Organohalogen contamination in breeding glaucous gulls from the Norwegian Arctic: Associations with basal metabolism and circulating thyroid hormones
Introduction
The concept of energy distribution for maintenance requirements, activity, growth, and reproduction constitutes a well-studied approach that integrates the physiology and ecology of individual animals. Attempts to identify the factors responsible for the variation in the maintenance energy requirements of vertebrates have typically focused on the minimal rate of energy expenditure, or basal metabolic rate (BMR). The BMR is commonly defined as the rate found in a thermoregulating, postabsorptive, adult endotherm resting in its thermoneutral zone, and has been characterized for a variety of wildlife species, including seabirds from a wide geographical range (Ellis, 1984, Ellis and Gabrielsen, 2002). The large variation in BMR within and between seabird species has been attributed to adaptations to specific behavioral traits of the species or in response to environmental conditions. For instance, seabirds living in arctic regions have been distinguished by higher BMR compared to species with characteristic southern distributions (Bech et al., 2002, Ellis, 1984, Gabrielsen et al., 1988, Gabrielsen and Mehlum, 1989). Yet, the factors influencing BMR among seabirds and wildlife in general, besides inherent seasonal and circadian rhythms, have rarely been investigated with respect to the physiological costs of exposure to environmental chemical pollution. It has been suggested that sublethal exposure to contaminants may impose a chemically induced stress in vertebrates by affecting respiratory processes and energy budgets via additional metabolic costs incurred by detoxification and excretion (Calow, 1991, Handy and Depledge, 1999).
The few studies that have measured energy expenditure in mammal and bird subjects following long- and short-term dosage regimes with chlorinated compounds are somewhat contradictory. In brief, increased metabolic rate was observed in dichloro-diphenyl-trichloroethane (DDT)-treated short-tailed shrews (Blarina brevicauda) (Braham and Neal, 1974) and white-footed mice (Peromyscus leucopus) dosed with low levels of polychlorinated biphenyls (PCBs) (Voltura and French, 2000). In contrast, other works have reported a decrease in metabolic rate: mourning doves (Zenaida macroura c.) exposed to Aroclor 1254 (Tori and Mayer, 1981) as well as pigeons (Columbidae sp.) (Jefferies et al., 1971) and lesser black-backed gulls (Larus fuscus) (Jefferies and Parslow, 1972) fed high doses of DDT and PCBs, respectively. Also reported has been unchanged metabolic rate as a function of contaminant dosage relative to control subjects, as for example in PCB-treated white-footed mice (French et al., 2001). Such increased or decreased metabolic rate following toxicant exposure may have partly been mediated through interactions of chemicals with the activities of certain hormones. One likely candidate is the thyroid hormones (THs).
The THs, i.e., thyroxine (T4) and particularly the primary metabolically active triiodothyronine (T3), are considered the prime controllers for the regulation of metabolic functions and thermogenesis in mammals and birds (Danforth and Burger, 1984, McNabb, 2000). Over the last few years, a number of observations have led to the speculation that contamination of certain environmental chemicals is the cause of thyroid function modulation in some avian species. Although somewhat less consistent in birds relative to mammals, a number of studies have reported abnormal TH concentrations and thyroid gland histology in birds exposed to organochlorine compounds under laboratory conditions and in free-ranging populations (Dawson, 2000, McNabb, 2005, Scanes and McNabb, 2003). More recently, in vitro and in vivo studies in non-avian species have reported effects on TH-dependent processes for chemicals of more recent environmental concern such as the polybrominated diphenyl ethers (PBDEs) (Legler and Brouwer, 2003) and their hydroxylated (OH)- and methoxylated (MeO)-PBDE analogues (Hakk and Letcher, 2003, Legler et al., 2002, Meerts et al., 2000), as well as the primary metabolically-derived PCB residues, the OH-PCBs (Letcher et al., 2000).
Recently, a study on breeding glaucous gulls (Larus hyperboreus) reported significant negative relationships between plasma concentrations of PCBs and selected organochlorine pesticides, and total and unbound plasma T4 and T3 concentrations (Verreault et al., 2004). It was suggested that the glaucous gull, a top-predator species in the Norwegian Arctic marine environment, might be particularly vulnerable to contaminant-mediated alteration in thyroid functions as a result of its high organohalogen burden. In fact, in eggs and plasma of glaucous gulls from the Norwegian Arctic, concentrations of PCBs, organochlorine pesticides (e.g., DDT- and chlordane [CHL]-related compounds), PBDEs, MeO-PBDEs and OH-PCBs/PBDEs were among the highest reported in any arctic seabird species and populations (Verreault et al., 2005a, Verreault et al., 2005b). Because a large suite of organohalogens occurring in glaucous gulls was demonstrated to have structure-related affinities with THs, and because THs exert strong control over regulation of metabolic functions, glaucous gulls exposed to high concentrations of these substances may experience altered circulating TH status, basal metabolism and capacity for adaptive thermogenesis. To test this assumption, we investigated the relationships between plasma concentrations of major legacy and emerging organohalogens (PCBs, DDTs, CHLs, PBDEs, MeO-PBDEs and OH-PCBs/PBDEs), circulating TH levels and BMR in breeding glaucous gulls from the Norwegian Arctic. We assumed that glaucous gull males and females during the breeding period would be more responsive to contaminant-induced changes on energetic and thyroid functions due to the particularly high energy expenditure associated with this critical stage of their life-history.
Section snippets
Field procedure
BMR measurements and blood samples were obtained from adult male (n = 11) and female (n = 12) glaucous gulls during the breeding season (May−June) of 2004 at Bear Island (74°22′ N, 19°05′ E) in the Norwegian Arctic. The study period at Bear Island was characterized by continuous daylight, a mean ambient temperature of 2.8 °C (range: -0.8–8.7 °C), and periods of rain, strong winds and even snowfalls. Randomly selected individuals were captured, while incubating, from three major colonies using a nest
Organohalogens
The selected chlorinated and brominated compound classes (i.e., PCBs, DDTs, CHLs, PBDEs, MeO-PBDEs and OH-PCBs/PBDEs) monitored in glaucous gull plasma were detected at mean sum concentrations ranging from 0.33 to 1183 ng g−1 wet weight (Table 1). The congener/compound concentrations and profiles of these organohalogens in glaucous gull plasma have been comprehensively reviewed elsewhere, and thus will not be further described here as they showed great consistency with those related studies (
Discussion
The results from the present study have shown that BMR, as a general proxy for the energy requirement for physiological maintenance, may be altered in glaucous gulls exposed to high loadings of persistent and bioaccumulative organohalogens, with possible enhanced contributions from CHL, PCB and DDT loadings. Current reduction of BMR in glaucous gulls was indeed supported by outcomes of experimental designs in which avian species were exposed to organochlorine compounds. In fact, a few research
Conclusions
The results from the present investigation suggest that variation in energy balance, measured as BMR, could be perceived as a valuable biomarker in health risk assessments of glaucous gull populations from the Norwegian arctic marine environment. We conclude that modification of adaptive thermogenic capacity in breeding glaucous gulls, as a potential result of exposure to enhanced environmental organohalogen contamination, may pose physiological constraints on vulnerable individuals in the
Acknowledgments
This project received funding from the Norwegian Polar Institute and the Norwegian Research Council (to J.V.). Supplemental funding also was provided by a grant from the Natural Sciences and Engineering Research Council of Canada and a Province of Ontario (Canada) Premier's Research Excellence Award (to R.J.L.). We wish to thank Dr. Shaogang Chu (University of Windsor, Windsor, Canada) for his assistance with the chemical analyses, Gunnar Sander (Norwegian Polar Institute) for technical help
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