Effect of cadmium on gonadal development in freshwater turtle (Trachemys scripta, Chrysemys picta) embryos

Abstract

Prior studies on painted turtle (Chrysemys picta) sub-populations near the Massachusetts Military Reservation (MMR), a Superfund site on Cape Cod, Massachusetts, USA, suggest several reproductive deficits which may be related to xenobiotics. Several heavy metals, including cadmium, have been detected in Cape Cod surface water and sediments. The present study was carried out to investigate the effect of an environmentally relevant dose of cadmium on gonadal development during the end of the germ cell migration phase and post-natal gonadal maturation in freshwater turtles. Comparison of cadmium concentration in eggs of C. picta from Cape Cod showed that eggs from the impacted site animals had significantly higher cadmium in yolk than eggs from the reference site animals (7.23 ± 1.95 ng/g vs. 1.31 ± 0.50 ng/g). Gonadal structure and the number of proliferating germ cells of neonates derived from eggs of adult females from these sites showed no marked difference between sites. However, apoptosis of oocytes was significantly increased in neonate C. picta from the impacted pond compared to the reference pond. The effect of an administered environmentally relevant dose of cadmium on germ cell number and oocyte apoptosis was subsequently assessed in lab-reared Trachemys scripta, a closely related freshwater turtle species. Assessment of isotopic cadmium transmission showed that 6.29% of cadmium applied to the eggshell was transmitted through the eggshell to the yolk. The results showed that the total number of germ cells in cadmium-treated (1 μg/g) embryos was less than half that found in control embryos. The reduced germ cell number in Cd-treated embryos suggests that cadmium may reduce proliferation and/or delay migration of germ cells to the genital ridge. The effects of cadmium on turtle gonadal development were found to extend into 3 months post hatch. Proliferation of oocytes was not influenced by exposure to cadmium in ovo. In contrast, apoptosis of oocytes was significantly increased in cadmium exposed T. scripta. Since a lesion at the gonial stages will lead eventually to the depletion of more mature germ cells, the results for neonate turtles suggest that an environmental impact due to a xenobiotic mixture may enhance the rate of apoptosis, thus resulting in the reduction in follicle number seen in adult turtles from the impacted site. Overall, the data provide evidence that environmentally relevant doses of cadmium may affect gonadal developmental processes of freshwater turtles during embryonic and post-natal stages that may result in disruption of reproductive processes later in life.

Keywords:

• Cadmium
• environment
• freshwater turtle
• gonadal development
• reproduction

Acknowledgments

We thank Louise Bolge (BU Department of Earth Sciences) for her help with ICP/MS analysis; Emily Marquez, Joseph St.George and Jim Sullivan (Boston University) for their assistance in the field. An educational grant (Advanced Degree Scholarship) and a new staff development grant (Ratchadaphiseksompot Endownment Fund) from Chulalongkorn University to NK and a research grant (NIH ES 07381) to IPC are fully acknowledged.

This paper was presented at the SETAC Asia/Pacific 2006 conference held at Peking University, China on September 18–20, 2006.

Notes

*Based on an isotopic cadmium transmission, 6.29% of the amount of cadmium applied onto eggshell transmitted through the eggshell into the yolk.