Environmentally relevant arsenic exposure affects morphological and molecular endpoints associated with reproduction in the Western mosquitofish, Gambusia affinis

Abstract

Arsenic (As) exposure, even at low environmentally relevant levels, may cause detrimental health outcomes through developmental toxicity and by acting as an endocrine disrupting compound (EDC). Although several studies indicate that wildlife bioaccumulate As, few evaluate the health impact on fish species in their natural environment. In the U.S., As has a drinking water regulatory limit of 10 μg/L. In many parts of Arizona, surface water and groundwater have naturally elevated levels of As from geologic deposits and contamination is exacerbated by anthropogenic activity. In aquatic environments, the Western mosquitofish, Gambusia affinis, is a good bioindicator for EDC exposure because of the distinct androgen-related development of an intromittent organ, the gonapodium, in males. We evaluated morphological and reproductive outcomes in mosquitofish exposed to As. In a laboratory experiment, juvenile male mosquitofish were exposed to sodium arsenite (0 μg/L, 0.75 μg/L, 7.50 μg/L, and 75 μg/L) for 30 days, and in a field study, populations of adult male mosquitofish were collected in Arizona waterways with As levels above and below the World Health Organization's regulatory limit. In both studies, higher As exposure was significantly associated with altered hepatosomatic indices, altered fish morphology, shortened gonopodia, and lower gonopodia-somatic indices. In the field experiment, populations from surface water with higher As concentrations exhibited lower condition factors, lower gonadal-somatic indices, distinct gonopodia shapes, and altered estrogen receptor alpha and vitellogenin gene expression; androgen receptor expression was unchanged. Together, laboratory and field results suggest that As exposure at environmentally-relevant levels affects general growth and reproductive development in mosquitofish. Observed effects may further influence individual health, mobility, or reproductive function, and because G. affinis is a species known to tolerate and adapt to a wide range of environments, it serves as a local bioindicator species as well as a model organism for parallel field and laboratory studies.