Conceived and designed the experiments: NLS MSM GMY LDR BM DW LR KDL JWD TKC. Performed the experiments: NLS MSM SGM JSL JKM LDR CAL CMS BLF BM DW LR SD JWD. Analyzed the data: NLS MSM SGM JSL GMY LDR CAL BLF BM DW LR KDL JWD TKC. Contributed reagents/materials/analysis tools: BM DW LR KDL SD JWD. Wrote the paper: NLS MSM JSL JKM GMY LDR CAL CMS BLF TKC. Led salmon spawner survey operations, including field team coordination and sample collection: SGM JSL JKM CAL CMS BLF SD. Interagency principal investigators: NLS MSM GMY LDR BM DW KDL JWD TKC.
The authors have declared that no competing interests exist.
Several Seattle-area streams in Puget Sound were the focus of habitat restoration projects in the 1990s. Post-project effectiveness monitoring surveys revealed anomalous behaviors among adult coho salmon returning to spawn in restored reaches. These included erratic surface swimming, gaping, fin splaying, and loss of orientation and equilibrium. Affected fish died within hours, and female carcasses generally showed high rates (>90%) of egg retention. Beginning in the fall of 2002, systematic spawner surveys were conducted to 1) assess the severity of the adult die-offs, 2) compare spawner mortality in urban vs. non-urban streams, and 3) identify water quality and spawner condition factors that might be associated with the recurrent fish kills. The forensic investigation focused on conventional water quality parameters (e.g., dissolved oxygen, temperature, ammonia), fish condition, pathogen exposure and disease status, and exposures to metals, polycyclic aromatic hydrocarbons, and current use pesticides. Daily surveys of a representative urban stream (Longfellow Creek) from 2002–2009 revealed premature spawner mortality rates that ranged from 60–100% of each fall run. The comparable rate in a non-urban stream was <1% (Fortson Creek, surveyed in 2002). Conventional water quality, pesticide exposure, disease, and spawner condition showed no relationship to the syndrome. Coho salmon did show evidence of exposure to metals and petroleum hydrocarbons, both of which commonly originate from motor vehicles in urban landscapes. The weight of evidence suggests that freshwater-transitional coho are particularly vulnerable to an as-yet unidentified toxic contaminant (or contaminant mixture) in urban runoff. Stormwater may therefore place important constraints on efforts to conserve and recover coho populations in urban and urbanizing watersheds throughout the western United States.
In lowland Puget Sound, many urban streams in the vicinity of Seattle were a focus of extensive physical and biological restoration activities in the 1990s. These projects, sponsored by the City of Seattle and other regional municipalities, served multiple purposes such as the creation of public green space, the removal of culverts and other impassable barriers for fish, the placement of large woody debris and gravel substrate, the removal of noxious weeds, and the planting of native vegetation. A related aim was to evaluate the extent to which adult salmon would return to spawn in the newly available and improved habitats. This post-project effectiveness monitoring was carried out via fall spawner surveys that were conducted weekly from 1999–2001, with a primary focus on coho (
These early monitoring efforts in 1999–2001 identified an unusual syndrome of pre-spawn mortality among adult coho returning to restoration sites to spawn. Coho typically spawn in small lowland streams in October through December. Eggs incubate in gravel nests (redds) from which fry emerge in the spring (March through May). Juveniles rear in freshwater for approximately a year and then outmigrate to estuaries the following spring. Coho spend at least one full year in the ocean before returning to their natal watersheds to spawn, after which they die (semelparous life history). Adult migration into freshwater is triggered by fall rain events that produce transient high flows in streams. Coho spawning in Seattle-area streams are often a mix of hatchery and natural origins, with hatchery fish distinguishable by a clipped adipose fin and, less commonly, the presence of a rostral-implant coded wire tag.
Affected coho spawners observed in post-restoration effectiveness monitoring surveys showed a consistent suite of symptoms that included surface swimming, gaping, loss of equilibrium, and pectoral fin splaying (
The recurrent die-off of coho in urban drainages appears to be a phenomenon distinct from other types of pre-spawn mortality that have previously been reported for other species of salmon. These include, for example, sockeye salmon in the Fraser River and watersheds of Bristol Bay, as well as Chinook salmon in the Klamath River. In those non-urban freshwater habitats, pre-spawn mortality is described as a chronic process where fish are weakened by a low energy status, poor physical condition, wasting, and eventual death. This process occurs over a protracted timeframe (i.e., weeks). The causes vary and include an abnormally early arrival on spawning grounds, thermal stress, and increased susceptibility to the myxosporean parasite
Here we report the results of an eight-year investigation (2002–09) to characterize the frequency and geographical extent of coho mortality, and to identify associated water quality and spawner condition factors. We conducted daily surveys of multiple creeks to assess rates of pre-spawning mortality across the entire duration of fall coho runs. We assessed the physical condition, pathogen exposure status, and disease status of affected female coho for comparison to 1) unaffected wild adult females collected from a non-urban reference stream, 2) unaffected adult females returning to several area hatcheries, and 3) seawater-phase adults collected from Elliott Bay along the Seattle waterfront, prior to their entry to restored freshwater habitats in urban drainages. Fish from a subset of these locations were profiled using biomarkers of exposure to common toxic contaminants in urban runoff, including metals, homeowner use insecticides, and petroleum hydrocarbons. Lastly, we monitored conventional water quality information (e.g., temperature, dissolved oxygen, specific conductance, and pH) for urban streams during adult coho die-off events.
A paucity of coho spawners in urban streams throughout this study placed important constraints on sample collection for the purposes of a forensic analysis. Spawner abundances were generally low and unpredictable in urban streams where the die-off phenomenon occurs. By contrast, in non-urban streams where coho are relatively abundant, spawners were unaffected. Therefore, tissue collections from coho in urban streams were ad hoc and opportunistic. The streams surveyed during the course of this study and associated samples collected are listed in
Location | Category | Years Sampled | Survey Frequency | Water Quality | Tissue Sampling | ||||
gills | brain | bile | pathogen screen | histopathology | |||||
|
urban stream | 2002–2009 | daily | ✓ |
✓ |
✓ |
✓ |
✓ |
✓ |
|
urban stream | 2006 | daily | ||||||
|
urban stream | 2004 | daily | ✓ |
✓ | ✓ | ✓ | ||
|
forested stream | 2002 | daily | ✓ | ✓ | ||||
|
urban hatchery | 2002 | one day | ✓ | |||||
|
rural hatchery | 2002 | one day | ✓ | |||||
|
urban hatchery | 2002, 2003 | one day | ✓ |
✓ | ✓ | |||
|
rural hatchery | 2003, 2008 | one day | ✓ |
✓ | ✓ | ✓ | ||
|
estuary | 2003 | one day | ✓ | ✓ | ✓ |
sampled only in 2002;
sampled only in 2003;
sampled only in 2004;
sampled only in 2008.
To ensure sample integrity, tissues were not collected from the decomposing carcasses found in streams. Conversely, we did not sacrifice live, non-symptomatic fish in urban streams because these coho may or may not have survived to successfully spawn. As a consequence, some types of samples (e.g., gill metals, bile PAHs; see below) had to be collected from spawners that were either overtly symptomatic or very recently dead, as evidenced by gill coloration (see below). As noted earlier, symptomatic fish progress to death rapidly. Stream surveys were generally less than two hours in a given day, and thus encounters with symptomatic fish were infrequent. This accounts for a relatively small sample size for some tissues despite an intensive overall survey effort.
Daily or weekly spawner surveys (including tissue collections) were conducted on several Seattle-area streams from 2002–2009. These included Longfellow, Thornton, Piper's, Des Moines, Taylor, and Fauntleroy Creeks (
The map indicates the greater Seattle metropolitan area, with gray shading representing the relative intensity of urbanization. Shown are the urban and non-urban creeks surveyed for coho spawner mortality, regional hatcheries, and the location of seawater-phase adult coho collections along the Seattle waterfront (Elliott Bay).
Tissue samples were also collected from regional hatcheries, including the Stillaguamish Tribal Hatchery (2002), the University of Washington Research and Teaching Hatchery (2002), the Wallace River State Hatchery (2003), and the Issaquah Creek State Hatchery (2002 & 2003). Salmon returning to both the University of Washington and Issaquah hatcheries traverse an urbanized landscape through a series of lakes separated from Puget Sound by a single set of locks. The Stillaguamish and Wallace River hatcheries are located on tributaries to the North Fork of the Stillaguamish River and the Snohomish River, respectively (
Adult seawater-phase coho salmon were collected in Elliott Bay (Seattle waterfront, lower Duwamish waterway) prior to freshwater entry. Animals were captured by gillnet in coordination with Muckleshoot tribal fishing operations in the early fall (September 11) of 2003. Adult coho were transferred live or recently dead (<3 hrs) to the NOAA research vessel
Coho typically return to Puget Sound urban streams in the early fall (i.e., early October), depending on the timing and intensity of rain events. Coho returned to the non-urban tributary of the North Fork Stillaguamish River (Fortson Creek) later in the fall relative to coho returning to urban creeks. Thus, daily surveys on Fortson Creek extended into late December in 2002 (approximately three weeks later than for surveys on urban creeks).
Daily surveys involved a visual inspection of most of the accessible freshwater habitat within a given stream. In some instances, poor visibility due to turbidity, high flows, or deep pools and wetlands precluded visual access. Surveyors began at the bottom of the reach and moved upstream, inspecting the stream channel for live adult salmon and carcasses. Where possible, the stream banks were also searched for carcasses that may have been dragged into the riparian zone by predators (predominantly river otters) or scavengers. Urban stream surveys spanned the entirety of the available spawning habitat within a given drainage. In some systems such as Longfellow Creek, impassable barriers restricted returning coho to spawning sites in the lower reaches of the stream.
The location and general or atypical behavior of live salmon were recorded. For all dead or moribund fish, information on collection location, species, gender, fork length, weight (with and without ovaries for females), condition (e.g., signs of physical injury), and egg retention (females only) were recorded. Because males may spawn multiple times (or not at all) within a season, a determination of pre-spawn mortality was only made for females, and the reported rates of coho mortality for different streams are based on data from females only. Although we classified all female carcasses with >50% egg retention as pre-spawn mortalities, in most cases retention was closer to 100% (representative female in
Rates of premature spawner mortality within and across urban drainages were quantified on the basis of egg-retaining female carcasses. Shown is a female affected by the mortality syndrome in Longfellow Creek in the fall of 2005. In most cases, egg retention was nearly 100%. Photo by Tiffany Linbo, NOAA Fisheries.
We collected tissue samples only from animals that were either overtly symptomatic or freshly dead (i.e., <3 hrs post-harvest or gill coloration was red to pink). Due to the limited availability of animals in some years, we collected tissues from symptomatic males as well as females.
Throughout the study we observed a mix of marked and unmarked fish returning to urban streams. In 2002, marked coho were identified by the absence of adipose fins. From 2003 through 2009, carcasses were scanned with a hand-held coded wire tag scanner (Northwest Marine Technology, Inc., Shaw Island, WA). To determine source hatcheries, retrieved tags were processed by U.S. Fish and Wildlife Service staff in the Fisheries Division of the Washington Fish and Wildlife Office (Lacey, WA).
Condition factor was determined for pre- and post-spawn female coho salmon collected from Longfellow Creek (2002–09), Des Moines Creek (2004), and Fortson Creek (2002) as well as for female coho from the University of Washington and Stillaguamish Hatcheries (2002). Pre-spawn mortalities were weighed, the gonads removed, and then the fish were weighed again. All post-spawn and hatchery fish were weighed without gonads. Weight of the fish without gonads was used as a standard index to compare condition factor between pre- and post–spawn mortalities and hatchery fish. Condition factor was calculated using Fulton's condition factor (K = [weight (g)/length (cm)3]×100;
Tissues were collected for histopathology in 2003 and 2004 from affected coho on Longfellow Creek (N = 21 animals) and Des Moines Creek (N = 22), healthy coho returning to the Wallace River (N = 20) and Issaquah (N = 24) hatcheries, and pre-freshwater entry coho from the Muckleshoot tribal fishery in Elliott Bay (N = 27). Samples of liver, head and trunk kidney, exocrine pancreas, pyloric caeca, small or upper intestine, large or lower intestine, stomach, heart, spleen, gonad, brain, and gill were preserved in Davidson's fixative
The Fisher's Exact Test
Fish collected in 2003 and 2004 were screened for infectious non-viral pathogens commonly observed in Pacific salmon, especially those pathogens affecting osmoregulatory tissues such as trunk kidney and gill. In 2003, fish were analyzed for the myxosporean parasite
For
For
For
Current use pesticides are commonly detected in urban streams
To assess the extent to which coho in urban streams may have been exposed to potentially toxic concentrations of insecticides, brains were collected from affected fish from Longfellow Creek (N = 32) as well as the non-urban reference stream (Fortson Creek; N = 18 pre-spawn, 38 post-spawn) and the Stillaguamish (N = 15 pre-spawn), University of Washington (N = 21 pre-spawn), and Issaquah (N = 21 pre-spawn) hatcheries. All samples were collected in the fall of 2002. Brains were dissected
Gill tissue was collected opportunistically from affected coho from Longfellow Creek and Des Moines Creek in the fall of 2004 and from Wallace River Hatchery spawners in the fall of 2008. Samples were collected with plastic forceps and titanium scissors to avoid metal contamination. Upon collection, gill tissue was placed in plastic bags on ice in coolers and transported to the King County Environmental Laboratory (KCEL). Samples were stored at −20°C until analysis. Prior to analysis, samples were homogenized in blenders that were rinsed with methanol and wiped down prior to and between samples.
All samples were analyzed for arsenic, cadmium, chromium, copper, lead, nickel, and zinc. Total metals were measured by inductively coupled plasma-mass spectrometry (ICP-MS) using KCEL standard operating procedures. Tissue was digested with nitric acid in conjunction with hydrogen peroxide to remove the analytes from the sample matrix and then further digested in nitric and sulfuric acid in the presence of potassium permanganate and potassium persulfate. Sodium chloride hydroxylamine hydrochloride was added after digestion to reduce the sample and stannous chloride was added immediately before analysis.
Measures for quality assurance/quality control (QA/QC) included checking measurement accuracy against certified reference materials such as DORM-2 (dogfish muscle) from the Institute for National Measurement Standards (Ottawa, Canada). Further QA/QC procedures included the measurement of background metal levels with method blanks, monitoring variability with duplicate laboratory samples, and measuring recovery of total metals from spiked samples without (spike blank) and with (matrix spike) the sample matrix. Accepted variability for laboratory duplicates was 20%, ±15% for spike blanks, and ±25% for matrix spikes.
Gill tissue metal concentrations were normalized using a log10 transformation. For each metal, differences in concentrations due to location were analyzed using a one-way ANOVA and Tukey-Kramer HSD posthoc test with the level of significance set at p≤0.05.
Bile was collected from the gallbladders of returning adult coho during the 2002–2004 field seasons and analyzed for metabolites of polycyclic aromatic hydrocarbons (PAHs) using established methods
The HPLC/fluorescence system was calibrated prior to analyzing field samples by analyzing a PHN/BaP calibration standard numerous times (N = 5) until a relative standard deviation <15% was obtained for each PAC as previously described
Concentrations of PHN and BaP equivalents, as well as protein values, were log10-transformed to increase the homogeneity of variances. Analysis of variance (ANOVA) and the Tukey-Kramer HSD test were used to determine if mean concentrations of PHN and BaP equivalents and protein content of bile varied among collection years or collection sites. The level of significance was set at p≤0.05.
Field meters were used to continuously monitor conventional water quality parameters during the fall of 2003 on both Longfellow Creek and Des Moines Creek. A 4a Minisonde™ (Hydrolab, Austin, TX) was installed by the City of Seattle in Longfellow Creek, in a pond at the terminus of the survey reach on this stream (just below an impassable culvert). A YSI 6600 multi-sonde unit (YSI Inc., Yellow Springs, OH) was installed by King County on Des Moines Creek. The unit was located in the stream channel below a footbridge in a community park, about 500 feet above the point at which the stream flows directly into Puget Sound. Both meters were programmed to measure and record water temperature, pH, dissolved oxygen, and specific conductance at 15-minute intervals. The Hydrolab was serviced and calibrated during the deployment period according to U.S. Geological Survey protocols
We surveyed Longfellow Creek over eight consecutive years in part to evaluate the influence of rainfall on spawner mortality within and between fall coho runs. Daily and total rainfall data were collected as the sum of 1-minute interval detections from the nearest City of Seattle rain gauge (Rain Gauge 17, or RG17), located approximately 5 km southeast of the upstream terminus of the surveyed portion of the stream. Rainfall was quantified from one week prior to encountering the first live fish in Longfellow Creek until the day the last carcass was found. When data were not available at RG17 they were transposed from the next nearest rain gauge (RG18, distance approximately 13 km).
The relationship between inter-annual spawner mortality and total rainfall was assessed using binary logistic regression. For the correlation coefficient, the natural log of the odds ratio [(% pre-spawn/(1 - % pre-spawn)] for each year was weighted by sample size and regressed (simple linear regression) against total rainfall. In 2006, only 4 females were encountered, and data from this year (100% mortality) were excluded from the linear regression because they produced an undefined odds ratio. Both analyses were performed using JMP version 8 (SAS Institute Inc., Cary, NC).
Consistent with initial observations of overtly symptomatic fish during early surveys in 1999–2001, we observed the same suite of behaviors in affected spawners during daily surveys from 2002–2009. These included circular surface swimming (loss of orientation), gaping, pectoral fin splaying, and loss of equilibrium (
Numerous adult coho carcasses were found in all monitored streams (
Creek | Year | N |
% Wild |
% Pre-Spawn Mortality Wild | % Pre-Spawn Mortality Total |
|
2002 | 57 | 4 | 100 | 86 |
2003 | 18 | 28 | 20 | 67 | |
2004 | 9 | 89 | 88 | 89 | |
2005 | 75 | 72 | 72 | 72 | |
2006 | 4 | 75 | 100 | 100 | |
2007 | 41 | 10 | 75 | 73 | |
2008 | 12 | 0 | n.a | 67 | |
2009 | 44 | 0 | n.a. | 79 | |
|
2006 | 9 | 78 | 100 | 100 |
|
2004 | 30 | 33 | 60 | 63 |
|
2002 | 114 | 100 | 0.9 | 0.9 |
*Sample size reflects female coho of known spawning condition, with no signs of predation.
**Presumed wild origin based on presence of adipose fin and absence of a coded wire tag.
The size and condition of affected fish from urban streams were comparable to those of wild coho returning to Fortson Creek and unaffected hatchery coho returning to regional hatcheries (
Site | Year | N | Mean Condition |
SD |
|
2002 | 20 | 0.893 | 0.111 |
|
2002 | 21 | 0.816 | 0.103 |
|
2002 | 5 | 0.840 | 0.047 |
|
2002 | 21 | 0.814 | 0.06 |
|
2002 | 47 | 0.856 | 0.077 |
2003 | 10 | 0.920 | 0.137 | |
2004 | 8 | 1.018 | 0.103 | |
2005 | 54 | 1.057 | 0.105 | |
2006 | 4 | 1.084 | 0.078 | |
2007 | 21 | 0.995 | 0.153 | |
2008 | 7 | 1.032 | 0.122 | |
2009 | 30 | 0.930 | 0.235 | |
|
2004 | 19 | 1.109 | 0.268 |
|
2006 | 9 | 1.055 | 0.107 |
*Condition Factor was Fulton's K = (weight/(length∧3))*100. Weights were for gravid females (i.e., with ovaries containing eggs).
The spawner mortality syndrome appears to be specific to coho in urban drainages. We observed no symptoms and less than 1% pre-spawn mortality among wild coho returning to spawn in the non-urban reference stream in 2002 (Fortson Creek;
We did not observe corresponding die-offs of resident fish in urban streams (e.g., sticklebacks, sculpins, or cutthroat trout), nor did we find the syndrome in other species of migratory salmon return to these same urban streams to spawn in the fall. Also, the phenomenon appears to be specific to adult coho. In 2003, water from Longfellow Creek was diverted into a flow-through streamside shed facility with juvenile coho housed individually in separate aquaria (N = 24). The juveniles were fed daily and monitored throughout the duration of the fall spawner run. Despite the presence of symptomatic adults in the adjacent stream, juveniles exposed to the same surface flows showed no overt symptoms, with 100% survival across the experimental group (data not shown).
Throughout the study, the general dearth of coho salmon returning to Seattle-area urban streams posed a challenge in terms of collecting tissues for forensic analyses. Longfellow Creek was chosen as a site for long-term monitoring in part because of the proportionally higher number of coho that typically enter this drainage relative to the other urban creeks in Seattle. Coded wire tag analysis of >50 tags collected from coho in Longfellow Creek (2003–2008) showed that many of these fish are hatchery strays originating from a net pen facility operated in Elliott Bay by the Muckleshoot and Suquamish Tribes. This facility serves to transition approximately 500,000 juvenile coho each year from the Soos Creek hatchery (Washington State Department of Wildlife) to the saltwater environment. Importantly, however, for certain high-return years (e.g., 2002 and 2005:
A systematic survey of histopathological conditions in pre-spawn carcasses (urban streams) and unaffected fish from Elliott Bay and two regional hatcheries (Wallace River and Issaquah Creek) was conducted in 2003 and 2004. Various infectious, parasitic and idiopathic (of unknown etiology) diseases were detected in the gill, heart, trunk kidney, gastrointestinal tract and liver of adult spawners. These findings are summarized in
Among the six pathogens screened by PCR or microscopy,
A reduction in the enzymatic rate of brain acetylcholinesterase is a bioindicator of exposure to common carbamate and organophosphate insecticides. As shown in
Shown are relative rates of brain acetylcholinesterase (AChE) activity, a target enzyme for common homeowner use insecticides, in adult coho salmon. The brain enzyme activities of affected fish from an urban stream (Longfellow Creek; LF) were not significantly inhibited relative to unaffected fish from a non-urban stream (Fortson Creek; FT) and three regional hatcheries; Issaquah (ISS-H), University of Washington (UW-H), and Stillaguamish (STI-H). Error bars are 1 standard error of the mean. Sample size is indicated in parentheses and letters indicate significant differences between locations (one-way ANOVA, Tukey's HSD; p<0.05).
The measured concentrations of arsenic, cadmium, chromium, copper, lead, nickel, and zinc in the gill tissue of adult salmon collected from two urban sites (Des Moines and Longfellow Creeks) and one non-urban site (Wallace River Hatchery) are shown in
The concentrations of metals in the gills of affected coho from two urban streams (Longfellow and Des Moines Creeks) are plotted relative to samples collected from a non-urban hatchery (Wallace River). Error bars are 1 standard error of the mean. Letters indicate significant differences in measured levels of metals between sampling locations (one-way ANOVA, Tukey's HSD; p<0.05) and horizontal bars indicate no significant differences (p>0.05).
In the fall of 2002, bile was collected from symptomatic and recently dead coho from Longfellow Creek, as well as from adults returning to spawn in the non-urban reference stream (Fortson Creek). Relative exposures to polycyclic aromatic hydrocarbons (PAHs) were quantified by measuring mean concentrations of phenanthrene (PHN) and benzo(a)pyrene (BaP) metabolites in bile. As shown in
Concentrations of fluorescent PAH metabolites (as phenanthrene [PHN] and benzo-
In 2003, the biliary levels of PAHs in fish from Longfellow Creek were compared to PAH levels in seawater-phase adults collected from a gillnet fishery in Elliott Bay, prior to freshwater entry, and adults returning to a non-urban hatchery (Wallace River Hatchery). As in 2002, fish from the urban stream showed significantly higher exposures to both PHN and BaP relative to the non-urban sampling location (
Monitoring results for conventional surface water quality parameters in urban drainages where premature coho mortality is prevalent have been published previously
During the first year of annual surveys on Longfellow Creek (2002), fall coho returns were several weeks late due to an unusually dry October and early November. The first significant rains in the second week of November triggered a large influx of spawners. As the rains continued over the next two weeks, every fish entering the drainage succumbed to the mortality syndrome, with many observations of overt symptomology during daily surveys (
Shown are the results of daily stream surveys throughout the 2002 coho spawning season in Longfellow Creek in relation to daily rainfall. Asterisks (*) indicate days when stream flows were too high to survey the creek.
Based in part on the apparent strength of this association between rainfall and mortality in 2002, we continued with daily surveys on Longfellow Creek in successive years (2003–2009). The relationship between inter-annual variation in total rainfall and the severity of spawner mortality was evaluated using binary logistic regression. The results suggest a pattern of higher coho survival in wetter years where more water moves through the watershed before many of the adults arrive on the spawning grounds. However, there was a large amount of inter-annual variability in both rainfall (timing and amount) and coho returns (timing and number). As a consequence, the logistic regression was not significant at p≤0.05 (not shown; χ2(1) = 1.70, p = 0.19). The slope for the regression was −0.021 (se = 0.016, p = 0.19) and the intercept was 1.674 (se = 0.403, p<0.0001). Across years, rainfall explained 29% of the variability in the spawner mortality syndrome (log odds ratio weighted linear regression, r2 = 0.288).
Notably, in each of the eight survey years, the first carcass found was always a pre-spawn mortality. Conversely, in six of the seven years in which at least one fish survived to spawn, the last carcass found was a successful spawner.
We have documented a distinct mortality phenomenon among adult coho salmon returning to spawn in urban watersheds of central Puget Sound. The syndrome has been recurrent for more than a decade, with a consistent symptomology across years and survey locations. The annual die-offs have claimed a large proportion of the fall runs in the drainages monitored during the course of this study. These high mortality rates (e.g., 60–100%) are likely to preclude sustainable natural production in urban drainages more generally
Factors that are known to cause spawner mortalities in other species of salmon do not appear to be involved in the coho pre-spawn syndrome that we have explored here. The temperatures and dissolved oxygen content of urban streams during mortality events were not unusually high or low, respectively. Although all fish of the fish we examined showed evidence of infection with common pathogens, there was no correlation with the high rates of mortality in urban drainages or the observed symptomology. Lastly, the stricken coho were generally in good physical condition, and we found no evidence that origin (i.e., wild or hatchery) influences an animal's susceptibility.
The weight of evidence therefore suggests that adult coho salmon are unusually vulnerable to the toxic effects of one or more chemical contaminants, most likely delivered to urban spawning habitats via stormwater runoff. The rapid progression of the syndrome and the specific nature of the symptoms are consistent with acute cardiorespiratory toxicity. Our current findings support this hypothesis, albeit indirectly by ruling out alternative, non-chemical explanations.
We found that affected coho show elevated exposure to metals and petroleum hydrocarbons, the latter after spawners transition to freshwater from a highly urbanized estuary (Elliott Bay). Evidence of exposure to metals and PAHs does not imply causality, but future studies should address these toxics, as they are specifically known to disrupt respiratory, osmoregulatory, and cardiovascular physiology in fish. The abrasion of vehicle tires and brake pads releases aluminum, barium, cadmium, cobalt, copper, lead, nickel, zinc, and other elements onto impervious surfaces
It is important to note, however, that the toxicological context (i.e., established literature) for anticipating possible acutely lethal toxic effects of stormwater contaminants on coho spawners is practically nonexistent. On the one hand, urban runoff typically contains organic chemicals and metals in the low parts per billion to parts per trillion range (e.g.,
Sensitivity related to freshwater transition might explain our observations of affected adults and unaffected juveniles exposed to the same surface waters, but not our observations of affected coho spawners side-by-side with unaffected spawners of other salmon species. For example, in 2006 there were temporally overlapping runs of coho and chum spawners in Piper's Creek. Whereas all of the coho succumbed, the egg retention rate for chum carcasses was <4% (5 of 135 females; data not shown). Moreover, symptomatic coho were observed in the stream side-by-side with healthy chum, the latter actively digging and defending redds (
More work is also needed to define the influence of rainfall on the spawner mortality syndrome. The clearest indication that rainfall plays a role was the 2002 survey results for Longfellow Creek. That year was characterized by an unusually long antecedent dry interval (presumably allowing a proportionally greater accumulation of pollutants on impervious surfaces within the watershed), a relative abundance of returning spawners, and consistent rainfall for approximately two weeks at the beginning of the compressed run. As in 2002, in subsequent years we observed a general tendency towards higher survival later in the run, after multiple fall rain events. However, the relationship was not statistically significant across the survey years, due in part to highly variable rainfall patterns, longer run durations, and very low spawner numbers in some years. Notably, the mortality syndrome is not a simple first-flush phenomenon, as spawned and unspawned carcasses were usually intermixed throughout the duration of each run in 2003–2009.
Additional evidence implicating urban runoff was recently provided by a spatial land use analysis of the watersheds surveyed during the course of this study. Feist et al.
Recent population-scale modeling has shown the potential for rapid local declines in coho population abundance across the range of spawner mortality rates observed in urban drainages during the course of this study
In closing, past efforts to restore salmon habitats in Seattle-area urban watersheds have revealed unexpected challenges for improving coho spawner abundance and survival. These restoration projects have been successful in numerous other ways, including revitalizing urban green spaces, extending watershed connectivity, enhancing public education and involvement, and improving habitat conditions for otters, waterfowl, amphibians, stream invertebrates, native plants, and other fish species. Restored urban streams have also provided an experimental setting to study what may become a very important threat to wild coho populations in the decades ahead as some healthy stream networks gradually acquire the land cover characteristics of the Longfellow Creek system and similar urban drainages. The next generation of urban watershed improvements is now underway, including the catchment-scale implementation of natural drainage systems (using green infrastructure and other emerging technologies), floodplain restoration, and new pollution mitigation activities such as vacuum sweeping of roadways. Moreover, Washington recently became the first state in the U.S. to legislatively mandate a phased reduction of metals in vehicle brake pads and other friction materials (SB6557). Future improvements in the survival of adult coho in urban streams will be an important indicator of success for these and other pollution reduction strategies.
A detailed description of the histopathology results from tissue samples collected during the study from urban and non-urban sites.
(DOC)
Number of pathogens per fish detected by pathogen screening methods for fish collected in 2003. Horizontal bar is positioned at the median. Longfellow Creek fish differ from fish from all other locations (Chi-square test,
(TIFF)
Prevalence of infectious (parasitic/bacterial) and idiopathic conditions detected by histopathology and by pathogen screening (molecular and microscopic) in adult coho salmon sampled from several creeks and hatcheries in the Puget Sound region in 2003 and 2004. H = histopathology; PS = pathogen screening methods; − = analysis not performed.
(DOC)
Symptomatic female coho salmon in Piper's Creek in 2000. The fish appears to be in good physical condition, with ocean-bright (silver) coloration. Characteristic symptoms include loss of equilibrium, gaping, and pectoral fin splaying.
(MP4)
Early onset symptomology of an affected adult coho salmon in Longfellow Creek in 2002. The fish has lost orientation (surface swimming) and is gaping.
(MP4)
Late-stage symptomology of an affected adult coho salmon in Longfellow Creek in 2002. The fish has lost equilibrium and is gaping, with pectoral fins splayed.
(MP4)
A symptomatic coho spawner in Piper's Creek in 2006, just downstream of unaffected chum spawners displaying normal spawning behavior.
(MP4)
Among staff from the NWFSC, we thank Gladys Yanagida for assistance with bile analyses, Kym Jacobsen and Todd Sandell for help with pathogen and parasite screening, Blake Feist for generating the map showing sampling locations (
The conclusions expressed in this article are those of the authors and do not necessarily represent the views of the U.S. Fish and Wildlife Service or the National Marine Fisheries Service.