Wildlife ecological risk assessment in the 21st century: Promising technologies to assess toxicological effects.

Despite advances in toxicity testing and the development of new approach methodologies (NAMs) for hazard assessment, the ecological risk assessment (ERA) framework for terrestrial wildlife (i.e., air-breathing amphibians, reptiles, birds, and mammals) has remained unchanged for decades. While survival, growth, and reproductive endpoints derived from whole-animal toxicity tests are central to hazard assessment, nonstandard measures of biological effects at multiple levels of biological organization (e.g., molecular, cellular, tissue, organ, organism, population, community, ecosystem) have the potential to enhance the relevance of prospective and retrospective wildlife ERAs. Other factors (e.g., indirect effects of contaminants on food supplies and infectious disease processes) are influenced by toxicants at individual, population, and community levels, and need to be factored into chemically based risk assessments to enhance the "eco" component of ERAs. Regulatory and logistical challenges often relegate such nonstandard endpoints and indirect effects to postregistration evaluations of pesticides and industrial chemicals and contaminated site evaluations. While NAMs are being developed, to date, their applications in ERAs focused on wildlife have been limited. No single magic tool or model will address all uncertainties in hazard assessment. Modernizing wildlife ERAs will likely entail combinations of laboratory- and field-derived data at multiple levels of biological organization, knowledge collection solutions (e.g., systematic review, adverse outcome pathway frameworks), and inferential methods that facilitate integrations and risk estimations focused on species, populations, interspecific extrapolations, and ecosystem services modeling, with less dependence on whole-animal data and simple hazard ratios. Integr Environ Assess Manag 2024;20:725-748. © 2023 His Majesty the King in Right of Canada and The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC). Reproduced with the permission of the Minister of Environment and Climate Change Canada. This article has been contributed to by US Government employees and their work is in the public domain in the USA.

Toxicological effects assessment for wildlife in the 21st century: Review of current methods and recommendations for a path forward.

Model species (e.g., granivorous gamebirds, waterfowl, passerines, domesticated rodents) have been used for decades in guideline laboratory tests to generate survival, growth, and reproductive data for prospective ecological risk assessments (ERAs) for birds and mammals, while officially adopted risk assessment schemes for amphibians and reptiles do not exist. There are recognized shortcomings of current in vivo methods as well as uncertainty around the extent to which species with different life histories (e.g., terrestrial amphibians, reptiles, bats) than these commonly used models are protected by existing ERA frameworks. Approaches other than validating additional animal models for testing are being developed, but the incorporation of such new approach methodologies (NAMs) into risk assessment frameworks will require robust validations against in vivo responses. This takes time, and the ability to extrapolate findings from nonanimal studies to organism- and population-level effects in terrestrial wildlife remains weak. Failure to adequately anticipate and predict hazards could have economic and potentially even legal consequences for regulators and product registrants. In order to be able to use fewer animals or replace them altogether in the long term, vertebrate use and whole organism data will be needed to provide data for NAM validation in the short term. Therefore, it is worth investing resources for potential updates to existing standard test guidelines used in the laboratory as well as addressing the need for clear guidance on the conduct of field studies. Herein, we review the potential for improving standard in vivo test methods and for advancing the use of field studies in wildlife risk assessment, as these tools will be needed in the foreseeable future. Integr Environ Assess Manag 2024;20:699-724. © 2023 His Majesty the King in Right of Canada and The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC). Reproduced with the permission of the Minister of Environment and Climate Change Canada. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Fragmentation effects on an endangered species across a gradient from the interior to edge of its range.

Understanding how habitat fragmentation affects individual species is complicated by challenges associated with quantifying species-specific habitat and spatial variability in fragmentation effects within a species' range. We aggregated a 29-year breeding survey data set for the endangered marbled murrelet (Brachyramphus marmoratus) from >42,000 forest sites throughout the Pacific Northwest (Oregon, Washington, and northern California) of the United States. We built a species distribution model (SDM) in which occupied sites were linked with Landsat imagery to quantify murrelet-specific habitat and then used occupancy models to test the hypotheses that fragmentation negatively affects murrelet breeding distribution and that these effects are amplified with distance from the marine foraging habitat toward the edge of the species' nesting range. Murrelet habitat declined in the Pacific Northwest by 20% since 1988, whereas the proportion of habitat comprising edges increased by 17%, indicating increased fragmentation. Furthermore, fragmentation of murrelet habitat at landscape scales (within 2 km of survey stations) negatively affected occupancy of potential breeding sites, and these effects were amplified near the range edge. On the coast, the odds of occupancy decreased by 37% (95% confidence interval [CI] -54 to 12) for each 10% increase in edge habitat (i.e., fragmentation), but at the range edge (88 km inland) these odds decreased by 99% (95% CI 98 to 99). Conversely, odds of murrelet occupancy increased by 31% (95% CI 14 to 52) for each 10% increase in local edge habitat (within 100 m of survey stations). Avoidance of fragmentation at broad scales but use of locally fragmented habitat with reduced quality may help explain the lack of murrelet population recovery. Further, our results emphasize that fragmentation effects can be nuanced, scale dependent, and geographically variable. Awareness of these nuances is critical for developing landscape-level conservation strategies for species experiencing broad-scale habitat loss and fragmentation.

Efectos de la fragmentación sobre las especies en peligro a lo largo de un gradiente desde el interior hasta el borde de su distribución Resumen Es complicado entender el efecto de la fragmentación del hábitat sobre las especies individuales debido a los retos asociados con la cuantificación de hábitats específicos por especie y la variabilidad espacial de los efectos de la fragmentación dentro de la distribución de la especie. Combinamos los datos de un censo reproductivo realizado durante 29 años para el mérgulo jaspeado (Brachyramphus marmoratus) de >42,000 sitios boscosos a lo largo del noroeste del Pacífico (Oregón, Washington, y el norte de California, EE. UU.). Construimos un modelo de distribución de especie (MDE) en el cual los sitios ocupados estuvieron vinculados con imágenes de Landsat para cuantificar el hábitat específico del mérgulo y después usamos los modelos de ocupación para comprobar la hipótesis de que la fragmentación afecta negativamente la distribución reproductiva de la especie y que estos efectos se amplifican con la distancia entre el hábitat de forrajeo marino y el borde de la distribución de anidación de la especie. El hábitat del mérgulo declinó en la zona en un 20% a partir de 1988, mientras que la proporción de hábitat que comprende bordes incrementó en un 17%, lo que indica un aumento en la fragmentación. Además, la fragmentación del hábitat del mérgulo a escala de paisaje (a de 2 km de las estaciones de censo) afectó negativamente a la ocupación de sitios potenciales de reproducción y estos efectos se amplificaron cerca del borde de la distribución. La probabilidad de ocupación disminuyó en un 37% (95% IC -54 a 12) por cada 10% de incremento en el hábitat de borde (es decir, fragmentación) en la costa, pero en el borde de la distribución (88 km tierra adentro), esta probabilidad disminuyó en un 99% (95% IC 98 a 99). De forma contraria, la probabilidad de ocupación incrementó en un 31% (95% IC 14 a 52) por cada 10% de incremento en el hábitat de borde local (a 100 m de las estaciones de censo). La evasión de la fragmentación a gran escala y el uso de hábitats con calidad reducida y fragmentados a nivel local podría explicar la falta de recuperación poblacional del mérgulo. Más allá, nuestros resultados resaltan que los efectos de la fragmentación pueden estar matizados, depender de la escala y tener variación geográfica. Es importante tener conciencia de estos matices para desarrollar estrategias de conservación a nivel paisaje para las especies que experimentan fragmentación y pérdida del hábitat a gran escala.

Method to assess the potential magnitude of terrestrial European avian population reductions from ingestion of lead ammunition.

Current estimates of terrestrial bird losses across Europe from ingestion of lead ammunition are based on uncertain or generic assumptions. A method is needed to develop defensible European-specific estimates compatible with available data that does not require long-term field studies. We propose a 2-step method using carcass data and population models. The method estimates percentage of deaths diagnosed as directly caused by lead poisoning as a lower bound and, as an upper bound, the percentage of possible deaths from sublethal lead poisoning that weakens birds, making them susceptible to death by other causes. We use these estimates to modify known population-level annual mortality. Our method also allows for potential reductions in reproduction from lead shot ingestion because reductions in survival and reproduction are entered into population models of species with life histories representative of the most groups of susceptible species. The models estimate the sustainability and potential population decreases from lead poisoning in Europe. Using the best available data, we demonstrate the method on two taxonomic groups of birds: gallinaceous birds and diurnal raptors. The direction of the population trends affects the estimate, and we incorporated such trends into the method. Our midpoint estimates of the reduction in population size of the European gallinaceous bird (< 2%) group and raptor group (2.9-7.7%) depend on the species life history, maximum growth rate, population trend, and if reproduction is assumed to be reduced. Our estimates can be refined as more information becomes available in countries with data gaps. We advocate use of this method to improve upon or supplement approaches currently being used. As we demonstrate, the method also can be applied to individual species of concern if enough data across countries are available.

Can Ingestion of Lead Shot and Poisons Change Population Trends of Three European Birds: Grey Partridge, Common Buzzard, and Red Kite?

Little is known about the magnitude of the effects of lead shot ingestion alone or combined with poisons (e.g., in bait or seeds/granules containing pesticides) on population size, growth, and extinction of non-waterbird avian species that ingest these substances. We used population models to create example scenarios demonstrating how changes in these parameters might affect three susceptible species: grey partridge (Perdix perdix), common buzzard (Buteo buteo), and red kite (Milvus milvus). We added or subtracted estimates of mortality due to lead shot ingestion (4-16% of mortality, depending on species) and poisons (4-46% of mortality) reported in the UK or France to observed mortality of studied populations after models were calibrated to observed population trends. Observed trends were decreasing for partridge (in continental Europe), stable for buzzard (in Germany), and increasing for red kite (in Wales). Although lead shot ingestion and poison at modeled levels did not change the trend direction for the three species, they reduced population size and slowed population growth. Lead shot ingestion at modeled rates reduced population size of partridges by 10%, and when combined with bait and pesticide poisons, by 18%. For buzzards, decrease in mean population size by lead shot and poisons combined was much smaller (≤ 1%). The red kite population has been recovering; however, modeled lead shot ingestion reduced its annual growth rate from 6.5% to 4%, slowing recovery. If mortality from poisoned baits could be removed, the kite population could potentially increase at a rapid annual rate of 12%. The effects are somewhat higher if ingestion of these substances additionally causes sublethal reproductive impairment. These results have uncertainty but suggest that declining or recovering populations are most sensitive to lead shot or poison ingestion, and removal of poisoned baits can have a positive impact on recovering raptor populations that frequently feed on carrion.

Evaluating risks to wildlife from coal fly ash incorporating recent advances in metals and metalloids risk assessment.

Current scientific advances in metal and metalloid risk assessment were applied to evaluate risk to aquatic and riparian wildlife species potentially impacted by residual coal fly ash after cleanup of an unprecedented large ash release into an aquatic environment-the first assessment of its kind. Risk was evaluated using multiple lines of evidence (LOE), including 1) tissue-based risk assessment of inorganic concentrations in piscivorous and insectivorous bird eggs and raccoon organs, 2) deterministic and probabilistic diet-based risk estimates for 10 receptors species, 3) raccoon health metrics, and 4) tree swallow nest productivity measures. Innovative approaches included use of tissue-based toxicity reference values (TRVs), adjustment of bioavailability in the dietary uptake models (using sequential metal extractions in sediment), partitioning chemical species into uptake compartments (e.g., prey gut, nongut, sediment), incorporating uncertainty in both modeled dose and dietary TRVs, matching TRVs to chemical forms of constituents, and pairing these LOEs with reproductive success or health status of sensitive receptor species. The weight of evidence revealed that risk to wildlife from residual ash was low and that risk, though low, was most pronounced for insectivorous birds from exposure to Se and As. This information contributes to the debate surrounding coal combustion residue regulations prompted by this ash release. Because of the responsible party's proactive approach of applying state-of-the-art methods to assess risk using several LOEs that produced consistent results, and because of their inclusion of the regulating agencies in decisions at every step of the process, the risk assessment results were accepted, and an effective approach toward cleanup protective of the environment was quickly implemented. This study highlights the value of using multiple LOEs and the latest scientific advances to assist in timely decision making to obtain an effective remedy for an emergency spill.

Effects of coal fly ash on tree swallow reproduction in Watts Bar Reservoir, Tennessee.

Coal-fly ash was released in unprecedented amounts (4.1 × 10(6) m(3) ) into the Emory River from the Tennessee Valley Authority Kingston Fossil Plant on Watts Bar Reservoir in Tennessee. Tree swallows were exposed to ash-related constituents at the ash release via their diet of emergent aquatic insects, whose larval forms can accumulate constituents from submerged river sediments. Reproduction of tree swallow colonies was assessed over a 2-year period by evaluating whether 1) ash constituent concentrations were elevated in egg, eggshell, and nestling tissues at colonies near ash-impacted river reaches compared to reference colonies, 2) production of fledglings per nesting female was significantly lower in ash-impacted colonies versus reference colonies, and 3) ash constituent concentrations or diet concentrations were correlated with nest productivity measures (clutch size, hatching success, and nestling survival, and fledglings produced per nest). Of the 26 ash constituents evaluated, 4 (Se, Sr, Cu, and Hg) were significantly elevated in tissues potentially from the ash, and 3 (Se, Sr, and Cu) in tissues or in swallow diet items were weakly correlated to at least one nest-productivity measure or egg weight. Tree swallow hatching success was significantly reduced by 12%, but fledgling production per nest was unaffected due to larger clutch sizes in the impacted than reference colonies. Bioconcentration from the ash to insects in the diet to tree swallow eggs appears to be low. Overall, adverse impacts of the ash on tree swallow reproduction were not observed, but monitoring is continuing to further ensure Se from the residual ash does not adversely affect tree swallow reproduction over time. Integr Environ Assess Manag 2015;11:56-66. © 2014 SETAC.

Differential tree and shrub production in response to fertilization and disturbance by coastal river otters in Alaska.

We explored the interacting effects of marine-derived nutrient fertilization and physical disturbance introduced by coastal river otters (Lontra canadensis) on the production and nutrient status of pristine shrub and tree communities in Prince William Sound, Alaska, USA. We compared production of trees and shrubs between latrines and non-latrines, while accounting for otter site selection, by sampling areas on and off sites. Nitrogen stable isotope analysis (delta15N) indicated that dominant tree and shrub species assimilated the marine-derived N excreted by otters. In association with this uptake, tree production increased, but shrub density and nonwoody aboveground shrub production decreased. The reduced shrub production was caused by destruction of ramets, especially blueberry (Vaccinium spp.), through physical disturbance by river otters. False azalea (Menziesia ferruginea) ramets were less sensitive to otter disturbance. Although surviving individual blueberry ramets showed a tendency for increased production per plant, false azalea allocated excess N to storage in leaves rather than growth. We found that plant responses to animal activity vary among species and levels of biological organization (leaf, plant, ecosystem). Such differences should be accounted for when assessing the influence of river otters on the carbon budget of Alaskan coastal forests at the landscape scale.