Pre-spawn mortality is a phenomenon where adult

coho salmon The coho salmon (''Oncorhynchus kisutch;'' Karuk: achvuun) is a species of anadromous fish in the salmon family and one of the five Pacific salmon species. Coho salmon are also known as silver salmon or "silvers". The scientific species name i ...

, ''Oncorhynchus kisutch'', die before spawning when returning to freshwater streams to spawn.Feist BE, Buhle ER, Arnold P, Davis JW, and Scholz NL. 2011. Landscape ecotoxicology of Coho salmon spawner mortality in urban streams. ''PLOS ONE'' 6(8): 1-11.Spromberg JA, and Scholz NL. 2011. Estimating the future decline of wild Coho salmon populations resulting from early spawner die-offs in urbanizing watersheds of the Pacific Northwest, USA. ''Integrated Environmental Assessment and Management'' 9999: 1-9. It is also known as Urban Runoff Mortality Syndrome in more recent studies.Peter, K. T., Tian, Z., Wu, C., Lin, P., White, S., Du, B., ... & Kolodziej, E. P. (2018). Using high-resolution mass spectrometry to identify organic contaminants linked to urban stormwater mortality syndrome in coho salmon. Environmental science & technology, 52(18), 10317-10327. This occurrence has been observed in much of the

Puget Sound Puget Sound ( ) is a sound of the Pacific Northwest, an inlet of the Pacific Ocean, and part of the Salish Sea. It is located along the northwestern coast of the U.S. state of Washington. It is a complex estuarine system of interconnected ma ...

region of the

Pacific Northwest The Pacific Northwest (sometimes Cascadia, or simply abbreviated as PNW) is a geographic region in western North America bounded by its coastal waters of the Pacific Ocean to the west and, loosely, by the Rocky Mountains to the east. Though ...

.McCarthy SG, Incardona JP, and Scholz NL. 2008. Coastal storms, toxic runoff, and the sustainable conservation of fish and fisheries. ''American Fisheries Society Symposium'' 64: 1-21. During fall migration,

salmonids Salmonidae is a family of ray-finned fish that constitutes the only currently extant family in the order Salmoniformes . It includes salmon (both Atlantic and Pacific species), trout (both ocean-going and landlocked), chars, freshwater whitefi ...

(trout and salmon) pass through urban watersheds which are contaminated with stormwater runoff. As the coho salmon pass through these waters, many will show symptoms of lethargy, loss of equilibrium and disorientation, and die within a few hours of showing these symptoms. These symptoms and behaviors are prevalent after rain events. Mortality often occurs before salmon have the opportunity to

spawn Spawn or spawning may refer to: * Spawn (biology), the eggs and sperm of aquatic animals Arts, entertainment, and media * Spawn (character), a fictional character in the comic series of the same name and in the associated franchise ** '' Spawn: Ar ...

, which is determined by cutting open female carcasses and observing for unfertilized eggs. Rates of pre-spawn mortality could impact the local salmon populations. Based on model projections, if rates continue, populations of coho salmon could become extinct within the next few decades. Weight of evidence suggests coho salmon pre-spawn mortality is due to exposure to

stormwater runoff Surface runoff (also known as overland flow) is the flow of water occurring on the ground surface when excess rainwater, stormwater, meltwater, or other sources, can no longer sufficiently rapidly infiltrate in the soil. This can occur when the s ...

. A ubiquitous tire rubber–derived chemical induces acute mortality in coho salmon. Scholz NL, Myers MS, McCarthy SG, Labenia JS, McIntyre JK, Ylitalo GM, Rhodes LD, Laetz CA, Stehr CM, French BL, McMillan B, Wilson D, Reed L, Lynch KD, Damm S, Davis JW, and Collier TK. 2011. Recurrent die-offs of adult Coho salmon returning to spawn in Puget Sound lowland urban streams. ''PLOS ONE'' 6(12): 1-12. A negative correlation exists between the incidence of pre-spawn mortality and urban land use, specifically with the

impervious surfaces Impervious surfaces are mainly artificial structures—such as pavements (roads, sidewalks, driveways and parking lots, as well as industrial areas such as airports, ports and logistics and distribution centres, all of which use considerable pav ...

, commercial property type, and local roads. Exposure to

metals A metal (from Greek μέταλλον ''métallon'', "mine, quarry, metal") is a material that, when freshly prepared, polished, or fractured, shows a lustrous appearance, and conducts electricity and heat relatively well. Metals are typicall ...

and petroleum hydrocarbons displayed some response to pre-spawn mortality, while exposure to pesticides, diseases, and water quality variables did not elicit this effect. This trend has not been observed in any other life history stage of the coho salmon nor in other salmon species in the Puget Sound region.

History

Pre-spawn mortality was first observed in the Puget Sound after efforts had gone into restoring urban watersheds in hopes of drawing salmon back to these areas. Restoration consisted of removing culverts, debris, and any other barriers. Restoration projects were successful in that salmon returned to these runs, however, in initial surveys of restoration success, the pre-spawn mortality symptoms were observed. It is now recognized that in restoring watersheds, water quality and contamination must also be considered for successful spawning events of coho salmon if the population is to persist. Upon displaying specific symptoms (below), mortality of the coho salmon can be expected within a few hours. Mortality usually occurs before these fish have had a chance to spawn. In fact, in observing the female coho salmon carcasses, most of the fish have retained greater than 90 percent of their eggs. Pre-spawn mortality occurs in both male and female salmon, however, it is difficult to determine if male salmon have spawned, thus, pre-spawn mortality is usually signified by egg retention of female salmon. Pre-spawn mortality has also been observed in both wild and hatchery fish alike.

Symptoms

Salmon of pre-spawn mortality display unusual behaviors and symptoms, such as swimming in circles or exhibiting other erratic swimming patterns. Other symptoms include lethargy, disorientation, loss of equilibrium, gaping, and fin splaying. Death of the coho salmon occurs within hours after observing these symptoms.

Fish behavior and swimming patterns

Coho salmon that are affected by pre-spawn mortality show behavioral symptoms that are easily identified. The fish displayed behaviors like swimming near the surface of the water, swimming in circular patterns, or consistently running into the river bank. This may be due to a loss of equilibrium and orientation of the fish.

Gaping

This symptom consists of the salmon repeatedly opening and closing its mouth. This action in some species of fish (e.g. eels) is used to push water over the gills to meet respiratory demands. For coho salmon, this could be an indication that the fish is not getting enough dissolved oxygen, signifying stress to the respiratory system or that the muscular system has been affected and this gaping is a forced action.

Fin splaying

Fin splaying occurs when the

pectoral fin Fins are distinctive anatomical features composed of bony spines or rays protruding from the body of a fish. They are covered with skin and joined together either in a webbed fashion, as seen in most bony fish, or similar to a flipper, as ...

of the salmon is rigid and extended perpendicular to the body of the fish instead of laying flat against the fish.Eaton RC, Bombardieri RA, and Meyer DL. 1977. The mauthner-initiated startle response in teleost fish. ''Journal of Experimental Biology'' 66: 65-81. In other fish, e.g. kelp bass, this action is a startle response.

Cause

A study indicated that road runoff and water samples collected at coho salmon URMS cases were chemically similar with tire tread wear particle leachate. Further investigation on URMS and tire wear leachate narrowed down the scope from thousands of chemicals to one unknown chemical, which was found as an ozonation product of the common antiozonant

6PPD 6PPD is an organic chemical widely used as stabilising additive (or antidegradant) in rubbers, such as NR, SBR and BR; all of which are common in vehicle tires. Although it is an effective antioxidant it is primarily used because of its excell ...

. This toxic transformation product, called 6PPD-quinone, kills coho salmon at nanogram per liter concentrations. It has been detected in road runoff and creek stormwater when URMS occurred.

Nonpoint source pollution

Urban and stormwater runoff

Many of the contaminants that are responsible for degrading urban watersheds come from

nonpoint source pollution Nonpoint source (NPS) pollution refers to diffuse contamination (or pollution) of water or air that does not originate from a single discrete source. This type of pollution is often the cumulative effect of small amounts of contaminants gathered ...

. This consists of a wide array of contaminants coming from a variety of sources and locations. The contaminants that have been found in stormwater runoff include metals, such as

aluminum Aluminium (aluminum in American and Canadian English) is a chemical element with the symbol Al and atomic number 13. Aluminium has a density lower than those of other common metals, at approximately one third that of steel. It has ...

barium Barium is a chemical element with the symbol Ba and atomic number 56. It is the fifth element in group 2 and is a soft, silvery alkaline earth metal. Because of its high chemical reactivity, barium is never found in nature as a free element. Th ...

cobalt Cobalt is a chemical element with the symbol Co and atomic number 27. As with nickel, cobalt is found in the Earth's crust only in a chemically combined form, save for small deposits found in alloys of natural meteoric iron. The free element, pr ...

iron Iron () is a chemical element with symbol Fe (from la, ferrum) and atomic number 26. It is a metal that belongs to the first transition series and group 8 of the periodic table. It is, by mass, the most common element on Earth, right in f ...

arsenic Arsenic is a chemical element with the symbol As and atomic number 33. Arsenic occurs in many minerals, usually in combination with sulfur and metals, but also as a pure elemental crystal. Arsenic is a metalloid. It has various allotropes, but ...

cadmium Cadmium is a chemical element with the symbol Cd and atomic number 48. This soft, silvery-white metal is chemically similar to the two other stable metals in group 12, zinc and mercury. Like zinc, it demonstrates oxidation state +2 in most of ...

chromium Chromium is a chemical element with the symbol Cr and atomic number 24. It is the first element in group 6. It is a steely-grey, lustrous, hard, and brittle transition metal. Chromium metal is valued for its high corrosion resistance and hardne ...

copper Copper is a chemical element with the symbol Cu (from la, cuprum) and atomic number 29. It is a soft, malleable, and ductile metal with very high thermal and electrical conductivity. A freshly exposed surface of pure copper has a pinkis ...

lead Lead is a chemical element with the symbol Pb (from the Latin ) and atomic number 82. It is a heavy metal that is denser than most common materials. Lead is soft and malleable, and also has a relatively low melting point. When freshly cu ...

nickel Nickel is a chemical element with symbol Ni and atomic number 28. It is a silvery-white lustrous metal with a slight golden tinge. Nickel is a hard and ductile transition metal. Pure nickel is chemically reactive but large pieces are slow to ...

, and

zinc Zinc is a chemical element with the symbol Zn and atomic number 30. Zinc is a slightly brittle metal at room temperature and has a shiny-greyish appearance when oxidation is removed. It is the first element in group 12 (IIB) of the periodi ...

,Lough GC, Schauer JJ, Park JS, Shafer MM, Deminter JT, and Weinstein JP. 2005. Emissions of metals associated with motor vehicle roadways. ''Environmental Science & Technology'' 39: 826-836.

polycyclic aromatic hydrocarbons A polycyclic aromatic hydrocarbon (PAH) is a class of organic compounds that is composed of multiple aromatic rings. The simplest representative is naphthalene, having two aromatic rings and the three-ring compounds anthracene and phenanthrene. P ...

(PAHs), petroleum hydrocarbons (motor oil and fuel), and

pesticides Pesticides are substances that are meant to control pests. This includes herbicide, insecticide, nematicide, molluscicide, piscicide, avicide, rodenticide, bactericide, insect repellent, animal repellent, microbicide, fungicide, and lampric ...

(including

insecticides Insecticides are substances used to kill insects. They include ovicides and larvicides used against insect eggs and larvae, respectively. Insecticides are used in agriculture, medicine, industry and by consumers. Insecticides are claimed to b ...

).Davis AP. 2005. Green engineering promote low: applying the principles of green engineering can help create more sustainable development. ''Environmental Science and Technology'' 338-344. Anthropogenic sources are responsible for many of the contaminants in stormwater runoff in urban areas. These anthropogenic sources include motor vehicles, which contribute metals, antifreeze or coolants, and petroleum hydrocarbons from brake pads and leaking fluids. Many of these contaminants will collect on impervious surfaces (e.g. roads and parking lots) and with rain, will wash into streams, rivers, and the ocean. Other sources of runoff include pesticides and

fertilizers A fertilizer (American English) or fertiliser (British English; see spelling differences) is any material of natural or synthetic origin that is applied to soil or to plant tissues to supply plant nutrients. Fertilizers may be distinct from ...

used on residential and commercial properties, which can be washed into storm drains during rain events.

Effects of runoff

There are a number of possibilities as to the cause of pre-spawn mortality. It is possible that this mortality is due to acute cardiorespiratory

toxicity Toxicity is the degree to which a chemical substance or a particular mixture of substances can damage an organism. Toxicity can refer to the effect on a whole organism, such as an animal, bacterium, or plant, as well as the effect on a subst ...

to the fish. The symptoms (discussed above) and rapid rate of mortality are consistent with this type of toxicity. The exact chemical combination or mixture responsible for this early mortality is not known. However, a few possible explanations are discussed below.

Narcotic effects

Narcosis is a phenomenon that occurs when a combination of organic toxicants, each at low concentrations, have a toxic effect on an organism.Veith GD, and Broderius SJ. 1990. Rules for distinguishing toxicants that cause Type I and Type II narcosis syndromes. ''Environmental Health Perspectives'' 87: 207-211. Narcosis has a nonspecific

mode of action A mode of action (MoA) describes a functional or anatomical change, resulting from the exposure of a living organism to a substance. In comparison, a mechanism of action (MOA) describes such changes at the molecular level. A mode of action is impor ...

, where it does not target one specific site of action, but instead affects the membranes and

protoplasm Protoplasm (; ) is the living part of a cell that is surrounded by a plasma membrane. It is a mixture of small molecules such as ions, monosaccharides, amino acid, and macromolecules such as proteins, polysaccharides, lipids, etc. In some defini ...

. These individual organic toxicants affect the fish at sublethal levels, however, the combination of contaminants can lead to mortality of the organism. However, if the stressor is removed narcotic effects can be reversed. Fish influenced by narcosis may display lethargic symptoms. Narcosis can also result in respiratory-cardiovascular responses to fish.McKim JM, Schmieder PK, Carlson RW, Hunt GJ, Niemi GJ. 1987. Use of respiratory-cardiovascular responses of rainbow trout (''Salmo gairdneri'') in identifying acute toxicity syndromes in fish: Part 1. Pentachlorophenol, 2,4-dinitrophenol, tricaine methanesulfonate and 1-octanol. ''Environmental Toxicology and Chemistry'' 6: 295-312.

Mixtures

Pre-spawn mortality may be attributed to a mixture of contaminants. In nonpoint source runoff, there is often more than one chemical, thus organisms may be influenced by the combination or mixture of different contaminants. Mixtures of chemicals may have the same mode of action, which can increase toxicity due to two or more chemicals influencing the same site of an organism.Laetz CA, Baldwin DH, Collier TK, Herbert V, Stark JD, and Scholz NL. 2009. The synergistic toxicity of pesticide mixtures: Implications for risk assessment and the conversation of endangered Pacific salmon. ''Environmental Health Perspectives'' 117(3): 348-353. The mixture of two or more contaminants may have a number of different effects to an organism, such as additive or synergistic effects. Additive toxicity occurs when the toxicity of individual contaminants (with a similar mode of action) can be summed to determine the final toxicity. Synergism occurs when the sum of two or more toxicants is greater than the sum of the individual components. Additional combinations of effects may result from contaminants and

pathogens In biology, a pathogen ( el, πάθος, "suffering", "passion" and , "producer of") in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a germ ...

or contaminants and physiological effects. As anadromous fish migrate from the ocean to freshwater streams, many changes take place in the osmoregulatory and ionregulatory systems due to the changes in composition between freshwater and saltwater.Cooke SJ, Hinch SG, Farrell AP, Lapointe MF, Jones SRM, Macdonald JS, Patterson DA, Healey MC, and Van Der Kraak G. 2004. Abnormal migration timing and high en route mortality of sockeye salmon in the Fraser River, British Columbia. ''Fisheries'' 29(2): 22-33. These changes in combination with chemical pollutants may cause the observed symptoms and death of these coho salmon. However, these specific symptoms and resulting pre-spawn mortality are not observed in other

anadromous fish Fish migration is mass relocation by fish from one area or body of water to another. Many types of fish migrate on a regular basis, on time scales ranging from daily to annually or longer, and over distances ranging from a few metres to thousan ...

, thus, the coho salmon may be a more sensitive species than other

Metals

Many metal contaminants enter the watershed due to motor vehicles and impervious surfaces near rivers and streams. Results from experiments analyzing the effects of metal contaminants on fish discovered an increase in cadmium, lead, and nickel in the gill tissue. Studies on copper and other metals demonstrate toxicity to fish due its ability to influence ionoregulation. The copper competes with other

cations An ion () is an atom or molecule with a net electrical charge. The charge of an electron is considered to be negative by convention and this charge is equal and opposite to the charge of a proton, which is considered to be positive by convent ...

for the binding site on the gill of fish, and mortality may result with high enough concentrations of copper binding to these sites (see

Biotic Ligand Model The Biotic Ligand Model (BLM) is a tool used in aquatic toxicology that examines the bioavailability of metals in the aquatic environment and the affinity of these metals to accumulate on gill surfaces of organisms. BLM depends on the site-specific ...

). Dissolved copper can also affect the olfactory nervous system in fish, by directly influencing the sensory neurons in the olfactory epithelium. This results in a reduction of

olfactory The sense of smell, or olfaction, is the special sense through which smells (or odors) are perceived. The sense of smell has many functions, including detecting desirable foods, hazards, and pheromones, and plays a role in taste. In humans, it ...

senses, increasing the vulnerability of the fish to predation, as they are no longer able to use chemical cues to locate and avoid predators. These olfactory neurotoxic effects may also influence the salmons ability to navigate and find adequate streams for spawning.

Polycyclic aromatic hydrocarbons (PAHs)

Impervious surfaces and vehicles also contribute contaminants such as

fossil fuels A fossil fuel is a hydrocarbon-containing material formed naturally in the Earth's crust from the remains of dead plants and animals that is extracted and burned as a fuel. The main fossil fuels are coal, oil, and natural gas. Fossil fuels ...

or gasoline, lubricating oils, and chemical

sealants Sealant is a substance used to block the passage of fluids through openings in materials, a type of mechanical seal. In building construction ''sealant'' is sometimes synonymous with ''caulking'' and also serve the purposes of blocking dust, so ...

for parking lots (e.g. coal tar based sealants). These contaminants are grouped as

(PAHs). Effects of PAHs on fish have shown that these contaminants can be

carcinogenic A carcinogen is any substance, radionuclide, or radiation that promotes carcinogenesis (the formation of cancer). This may be due to the ability to damage the genome or to the disruption of cellular metabolic processes. Several radioactive substan ...

and also impact early life history stages of fish. They may also influence cardiovascular physiology in fish. Additional studies are needed to determine the full effect of PAHs on fish.

Efforts to reduce urban stormwater runoff

One approach to decrease runoff from entering streams and rivers is the implementation of low-impact development practices. These

bioretention Bioretention is the process in which contaminants and sedimentation are removed from stormwater runoff. The main objective of the bioretention cell is to attenuate peak runoff as well as to remove stormwater runoff pollutants. Construction of ...

practices aim to filter water and contaminants in the soil and vegetation with the goal of reducing the volume of water and contaminants that enter the streams. Bioretention practices include

rain gardens Rain gardens, also called bioretention facilities, are one of a variety of practices designed to increase rain runoff reabsorption by the soil. They can also be used to treat polluted stormwater runoff. Rain gardens are designed landscape sites t ...

, vegetated

swale Swale or Swales may refer to: Topography * Swale (landform), a low tract of land ** Bioswale, landform designed to remove silt and pollution ** Swales, found in the formation of Hummocky cross-stratification Geography * River Swale, in North ...

s, decrease impervious surfaces (instead using

Pervious concrete Pervious concrete (also called porous concrete, permeable concrete, no fines concrete and porous pavement) is a special type of concrete with a high porosity used for concrete Concrete slab, flatwork applications that allows water from Precipitati ...

), and

green roofs A green roof or living roof is a roof of a building that is partially or completely covered with vegetation and a growing medium, planted over a waterproofing membrane. It may also include additional layers such as a root barrier and drainage ...

Additional examples

Pre-spawn mortality has been observed in other species of fish, including Chinook and

sockeye salmon The sockeye salmon (''Oncorhynchus nerka''), also called red salmon, kokanee salmon, blueback salmon, or simply sockeye, is an anadromous species of salmon found in the Northern Pacific Ocean and rivers discharging into it. This species is a P ...

and

steelhead Steelhead, or occasionally steelhead trout, is the common name of the anadromous form of the coastal rainbow trout or redband trout (O. m. gairdneri). Steelhead are native to cold-water tributaries of the Pacific basin in Northeast Asia and N ...

. The cause of pre-spawn mortality in these fish in the

Fraser River The Fraser River is the longest river within British Columbia, Canada, rising at Fraser Pass near Blackrock Mountain in the Rocky Mountains and flowing for , into the Strait of Georgia just south of the City of Vancouver. The river's annual d ...

(sockeye salmon) and

Klamath River The Klamath River (Karuk: ''Ishkêesh'', Klamath: ''Koke'', Yurok: ''Hehlkeek 'We-Roy'') flows through Oregon and northern California in the United States, emptying into the Pacific Ocean. By average discharge, the Klamath is the second larges ...

(

Chinook salmon The Chinook salmon (''Oncorhynchus tshawytscha'') is the largest and most valuable species of Pacific salmon in North America, as well as the largest in the genus ''Oncorhynchus''. Its common name is derived from the Chinookan peoples. Other ve ...

and steelhead trout) differ than that observed in the coho salmon. The cause of pre-spawn mortality for the sockeye salmon in the Fraser River, BC, and

Bristol Bay Bristol Bay ( esu, Iilgayaq, russian: Залив Бристольский) is the easternmost arm of the Bering Sea, at 57° to 59° North 157° to 162° West in Southwest Alaska. Bristol Bay is 400 km (250 mi) long and 290 km, ( ...

, Alaska, can be attributed to factors such as fish returning to spawn too early, warmer water temperatures, low dissolved oxygen and disease or parasites. In the Klamath River, mortality before spawning was due to disease, thermal stress, a low water flow and increasing numbers of salmon migrating within the same time period.California Department of Fish and Game (2004) September 2002 Klamath River fish-kill: final analysis of contributing factors and impacts. State of California, Northern California-North Coast Region, The Resources Agency, Sacramento CA.

References

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