Roads to ruin: conservation threats to a sentinel species across an urban gradient.

Urbanization poses a global challenge to species conservation. This is primarily understood in terms of physical habitat loss, as agricultural and forested lands are replaced with urban infrastructure. However, aquatic habitats are also chemically degraded by urban development, often in the form of toxic stormwater runoff. Here we assess threats of urbanization to coho salmon throughout developed areas of the Puget Sound Basin in Washington, USA. Puget Sound coho are a sentinel species for freshwater communities and also a species of concern under the U.S. Endangered Species Act. Previous studies have demonstrated that stormwater runoff is unusually lethal to adult coho that return to spawn each year in urban watersheds. To further explore the relationship between land use and recurrent coho die-offs, we measured mortality rates in field surveys of 51 spawning sites across an urban gradient. We then used spatial analyses to measure landscape attributes (land use and land cover, human population density, roadways, traffic intensity, etc.) and climatic variables (annual summer and fall precipitation) associated with each site. Structural equation modeling revealed a latent urbanization gradient that was associated with road density and traffic intensity, among other variables, and positively related to coho mortality. Across years within sites, mortality increased with summer and fall precipitation, but the effect of rainfall was strongest in the least developed areas and was essentially neutral in the most urbanized streams. We used the best-supported structural equation model to generate a predictive mortality risk map for the entire Puget Sound Basin. This map indicates an ongoing and widespread loss of spawners across much of the Puget Sound population segment, particularly within the major regional north-south corridor for transportation and development. Our findings identify current and future urbanization-related threats to wild coho, and show where green infrastructure and similar clean water strategies could prove most useful for promoting species conservation and recovery.

A fish of many scales: extrapolating sublethal pesticide exposures to the productivity of wild salmon populations.

For more than a decade, numerous pesticides have been detected in river systems of the western United States that support anadromous species of Pacific salmon and steelhead. Over the same interval, several declining wild salmon populations have been listed as either threatened or endangered under the U.S. Endangered Species Act (ESA). Because pesticides occur in surface waters that provide critical habitat for ESA-listed stocks, they are an ongoing concern for salmon conservation and recovery throughout California and the Pacific Northwest. Because pesticide exposures are typically sublethal, a key question is whether toxicological effects at (or below) the scale of the individual animal ultimately reduce the productivity and recovery potential of wild populations. In this study we evaluate how the sublethal impacts of pesticides on physiology and behavior can reduce the somatic growth of juvenile chinook salmon (Oncorhynchus tshawytscha) and, by extension, subsequent size-dependent survival when animals migrate to the ocean and overwinter in their first year. Our analyses focused on the organophosphate and carbamate classes of insecticides. These neurotoxic chemicals have been widely detected in aquatic environments. They inhibit acetylcholinesterase, an enzyme in the salmon nervous system that regulates neurotransmitter-mediated signaling at synapses. Based on empirical data, we developed a model that explicitly links sublethal reductions in acetylcholinesterase activity to reductions in feeding behavior, food ration, growth, and size at migration. Individual size was then used to estimate size-dependent survival during migration and transition to the sea. Individual survival estimates were then integrated into a life-history population projection matrix and used to calculate population productivity and growth rate. Our results indicate that short-term (i.e., four-day) exposures that are representative of seasonal pesticide use may be sufficient to reduce the growth and size at ocean entry of juvenile chinook. The consequent reduction in individual survival over successive years reduces the intrinsic productivity (lambda) of a modeled ocean-type chinook population. Overall, we show that exposures to common pesticides may place important constraints on the recovery of ESA-listed salmon species, and that simple models can be used to extrapolate toxicological impacts across several scales of biological complexity.

Legacy habitat contamination as a limiting factor for Chinook salmon recovery in the Willamette Basin, Oregon, USA.

In the western United States, the long-term recovery of many Pacific salmon populations is inextricably linked to freshwater habitat quality. Industrial activities from the past century have left a legacy of pollutants that persist, particularly near working waterfronts. The adverse impacts of these contaminants on salmon health have been studied for decades, but the population-scale consequences of chemical exposure for salmonids are still poorly understood. We estimated acute and delayed mortality rates for seaward migrating juvenile Chinook salmon that feed and grow in a Superfund-designated area in the Lower Willamette River in Portland, Oregon. We combined previous, field-collected exposure data for juvenile Chinook salmon together with reduced growth and disease resistance data from earlier field and laboratory studies. Estimates of mortality were then incorporated into a life cycle model to explore chemical habitat-related fish loss. We found that 54% improved juvenile survival-potentially as a result of future remediation activities-could increase adult Chinook salmon population abundance by more than 20%. This study provides a framework for evaluating pollution remediation as a positive driver for species recovery.

Coho salmon spawner mortality in western US urban watersheds: bioinfiltration prevents lethal storm water impacts.

Adult coho salmon Oncorhynchus kisutch return each autumn to freshwater spawning habitats throughout western North America. The migration coincides with increasing seasonal rainfall, which in turn increases storm water run-off, particularly in urban watersheds with extensive impervious land cover. Previous field assessments in urban stream networks have shown that adult coho are dying prematurely at high rates (>50%). Despite significant management concerns for the long-term conservation of threatened wild coho populations, a causal role for toxic run-off in the mortality syndrome has not been demonstrated.We exposed otherwise healthy coho spawners to: (i) artificial storm water containing mixtures of metals and petroleum hydrocarbons, at or above concentrations previously measured in urban run-off; (ii) undiluted storm water collected from a high traffic volume urban arterial road (i.e. highway run-off); and (iii) highway run-off that was first pre-treated via bioinfiltration through experimental soil columns to remove pollutants.We find that mixtures of metals and petroleum hydrocarbons - conventional toxic constituents in urban storm water - are not sufficient to cause the spawner mortality syndrome. By contrast, untreated highway run-off collected during nine distinct storm events was universally lethal to adult coho relative to unexposed controls. Lastly, the mortality syndrome was prevented when highway run-off was pretreated by soil infiltration, a conventional green storm water infrastructure technology.Our results are the first direct evidence that: (i) toxic run-off is killing adult coho in urban watersheds, and (ii) inexpensive mitigation measures can improve water quality and promote salmon survival. Synthesis and applications. Coho salmon, an iconic species with exceptional economic and cultural significance, are an ecological sentinel for the harmful effects of untreated urban run-off. Wild coho populations cannot withstand the high rates of mortality that are now regularly occurring in urban spawning habitats. Green storm water infrastructure or similar pollution prevention methods should be incorporated to the maximal extent practicable, at the watershed scale, for all future development and redevelopment projects, particularly those involving transportation infrastructure.

Modeling the effects of chronic toxicity on fish populations: the influence of life-history strategies.

Five life-history scenarios were composed to simulate fish population adaptations for survival under various environmental conditions. The scenarios encompassed differences in stage-specific survival, fecundity and hatch success, number of spawning events, and life-span effect response to chronic toxic impacts. The strategies represent a good survivor/generalist (GS), a species exhibiting high young-of-the-year survival, a species exhibiting high adult survival, a species with no parental care or guarding behavior, and an anadromous salmonid strategy. Although the modeled scenarios were similar in population growth rate and imposed toxic effects, differences concerning the influence of various traits were found. Scenarios characterized by a short life span, short time to reproductive maturity, moderate to high survival to reproductive maturity, large number of spawning events, and parental guarding behaviors experienced less perturbation from the imposed chronic stresses. The GS scenario, modeled after the round goby (Neogobius melanostomus), exemplified these characteristics. Scenarios exhibiting little difference between reproductive effort for younger and older adults recovered quickly from stressors on fecundity and adult survival rates. Greater population decline in response to commensurate impacts was seen for life-history strategies with long life span, no parental guarding behaviors, semelparity and annual iteroparity, high adult survival rates, and moderate to low fecundity.

Population survivorship index for fish and amphibians: application to criterion development and risk assessment.

Criterion development currently focuses on physiological responses when determining permitted chemical concentrations in environmental media. Losses of biodiversity attributed to chemical pollution may be related not only to physiological sensitivity but also to inherent population characteristics that are not included in risk assessment or criterion development. In the present study, we proposed a process and a tool for summarizing population- and species-level information that contributes to long-term survivorship. We investigated the influences of life-history strategies of fish and amphibians that contribute to variations in population sensitivity or resiliency. A life-history survivorship index for application in criterion development and risk assessment was developed to help identify which species in a study system possess life-history strategies inherently sensitive to chemical stressors. It includes life-history characteristics of fecundity, number of spawning events, life stages, parental care, attrition rates, time to reproductive maturity, and other factors. Survivorship index values may be used as multipliers to permitting criteria, resulting in toxicological-ecological guidelines that incorporate toxicological information with regional ecological and population characteristics for local or regional application. We intended the procedure to serve as a step toward incorporating population and ecological information into regulatory procedures with the goal of protecting biodiversity from chronic toxic impacts.

A modeled comparison of direct and food web-mediated impacts of common pesticides on Pacific salmon.

In the western United States, pesticides used in agricultural and urban areas are often detected in streams and rivers that support threatened and endangered Pacific salmon. Although concentrations are rarely high enough to cause direct salmon mortality, they can reach levels sufficient to impair juvenile feeding behavior and limit macroinvertebrate prey abundance. This raises the possibility of direct adverse effects on juvenile salmon health in tandem with indirect effects on salmon growth as a consequence of reduced prey abundance. We modeled the growth of ocean-type Chinook salmon (Oncorhynchus tshawytscha) at the individual and population scales, investigating insecticides that differ in how long they impair salmon feeding behavior and in how toxic they are to salmon compared to macroinvertebrates. The relative importance of these direct vs. indirect effects depends both on how quickly salmon can recover and on the relative toxicity of an insecticide to salmon and their prey. Model simulations indicate that when exposed to a long-acting organophosphate insecticide that is highly toxic to salmon and invertebrates (e.g., chlorpyrifos), the long-lasting effect on salmon feeding behavior drives the reduction in salmon population growth with reductions in prey abundance having little additional impact. When exposed to short-acting carbamate insecticides at concentrations that salmon recover from quickly but are lethal to invertebrates (e.g., carbaryl), the impacts on salmon populations are due primarily to reductions in their prey. For pesticides like carbaryl, prey sensitivity and how quickly the prey community can recover are particularly important in determining the magnitude of impact on their predators. In considering both indirect and direct effects, we develop a better understanding of potential impacts of a chemical stressor on an endangered species and identify data gaps (e.g., prey recovery rates) that contribute uncertainty to these assessments.

Predicted transport of pyrethroid insecticides from an urban landscape to surface water.

The authors developed a simple screening-level model of exposure of aquatic species to pyrethroid insecticides for the lower American River watershed (California, USA). The model incorporated both empirically derived washoff functions based on existing, small-scale precipitation simulations and empirical data on pyrethroid insecticide use and watershed properties for Sacramento County, California, USA. The authors calibrated the model to in-stream monitoring data and used it to predict daily river pyrethroid concentration from 1995 through 2010. The model predicted a marked increase in pyrethroid toxic units starting in 2000, coincident with an observed watershed-wide increase in pyrethroid use. After 2000, approximately 70% of the predicted total toxic unit exposure in the watershed was associated with the pyrethroids bifenthrin and cyfluthrin. Pyrethroid applications for aboveground structural pest control on the basis of suspension concentrate categorized product formulations accounted for greater than 97% of the predicted total toxic unit exposure. Projected application of mitigation strategies, such as curtailment of structural perimeter band and barrier treatments as recently adopted by the California Department of Pesticide Regulation, reduced predicted total toxic unit exposure by 84%. The model also predicted that similar reductions in surface-water concentrations of pyrethroids could be achieved through a switch from suspension concentrate-categorized products to emulsifiable concentrate-categorized products without restrictions on current-use practice. Even with these mitigation actions, the predicted concentration of some pyrethroids would continue to exceed chronic aquatic life criteria.

Estimating the future decline of wild coho salmon populations resulting from early spawner die-offs in urbanizing watersheds of the Pacific Northwest, USA.

Since the late 1990 s, monitoring efforts evaluating the effectiveness of urban stream restoration projects in the greater metropolitan area of Seattle, Washington, USA, have detected high rates of premature mortality among adult coho salmon (Oncorhynchus kisutch) in restored spawning habitats. Affected animals display a consistent suite of symptoms (e.g., disorientation, lethargy, loss of equilibrium, gaping, fin splaying) that ultimately progresses to death on a timescale of a few hours. Annual rates of prespawn mortality observed over multiple years, across several drainages, have ranged from approximately 20% to 90% of the total fall run within a given watershed. Current weight-of-evidence suggests that coho prespawn mortality is caused by toxic urban stormwater runoff. To evaluate the potential consequences of current and future urbanization on wild coho salmon, we constructed life-history models to estimate the impacts of prespawn mortality on coho populations and metapopulations. At the low (20%) and high (90%) ends of the range of observed mortality, model results indicated the mean time to extinction of localized coho populations in 115 and 8 y, respectively. The presence of productive source populations (i.e., unaffected by prespawn mortality) within a metapopulation reduced local extinction risk. However, as more populations within a metapopulation become affected by spawner die-offs prior to spawning, the source population's productivity declined. These simple models demonstrate the potential for rapid losses from coho populations in urbanizing watersheds. Because the models do not account for possible impacts of toxic runoff to other coho life stages, they likely underestimate the cumulative impacts of nonpoint source pollution on wild populations.

Adverse outcome pathways and ecological risk assessment: bridging to population-level effects.

Maintaining the viability of populations of plants and animals is a key focus for environmental regulation. Population-level responses integrate the cumulative effects of chemical stressors on individuals as those individuals interact with and are affected by their conspecifics, competitors, predators, prey, habitat, and other biotic and abiotic factors. Models of population-level effects of contaminants can integrate information from lower levels of biological organization and feed that information into higher-level community and ecosystem models. As individual-level endpoints are used to predict population responses, this requires that biological responses at lower levels of organization be translated into a form that is usable by the population modeler. In the current study, we describe how mechanistic data, as captured in adverse outcome pathways (AOPs), can be translated into modeling focused on population-level risk assessments. First, we describe the regulatory context surrounding population modeling, risk assessment and the emerging role of AOPs. Then we present a succinct overview of different approaches to population modeling and discuss the types of data needed for these models. We describe how different key biological processes measured at the level of the individual serve as the linkage, or bridge, between AOPs and predictions of population status, including consideration of community-level interactions and genetic adaptation. Several case examples illustrate the potential for use of AOPs in population modeling and predictive ecotoxicology. Finally, we make recommendations for focusing toxicity studies to produce the quantitative data needed to define AOPs and to facilitate their incorporation into population modeling.

Relating results of chronic toxicity responses to population-level effects: modeling effects on wild Chinook salmon populations.

Standard toxicity tests assess the physiological responses of individual organisms to exposure to toxic substances under controlled conditions. Time and space restrictions often prohibit the assessment of population-level responses to a toxic substance. Compounds affecting various toxicity endpoints, such as growth, fecundity, behavior, or immune function, alter different demographic traits and produce different impacts on the population. Chronic effects of immune suppression, reproductive impairment, and growth reduction were examined using life history models for Chinook salmon (Oncorhynchus tshawytscha). Modeled immune suppression acted through reductions in age-specific survival, with first- and second-year survival producing the greatest changes in the population growth rate (lamda). A 10% reduction in various reproductive parameters all produced a similar lamda, but different sensitivity and stable age distributions. Growth reduction models incorporated effects to both survival and reproduction and produced additive effects. Overall, model output indicated that for Chinook salmon, alteration of first-year survival has the greatest relative impact on lamda. Results support the importance of linking toxicity endpoints to the demographic traits that they influence and help generate toxicity tests that are more relevant for the species. Life history modeling provides a useful tool to develop testable hypotheses regarding specific and comparative population-level impacts.