Elsevier

Chemosphere

Volume 93, Issue 2, September 2013, Pages 441-447
Chemosphere

Comparative embryotoxicity of a pentabrominated diphenyl ether mixture to common terns (Sterna hirundo) and American kestrels (Falco sparverius)

https://doi.org/10.1016/j.chemosphere.2013.05.030Get rights and content

Highlights

  • Forster’s tern eggs from San Francisco Bay contain high residues of PBDEs.

  • Relative sensitivity of terns to PBDEs is of importance to natural resource managers.

  • PBDE-treated common tern and American kestrel eggs hatched later than controls.

  • Oxidative stress and DNA damage was more pronounced in hatchling kestrels than terns.

  • Findings suggest that tern embryos are less sensitive to PBDEs than kestrel embryos.

Abstract

Concentrations of polybrominated diphenyl ethers (PBDEs) in Forster’s tern (Sterna forsteri) eggs from San Francisco Bay have been reported to range up to 63 μg g−1 lipid weight. This value exceeds the lowest-observed-adverse-effect level (1.8 μg g−1 egg wet weight; ∼32 μg−1 lipid weight) reported in an embryotoxicity study with American kestrels (Falco sparverius). As a surrogate for Forster’s terns, common tern (Sterna hirundo) eggs were treated by air cell injection with corn oil vehicle (control) or a commercial penta-BDE formulation (DE-71) at nominal concentrations of 0.2, 2, and 20 μg g−1 egg. As a positive control, kestrel eggs received vehicle or 20 μg DE-71 g−1 egg. In terns, there were no effects of DE-71 on embryonic survival, and pipping or hatching success; however, treated eggs hatched later (0.44 d) than controls. Organ weights, organ-to-body weight ratios, and bone lengths did not differ, and histopathological observations were unremarkable. Several measures of hepatic oxidative stress in hatchling terns were not affected by DE-71, although there was some evidence of oxidative DNA damage (8-hydroxy-deoxyguanosine; 8-OH-dG). Although DE-71 did not impair pipping and hatching of kestrels, it did result in a delay in hatch, shorter humerus length, and reduced total thyroid weight. Concentrations of oxidized glutathione, reduced glutathione, thiobarbituric acid reactive substances, and 8-OH-dG in liver were greater in DE-71-treated kestrels compared to controls. Our findings suggest common tern embryos, and perhaps other tern species, are less sensitive to PBDEs than kestrel embryos.

Introduction

San Francisco Bay provides critical habitat for millions of birds, contains three Important Bird Areas, and has been designated as a Wetland of Hemispheric Importance (Chipley et al., 2003). Pesticides, industrial chemicals, metals and other anthropogenic compounds enter the Bay through runoff, sewage outfalls, atmospheric deposition, and constitute a potential threat to fish and wildlife resources. Since the 1970s, polybrominated diphenyl ethers (PBDEs) have been used as additive flame retardants in polymers, textiles, and electronics. Due to their persistence, bioaccumulation and potential toxicity, the United States Environmental Protection Agency (US EPA) and manufacturers reached agreement to phase out the use of certain penta- and octa-BDE formulations by 2004, and more recently agreed to phase out the use of the deca-BDE formulation by the end of 2013 (US EPA, 2012). Many BDE congeners have been demonstrated to biomagnify in aquatic and terrestrial food webs, with concentrations in eggs of high trophic level birds in North America ranging up to 6.61 μg g−1 wet weight (ww) (Chen et al., 2008, Henny et al., 2009, Chen and Hale, 2010; D. Chen, Southern Illinois University, personal communication). However, in San Francisco Bay, total PBDE concentrations range up to 63 μg g−1 lipid weight (lw) (∼10 μg g−1 ww) in eggs of Forster’s terns (Sterna forsteri), a lower trophic level species (She et al., 2008). These findings are of concern to natural resource managers since the closely related endangered California least tern (Sterna antillarum browni) breeds in this region. There is some evidence that PBDEs may adversely affect reproduction in wild birds. Henny et al. (2009) suggested that osprey (Pandion haliaetus) productivity decreases at PBDE concentrations exceeding 1 μg g−1 ww in eggs, although this finding was not supported in a subsequent study (Henny et al., 2011). In peregrine falcons (Falco peregrinus), brood size was found to be inversely related to total PBDE residues in eggs (0.68–39 ng g−1 lw) (Johansson et al., 2009).

Studies of birds have examined sublethal biochemical, immunological, developmental and reproductive effects of environmentally relevant concentrations of PBDEs (Chen and Hale, 2010). Using American kestrels (Falco sparverius), Fernie et al. (2006) injected 1.43 μg of a PBDE mixture g−1 egg on d 19 of incubation, followed by daily oral gavage of nestlings with 15.6 ng g−1 body weight for 29 d post-hatch. Using this combined egg injection/gavage exposure regime, there was some evidence that PBDEs increased growth (i.e., body weight, tarsometatarsus and feather length), caused structural changes in immune organs and alterations in immune function, and evoked hepatic oxidative stress (Fernie et al., 2005a, Fernie et al., 2005a, Fernie et al., 2006). Concentrations of plasma thyroxine and retinol, and hepatic retinol were found to be inversely related to carcass concentrations of BDE-47 and -99 (Fernie et al., 2005b). Changes in reproductive behavior, delays in egg laying, smaller eggs and reduced fertility were observed in kestrels receiving daily dietary doses of 0.3 or 1.66 ppm of DE-71 (Fernie et al., 2008). Perhaps more germane to the interpretation of avian egg PBDE concentrations, chicken (Gallus gallus), mallard (Anas platyrhynchos) and kestrel eggs were treated with the penta-BDE formulation DE-71 at doses ranging from 0.01 to 20 μg g−1 egg (McKernan et al., 2009, McKernan et al., 2010). Measurement of the quantity of the air cell injected DE-71 that actually entered the egg contents indicated that the lowest-observed-adverse-effect level on pipping and hatching success in kestrels was 1.8 μg g−1 egg ww (∼32 μg g−1 lw). This threshold has been exceeded in some egg samples from free ranging birds (Chen et al., 2008, She et al., 2008, Henny et al., 2009, Johansson et al., 2009).

Toxicological information about the effects of PBDEs on common terns, a surrogate for Forster’s and California least terns nesting in San Francisco Bay, would be of assistance to natural resource managers assessing the risk these flame retardants pose to birds. The present study evaluated embryonic survival, pipping and hatching success of common terns following air cell administration of DE-71, examined embryos and tern hatchlings for evidence of sublethal effects (deformities, growth, histopathologic lesions, and oxidative stress), and compared their relative sensitivity to kestrels and other similarly tested species.

Section snippets

Egg collection

All procedures involving eggs were approved by the Institutional Animal Care and Use Committee of the Patuxent Wildlife Research Center (PWRC). On May 25, 2010, a visit was made to the common tern colony on Poplar Island (38.7519°N, −76.3792°W) in Chesapeake Bay, MD, USA. Nests containing only one egg were marked to enable identification of new eggs during a second visit. In accord with our state and federal migratory bird permits, on May 27, a total of 60 freshly laid common tern eggs were

Background contamination of eggs

Low levels of contaminants were detected in control tern and kestrel eggs that were infertile or died early in incubation. Tern eggs (n = 5; 1 egg excluded due to poor recovery of analytes) contained <0.08 μg g−1 ww of p,p′-DDE, DDMU (1-chloro-2,2-bis(p-chlorophenyl)ethylene), cis-nonachlor, trans-nonachlor, MC5 (octachloro isomer in technical chlordane; Karlsson et al., 2009), mirex, and hexachlorobenzene, <0.45 μg g−1 of total PCBs, <0.052 μg g−1 of total PBDEs. Kestrels eggs (n = 3) contained <0.002 μg g

Background contamination and use of common tern and American kestrel eggs

Concentrations of polyhalogenated contaminants in common tern eggs from Poplar Island and American kestrel eggs from our captive colony, were well-below known reproductive effect thresholds in birds (Beyer and Meador, 2011). Notably, values of p,p′-DDE and total PCBs in tern eggs collected in the present study (i.e., <0.08 and <0.45 μg g−1 ww, respectively) were lower than levels found in Chesapeake Bay tern eggs collected in 1994 (South Sand Point off Barren Island) and 1997 (Bodkin Island)

Conclusions

Although the toxic effects of DE-71 on developing kestrels were not as remarkable as in our previous work (McKernan et al., 2009), a qualitative evaluation of a combination of endpoints (weight of evidence approach) suggests that common tern embryos, and perhaps other tern species are less sensitive to PBDEs than are kestrels. Limited sample size is often a challenging issue in comparative toxicity studies with wild bird eggs. Nonetheless, this pattern of embryotoxicity, with kestrels being

Acknowledgements

The authors thank R. Michael Erwin, P.C. McGowan, S.E. Warner, W.C. Bauer and M.M. Maxey for assistance in collecting tern and kestrel eggs, E. Harvey and M.J. La Guardia for analysis of eggs and dosing solutions, K.M. Eisenreich for bone length measurements, J.C. Wolf for histopathological evaluations, M. Sedlak and K. Taberski for valuable discussions at various stages of the study, and M.A. McKernan and H.M. Ohlendorf for reviewing a draft of this manuscript. This work was funded in part by

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