Immunomodulation in Post-metamorphic Northern Leopard Frogs,Lithobates pipiens, Following Larval Exposure to Polybrominated Diphenyl Ether

Abstract

Pollutants and disease are factors implicated in amphibian population declines, and it is hypothesized that these factors exert a synergistic adverse effect, which is mediated by pollutant-induced immunosuppression. Polybrominated diphenyl ethers (PBDEs) are ubiquitous pollutants that can exert immunotoxicity, making them of interest to test effects on amphibian immune function. We orally exposed Lithobates (Rana) pipiens tadpoles to environmentally realistic levels (0-634 ng/g wet diet) of a pentabromodiphenyl ether mixture (DE-71) from as soon as they became free-swimming through metamorphic climax. To assess adaptive immune response in juvenile frogs, we used an enzyme-linked immunosorbent assay to measure specific IgY production following immunization with keyhole limpet hemocyanin (KLH). Specific KLH antibody response was significantly decreased in juvenile frogs that had been exposed to PBDEs as tadpoles. When assessing innate immune responses, we found significantly different neutrophil counts among treatments; however, phagocytic activity of neutrophils was not significantly different. Secretion of antimicrobial skin peptides (AMPs) nonsignificantly decreased with increasing PBDE concentrations, and no significant effect of PBDE treatment was observed on efficacy of AMPs to inhibit chytrid fungus (Batrachochytrium dendrobatidis) growth. Our findings demonstrate that environmentally realistic concentrations of PBDEs are able to alter immune function in frogs; however, further research is needed to determine how these alterations impact disease susceptibility in L. pipiens.

Warmer temperature modifies effects of polybrominated diphenyl ethers on hormone profiles in leopard frog tadpoles (Lithobates pipiens)

“…Endocrine alterations due to brominated compound exposure are consistent with previous studies from our laboratory, showing that northern leopard frog ( Lithobates pipiens ) tadpoles exposed via their diet to environmentally relevant concentrations of PBDEs, throughout larval development, showed diminished growth and delayed metamorphosis , altered gonadal development , and altered immune function . Developmental impairments such as inhibited tail resorption and delayed metamorphosis were also observed in Xenopus laevis exposed to the commercial PBDE mixture DE‐71 .…”

“…In addition, interactions between PBDE exposure and temperature seem apparent, because thyroid hormone profile during metamorphosis was affected in a distinctive way, depending on the temperature at which tadpoles were raised. Although we did not find any overall significant alterations in growth and development in PBDE‐exposed tadpoles, the hormonal changes found in the present study support earlier findings of delayed metamorphosis in PBDE‐exposed tadpoles reared at 23 °C . Further investigations are necessary to address the implications of these changes for the species’ reproduction and survival considering a continuous contaminant exposure under a warming climate scenario.…”

“…We performed limited chemical analyses to confirm exposure differences, and several earlier studies demonstrated that PBDE kinetics are first order and rapid enough that tissue concentrations in tadpoles exposed for 34 d (the day of exposure we chose to collect the samples) correspond closely to those in the diets (; W. Karasov, unpublished data). Diet and tissue samples were sent to ALS Environmental, ALS Group USA to measure PBDE concentrations.…”

Splenic immunotoxicity in developing cane toads (Rhinella marina) from Bermuda

“…Overall, exposure to these pesticides caused both stimulation and suppression of immune function in field populations of frogs. Most recently, Cary et al [23] demonstrated that environmentally realistic concentrations of polybrominated diphenyl ethers were capable of altering immune function in frogs. However, further study is needed to determine how these alterations impact disease susceptibility in L. pipiens.…”

Long‐term exposure to high levels of decabrominated diphenyl ether inhibits CD4 T‐cell functions in C57Bl/6 mice

“…In a longitudinal cohort study of 33 children in the Netherlands, serum ∑PBDE levels were inversely correlated with the number of lymphocytes (Leijs et al ., ). Dietary exposure to penta‐ and/or tetra‐BDE altered the innate or adaptive immune response of fishes (Arkoosh et al ., ), amphibians (Cary et al ., ) and mink (Martin et al ., ), and may have increased their susceptibility to infectious diseases. Alterations of some immune parameters were also reported in mice orally exposed to DE‐71, a commercial pentaBDE mixture (Fair et al ., ).…”