A Sensory System at the Interface between Urban Stormwater Runoff and Salmon Survival

Department of Environmental and Molecular Toxicology, Oregon State University, Corvallis, Oregon, United States
Environmental Science and Technology (Impact Factor: 5.33). 05/2007; 41(8):2998-3004. DOI: 10.1021/es062287r
Source: PubMed


Motor vehicles are a major source of toxic contaminants such as copper, a metal that originates from vehicle exhaust and brake pad wear. Copper and other pollutants are deposited on roads and other impervious surfaces and then transported to aquatic habitats via stormwater runoff. In the western United States, exposure to non-point source pollutants such as copper is an emerging concern for many populations of threatened and endangered Pacific salmon (Oncorhynchus spp.) that spawn and rear in coastal watersheds and estuaries. To address this concern, we used conventional neurophysiological recordings to investigate the impact of ecologically relevant copper exposures (0-20 microg/L for 3 h) on the olfactory system of juvenile coho salmon (O. kisutch). These recordings were combined with computer-assisted video analyses of behavior to evaluate the sensitivity and responsiveness of copper-exposed coho to a chemical predation cue (conspecific alarm pheromone). The sensory physiology and predator avoidance behaviors of juvenile coho were both significantly impaired by copper at concentrations as low as 2 microg/L. Therefore, copper-containing stormwater runoff from urban landscapes has the potential to cause chemosensory deprivation and increased predation mortality in exposed salmon.

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    • "Although urban storm water is chemically complex, field collected samples consistently contain motor vehiclederived mixtures of metals and polycyclic aromatic hydrocarbons (PAHs), many of which are toxic to salmon at other life stages (e.g. copper, McIntyre et al. 2012; Sandahl et al. 2007; PAHs, Meador et al. 2006; Heintz et al. 2000). If the mortality syndrome could be reproduced with an environmentally realistic mixture of metals and PAHs, it would then be possible to identify the causal agents by removing different components of the mixture. "
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    ABSTRACT: 1. 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 runoff , 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 runoff in the mortality syndrome has not been demonstrated. 2. 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 runoff ; (ii) undiluted storm water collected from a high traffic volume urban arterial road (i.e. highway runoff); and (iii) highway runoff that was first pre-treated via bioinfiltra-tion through experimental soil columns to remove pollutants. 3. 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 runoff collected during nine distinct storm events was universally lethal to adult coho relative to unexposed controls. Lastly, the mortality syndrome was prevented when highway runoff was pretreated by soil infiltration, a conventional green storm water infrastructure technology. 4. Our results are the first direct evidence that: (i) toxic runoff is killing adult coho in urban watersheds, and (ii) inexpensive mitigation measures can improve water quality and promote salmon survival. 5. 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 runoff. 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.
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    • "The rhizocephalan may also reduce crab foraging by impairing the ability of crabs to detect prey. Infected crabs took substantially longer than uninfected crabs to react to prey in both our experiments and those of Toscano et al. (2014), which can be indicative of decreased sensory perception (Sandahl et al., 2007). Infections by rhizocephalans are known to damage the nervous system of their hosts as the interna rootlets penetrate the thoracic ganglion and ventral nerve cord (Neilson, 1970). "
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    ABSTRACT: Although castration by rhizocephalans on crab species is well documented, the accompanying effects of infection on behavior and metabolism have remained relatively unstudied. In this investigation, we examined flat back mud crab (Eurypanopeus depressus) physiology and behavior in an attempt to elucidate why infected crabs exhibit a previously documented reduced functional response. Crab respiration and digestion rates were analyzed to determine if infection altered metabolic rate. Laboratory behavioral experiments and a field survey were conducted to determine how infection alters crab feeding behavior and activity levels. Although we found no statistical difference between infected and uninfected crab metabolic or digestive rates, we discovered that, both in the lab and in the field, infected crabs exhibited substantially altered behavior. In the laboratory infected crabs reacted nearly 3 times slower to the presence of prey and spent over 22% more of their time hiding, whereas uninfected crabs were significantly more active. During field sampling, infected crabs were significantly more likely to be found hiding within empty oyster shells while uninfected crabs spent more time in the exposed positions of the habitat. We conclude that rhizocephalans can reduce the host functional response by altering host behavior. Here, these induced changes can impact community structure by altering trophic interactions so that infected crabs spend less time foraging and more time hiding, potentially reducing their predation risk.
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    • "Chemical pollutants can impact one or more links in the chain of chemical communication between individual organisms (Brown et al., 1982; Lürling, 2012; Olsén, 2011). Unlike terrestrial animals, fish and aquatic crustaceans possess olfactory and taste receptors that are in direct contact with chemicals in the surrounding fluid medium which can disturb receptor function (Baldwin et al., 2003; Olsén, 2011; Sandahl et al., 2007). Elevated levels of numerous toxicants can impair chemoreception through irreversible physiological damage to receptor cells and organs, and by binding to active sites and preventing signal molecules from being able to reach the binding site (Blinova and Cherkashin, 2012; Tierney et al., 2010). "
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    ABSTRACT: Before reaching concentrations that are high enough to cause mortality, elevated levels of chemical pollution can significantly alter a keystone indicator species’ ability to extract sensory information. To organisms that rely on chemical signals to make crucial ecological decisions, increased amounts of a pollutant may impact chemoreceptive abilities by altering the perception of the sensory landscape or impairing the functioning of sensory organs. Heavy metal pollutants entering an aquatic ecosystem are of increasing concern due to discernible effects on chemoreception in many ecologically and economically important species. In order to determine the effects of sublethal copper toxicity on chemically mediated behavior, male and female rusty crayfish, Orconectes rusticus, were exposed to ecologically relevant concentrations of copper (4.5, 45, and 450 µg/l) for 120 h. Following exposure, crayfish were allowed to orient toward a food odor stimulus. During orientation trials, select crayfish oriented under a point or nonpoint source copper background pollutant at the same concentration as the exposure period. Orientation trials were videotaped and analyzed using EthoVision XT 8.5 (Noldus Information Technology, The Netherlands) for differences in overall success in locating the food source and orienting parameters. Significant differences were found in the overall orientation ability of O. rusticus to locate an odor source when previously exposed to copper in combination with a source of pollution in the background of orientation trials. Crayfish exposed to copper in any capacity during the experiment (regardless of concentration or background during trials) showed slower walking speeds toward the source, decreased turning angles, increased heading angles toward the source, and decreased upstream heading angles. Results from this experiment support that copper impairs the ability of crayfish to detect, process, and/or respond appropriately to chemosensory information in order to successfully localize a food odor source.
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