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Polychlorinated Biphenyls and Polybrominated Diphenyl Ethers in Galapagos Sea Lions (Zalophus Wollebaeki)

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Polychlorinated Biphenyls and Polybrominated Diphenyl Ethers in Galapagos Sea Lions (Zalophus Wollebaeki) Environmental Toxicology and Chemistry, Vol. 28, No. 11, pp. 2271–2282, 2009 ’ 2009 SETAC Printed in the USA 0730-7268/09 $12.00 + .00 POLYCHLORINATED BIPHENYLS AND POLYBROMINATED DIPHENYL ETHERS IN GALAPAGOS SEA LIONS (ZALOPHUS WOLLEBAEKI) JUAN J. ALAVA,{ MICHAEL G. IKONOMOU,{ PETER S. ROSS,{ DANIEL COSTA,§ SANDIE SALAZAR,I DAVID AURIOLES-GAMBOA,# and FRANK A.P.C. GOBAS*{ {School of Resource and Environmental Management (Environmental Toxicology Research Group), Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A 1S6, Canada {Institute of Ocean Sciences, Fisheries and Oceans Canada, 9860 West Saanich Road, P.O. Box 6000, Sidney, British Columbia V8L 4B2, Canada §Center for Ocean Health, University of California, 100 Shaffer Road, Santa Cruz, California 95060, USA ICharles Darwin Foundation, Puerto Ayora, Santa Cruz, Gala´pagos, P.O. Box 17-1-3891, Quito, Ecuador #Centro Interdisciplinario de Ciencias Marinas, Instituto Polite´cnico Nacional, Avenue IPN s/n. Colonia Playa Palo de Santa Rita, La Paz Baja California Sur, C. P. 23060, Mexico (Received 16 July 2008; Accepted 27 May 2009) Abstract—Concentrations of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), polychlorinated dibenzo-p- dioxins (PCDDs), and polychlorinated dibenzofurans (PCDFs) were measured in muscle–blubber biopsy samples from 21 Galapagos sea lion (Zalophus wollebaeki) pups that were live captured in the Galapagos Islands (Ecuador) using gas chromatography/high- resolution mass spectrometry. Only traces of PBDEs were detected in one male pup, whereas PCDDs and PCDFs were not detected in any sample. The total concentration of PCBs (SPCB) in the pups averaged 104 mg/kg lipid (range, 49–384 mg/kg). No statistically significant differences in SPCB were observed among the four study sites in the Galapagos Islands. Concentrations of PCB congeners in Galapagos sea lion pups were dominated by low-molecular-weight congeners. These results suggest that global transport is the main source for PCBs in Galapagos sea lions. The SPCB levels were below immunotoxic and endocrine-disruption thresholds in pinnipeds, suggesting a limited risk of adverse health effects. The present study indicates that Galapagos sea lions can serve as a useful sentinel of pollutants with a long-range transport capacity and that Galapagos Islands are not exempt from the threats of global pollutants despite its remote locale. Keywords—Polybrominated diphenyl ethers Polychlorinated biphenyls Galapagos sea lions Galapagos Islands Atmospheric transport INTRODUCTION have been associated with effects on the immune and endocrine Polychlorinated biphenyls (PCBs), polybrominated diphe- systems of marine mammals [13–16], which can compromise nyl ethers (PBDEs), polychlorinated dibenzo-p-dioxins survival and reproduction. (PCDDs), and polychlorinated dibenzofurans (PCDFs) repre- Polybrominated diphenyl ethers (PBDEs) have been used as sent persistent, bioaccumulative, and toxic compounds of flame retardants in foams, textiles, coatings, furniture, global concern. Whereas the legacy PCB, PCDD, and PCDF construction materials, electronic devices (e.g., television sets, production or by-production has been curtailed, in part appliances, and computers), plastics, and paints since 1970 [2– because of the global Stockholm Convention on persistent 4,17,18]. The production and use of PBDEs have been organic pollutants [1], PBDEs represent chemicals of emerging restricted in Europe and Canada, but the deca-PBDE environmental concern [2–5]. formulation is still used extensively elsewhere [5]. The In the industrialized world, PCBs were banned during the worldwide production of brominated flame retardants, includ- ing PBDEs, during the 1990s and the year 2000 was late 1970s as a result of concerns about their persistence, approximately 150,000 to 350,000 tons/year [2–4]. Similar to bioaccumulation, and toxicity to wildlife [1]. Polychlorinated PCBs, a total of 209 PBDE congeners are possible, although biphenyls are found at relatively high concentrations in the commercial mixtures and environmental samples typically northern hemisphere, but their presence in the tropics can be contain a small number of dominant PBDE congeners [4,19– attributed, in part, to long-range transport [6–9]. Polychlori- 21]. Polybrominated diphenyl ethers also have been detected in nated biphenyl concentrations in pinniped species have marine mammals, including polar bears (Ursus maritimus), declined since the 1970s, as source control and regulations seals, and cetaceans [22–25]. For example, PBDE concentra- served to reduce inputs into the environment [10]. Before tions in ringed seals (Pusa hispida) increased exponentially in national controls, both PCDDs and PCDFs were formed as the Canadian Arctic from 1981 to 2000 [26]. In Europe, by-products of pulp and paper mill processes [11], but they however, declines in PBDE concentrations have resulted from also can be formed as by-products of combustion [12]. the regulation of penta- and octa-formulations in 1998 Assessing PCB, PCDD, and PCDF exposure is an important [17,27,28]. Polybrominated diphenyl ethers are relatively part of marine wildlife conservation, because these compounds persistent environmental contaminants that bioaccumulate in * To whom correspondence may be addressed ([email protected]). organisms and can undergo long-range transport to remote Published on the Web 6/5/2009. regions [6,29]. In addition, PBDEs can cause toxic effects, 2271 2272 Environ. Toxicol. Chem. 28, 2009 J.J. Alava et al. Fig. 1. Map of the Galapagos Islands in relation to Ecuador and South America showing sampling sites (white dots) indicated by black arrows and distribution of the Galapagos sea lion rookeries (small black dots). including neurotoxicity, disruption of steroid and thyroid MATERIALS AND METHODS hormone regulation, teratogenicity, and carcinogenicity [30– Sampling 32]. Evidence for the propensity of PCBs, PBDEs, PCDDs, and Muscle–blubber biopsy samples (sample size, 100 mg; PCDFs to undergo long-range transport typically has been biopsy punch, 6 mm) of 21 Galapagos sea lion pups were gauged by their occurrence in polar regions. The protection of obtained from four rookeries of the Galapagos Islands peoples inhabiting Arctic regions from the adverse health Archipelago (Fig. 1) at 1,000 km (600 miles) off the Ecuador- effects of persistent organic pollutants is an integral compo- ian continental coast, between 01u409N and 01u259S and nent of the Stockholm Convention, which became interna- 89u159W and 92u009W, during a field research expedition on tional law on May 17, 2004 [1]. Long-range transport to March 13 to 21, 2005. Pups were sampled from the Caaman˜o tropical regions, however, is not receiving comparable (n 5 11) and Plaza Sur (n 5 4) colonies on Santa Cruz Island, attention. In the case of PBDEs and PCBs, no studies, to from Punta Espinoza (n 5 3) on Fernandina Island, and from our knowledge, have been conducted in pinnipeds from Cabo Chaimbers (n 5 3) on Pinta Island. Santa Cruz is a equatorial or tropical areas. semiurbanized island, whereas Fernandina and Pinta islands Despite its protected status, the Galapagos sea lion are noninhabited, pristine environments. Nursing pups were (Zalophus wollebaeki) population decreased by 60% between chosen for the following reasons: They are readily accessible the 1970s and the year 2000 [33]. Several hypotheses have been and easy to capture in most of the rookeries of the Galapagos proposed to explain this decline. These include El Nin˜o events, Islands year-round; they are of approximately the same age, nutritional stress, fisheries interactions, illegal hunting, as well thus minimizing the influence of life history on contaminant as diseases (e.g., Leptospira and Morbillivirus sp.) introduced concentrations; they are nursed by adult reproductive females by feral mammals, such as dogs [33,34]. As a result, the with a similar diet item (i.e., milk); and they are in a high Galapagos sea lion is listed as ‘‘threatened’’ under the IUCN trophic position, feeding on mother’s tissue (i.e., milk). (World Conservation Union) endangered category [35]. To our Galapagos sea lions reproduce year-round. The main period knowledge, the potential impact of endocrine-disrupting of birth is between August and November, and the young are persistent organic pollutants has not been investigated and weaned after approximately 12 to 24 months [37,38]. The could represent another factor contributing to the decline in capture and immobilization of pups followed the field Galapagos sea lions. anesthesia methodology for studies of Galapagos sea lions The present study measured PCB, PBDE, PCDD, and and fur seals developed by Para´s et al. [39]. Pups were selected PCDF concentrations in Galapagos sea lions to characterize based on observed nursing behavior, and estimated age based the presence of these priority contaminants in these pinnipeds on size and weight which ranged from 2 to 12 months (i.e., less and to evaluate any possible risks associated with exposure. than two years). The animals’ weight, length, and girth were The Galapagos Island Archipelago (Ecuador) is a United measured. Further details on the pups’ capture, determination Nations Educational, Scientific, and Cultural Organization of body condition index (i.e., Fulton condition factor), and (UNESCO) World Heritage Site that recently was listed as immobilization are described in the Supporting Information being at risk [36]. Understanding the fate and potential
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