LIFE AND DEATH OF A SALMON
THERE ARE some remarkable traits common to all Pacific salmon regardless of taxonomic etymology and the numerous variations in each species’ coloration, size, or shape of mouth. They all live in the northern hemisphere and have adipose fins, small smooth-edged scales, forward-stretching gill tissues, and peculiarities in vertebra shape, but the most important commonality that explains much of the essence of the Salmon Forest and separates them from their trout brethren is that the salmon in genus Oncorhynchus are semelparous. Taken from the Latin, semelparous means “begotten once,” a reference to their lyrical existence: they die soon after they reproduce. This one characteristic separates them from all the closely related trout and the Atlantic Salmo salar. And because these spawning salmon return to the streams whence they were born, they fulfill their poetic life to the utmost: their birthplace, and that of their offspring, becomes their grave.
What may seem to be a counterintuitive life strategy, to “live fast and die young” just as they reach their reproductive potential, is a finely tuned and effective evolutionary strategy that, above all other things, seeks to maximize the transfer of genetic material from one generation to the next. Life as a maturing salmon is rife with hazards and mortality is very high during a lifetime of migration from a freshwater mountain stream to the open ocean and then back again. It is astonishing that any reproductively viable adults return to spawn at all considering the gauntlet of predators, from fishes to fishermen, and the host of environmental challenges, from blocked or silted river beds to radical changes in temperature and salinity, that salmon must navigate. In a final effort to maximize their reproductive potential, adult Pacific salmon expend all their energy during their upstream spawning run and the final acts of reproduction itself. Males fight and compete for mates until scarred and emaciated, and females invest their last metabolic energy in egg production and in guarding their nests until they become too weak and battered to hold their position in the current, and then they drift away to die.
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SALMON LIFE, like much in the animal kingdom, begins with an egg. Salmon are oviparous, which means that females lay their eggs and the embryos develop and hatch outside the female’s body. Salmon eggs are among the largest of all the bony fish eggs and a magnificent example of practical and aesthetic beauty. They are exquisite golden orange and red spheres, just less than a centimeter across, holding a nucleus of maternal genetic material and packed full of nutritious yolk. They are surrounded by a tough yet porous membrane that is strong enough to withstand the rigors of being buried in gravel and sand at the bottom of a rushing stream, yet permeable enough to allow oxygen to enter and carbon dioxide and other wastes to be flushed from the egg as the embryo develops.
A female salmon produces these large nutritious eggs at great metabolic expense, particularly because salmon do not feed during their final spawning migration. In essence, she sacrifices herself in order to produce offspring that have the highest chance of survival because they develop with their own integrated food reserve—the large yolk. At the same time, the salmon must strike an evolutionary balance between the size of an individual egg and the number of eggs she can produce. Large eggs enhance the early survival of offspring, but being more fecund increases the number of offspring in the nest as they begin a life that has a high chance of early mortality, and so salmon typically lay a few thousand eggs in a nest (although a large chinook can lay more than fifteen thousand eggs). A large yolk can provide enough energy for an embryo and then a newly hatched young still attached to the yolk sac (an “alevin”) to survive a fall spawn through the winter. But the large nutrient-filled yolk also makes the eggs (as well as egg-laden females) a preferred food for a host of forest predators. Indeed, when streams are flush with spawning salmon and the fishing is relatively easy, salmon-feeding bears are known to strip and eat only the egg-filled gonad and leave the rest of the salmon carcass on the forest floor or stream bank. Female salmon expend energy not just producing their eggs but investing in parental care. The act of locating a suitable spot and digging a nest, or “redd,” by beating the bottom with her sides and tail to form a clean depression, and then burying the eggs further once fertilized by a suitor’s milt, increases the odds that her offspring will survive, but it is ultimately costly to the mother. Although spent from these acts, she guards the nest until all her energy reserves are consumed, then leaves behind orphans with the best achievable chance of hatching.
Because the eggs are incubated under a layer of sediment for protection, optimal nesting areas are in streams and rivers with well-aerated waters and beds of clean, well-sorted gravel and sand. The exact timing of embryonic development and hatching, like much of the salmon’s life history, varies among species and even among subpopulations of the same species, because it is closely adapted to the particular local environment that each population inhabits. Development is a function of water temperature (with slower development in colder waters) and the amount of dissolved oxygen present (with slower development in waters with lower oxygen levels). Populations living in the coldest northern waters, and that spawn late in the year, inherently develop slowly, and hatching and further development then occur in the spring, when temperatures increase and more food is available. Mortality is very high in the nest, approaching 90 percent in some species, because the eggs and hatchlings are at the mercy of a profusion of physical challenges besides the risk of being eaten. They are susceptible to reduced oxygen levels from siltation, to unfavorable displacement, and to damage and death from scouring of the bottom. After hatching, the alevins, which are still attached to their yolk sacs, are physically incapable of swimming against any current, so their first behavior is to push downward, away from light and further into the gravel, and then gravitate toward water flow and higher oxygen levels as they slowly disperse. For the most part, they remain inactive and survive off the nutrients provided by their yolk, which feeds the development of their internal organ systems as it is metabolized. Once the yolk is fully consumed, the alevin, now known as “fry,” typically wriggle up through the gravel and emerge into the overlying water at night to begin their residence in streams and small rivers, or in the case of some, like the sockeye, in the shallows of adjoining lakes.
Salmon eggs are glistening orange-red spheres whose yolks are packed with nutrients to feed the growing embryo. Their beauty is matched by their robust utility; the eggs are tough enough to withstand burial in stream sediments but also allow oxygen and waste products to diffuse across their outer skin. The dark spots are the rapidly developing eyes of the young larvae.
Recently hatched larvae, or alevin, still attached to their yolk sacs. The yolk provides the nutrients for alevin growth and development even through the winter months; however, its high caloric content makes the alevin a prime target for predation.
Salmon fry, and the larger juvenile stage, “parr,” continue to slowly develop and grow in the freshwaters of the forest, and in order to survive must balance their own need to feed on insects, insect larvae, and plankton with the task of avoiding being eaten themselves. They are at risk even from other salmon. Some species, like the pink salmon, seek almost immediately to swim to the ocean, where planktonic food is much more abundant and growth is accelerated, but which is also populated by a much larger number of predators. Juveniles take advantage of whatever habitat is available to maximize feeding and avoid predators. They will shift between habitats seasonally and from day to night, hiding under river banks during the day and moving into more open water in the evening. In fact it is the quantity and quality of the salmon-friendly habitable spaces in a stream that ultimately determine the number and size of developing salmon that it can support. Because the lakes, rivers, and streams are intrinsically variable in the Pacific Northwest due to seasonal changes in flow, local rainfall patterns, and the wooded terrain, the landscape we refer to as the Salmon Forest reveals itself as an optimal environment for salmon. A local flooding event, a debris flow that alters watershed drainage, or even a fallen tree that partially blocks a stream may appear catastrophic in the short run, but in the long term these events create a diversity of microhabitats that can accommodate many different life stages and even different species of salmon all in one region.
Towering old-growth forest on the Olympic Peninsula, Washington State.
The plankton-rich waters of the north Pacific Ocean can provide much more food to a growing salmon than can a freshwater river or stream, and the high metabolic rates of developing salmon can sustain rapid growth as long as food is available. Rapid growth is critical because survival in the ocean is generally size selective—small fish get eaten—so salmon must either enter the ocean at a large size or grow rapidly once they enter salt water. Each spring, salmon populations face the challenge of whether or not they should migrate from their freshwater havens to the ocean bounty. As we know from the kokanee, some select not to migrate at all. Larger juveniles in good health tend to migrate downstream to the sea, while smaller ones are more likely to persist in their freshwater habitats for another year. The evolutionary need for migration is prompted by parr size and the internal physiological rhythms of development and is linked to environmental cues such as increases in temperature and day length. A salmon parr that is undergoing the behavioral, developmental, and physical transition from freshwater to salt water is known as a “smolt.”
The Pacific salmon life that has evolved to include development stages initiating in freshwater, maturity in the ocean, and then the critical return to freshwater to spawn is called an anadromous life history, and smolting is essential to it. Anadromy (from the Greek meaning “up running”) is another common trait of salmon and some trouts that differentiates them from other members of Salmonidae. For instance, the steelhead form of rainbow trout, O. mykiss, is an anadromous trout that spends two or three years at sea and returns to freshwater to spawn (however, it is not semelparous and can spawn up to four times, so it is not referred to as a salmon). The converse life history, known as catadromy, wherein a life spent predominantly in freshwater is punctuated by the requirement to migrate and spawn in the ocean, is also found in fishes. Anguilla anguilla and A. rostrata, the freshwater eels of Europe and America, are the most famous catadromous fishes, migrating thousands of kilometers from rivers and lakes to spawn in the Sargasso Sea in the mid-Atlantic.
Anadromy and the requirement that a salmon be adapted to live in both fresh- and salt water necessitate a physiological miracle. To explain this, we need to develop a new analogy for our salmon archetype. I suggest that of a leaky boat—even though a leaky boat might seem to be the antithesis of everything that equates with being a fish.
It is a testament to evolution, ours and the salmon’s, that each cell in the body of a human or fish or bear in the forest contains vital fluid—cytoplasm—that closely mimics the composition of seawater. Each cell is a finely tuned machine of its own, adapted to a life in seawater in our ancestors eons ago. Even after innumerable generations and adaptations for survival as a single entity or as one small part of an organ system in the complex mechanism that is a salmon, a cell’s internal components only function properly when they are bathed in a cytoplasm with the correct concentration of salts and ions. And water itself is essential for the physiological and biochemical functioning of every organism on earth. If a fish were perfectly sealed, it might be able to maintain the correct internal chemistry regardless of where it lived, but it is not. It is a leaky boat because a fish contains millions of semipermeable membranes that are exposed to the environment, and it must eat and breathe and excrete, and doing so changes the chemistry of its body fluids. A tuna placed in a lake or a goldfish placed in the sea quickly dies because an imbalance in internal chemistry leads to a failure at the cellular level, which cascades to a failure of the whole. A fish’s gills are its leakiest organ. The tissues there are thin, folded, and extend into long filaments, adaptations that maximize surface area in order to absorb oxygen most efficiently from the water flushing over the gills and pass that oxygen into the bloodstream. While very effective for respiration, this design allows other molecules, both beneficial and detrimental, to enter and leave the body. A fish must breathe, yet the gills act like a gaping hole in the bottom of a boat, with water wanting to rush either in or out, depending on whether the boat is sitting in the sea or drifting down a river. Life in a stream and life in the ocean are physiologically very different, yet a salmon manages to stabilize the ionic chemistry of its internal fluids and can therefore live in both.
The process that governs the movement of molecules between solutions and through permeable membranes, like those in cell walls and salmon gills, is osmosis. It is actually a result of the essential thermodynamic principle of entropy—a statistical measure of the degree of randomness in the world. Molecules will move about fluids and through permeable membranes so that the entropy of the total system is maximized. In cells and salmon this means that water molecules tend to move automatically through permeable membranes from regions that have a low concentration of dissolved ions into areas that have a higher concentration of dissolved ions. Osmosis controls many passive biochemical processes in all living things because life tends to be assembled of inordinate numbers of tiny fluid-filled compartments (tissues and cells and the microscopic organelles within cells), each filled with various dissolved ions and molecules, all separated by membranes. If a cell is placed into a solution that has a higher concentration of dissolved ions, water escapes the cell and it will wither and collapse. If it is kept in a solution with a lower concentration of ions, water will rush into the cell and it will expand and eventually burst. Most simply, any fish in a river tends to swell because water molecules osmotically flow into the fish’s tissues, where the ions are maintained at a higher concentration relative to the freshwater. In the ocean the opposite is true: water flows out of the fish’s body because the concentration of dissolved ions is lower there than in the sea.
In this discussion of the leaky salmon we are most interested in the balance of sodium and chloride ions—that is, the “salt” in seawater—that surrounds the fish, and the constituents of the body fluids, like the blood and the cell cytoplasm. Cells require the correct concentration of many different dissolved ions and molecules, which includes dissolved nutrients as well as salts, and complex osmoregulatory mechanisms have evolved in order to maintain a delicate balance of stable internal osmotic conditions. For a fish this means maintaining relatively high levels of sodium and chloride ions and low levels of other ions like potassium, calcium, and magnesium. Osmoregulation—controlling the internal ionic chemistry—requires metabolic energy, not just to conserve ion balance and the correct volume of water, but also to aid the transport of toxic organic and inorganic waste molecules out of cells, where they are produced as a result of constant cellular metabolism. This metabolism is the life-sustaining series of chemical reactions that occur in all living beings either to consume energy in order to assemble new molecules, like proteins, or to break down larger molecules in order to release energy that can be used for other processes, like those necessary for maintaining ionic balance. Osmosis itself is passive and is exploited by the cell to aid in the transport of substances across cellular membranes. Osmotic flow, or pressure, is developed across membranes where a gradient exists between low and high concentrations of ions, and for the case of sodium and potassium ions, these gradients are exploited as a potential energy source for trans-membrane transport. But maintaining the ionic gradients requires the actions of special structures—microscopic protein pumps—that span cell membranes and that can shuttle ions against osmotic gradients as long as there is metabolic energy available to power them.
Details aside, it is paramount for a salmon, or any fish, or any animal for that matter, to maintain the correct composition of its internal fluids, because that composition is critical for cellular function and hence life. Osmoregulatory mechanisms exist at the level of individual cells, as well as in tissues and organs that have evolved to actively filter or compartmentalize fluids that are waste filled or in osmotic disequilibrium and then transport them away from cells and out of the body. Salmon are special because they can perform this critical osmoregulation in either freshwater or salt water.
In freshwater, a salmon is a leaky boat that is continuously flooding with water, and to continue the nautical analogy, the salmon’s kidneys must then perform as extremely efficient bilge pumps to help maintain the osmotic balance of the body. The kidney functions to remove the excess water absorbed into the bloodstream and then excretes it as a very dilute urine. Because a salmon in freshwater is swimming in a medium that is more dilute, with fewer salts, than are in its internal body fluids and cells, it constantly loses critical ions back into the environment. So a freshwater-adapted kidney is designed with glomerulii and renal tubules (specialized tissues forming the internal filtering apparatus of the kidney) that are very efficient at resorbing crucial salts and electrolytes back into the bloodstream. The process isn’t 100 percent effective and important ions are always lost, so the salmon must replace them by other means. Some are replaced during the ingestion of food, and critical salts are absorbed through the intestine. But more important, critical ions like sodium and chloride are actively transported, against osmotic gradients from the surrounding water, into the blood by special cells in the gills. The huge surface area of the gill makes it an osmotic liability, yet is vitally important for oxygen intake and is packed with specialized chloride cells that have deeply folded or “invaginated” membranes and are full of mitochondria (the microscopic “power engines” within cells) and important enzymes. By consuming metabolic energy, the chloride cells actively absorb key ions from the environment and maintain the supply of crucial ions to the body.
As a smolt swims downstream into salt water, the osmotic forces are effectively reversed. In fact, from an osmoregulatory standpoint, a life in seawater is much more challenging than one in freshwater, because the osmotic gradient between a salmon and the ocean is much larger than that between a salmon and a stream. The leaky boat now loses water into the surrounding sea. The salmon replaces the lost water by actively gulping seawater that is absorbed by the intestine. But the intestine cannot absorb water without also absorbing the ocean’s salts into the bloodstream. To retain the ionic balance, the kidney now must function to filter and retain water, and in the gill, the chloride cells and their internal structure reorganize to excrete sodium and chloride ions out of the bloodstream and back into the ocean. What of a sailor lost at sea—Coleridge’s drifting mariners, perhaps? Unlike oceanadapted salmon, human sailors cannot survive drinking seawater because our kidneys can’t produce a urine sufficiently concentrated to preserve our body’s delicate ionic balance and conserve water while eliminating all the excess salt ingested with the seawater.
The physiological processes involved during smolting are under the developmental control of a complicated mix of hormones. This hormone bath is secreted by the salmon’s thyroid, pituitary, and interrenal glands, which themselves receive environmental and developmental cues to regulate the timing of the physiological and cellular transformations. The changes required to adapt fully to a life in the sea take some time before they are fully functional; some shifts in cellular ion pumping can occur in less than a day, while other more complex tissue adaptations take longer. Salmon smolts are fortunately very tolerant of shifts in ionic and osmotic balance and can survive the transition to salt water while their bodies are still transforming from a former life in streams and rivers.
With its physiology and anatomy at least partially prepared for a life in salt water, a smolt leaves the rivers of the coastal watershed for the sea. Intermediate between rivers and the open sea are the estuaries at river mouths along the coast, and these serve as transitional stops for salmon en route to the ocean. Estuaries have complex physical environments driven by interactions between river flows and ocean tides. Water depth, temperature, current speeds and directions, turbidity and salinity, and food sources all vary over small distances and on time scales varying from tidal to seasonal cycles. The growth of salmon is rapid in estuaries, and the wide diversity of habitats allows these coastal zones to be exploited to different extents by different salmon species; they feed, changing their diet as they grow, and may use the brackish water found in parts of an estuary to ease the physiological transition of smolting. Some species remain longer than others and linger in estuaries, fjords, or near shore before heading into the open ocean, usually by late summer, and then don’t return to the Salmon Forest until they are fully mature and ready to spawn.
In the open sea, salmon life is enigmatic. This is true for most pelagic fishes because of the extreme difficulty of studying creatures that roam vast areas of the planet. Our only glimpse of their peripatetic lives comes from the brief hint of their ecology we can deduce when they are caught. There is some evidence that their patterns of dispersal have some genetic basis: sockeye, pink, and chum salmon tend to favor the open ocean, while chinook and coho salmon are often found in coastal areas. And oceanic conditions undoubtedly affect their ranging and life at sea, for despite its overwhelming size, the ocean does not provide a uniform environment from season to season and year to year. In the Pacific, the El Niño / Southern Oscillation (ENSO), which is the periodic variation in ocean surface temperature and climate, causes changes in the thermal structure of the sea and alters coastal current flow and the strength of upwelling current features along the coast of the Americas. These changes then affect the biology and distribution not just of salmon but of the organisms that the salmon feed on. When surface temperatures warm and the amount of nutrient-rich upwelling waters decreases (during an El Niño), warm-water tropical species move northward and colder-water species, like the salmon, must forage farther north or into deeper, cooler waters. The changes in their environment can cause reduced growth and increase the chance of mortality because growth is coupled with prey availability and temperature.
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SALMON HAVE evolved to leave the freshwater terrestrial ecosystems where they are born and then to feed and rapidly grow in the rich waters of the north Pacific. They are one of the most numerous of the fishes that swim the upper waters of the seas and thus are a critical component in the north Pacific Ocean ecosystem; by their numbers alone they affect an incredible diversity of organisms either as a competitor for resources, a predator, or prey. Because survival in the ocean is very size selective, the majority of salmon that manage to survive the perils of development in a streambed nest, through smolting, do not to manage to return to the forest. Small creatures survive either by existing in vast numbers and reproducing quickly (like many zooplankton and phytoplankton) or by growing very rapidly beyond the size that makes them an easy one-gulp meal. In the ocean arena, where the size of an animal’s gape and the ferocity of its feeding bite often determine what eats what, salmon are opportunistic hunters and feed on a diet of zooplankton, krill, small fishes (even other salmon), and small crustaceans when they are immature and then move to larger fishes and squid as they continue to grow. Similarly, salmon are preyed upon by an abundance of predators like seabirds, dogfish, and other larger salmon when they are small, and when larger become the preferred prey of seals, sea lions, sharks, orca, and humans.
A salmon must continuously traverse a gauntlet of predators that includes some of the largest and fiercest of the ocean’s inhabitants. Among the largest, humpback whales (Megaptera novaeangliae) are important seasonal visitors to north Pacific pelagic and coastal waters. Curiously, despite their enormous size they feed on the smaller salmon. It is estimated that up to 20,000 humpbacks migrate into the region to feed in the nutrient-rich waters during the summer months and then migrate south into tropical waters to mate and calve during the winter. Different subpopulations of humpback whales migrate from these feeding grounds to breeding sites off Mexico and the Hawaiian Islands, and southeast of Japan. Like the other great baleen whales that frequent the northern waters to feed, such as the sei (Balaenoptera borealis), the fin (Balaenoptera physalus), and the much smaller minke (Balaenoptera acutorostrata), they feed primarily on krill and small schooling fishes like herring, pilchard, mackerel, and small salmon. Although not always preying on the salmon directly, they are important to the salmon’s life-history cycle because they also feed on fishes that compete directly with the salmon for food. Their sieve-like feeding anatomy, their baleen-stuffed mouths, which gives this group of whales its name, is optimized for separating small prey items from the huge gulps of water the whales capture in their mouths and expandable throats. After a gulp, they squeeze out the water, past the baleen plates that separate and concentrate the krill and small fishes for ingestion.
Humpback whales that winter in Alaska and British Columbia are unique in their use of cooperative bubble-net feeding techniques. In a spectacular display of organized feeding, groups of whales encircle schools of prey in a ring of exhaled bubbles that serves to concentrate the fish in a small area, maximizing feeding efficiency for the entire group. The whole event is extremely well choreographed. Deep-diving individuals locate the prey school and begin to envelop it in a curtain of air bubbles expelled from their blowholes. Other whales use loud vocalizations to herd errant prey into the rising bubble net. By carefully spiraling upward and continuing to exhale, the whales drive the school of prey fish toward the surface and into an ever-tightening ball. Then, on cue, the whales surface through the center of the bubble net, mouths agape, capturing hundreds or thousands of fish in titanic gulps.
The pelagic crab (Pleuroncodes planipes), which extends its range into the Northern California current during El Niño periods, is just one of a multitude of planktonic creatures that are part of the salmon’s north Pacific food web.
Beautiful Pacific white-sided dolphins (Lagenorhynchus obliquidens) roam deeper waters off the Pacific continental shelves from Mexico to Alaska. They are a small part of a gauntlet of predators that feed on maturing salmon in the open seas.
Harbor seal (Phoca vitulina) resting on an ice floe in Misty Fjord, Alaska. Salmon form an important part of the seasonal diet of north Pacific seals and sea lions. Unfortunately, competition between these animals and people for increasingly scarce salmon resources has led to the euthanization of seals and sea lions, which are considered a nuisance to fishing stocks.
Humpback whales (Megaptera novaeangliae) are influential seasonal visitors to the north Pacific. They feed primarily on krill and small schooling fishes, including immature salmon. Even when not preying on salmon directly, humpbacks are linked to them trophically because they feed on fishes that compete with salmon for food.
Among the fiercest of the oceanic marine predators, orca (Orcinus orca), like salmon, are iconic animals of the Pacific Northwest. Adult orca are apex predators in oceanic ecosystems, with no predators of their own, and they are the largest of the Delphinidae (dolphins). They are toothed whales with distinctive black and white coloration, large dorsal fins, and powerful bodies that can attain about ten meters in length. Some orca live in complex matriarchal societies, although all tend to form pods of at least a few related individuals and engage in sophisticated cooperative behavior.
There are three separate races of orca from Washington State through Canada, Alaska, and the Aleutian Islands, and these differ in distribution, behavior, and social structure. The “offshore” race seldom approaches the shore and is believed to feed primarily on schooling fish, like the salmon, and occasionally other marine mammals and sharks. The other two races have overlapping ranges along the coast but seldom interact or collocate. The “transient” orca race forms small pods of less than ten individuals and feeds almost exclusively on other marine mammals and birds, including sea lions, seals, porpoise, small baleen whales, and other dolphins. Although they can echolocate and have an extensive vocal repertoire, they remain relatively quiet when hunting, presumably to avoid alerting their prey.
The third orca race, “residents,” has a more complex pod social structure and feeds primarily on fish. Resident pods tend to follow salmon in their spawning migration, and even though they are known to prey on about two dozen different fish species, salmon make up over 95 percent of their diet. They feed primarily on chinook and coho, presumably because they are the largest and have the highest lipid content of the salmon species, and they continue to target chinook and coho even when those species are present in low numbers and other salmon are locally more abundant. A single orca can consume more than 200 kilograms of salmon a day. When captured, large salmon are sometimes carried to the surface and torn apart for sharing with other pod members. Fish-hunting orca use high-intensity echolocating clicks to localize their prey from as far as 100 meters away, and it is possible that the returning sound pulses provide enough information to the whales to allow them to discriminate different fish species. Experiments on the sensory physiology of salmon have shown that they are incapable of detecting sound frequencies higher than about 400 hertz. The echolocating clicks generated by the orca produce most of their energy in frequencies between 45 and 80 kilohertz, a frequency at least 100 times higher, which would be undetectable to salmon prey.
Some pods of humpback whales use cooperative bubble-net feeding techniques when hunting fish, surrounding their prey with a ring of bubbles from their blowholes. The rising bubble ring concentrates the prey, which are then swallowed from below as the whales rush toward the surface.
It is only recently, in a geologic time sense, that a more fearsome salmon predator has arrived in the Salmon Forest and north Pacific—humans. Our predatory capabilities have rapidly evolved from the first native fishermen who stalked the banks of salmon streams with nets and spears. Now our nets have mouths that gape much farther than the mouths of the largest baleen whales, our longlines have hooks for teeth and form jaws that stretch for kilometers, and our fishing ships range tirelessly along the coast and into the roughest of seas and are equipped with echolocating sensors that rival those of the orca. Very quickly we have become the most important salmon predator and the apex predator for the entire world.
Survival isn’t merely a question of eating or being eaten; salmon have intricate ecological relationships that affect their chances of ever reaching reproductive maturity. They compete with other fishes like herring and hake for similar prey, and the degree of competition depends on their age and size and the availability of the food resource, which varies in time and space. And salmon succumb to a host of different parasites and pathogens. As it is for most creatures on earth, life as a salmon is difficult, and living long enough to procreate can seem nothing short of a miracle.
The saying goes that “the star that burns twice as bright burns half as long,” and a salmon burns very, very bright. Their high metabolic rate allows salmon to grow rapidly as long as food is available, and they obtain more than 95 percent of their body mass while at sea. But they sacrifice longevity for their rapid growth rate, and therefore become fully mature quite quickly. The more northerly salmon tend to be slightly older when mature—a chinook salmon in the cold Bering Sea may be as old as nine. However, most salmon are fully mature in two to five years, depending on the species, which is not a long period considering that much of that time may be spent in freshwater prior to smolting. Assuming that a salmon can survive until it is sexually mature, it then responds to a mix of inherent developmental cues and environmental signals and begins another epic migration; it stops roaming the ocean and returns to its natal stream, sometimes traveling thousands of kilometers.
Returning to its natal stream is a daunting challenge for a fish that can range so widely. Again the salmon must manage a transition in environments, from the relatively stable conditions of the open ocean to the much more complex physical environment of the coastal zone, with its bays, reefs, islands, strong and reversible tidal currents, fluctuating temperatures, and changing salinity. But first, a salmon must navigate back to the coast, and to the correct river mouth location, and at precisely the right time to meet and run upstream with its cohort.
The exact means by which salmon can navigate so accurately while in the open ocean are not well understood. They don’t wander randomly through the varying oceanic conditions; instead, they migrate on a relatively straight course toward their birthplace. This implies that they have some type of internal map and compass capability that allows them to navigate as well as to be temporally and geospatially aware. Juvenile and larval salmon are sensitive to the overhead position of the sun as well as to patterns of polarization in the sky, and although it has not been shown unequivocally in adult salmon, it is assumed that they retain the same sensory abilities. A solar compass providing orientation cues is of limited use when the sun isn’t visible, so an additional sense is presumably utilized, and effective navigation requires that the navigator can deduce position in the ocean as well as position relative to a destination. It is believed that adult salmon can sense and orient in the earth’s geomagnetic field, a capability that has been demonstrated in some birds, bees, and other fish, even salmon fry. Exactly how the magnetoreceptive mechanism works is not known; however, tiny chains of magnetite particles have been found in the dermethoid skull bones of chinook salmon and within the lateral line of Atlantic salmon. They may function as part of a sensory system, because the magnetite particles carry their own permanent magnetic field and rotate to align with earth’s magnetic field, creating a tiny yet measurable force, which is monitored by specialized nerve receptors and tissue. At critical times in its development, geomagnetic information unique to a particular location is imprinted on the salmon’s memory. It can be recalled to form a piscine map of the world and to navigate to natal rivers, where other sensory modalities take over.
For salmon, finding their way back to their natal nesting site in the Salmon Forest is based on multiple navigation techniques, depending on their proximity to their destination. Once they are in the vicinity of the estuaries and rivers that will take them to their spawning grounds, the “map and compass” navigational scheme used in the open ocean gives way to navigation based primarily on olfactory cues; they begin to smell their way home. The chemical cues that enable the salmon to differentiate water originating from their natal nesting sites are too dilute once the freshwaters have been mixed in the ocean, so this olfaction-based scheme is of most use once the salmon have reached a freshwater source that provides a steady current of odors to guide them. And it is important to remember that the chemical signatures from their spawning beds are hidden within a turbulent mixture of fresh- and salt water of varying temperature and salinity and mixed with innumerable other molecules and pheromones that may attract or repel the migrating salmon. That a salmon can do this so successfully indicates that individual streams and nesting areas have unique chemical characteristics that remain stable, at least during the life cycle of the salmon, and that a salmon can actually distinguish these characteristics from those of surrounding streams. Its ability to return to its place of origin implies that a salmon must learn or imprint the chemical characteristics of its natal stream around the time of its emergence from the nest and during its downstream migration prior to and during smolting, and it requires that the salmon remember and respond to the olfactory cues when returning as an adult.
The sensory details of olfactory homing, like those of magnetoreception, are not completely understood. What chemicals are involved and their exact origin, and whether there are speciesor population-specific pheromones that may have a genetic basis have not been deduced. The sensory cells responsible for chemoreception—the sense of smell—are primarily found lining the walls of invaginated pits behind the nares, which are nostril-like openings on the salmon’s nose. These cells have evolved to be extremely sensitive to minute quantities of very specific chemicals; as little as a single molecule contacting the outer cell membrane triggers an electrical nervous response. This response is conducted, either by long axons on the end of the sensory cell or through a secondary nerve, directly to the olfactory bulb, a structure in the most forward part of the brain that controls the chemical perception of odors. Salmon have hundreds of thousands of odor-sensing cells in close proximity to the brain, capable of responding to a multitude of dissolved chemicals, but they must still be able to distinguish those scents particular to their natal nest sites and then coordinate their behavior.
Recent studies have shown that salmon may accomplish the imprinting of olfactory information, their “scent memory,” into their sensory cells and nervous tissue in several ways. At specific times in salmon development, like when first leaving the nest or during smolting, as well as under changing environmental conditions, there is a distinct surge in the release of certain endocrine hormones from the thyroid gland. These hormone surges result in the proliferation of olfactory neurons with a sensitivity specific to scents present in the water at that time, as well as to an increased responsiveness of the individual sensor cells themselves. These cellular changes are concomitant with growth in the nerve cells within the olfactory bulb of the brain and together presumably form the base material in which to imprint a scent memory. This imprinting mechanism forms a pliant system that can be tuned to critical chemical markers in the environment present at key stages in salmon development. It also allows salmon to imprint sensory information opportunistically, in response to new environmental stimuli encountered during their early migration. Exactly how a salmon retrieves and compares its internal scent map with the olfactory information it perceives as it swims upriver—what, if anything, a salmon thinks—is of course unknown, but suffice it to say it has worked extraordinarily well for many thousands of years.
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A SALMON returning to freshwater from a life in the ocean requires a change in its osmoregulatory system similar to that at smolting, but in reverse. The salmon’s bodies undergo cellular and physiological changes in order to rid their systems of excess water and actively absorb the necessary ions from their environment. They also go through profound physiological modifications in preparation for reproduction. Their bodies flood with the hormones involved in gonad development, maturing their ovaries and testes and packing their bodies with eggs and sperm. These changes place an enormous requirement on the metabolism during a time of increased physical exertion, when the fish are fighting their way upstream, and during a time of starvation, because they stop feeding once they begin their spawning run. This incredible metabolic feat is made possible by the sacrificial assimilation of other body tissues; over 50 percent of the salmon’s muscle protein and 90 percent of its fat are absorbed while migrating, although their body weight remains relatively constant because the missing tissue is replaced by water. Even the kidney, which is critical for osmoregulation, begins to deteriorate just as the higher physiological demands are being incurred. During these last stages of its life cycle a salmon’s behavior and physiology focus only on reproduction, at the expense of all else, and lead to the genetically programmed death of the salmon on its spawning bed.
Between 95 and 99 percent of the salmon that reach reproductive age manage to return to their birth site. But what is the advantage of struggling a thousand kilometers upriver, over rushing cataracts and past a gauntlet of predators, to spawn in a place that may appear to be just like any other? An optimum nest site has water of the correct depth and suitable velocity: if the flow is too weak, the water can stagnate; if it is too strong, females may be unable to dig nests or will waste precious energy fighting the current, and strong currents can shift sediments that may damage eggs beneath the substrate. The sediment must be of the correct size to facilitate digging and allow water to permeate the nest to flush the eggs with fresh oxygen and remove waste products. And the water itself has to be clean, clear, and well oxygenated, as well as the correct temperature to incubate the eggs. The nesting sites must also be located in areas with nearby habitat suitable for emerging alevins, as well as protected from extremes in flow that might come during times of flood or drought. By returning to the very nesting site where it was born, a salmon increases the chance of survival of its own offspring; the adult survived, ipso facto, the nesting site was a good one. And it takes two salmon to reproduce, so returning to the natal stream ensures that there are appropriate numbers of males and females present to compete for mates. In an evolutionary context, their excellence at homing strengthens the reproductive isolation of the different salmon populations, which then adapt to the environmental conditions (temperature, sediment size, flow rates, etc.) that are characteristic of their home river. An anadromous life history that includes long and complex migratory paths tends to disperse a population as well as disperse the population’s gene pool over a larger area (which could be considered an advantage or a disadvantage); homing helps salmon adapt to local conditions, fine-tuning the species to optimize its chances of passing on its genes to its progeny.
There is a very small fraction of the migrating salmon population that doesn’t return to its natal stream. These fish are referred to as “strays,” and it is not known whether this behavior is based on an impulse by the salmon to spawn elsewhere or a failure of their homing instinct. The occasional failure or stray is actually of benefit. If homing were absolutely perfect, the population would be literally and figuratively keeping all its eggs in one basket. Unerring return to the natal stream helps salmon populations adapt to their environment, but it puts the entire stock at risk should there be some sort of catastrophic disturbance. Should a landslide smother or divert a spawning stream, or an advancing continental ice sheet dam an entire watershed, those migrating salmon that stray allow the recolonization of other habitats and the continuation of at least some of the population. Straying salmon also allow the mixing of genes between different populations, which provides vigor to the species as a whole and is the mechanism by which salmon have naturally extended their range around the Pacific rim.
The collapse of the sockeye salmon fishery on the Fraser River in British Columbia should have been a prescient example of what can happen to salmon and other natural resources when disrupted. Between 1912 and 1914, a series of landslides initiated by railroad construction on the steep hillsides around Hells Gate, a particularly narrow gorge in the Fraser River canyon, partially dammed the river with debris. The constriction in the flow increased the velocity and turbulence in the river to such an extent that the salmon were no longer able to pass. Instead they struggled against the currents and rapids until they were exhausted and then milled about in side pools and eddies without ever reaching their nesting sites in lakes and tributaries farther upstream. During the peak sockeye spawning run in 1913, millions of sockeye were seen backed up along more than fifteen kilometers of the river below Hells Gate, and the Fraser River was crimson in places from the bodies of struggling salmon. A witness recounted, “The fish were doing their best, throwing themselves out of the water in their eagerness and wounding themselves against the rocks or the slide to get a purchase against the current” (quoted in Evenden 2004). Heroic, but mostly futile, attempts were made to aid the salmon by shuttling them by hand-dipped net and using wooden flumes to divert them around the rapids while workers struggled to remove the debris from the landslides. Despite these efforts, only a handful of fish ever reached their spawning sites. This had a devastating effect on important aboriginal fishing grounds upstream, which had been used for over four thousand years by the Nlaka’pamux and earlier First Nation tribes. At the time, the Fraser River spawning population was also the nucleus of American and Canadian commercial fisheries, which caught more than thirty million sockeye from the waters around Vancouver Island and Juan de Fuca Strait in 1913. There were over forty canneries around Vancouver on the Canadian side alone.
The catastrophe of the Hells Gate landslides, and the coincident heavy fishing pressure, is reflected in the fisheries’ catches in the years after the slides. In 1917, which should have seen the return of the 1913 Fraser River offspring after four years of maturation, the catch was only one-quarter the 1913 level. By 1921 it was only onethirtieth, and the regional sockeye salmon fishery had collapsed. However, both the salmon and the fisheries ultimately survived. The remaining Fraser River sockeye population and strays from other rivers have slowly repopulated the watershed, although it is only recently that they have returned to spawn in numbers remotely close to the those experienced prior to the collapse. The people of the region adapted as well. With the loss of their native fishery, the First Nation peoples shifted away from a salmon-based economy to one with more agriculture, hunting, and wage labor in the expanding cities and towns. The commercial fishing industry survived by shifting its focus to other salmon species, like the pink and coho; and like a straying salmon, the commercial fisheries expanded their geographic range and dispersed to begin catching fish farther and farther to the north.
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EVEN AFTER a migratory life as strenuous and eventful as that of a salmon—surviving thousands of kilometers of river and ocean—the final act of reproduction is anything but peaceful. Males and females both struggle until the very end in a competition for limited resources. Females must locate and then compete for the best nesting locations, and males compete for the chance to access a mate. The best nesting sites have an optimum combination of water flow and sediment size, and females aggressively defend their selected sites from intruders. Males bite, block, and bash each other in displays of physical dominance; usually the largest and best-conditioned males win. Some smaller males adopt “sneak” tactics in a clandestine mating behavior that is not unique to the kokanee; they quickly assume a coloration more similar to that of the female and slip unnoticed past larger, aggressive males and attempt to mate.
At the chosen nesting site the female rapidly flexes her tail and the side of her body against the bottom, flushing fine sediments away and digging a depression of gravel and small stones that is about eighteen to fifty centimeters deep. The entire process may take a few hours; when she is ready to release her eggs, she sinks her belly to the bottom of the nest. The ever-vigilant dominant males monitor the female behavior and the state of her nest preparations and when finally ready to spawn, they swim tightly alongside her while posturing and vibrating their bodies. Egg release by the females takes less than a minute; the males release their milt synchronously, and fertilization, the union of egg and sperm, takes place in the water column as the eggs fall down into the gravel below the spawning pair. In densely populated nesting areas, with sometimes hundreds of males vying for the opportunity to spawn, multiple males may stack up above mating pairs and simultaneously release their milt, so eggs in a nest may actually have been fertilized by more than one father.
Adult male sockeye salmon (Oncorhynchus nerka) fighting in shallow water. Adult males engage in fierce biting and tail slapping in order to prove dominance and establish mating access to females.
After spawning, adults are emaciated and their bodies torn and battered. The males are exhausted by competition for mates; the females guard their nests until they are too weak to hold their position in the current, then they drift away and die.
After she has released her eggs, the salmon female immediately covers the area with gravel and starts digging a new nest, just upstream of the first, and the entire spawning process begins again, until all her eggs have been shed. The entire redd may eventually consist of four or five individual nests made by the female over two or three days. Once all her eggs have been released the female patrols and protects the redd to prevent other females from digging there and disrupting her eggs, as later-arriving salmon also want to select optimum locations to spawn. She will continue her guardian duties until completely exhausted. Males continue competing for the opportunity to mate with ripe females until all remaining salmon have perished and drifted away in the current. Then their carcasses choke the shallows, get caught in streamside foliage, and rot upon the shores. Their bodies disappear quickly and there are no visible traces of the previous generation when the next spawning adults return.
The story of the salmon has come full circle: from the freshwater streams of the forest, to the open ocean, and then back to the lakes, rivers, and streams beneath the forest canopy, birth and death and life are renewed. Because of the sheer numbers of salmon returning to their birthplace, at least in times past, and because salmon achieve nearly all of their body mass while living in the sea, there is an enormous transport of biomass from the ocean to the freshwater ecosystems where they die. The salmon life cycle creates an incredible conveyor belt of nutrients and energy from marine ecosystems to terrestrial ones in a world where, typically, gravity pulls all things downhill from the mountains and deposits them in the sea. Their life history of anadromy and semelparity transports millions of tons of salmon flesh into nutrient-poor freshwaters that then shape the entire Salmon Forest. By the time the last of their watery flesh has tumbled from their bones and the last bits of their cartilage have melted into the streamside shore, they will have been preyed upon, scavenged, and decomposed by a multitude of creatures, from sharks to bears, gulls, beetles, and bacteria. All living things possess a unique gestalt, perhaps none more so than the salmon, whose life, we now see, extends far beyond the boundaries of its body, encompassing the entire forest and expanding far into the Pacific Ocean.