (marine ecosystem), Northern Goshawk (woodland ecosystem) and Golden Eagle (mountainous ecosystem). White-tailed Eagle and Northern Goshawk resided
Intraspecific variation
In Northern Goshawk, δ15N differed significantly between local habitats (F1,63 = 6.17; P = 0.02), with coastal nestlings being + 1.40‰ enriched in 15N compared to those inland (Padj = 0.02). No inter-annual (F2,63 = 1.14; P = 0.33) nor sex differences (F1,63 = 1.33; P = 0.25) in δ15N were observed. In contrast, δ13C differed significantly among sampling years (F2,63 = 9.30; P < 0.01), but not between local habitats (F1,63 = 0.01; P = 0.92) or sexes (F1,63 = 0.06; P = 0.80). Northern Goshawk nestlings sampled in 2009 and
Discussion
In the present study, the first aim was to identify biological and spatial variables that may drive the observed intraspecific variation in POP exposure. The most parsimonious LMEMs revealed that intraspecific variation in exposure was driven by a combination of factors, often different among individual compounds, and that combinations for individual compounds differed among species (Table 2). Generally, but not always significantly, ecological factors such as trophic level, local habitat, or
Conclusions
To the best of our knowledge, the present study integrated for the first time the analysis of POPs and SIs in predatory bird nestling body feathers. This novel methodology successfully identified ecological and spatial factors that may influence variation in POP exposure over the larger part of the nestling stage. Ecological factors, such as trophic level and dietary carbon source, as well as spatial factors, such as local habitat and regional nest location, contribute to explain variation in
Acknowledgements
This study was performed within the RAPTOR 2015 project (NFR project ES421785: Persistent organic pollutants and natural stress in avian top predators of northern ecosystems: potential vulnerability to environmental change). RAPTOR 2015 was supervised by J.O. Bustnes and funded by the Norwegian Research Council. We also thank the University of Antwerp and FWO Flanders for funding Eulaers, Jaspers, Covaci, Pinxten and Eens. Finally, we acknowledge Bård Bårdsen, Erik Fransen and Stefan Van Dongen
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