Bioaccumulation of organochlorine contaminants and ethoxyresorufin‐o‐deethylase activity in southern California round stingrays (Urobatis halleri) exposed to planar aromatic compounds

Abstract

While contaminant concentrations have been reported for elasmobranchs around the world, no studies have examined bioaccumulation patterns across male and female age classes. The round stingray (Urobatis halleri) is a local benthic species that forages near areas of high organochlorine contamination and represents a good elasmobranch model. Polychlorinated biphenyls (PCBs), DDT, and chlordanes were measured in juvenile and adult male and female stingrays from areas in southern California, USA (n = 208), and a nearby offshore island, Santa Catalina (n = 34). Both mainland juvenile male and female stingrays showed a significant dilution effect. After maturity, summed contaminant concentrations significantly increased with size for adult males (median 11.1 µg/g lipid wt) and females (5.2 µg/g lipid wt). However, the rate of bioaccumulation was substantially greater in male stingrays than in females, likely a result of the females' ability to offload contaminants to offspring during pregnancy. In addition, males and females showed significant differences in their contaminant profiles, suggesting differential habitat use. Male and female stingrays collected from Santa Catalina Island had significantly lower concentrations (0.51 µg/g and 0.66 µg/g lipid wt, respectively), approximately 5 times less than those of mainland animals. Potential toxicity effects mediated through activation of the aryl hydrocarbon receptor were explored through ethoxyresorufin-O-deethylase (EROD) activity assays. Mainland male stingrays exhibited significantly greater EROD activities than Catalina males (481 pmol/min/mg protein and 55 pmol/min/mg protein, respectively); however, activity levels in female stingrays from both locations were comparable (297 pmol/min/mg protein and 234 pmol/min/mg protein, respectively) and lower than those in mainland males. The results suggest that PCBs and/or other structurally related contaminants may be inducing a biological response in mainland males but not females, possibly the result of a dampening effect of estradiol; however, the exact physiological repercussions of exposure remain to be determined.

Legacy polychlorinated biphenyl contamination impairs male embryonic development in an elasmobranch with matrotrophic histotrophy, the round stingray (Urobatis halleri)

“…Rather than representing an accessible energy reserve for growth, the larger embryos with smaller liver weight at the reference site could indicate that reference male embryos are more efficient at converting maternal resources (i.e., histotroph) into extrahepatic somatic growth because they had a relatively heavier total body mass. These findings support earlier evidence of adult male vulnerability to contaminants at the same sites (Lyons et al ), where males from the contaminated site exhibited biochemical responses to exposure but females did not. The liver has a propensity to accumulate organochlorine contaminants, making it particularly susceptible to contaminant effects.…”

“…Although previous studies documented significant differences in PCB concentrations in the livers of reference and contaminant‐exposed stingrays (Lyons et al ; Sawyna et al ), this observation was confirmed by measuring PCB contaminants in a subset of female liver samples ( n = 16, 8 from each location). Fifty‐three PCB congeners (Supplemental Data, Table S1) were analyzed following the methods of Lyons et al (). As expected, hepatic PCB concentrations averaged significantly (4‐fold) higher in contaminant‐exposed females than reference females (Welch's t test, t 8 = 3.09, p < 0.02; Supplemental Data, Table S2).…”

“…Despite the preponderance of DDT in the Southern California Bight, PCBs comprise the majority (>75%) of organochlorine contaminants in stingrays (Lyons et al ). This is attributed to stingray ecology and preference for nearshore habitats that separate them from deeper, more diversely contaminated sediment where historic and current outfall pipes release wastewater (∼8 km offshore and >60 m deep).…”

“…Thus, the round stingray has one of the shortest gestational periods (3–4 mo) among elasmobranchs. Because maternal contaminant offloading has been demonstrated in this species (Lyons and Lowe ) and 2 populations of round stingrays with differential exposure to primarily PCB contaminants have been identified (Lyons et al ; Sawyna et al ), the present study was designed to test the hypothesis that stingrays sampled from the contaminant‐exposed site would have impaired reproductive success (measures of fecundity, embryo growth rate, and offspring quality) compared to stingrays sampled from the reference site.…”

Organochlorine contaminants and maternal offloading in the lecithotrophic Pacific angel shark ( Squatina californica ) collected from southern California

“…Compared to other benthic elasmobranchs in this region, the angel sharks sampled from this study had much greater hepatic concentrations of total organochlorines (10.1 ± 7.7 lg/g ww) than that measured from other local benthic elasmobranchs such as male round stingrays Urobatis halleri (2.1 ± 1.7 lg/g ww; Lyons et al, 2014) and bat rays Myliobatis californica (5.0 ± 3.5 lg/g ww, n = 4; unpublished data). In addition, the average DDT:PCB ratio was much greater in the female angel sharks (4.1 ± 0.7) than these two other elasmobranch species (0.09 ± 0.06 and 0.9 ± 0.8, respectively).…”