The Roles of Diet and Habitat Use in Pesticide Bioaccumulation by Juvenile Chinook Salmon: Insights from Stable Isotopes and Fatty Acid Biomarkers.

Stable isotopes (SI) and fatty acid (FA) biomarkers can provide insights regarding trophic pathways and habitats associated with contaminant bioaccumulation. We assessed relationships between SI and FA biomarkers and published data on concentrations of two pesticides [dichlorodiphenyltrichloroethane and degradation products (DDX) and bifenthrin] in juvenile Chinook Salmon (Oncorhynchus tshawytscha) from the Sacramento River and Yolo Bypass floodplain in Northern California near Sacramento. We also conducted SI and FA analyses of zooplankton and macroinvertebrates to determine whether particular trophic pathways and habitats were associated with elevated pesticide concentrations in fish. Relationships between DDX and both sulfur (δ34S) and carbon (δ13C) SI ratios in salmon indicated that diet is a major exposure route for DDX, particularly for individuals with a benthic detrital energy base. Greater use of a benthic detrital energy base likely accounted for the higher frequency of salmon with DDX concentrations > 60 ng/g dw in the Yolo Bypass compared to the Sacramento River. Chironomid larvae and zooplankton were implicated as prey items likely responsible for trophic transfer of DDX to salmon. Sulfur SI ratios enabled identification of hatchery-origin fish that had likely spent insufficient time in the wild to substantially bioaccumulate DDX. Bifenthrin concentration was unrelated to SI or FA biomarkers in salmon, potentially due to aqueous uptake, biotransformation and elimination of the pesticide, or indistinct biomarker compositions among invertebrates with low and high bifenthrin concentrations. One FA [docosahexaenoic acid (DHA)] and DDX were negatively correlated in salmon, potentially due to a greater uptake of DDX from invertebrates with low DHA or effects of DDX on FA metabolism. Trophic biomarkers may be useful indicators of DDX accumulation and effects in juvenile Chinook Salmon in the Sacramento River Delta.

Effects of temperature and salinity on bioconcentration and toxicokinetics of permethrin in pyrethroid-resistant Hyalella azteca.

Recent studies demonstrated pyrethroid resistance associated with voltage-gated sodium channel mutations in populations of the epibenthic amphipod, Hyalella azteca. Resistant populations were able to tolerate and bioconcentrate pyrethroids at concentrations significantly higher than toxic levels for non-resistant populations. In conjunction with elevated bioconcentration potential, environmental alteration particularly as a result of global climate change is anticipated to significantly alter abiotic parameters including temperature and salinity. These changes are expected to influence uptake and biotransformation of contaminants. Thus, the aims of the current study were a) to examine the bioconcentration potential of permethrin in two pyrethroid-resistant clades of H. azteca and b) assess the influence of temperature and salinity changes on toxicokinetic parameters. Two pyrethroid-resistant clades of H. azteca were exposed to 14C-permethrin at three salinities (0.2, 1.0 and 6.0 practical salinity units (PSU)) and temperatures (18, 23 and 28 °C). Tests were conducted for up to 36 h and uptake, elimination and biotransformation rates were calculated. Both populations demonstrated bioconcentration factors (BCFs) between five and seven times greater than published data for non-resistant H. azteca, with significant differences between clades. Calculated BCF values were comparable to field populations of resistant H. azteca, emphasizing the potential for elevated pyrethroid bioconcentration in the natural environment and increased exposure for predators consuming pyrethroid-resistant aquatic invertebrates. Alterations to temperature and salinity had no statistically significant effect on uptake or parent compound half-life in either population, though biotransformation was elevated at higher temperatures in both populations. Salinity had a variable effect between the two populations, with lower BCF values at 1.0 PSU in clade D H. azteca and greater BCFs at 6.0 PSU in clade C H. azteca. This is the first study to demonstrate the potential for future climate scenarios to influence toxicokinetics in pyrethroid-resistant aquatic organisms.

Pesticide residues in juvenile Chinook salmon and prey items of the Sacramento River watershed, California - A comparison of riverine and floodplain habitats.

Juvenile Chinook salmon (Oncorhynchus tshawytscha) of the Sacramento River system encounter many anthropogenically-induced stressors while rearing and migrating to the Pacific Ocean. Located in a prominent agricultural region, the watershed serves as a source of notable contaminants including pesticides. Salmon rearing in riverine and floodplain areas are potentially exposed to these compounds via dietary exposure, which can vary based on selected food webs. Previous studies have suggested that juvenile Chinook salmon rearing in riverine and floodplain environments of the Sacramento River watershed are characterized by different dietary preferences, with potential for contrasting pesticide exposure between habitats. To examine the potential for pesticide exposure, juvenile Chinook salmon and known dietary items were collected in the mainstem Sacramento River and an adjacent floodplain, the Yolo Bypass, in 2019 and 2020, and analyzed for 33 pesticides, including degradates and isomers. Organochlorine pesticides including the DDX group (p,p'-DDT, p,p'-DDD and p,p'-DDE) were prevalent in all examined biota. There was a significantly greater number of total pesticide detections across all classes in zooplankton compared to macroinvertebrates, coupled with higher bifenthrin concentrations in zooplankton across regions and years, which may indicate different exposure potential depending on fish dietary preferences. Detection frequencies and concentrations of organochlorines were higher in prey items during flooding than in drought conditions, suggesting resuspension of legacy compounds. Significantly higher concentrations of organochlorines were recorded in floodplain rearing fish compared to the Sacramento River. These findings suggest that within these habitats, juvenile Chinook salmon feeding primarily on zooplankton within the water column may be exposed to a greater range of pesticides than those feeding on benthic macroinvertebrates, and that the benefits of floodplain rearing may come at a cost of increased organochlorine exposure.

Trophic transfer, bioaccumulation and transcriptomic effects of permethrin in inland silversides, Menidia beryllina, under future climate scenarios.

Global climate change (GCC) significantly affects aquatic ecosystems. Continual use of pyrethroid insecticides results in contamination of these ecosystems and concurrent GCC raises the potential for synergistic effects. Resistance to pyrethroids has been documented in Hyalella azteca, a common epibenthic amphipod and model organism. Resistant H. azteca can bioconcentrate elevated amounts of pyrethroids and represent a threat to consumers via trophic transfer. In the present study, a predator of H. azteca, the inland silverside (Menidia beryllina), was used to examine the impacts of GCC on pyrethroid bioaccumulation via trophic transfer from resistant prey organisms. M. beryllina were fed 14C-permethrin dosed pyrethroid-resistant H. azteca for 14 days at three salinities (6, 13 and 20 practical salinity units (PSU)) and two temperatures (18 and 23 °C). Fish were analyzed for total body residues, percent parent compound and percent metabolites. Gene expression in liver and brain tissue were evaluated to assess whether dietary bioaccumulation of permethrin would impact detoxification processes, metabolism, and general stress responses. M. beryllina bioaccumulated significant amounts of permethrin across all treatments, ranging from 39 to 557 ng g-1 lipid. No statistically significant effect of temperature was found on total bioaccumulation. Salinity had a significant effect on total bioaccumulation, owing to greater bioaccumulation at 6 PSU compared to 13 and 20 PSU, which may be due to alterations to xenobiotic elimination. Permethrin bioaccumulation and the interaction with temperature and salinity elicited significant transcriptional responses in genes relating to detoxification, growth, development, and immune response. Given the increased prevalence of pesticide-resistant aquatic invertebrates, GCC-induced alterations to temperature and salinity, and the predicted increase in pesticide usage, these findings suggest trophic transfer may play an important role in pesticide bioaccumulation and effects in predatory fish.

Fitness costs of pesticide resistance in Hyalella azteca under future climate change scenarios.

Global climate change continues to cause alterations in environmental conditions which can be detrimental to aquatic ecosystem health. The development of pesticide resistance in organisms such as Hyalella azteca can lead to increased susceptibility to environmental change. This research provides a robust assessment of the effects of alterations in salinity on the fitness of H. azteca. Full-life cycle bioassays were conducted with non-resistant and pyrethroid-resistant H. azteca cultured under two salinity conditions representing a rise from freshwater control (0.2 psu) to increased salinity due to salt-water intrusion, reduced snowpack and evaporative enrichment (6.0 psu). Additionally, the upper thermal tolerance was defined for each population at each salinity. Pyrethroid-resistant H. azteca exhibited reduced thermal tolerance; however, they produced more offspring per female than non-resistant animals. Compared to the low salinity water, both non-resistant and pyrethroid-resistant H. azteca produced more offspring, grew larger (based on dry mass), and produced larger offspring in elevated salinity, although pyrethroid-resistant animals had lower survival and lipid levels. This study provides fundamental information about the fitness potential of H. azteca in a changing climate, suggesting advantages for non-resistant animals under future climate scenarios. In addition, this research further supports the need to consider the effects of global climate change when conducting risk assessment of contaminants of concern, as well as the contribution of contaminants when investigating climate change impacts on populations, as exposure may contribute to niche contraction.