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

Abstract

Abstract. 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 sizedependent 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 neurotransmittermediated 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 sizedependent 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 oceantype 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.

Adverse outcome pathways and ecological risk assessment: Bridging to population‐level effects

“…An individual-based model was developed based on empirical data that explicitly links sublethal reductions in acetylcholinesterase activity to reductions in feeding behavior, food consumption, growth, and size at outmigration of sub-yearling chinook salmon (Oncorhynchus tshawytscha; [56]). Individual size was used to estimate sizedependent sub-yearling survival during the migration and transition to the sea.…”

Adding Value to Ecological Risk Assessment with Population Modeling

“…For ethical reasons there may be restrictions on the quantity and type of laboratory testing permitted on such species, and in such cases application of population modeling can make the most out of limited test data. For example, Baldwin et al (2009) investigated the population-level effects of acetylcholinesterase (AChE) inhibiting pesticides on endangered Chinook salmon. Limited laboratory studies demonstrated that sublethal reductions of AChE activity resulted in decreased swimming and feeding behaviors.…”

“…For example, a number of studies investigating the effects of spatial complexity in exposure scenarios indicate that inter-individual variability in exposure can either increase (Palmqvist and Forbes 2008) or reduce (Dalkvist et al 2009) risk compared to the standard homogeneous exposure scenarios typically assumed in risk assessment. Likewise, by incorporating realistic information on the species' ecology into a population model, Baldwin et al (2009) were able to show that the change in size when fish migrated to the ocean caused a reduction in individual survival over successive years and thereby reduced the population growth rate.…”

Interactive effects of pesticide exposure and habitat structure on behavior and predation of a marine larval fish

“…Larval and juvenile stages of resident organisms are at particular risk in that they may be exposed during their most vulnerable developmental stages while using these habitats as nursery grounds (Beck et al 2003;Courrat et al 2009). Ultimately, the impacts of pesticides in aquatic environments can cascade from individuals to populations (Baldwin et al 2009), and subsequently decrease biodiversity (Beketov et al 2013) and alter community structure (Fleeger et al 2003;Rohr et al 2006;Macneale et al 2010), although the mechanisms behind these impacts can be varied and complex.…”

“…Importantly, the population ecology of organisms often depends on behavioral outcomes (Weis et al 1999;Murphy et al 2008;Relyea and Edwards 2010). Behavior can thus be a powerful tool to link the sub-organismal effects of sublethal pesticide exposure to species interactions and populationlevel processes (Weis et al 2001;Baldwin et al 2009;Weis and Candelmo 2012).…”