Elsevier

Aquatic Toxicology

Volume 80, Issue 2, 16 November 2006, Pages 149-157
Aquatic Toxicology

Mobilization of PCBs from blubber to blood in northern elephant seals (Mirounga angustirostris) during the post-weaning fast

https://doi.org/10.1016/j.aquatox.2006.08.002Get rights and content

Abstract

Northern elephant seals (Mirounga angustirostris) are characterized by extended fasting during which they rely entirely on their own body reserves. During fasts, lipids are mobilized from blubber to match the energy requirements of the animal. This transfer frees toxic fat-soluble pollutants into the blood circulation, which may exert adverse health effects, especially in young and developing animals. We investigated the dynamics of mobilization of polychlorinated biphenyls (PCBs) from the blubber of northern elephant seal pups during the post-weaning fast. Longitudinal samples of blubber and serum were collected from free-ranging animals throughout the fast at Año Nuevo, California. Blubber biopsies were separated into inner and outer layers. The PCB profiles of blubber and serum consisted mainly of penta- (PCB-101, -110, -118), hexa- (PCB-138, -153) and hepta- (PCB-180, -183, -187) chlorobiphenyls, which accounted for almost 90% of the total PCB burden. Total PCB concentrations in inner blubber increased significantly between early and late fasting (563.6 ± 162.0 μg/kg lipids at early versus 911.6 ± 513.1 μg/kg lipids at late fasting) whereas they remained fairly constant in outer blubber (572.6 ± 134.8 μg/kg lipids at early versus 659.2 ± 158.8 μg/kg lipids at late fasting). A corresponding rise of PCB concentrations was observed in serum during the second half of the fast (3.8 ± 1.1 μg/l serum at early versus 7.2 ± 0.9 μg/l at late fasting). The longitudinal changes in circulating total PCBs could not be explained by the changes in serum lipid fractions (cholesterol, phospholipids, triacylglycerols and free fatty acids). The increases in total PCB concentrations in inner blubber and serum were more pronounced in leaner animals, which suggests that they might be more at risk to potential toxic effects.

Introduction

Fat-soluble organochlorine pollutants such as polychlorinated biphenyls (PCBs) contaminate terrestrial and marine ecosystems. Because of their stability and lipophilicity, they accumulate in high trophic level fauna. High levels of these chemicals in marine mammal tissues have been linked to toxic effects such as immunotoxicity, endocrine disruption, cancer development, skeletal abnormalities and reproductive failure (Reijnders, 1986, Zakharov and Yablokov, 1990, Ross et al., 1996, Ross, 2000, Hall et al., 2003, Ylitalo et al., 2005). Few studies, however, have focused on the toxicokinetics of these pollutants during physiological status that induce fat transfer inside the body.

Fasting plays a key role in the life history of many marine mammals and phocid seals in particular, e.g., during reproduction, migration, moulting and post-weaning. During such periods, the mobilization of blubber lipid reserves liberates PCBs and other fat-soluble chemicals into the circulation (Aguilar et al., 1999, Lydersen et al., 2002, Debier et al., 2003), which could induce physiological and health problems. An increase of serum concentrations has indeed been noticed in grey seal females (Halichoerus grypus), at the end of lactation, when they have fasted for almost 3 weeks (Debier et al., 2003). Similarly, dramatically higher PCB levels have been reported in the serum of thin adult harp seals (Phoca groenlandica), sampled during the moult, when body condition is poor, as compared to fat individuals, sampled during the breeding season (Lydersen et al., 2002). A rise of concentrations is usually also reported in the blubber, when its weight declines to minimum levels, suggesting a concentration effect of the contaminants which are progressively stored in a smaller total lipid mass (Addison and Stobo, 1993, Lydersen et al., 2002, Debier et al., 2003). To date, the exact effects that lipid mobilization exerts on tissue contaminant concentrations, distribution and dynamics, however, remain unclear.

The northern elephant seal (Mirounga angustirostris) provides an excellent model to study the dynamics of mobilization of organochlorine pollutants from body lipid stores during periods of natural fasting. Indeed, these large and sexually dimorphic pinnipeds exhibit some of the longest voluntary fasts, lasting up to 3 months long (Le Boeuf, 1974, Deutsch et al., 1990). During the breeding season, northern elephant seals (NES) gather on rookeries in California and Mexico between December and March. Males arrive first on the colony and compete for social rank and harem defence while fasting entirely. Females group together in harems and give birth to a single pup (Le Boeuf et al., 1972). They fast during the entire nursing period (∼25 days), secreting a fat-rich milk (up to 55% fat) synthesized from their body stores (Le Boeuf and Ortiz, 1977). Lactating females lose almost 60% of their body fat (Crocker et al., 2001). The mass transfer to the pup is efficient, excess of 50%. During the nursing period, the pup gains around 90 kg, more than half of it being composed of lipids (Crocker et al., 2001). Pups are weaned abruptly and remain on land, fasting for up to 2.5 months, while learning to swim and dive (Reiter et al., 1978). During this period, they rely on reserves deposited during the suckling period. At weaning, pup lipid content averages 40% of body mass (Crocker et al., 2001). They lose almost 30% of their weaning mass during the fast, 35% of their mass loss being composed of lipids (Noren et al., 2003). Their energy requirements during long fasts are mainly met by the oxidation of blubber fatty acids, thus limiting protein loss (Castellini et al., 1987, Houser and Costa, 2001, Noren et al., 2003).

The contaminant body burden of NES pups is obtained exclusively from maternal milk and transplacental transfer and is mainly stored in blubber. It therefore reflects the contamination of the mother through her dietary intake. Part of this burden might then be released into the circulation during the post-weaning fast, when fat is mobilized from the blubber. A preliminary article has reported PCB, polychlorinated dibenzo-p-dioxin (PCDD) and polychlorinated dibenzofuran (PCDF) levels in the blubber of six NES pups at weaning (Debier et al., 2005). In the present study, we describe for the first time the dynamics of mobilization of PCBs from blubber stores to serum during the post-weaning fast. PCB concentrations were measured in the inner and outer blubber as well as in the serum of 15 free-ranging, individually marked NES pups that were serially captured throughout the post-weaning fast. Results are discussed in the context of blubber fat mobilization and blood transport. The mobilization of PCBs from different blubber body areas is also investigated.

Section snippets

Field techniques

The study was conducted at the colony of Año Nuevo, CA, USA (37°06′30″N, 122°20′10″W) in 2002. Fifteen NES pups (seven females and eight males) were captured from 3 to 4 times during the post-weaning fast (Table 1). The pups were initially marked with bleach and re-marked with hair-dye (Clairol, Stamford, CT, USA) after the moult in order to allow identification throughout the fast. Weaning dates were recorded by daily observations of the colony. The first capture was within 1–8 days

Results

The mean weight loss of the pups was 25 ± 7 kg over a period of 36 ± 8 days (Table 1), which corresponds to a daily weight loss of 0.7 ± 0.2 kg. The body lipid content of the pups at weaning, which was calculated according to Noren et al. (2003), was 36.4 ± 2.3%.

The PCB profiles of blubber and serum consisted mainly of penta- (PCB-101, -110, -118), hexa- (PCB-138, -153) and hepta- (PCB-180, -183, -187) chlorobiphenyls (CBs), which accounted for almost 90% of the total PCB burden. Among the other

Discussion

NES weaned pups exhibit a relatively low level of PCB contamination compared to other young pinnipeds (Espeland et al., 1997, Bernt et al., 1999, Kajiwara et al., 2001, Le Bœuf et al., 2002, Debier et al., 2003, Sormo et al., 2003, Ross et al., 2004). This probably results from the feeding habits of the mothers that forage pelagically in the open northeastern Pacific ocean on prey in the deep scattering layer and spend only a limited amount of time in coastal areas near the contamination

Conclusion

Although NES pups are exposed to relatively low levels of PCBs, the increase of circulating PCB concentrations at the end of their extended post-weaning fast may pose a potential risk because they are still developing and may be more sensitive to the contamination. The problem might be more acute for leaner pups that undergo the sharpest increase of circulating PCBs. The potential role of PCBs and other organochlorines in the mortality rates of young NES warrants study. Indeed, more than 50% of

Acknowledgements

This work was performed in Año Nuevo State Reserve, a part of the University of California Natural Reserve System. The authors thank D.P. Noren, B. Mc Donald and P. Morris for their help and advice during sample collection. We thank R.M. Ortiz, S. Dovel, S. Simmons and N. Miller for additional fieldwork support, the Año Nuevo Rangers for their cooperation and Clairol Corporation for providing marking solutions. The authors thank M. Louvet from the “Laboratoire d’Ecologie animale et

References (41)

  • T. Raclot

    Selective mobilization of fatty acids from adipose tissue triacylglycerols

    Prog. Lipid Res.

    (2003)
  • P.S. Ross et al.

    Contaminant-induced immunotoxicity in harbour seals: wildlife at risk?

    Toxicology

    (1996)
  • T. Severinsen et al.

    Spatial distribution of persistent organochlorines in ringed seal (Phoca hispida) blubber

    Mar. Environ. Res.

    (2000)
  • E.G. Sormo et al.

    Partitioning of persistent organic pollutants in grey seal (Halichoerus grypus) mother-pup pairs

    Sci. Total Environ.

    (2003)
  • G.M. Ylitalo et al.

    The role of organochlorines in cancer-associated mortality in California sea lions (Zalophus californianus)

    Mar. Pollut. Bull.

    (2005)
  • R.F. Addison et al.

    Transfer of organochlorine residues from blubber through the circulatory system to milk in the lactating grey seal Halichoerus grypus

    Can. J. Fish. Aquat. Sci.

    (1987)
  • R.F. Addison et al.

    Organochlorine concentrations and burdens in grey seal (Halichoerus grypus) blubbe during the first year of life

    J. Zool. Lond.

    (1993)
  • A. Aguilar et al.

    Biological factors affecting variability of persistent pollutant levels in cetaceans

    J. Cetacean. Res. Manag.

    (1999)
  • M.A. Castellini et al.

    Fatty acid metabolism in fasting elephant seal pups

    J. Comp. Physiol. (B)

    (1987)
  • D.E. Crocker et al.

    Maternal traits and reproductive effort in northern elephant seals

    Ecology

    (2001)
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