Endosulfan Exposure Disrupts Pheromonal Systems in the Red-Spotted Newt: A Mechanism for Subtle Effects of Environmental Chemicals

Environmental Health Perspectives, July, 2001 by Daesik Park, Steven Hempleman, C., Catherine R. Propper

Effect of endosulfan exposure on mating success. Female newts exposed to endosulfan had lower mating success than that of controls (chi-square, p = 0.035; Figure 1). The decrease in mating success was more distinctive in the high-concentration group (z-test, p = 0.002) than in the low-concentration group (z-test, p = 0.009).

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Effects of endosulfan on gland morphology. Histomorphometric examination of pheromonal glands of control and exposed females revealed anatomical changes. The alveolar size and luminal area of alveoli differed significantly as a function of treatment (Figure 2A; one-way ANOVA, F = 15.32, p [is less than] 0.001 for alveoli; Figure 2B; F= 15.59, p [is less than] 0.001 for lumen). Females exposed to the high concentration of endosulfan had smaller alveoli than control females (Figure 2A; Tukey test, p [is less than] 0.001), and the alveoli of the low-concentration exposure group exhibited reduced luminal area (Figure 2B; Tukey test, p [is less than] 0.001). Effects of endosulfan on pheromone production. Compared to odor sources from control females, odor sources from endosulfan-exposed females at both concentrations induced a significantly lower magnitude in EOG responses from male olfactory sensory cells (Figure 3; one-way ANOVA, F = 9.15, p [is less than] 0.001). There was no significant difference in response between the two different concentrations of endosulfan (Tukey test, p = 0.40).

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Effects of endosulfan on plasma estradiol concentrations. The plasma concentration of 17[Beta]-estradiol was not different between control and treated groups (mean [ or -] SD: control, 11.90 [ or -] 1.40 pg/100 [micro]L plasma, n = 20; low concentration, 14.80 [ or -] 2.60, n = 22; high concentration, 13.80 [ or -] 1.60, n = 20; one-way ANOVA, p = 0.77).

Discussion

Our morphologic, electrophysiologic, and behavioral results suggest that low-concentration exposure to a commonly used insecticide disrupts the mate selection process in red-spotted newts specifically by interfering with olfactory communication and that this disruption consequently leads to lowered mating success.

Previously reported toxicologic observations were not induced by the concentration of endosulfan we administered. During our study, endosulfan did not affect general activity, food consumption, surfacing to breathe oxygen, or weight of the ovaries and oviducts. Nor did exposure affect visual attractivity of females. Other studies where higher concentrations of endosulfan were administered, however, have reported traditional toxicologic effects. For example, neonatal rats exposed to 4.5 mg/kg body weight endosulfan by subcutaneous injection had decreased testis, seminal vesicle, ovary, and oviduct weight and also had low levels of testosterone and estradiol (9). The freshwater fish Channa punctatus exposed to similar levels of endosulfan as in our study (6 ppb and 10 ppb) showed tremors, convulsions, increased surfacing activity, and increased general activity, as well as altered concentrations of neurotransmitters in the brain including acetylcholine, serotonin, and dopamine (11). Harris et al. (28) reported deformities in American toads (Bufo americanus) and northern leopard frogs (Rana pipiens) exposed to 0.1 ppm endosulfan. Considering these previous results, our findings suggest that the sensitivity to changes in pheromonal function in newts may be similar to that of more overt toxicologic effects that indicate marked neurologic dysfunction in C. punctatus.