Julann Spromberg

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.

Relating Results of Chronic Toxicity Responses to Population-Level Effects: Modeling Effects on Wild Chinook Salmon Populations

Abstract 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 (λ). A 10% reduction in various reproductive parameters all produced a similar λ, 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 λ. 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.

Adding Value to Ecological Risk Assessment with Population Modeling

ABSTRACT Current measures used to estimate the risks of toxic chemicals are not relevant to the goals of the environmental protection process, and thus ecological risk assessment (ERA) is not used as extensively as it should be as a basis for cost-effective management of environmental resources. Appropriate population models can provide a powerful basis for expressing ecological risks that better inform the environmental management process and thus that are more likely to be used by managers. Here we provide at least five reasons why population modeling should play an important role in bridging the gap between what we measure and what we want to protect. We then describe six actions needed for its implementation into management-relevant ERA.

Integrating Population Modeling into Ecological Risk Assessment

This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln.It has been accepted for inclusion in Valery Forbes Publications by an authorized administrator of DigitalCommons@University of Nebraska -Lincoln. For more information, please contact proyster@unl.edu.

Effects of Legacy Persistent Organic Pollutants (POPs) in Fish—Current and Future Challenges

Persistent organic pollutants (POPs) are ubiquitous environmental contaminants that are not readily degraded in the environment. They are typically lipophilic, bioaccumulating in tissues of aquatic organisms and biomagnifying in freshwater and marine food webs. POPs include a wide range of halogenated legacy contaminants [e.g., polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethanes (DDTs), chlordanes, hexachlorobenzene (HCB)] that have been banned because of their toxicity to humans and wildlife; compounds such as polychlorinated dibenzofurans (PCDFs) and polychlorinated dibenzodioxins (PCDDs) that can be produced naturally (e.g., through forest fires and volcanic eruptions) or through industrial processes; and chemicals of emerging concern [e.g., polybrominated diphenyl ethers (PBDEs) and perfluorinated compounds]. Although many POPs are no longer being released into the environment, they continue to be reported at toxic concentrations in fish, and there is much that is not yet understood about their modes of action and their ecological effects on aquatic habitats. This chapter reviews current information on (1) uptake and metabolism of these compounds by fish; (2) their biological effects, including their actions as endocrine disruptors, reproductive, developmental, neurological, immunological, and metabolic toxicants and carcinogens; and (3) recent efforts to evaluate the ecological risks of exposure to such compounds on fish populations and aquatic communities.

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

Summary 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.

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

Abstract 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.