Jill A. Awkerman

Developmental toxicity of Louisiana crude oil-spiked sediment to zebrafish

Embryonic exposures to the components of petroleum, including polycyclic aromatic hydrocarbons (PAHs), cause a characteristic suite of developmental defects and cardiotoxicity in a variety of fish species. We exposed zebrafish embryos to reference sediment mixed with laboratory weathered South Louisiana crude oil and to sediment collected from an oiled site in Barataria Bay, Louisiana in December 2010. Laboratory oiled sediment exposures caused a reproducible set of developmental malformations in zebrafish embryos including yolk sac and pericardial edema, craniofacial and spinal defects, and tissue degeneration. Dose-response studies with spiked sediment showed that total polycyclic aromatic hydrocarbons (tPAH) concentrations of 27mg tPAH/kg (dry weight normalized to 1 percent organic carbon [1 percent OC]) caused a significant increase in defects, and concentrations above 78mg tPAH/kg 1 percent OC caused nearly complete embryo mortality. No toxicity was observed in Barataria sediment with 2mg tPAH/kg 1 percent OC. Laboratory aging of spiked sediment at 4°C resulted in a nearly 10-fold decrease in sensitivity over a 40-day period. This study demonstrates oiled sediment as an exposure pathway to fish with dose-dependent effects on embryogenesis that are consistent with PAH mechanisms of developmental toxicity. The results have implications for effects on estuarine fish from oiled coastal areas during the Deepwater Horizon spill.

Augmenting aquatic species sensitivity distributions with interspecies toxicity estimation models.

Species sensitivity distributions (SSDs) are cumulative distribution functions of species toxicity values. The SSD approach is being used increasingly in ecological risk assessment but is often limited by available toxicity data needed for diverse species representation. In the present study, the authors evaluate augmenting aquatic species databases limited to standard test species using toxicity values extrapolated from interspecies correlation estimation (ICE) models for SSD development. The authors compared hazard concentrations at the 5th centile (HC5) of SSDs developed using limited measured data augmented with ICE toxicity values (augmented SSDs) with those estimated using larger measured toxicity datasets of diverse species (reference SSDs). When SSDs had similar species composition to the reference SSDs, 0.76 of the HC5 estimates were closer to the reference HC5; however, the proportion of augmented HC5s that were within 5-fold of the reference HC5s was 0.94, compared with 0.96 when predicted SSDs had random species assemblages. The range of toxicity values among represented species in all SSDs also depended on a chemicals mode of action. Predicted HC5 estimations for acetylcholinesterase inhibitors showed the greatest discrepancies from the reference HC5 when SSDs were limited to commonly tested species. The results of the present study indicate that ICE models used to augment datasets for SSDs do not greatly affect HC5 uncertainty. Uncertainty analysis of risk assessments using SSD hazard concentrations should address species composition, especially for chemicals with known taxa-specific differences in toxicological effects. This article is a US Government work and is in the public domain in the USA.

Evaluation of in silico development of aquatic toxicity species sensitivity distributions

Determining the sensitivity of a diversity of species to environmental contaminants continues to be a significant challenge in ecological risk assessment because toxicity data are generally limited to a few standard test species. This study assessed whether species sensitivity distributions (SSDs) could be generated with reasonable accuracy using only in silico modeling of toxicity to aquatic organisms. Ten chemicals were selected for evaluation that spanned several modes of actions and chemical classes. Median lethal concentrations (LC50s) were estimated using three internet-based quantitative structure activity relationship (QSAR) tools that employ different computational approaches: ECOSAR (Ecological Structure Activity Relationships), ASTER (Assessment Tools for the Evaluation of Risk), and TEST (Toxicity Estimation Software Tool). Each QSAR estimate was then used as input into the SSD module of the internet-based toxicity estimation program Web-ICE to generate an in silico estimated fifth percentile hazard concentration (HC5) for each of the ten chemicals. The accuracy of the estimated HC5s was determined by comparison to measured HC5s developed from an independent dataset of experimental acute toxicity values for a diversity of aquatic species. Estimated HC5s showed generally poor agreement with measured HC5s determined for all available aquatic species, but showed better agreement when species composition of the chemical specific SSDs were identical. These results indicated that LC50 variability and species composition were large sources of error in estimated HC5s. Additional research is needed to reduce uncertainty in HC5s using only in silico approaches and to develop computational approaches for predicting species sensitivity.

Effects of Louisiana crude oil on the sheepshead minnow (Cyprinodon variegatus) during a life-cycle exposure to laboratory oiled sediment.

Determining the long‐term effects of crude oil exposure is critical for ascertaining population‐level ecological risks of spill events. A 19‐week complete life‐cycle experiment was conducted with the estuarine sheepshead minnow (Cyprinodon variegatus) exposed to reference (uncontaminated) sediment spiked with laboratory weathered South Louisiana crude (SLC) oil at five concentrations as well as one unspiked sediment control and one seawater (no sediment) control. Newly hatched larvae were exposed to the oiled sediments at measured concentrations of < 1 (sediment control), 50, 103, 193, 347, and 711 mg total polyaromatic hydrocarbons (tPAH)/kg dry sediment. Juveniles were exposed through the reproductively active adult phase at measured concentrations of <1 (sediment control), 52, 109, 199, 358, and 751 mg tPAH/kg sediment. Throughout the exposure, fish were assessed for growth, survival, and reproduction. Resulting F1 embryos were then collected, incubated, and hatched in clean water to determine if parental full life‐cycle exposure to oiled sediment produced trans‐generational effects. Larvae experienced significantly reduced standard length (5–13% reduction) and wet weight (13–35% reduction) at concentrations at and above 50 and 103 mg tPAH/kg sediment, respectively. At 92 and 132 days post hatch (dph), standard length was reduced (7–13% reduction) at 199 and 109 mg tPAH/kg dry sediment, respectively, and wet weight for both time periods was reduced at concentrations at and above 109 mg tPAH/kg dry sediment (21–38% reduction). A significant reduction (51–65%) in F0 fecundity occurred at the two highest test concentrations, but no difference was observed in F1 embryo survival. This study is the first to report the effects of chronic laboratory exposure to oiled sediment, and will assist the development of population models for evaluating risk to benthic spawning fish species exposed to oiled sediments.

Estimation of Wildlife Hazard Levels Using Interspecies Correlation Models and Standard Laboratory Rodent Toxicity Data

Toxicity data from laboratory rodents are widely available and frequently used in human health assessments as animal model data. This study explores the possibility of using single rodent acute toxicity values to predict chemical toxicity to a diversity of wildlife species and estimate hazard levels from modeled species sensitivity distributions (SSD). Interspecies correlation estimation (ICE) models predict toxicity values for untested species using the sensitivity relationship between measured toxicity values of two species. Predicted toxicity values can subsequently populate SSD for application in ecological risk assessments. Laboratory mouse and rat toxicity values were used to estimate toxicity to wildlife and the predicted values then were used to derive SSD hazard dose levels. Toxicity values were predicted within fivefold of measured toxicity values for 78% of ICE models using laboratory rat or mouse toxicity as a surrogate value. Hazard dose levels (HD5) were within fivefold of measured estimates for 72% of SSD developed using laboratory rodent ICE models. Rodents were most often in the least sensitive quartile of species sensitivity distributions, and therefore toxicity values alone may not adequately represent the toxicity to many species of concern without appropriate safety or assessment factors. Laboratory rodent toxicity data offer an additional source of information that can be used to predict hazard levels for wildlife species, and thus offer a starting point for both health and ecological risk assessment.

FEMALE-BIASED SEX RATIO ARISES AFTER PARENTAL CARE IN THE SEXUALLY DIMORPHIC WAVED ALBATROSS (PHOEBASTRIA IRRORATA)

Abstract In response to evidence of sexual segregation at foraging grounds as well as male-biased band recoveries, we investigated the ontogeny of the female- biased adult sex ratio in the Waved Albatross (Phoebastria irrorata), an IUCN “critically endangered species” essentially endemic to Isla Española, Galapagos, Ecuador. Using a molecular technique to determine the sex of chicks and adults and known fate analysis of chicks during rearing, we found no evidence of a sex-ratio bias at hatching or fledging in three consecutive years with variable reproductive success. Although male chicks were significantly larger than females at fledging, survival to fledging of a large sample of male and female chicks did not differ. The sex ratio among a cohort of young adults at approximately the age of first breeding (eight years) also did not differ significantly from parity. Differential adult mortality, including male-biased mortality in fisheries, is the most probable cause of a female- biased population sex ratio, and is at least partially responsible for an apparent reduction in the number of breeding pairs of this species. El Albatros Phoebastria irrorata, una Especie con Dimorfismo Sexual, Presenta una Mayor Proporción de Hembras Luego del Cuidado Parental

A framework for linking population model development with ecological risk assessment objectives

The value of models that link organism-level impacts to the responses of a population in ecological risk assessments (ERAs) has been demonstrated extensively over the past few decades. There is little debate about the utility of these models to translate multiple organism-level endpoints into a holistic interpretation of effect to the population; however, there continues to be a struggle for actual application of these models as a common practice in ERA. Although general frameworks for developing models for ERA have been proposed, there is limited guidance on when models should be used, in what form, and how to interpret model output to inform the risk managers decision. We propose a framework for developing and applying population models in regulatory decision making that focuses on trade-offs of generality, realism, and precision for both ERAs and models. We approach the framework development from the perspective of regulators aimed at defining the needs of specific models commensurate with the assessment objective. We explore why models are not widely used by comparing their requirements and limitations with the needs of regulators. Using a series of case studies under specific regulatory frameworks, we classify ERA objectives by trade-offs of generality, realism, and precision and demonstrate how the output of population models developed with these same trade-offs informs the ERA objective. We examine attributes for both assessments and models that aid in the discussion of these trade-offs. The proposed framework will assist risk assessors and managers to identify models of appropriate complexity and to understand the utility and limitations of a models output and associated uncertainty in the context of their assessment goals. Integr Environ Assess Manag 2018;14:369-380. Published 2017. This article is a US Government work and is in the public domain in the USA.

Spatially explicit assessment of estuarine fish after Deepwater Horizon oil spill: trade-off in complexity and parsimony

Evaluating long-term contaminant effects on wildlife populations depends on spatial information about habitat quality, heterogeneity in contaminant exposure, and sensitivities and distributions of species integrated into a systems modeling approach. Rarely is this information readily available, making it difficult to determine the applicability of realistic models to quantify population-level risks. To evaluate the trade-offs between data demands and increased specificity of spatially explicit models for population-level risk assessments, we developed a model for a standard toxicity test species, the sheepshead minnow (Cyprinodon variegatus), exposed to oil contamination following the Deepwater Horizon oil spill and compared the output with various levels of model complexity to a standard risk quotient approach. The model uses habitat and fish occupancy data collected over five sampling periods throughout 2008-2010 in Pensacola and Choctawhatchee Bays, Florida, USA, to predict species distribution, field-collected and publically available data on oil distribution and concentration, and chronic toxicity data from laboratory assays applied to a matrix population model. The habitat suitability model established distribution of fish within Barataria Bay, Louisiana, USA, and the population model projected the dynamics of the species in the study area over a 5-yr period (October 2009-September 2014). Vital rates were modified according to estimated contaminant concentrations to simulate oil exposure effects. To evaluate the differences in levels of model complexity, simulations varied from temporally and spatially explicit, including seasonal variation and location-specific oiling, to simple interpretations of a risk quotient derived for the study area. The results of this study indicate that species distribution, as well as spatially and temporally variable contaminant concentrations, can provide a more ecologically relevant evaluation of species recovery from catastrophic environmental impacts but might not be cost-effective or efficient for rapid assessment needs.

Assessment of indirect pesticide effects on worm‐eating warbler populations in a managed forest ecosystem

Ecological risk assessments rarely evaluate indirect pesticide effects. Pesticides causing no direct mortality in wildlife can still reduce prey availability, resulting in a lower reproductive rate or poor juvenile condition. Few studies have examined these consequences at the population level. We use a four-year data set from a forest ecosystem in which Bacillus thuringiensis kurstaki (Btk) was applied to control gypsy moths (Lymantria dispar L.). Lower worm-eating warbler (Helmitheros vermivorus) productivity on Btk plots contributed to an intrinsic growth rate <1. Altered provisioning behavior by adults led to lower nestling mass in Btk-treated plots, and simulations of reduced juvenile survival expected as a result further reduced population growth rate. The present study explored different spatial representations of treated areas, using a two-patch matrix model incorporating dispersal. Minimal migration from areas with increasing subpopulations could compensate for detrimental reductions in reproductive success and juvenile survival within treated subpopulations. We also simulated population dynamics with different proportions of treated areas to inform management strategies in similar systems. Nontoxic insecticides are capable of impacting nontarget populations with consistent, long-term use and should be evaluated based on the spatial connectivity representative of habitat availability and the time period appropriate for risk assessment of pesticide effects in wildlife populations.

Simulated developmental and reproductive impacts on amphibian populations and implications for assessing long-term effects

Fish endpoints measured in early life stage toxicity tests are often used as representative of larval amphibian sensitivity in Ecological Risk Assessment (ERA). This application potentially overlooks the impact of developmental delays on amphibian metamorphosis, and thereby reduced survival, in amphibian populations constrained by habitat availability. Likewise, the effects of reduced productivity or altered sexual development as a result of chemical exposure are not presented in terms of lower population fecundity in these surrogate tests. Translating endpoints measured in toxicity tests to those that are more representative of amphibian ecology and population dynamics provides a means of identifying how developmental effects result in long-term impacts. Here we compare effects of developmental delay on metamorphosis success in six anuran species and simulate population-level impacts of subsequent reductions in larval survival as well as potential reductions in fecundity as a result of developmental impacts. We use deterministic matrix models to compare realistic combinations of amphibian demographic rates and relative impacts of reduced growth on larval survival and subsequently on population growth. Developmental delays are less detrimental in species with longer and less synchronous larval periods. All six species were most sensitive to changes in first-year survival, and damping ratios were generally a good indicator of resilience to perturbations in both larval survival and fecundity. Further identification of species and population-level vulnerabilities can improve the evaluation of sublethal effects in relevant context for ERA.