salmoniform

▪ fish

Introduction

      any member of the order Salmoniformes, a diverse and complex group of fishes. The order consists of about 1,000 species in the freshwaters and in the oceans of the world. Included are the familiar trout, salmon, and pike, as well as most of the bizarre forms of fishes inhabiting the middepths of the oceans.

      The framework of the order Salmoniformes in the discussion below should not be considered as a definitive taxonomic category but rather as an assemblage of diverse fishes possessing several primitive anatomical features representative of an early stage in the evolution of modern bony fishes (teleostean fishes).

General features

Evolutionary importance of the order

      The significance of the order Salmoniformes as presently classified—a major departure from early schemes of fish classification—is in the evolutionary position of the group; the Salmoniformes are now considered a basal stock in the mainstream of modern bony-fish (teleost) evolution. The present classification implies that the ancestors of salmoniform fishes developed several evolutionary trends in the Late Mesozoic Era, about 100,000,000 years ago, providing the necessary source of evolutionary raw material to initiate several successful evolutionary lineages, ultimately leading to most of the modern bony fishes.

      The order Salmoniformes, as treated in this article, is based on the combined work of a British ichthyologist and several American ichthyologists, who have divided the order into eight suborders and 37 families. Constructed in this way, the order Salmoniformes brings together a variety of extremely diverse groups. Several major alterations have recently been proposed for the classification of salmoniform fishes; thus the classification used in this article is provisional and may be subject to extensive changes when more precise information is available. The order Salmoniformes can be considered more as an evolutionary grade in the phylogeny of teleostean fishes than a well-defined taxonomic category. No single character or group of characters (char) can distinguish all salmoniform fishes from all other fishes.

Reasons for interest in the order

      The trouts, salmons, chars, whitefishes (whitefish), and graylings (grayling) of the family Salmonidae are the most widely known and intensively studied family of fishes. Their famed sporting qualities and excellent taste ensure their economic importance. At the other extreme, some deep-sea families of salmoniform fishes are known only to a few ichthyologists, and often only on the basis of a few imperfectly preserved specimens. The bulk of salmoniform species are fishes of the middepths (mesopelagic and bathypelagic zones) of the open oceans. The deep-sea salmoniforms have evolved unusual body forms and structures—such as luminous organs, telescopic eyes, complex appendages, and enormous and well-developed jaws and teeth—to cope with existence in the twilight and dark zones of the ocean and are of great interest in the study of evolutionary and developmental biology. Some of the anatomical structures evolved by the deep-sea salmoniforms are among the most striking and strange ones found in the animal kingdom.

Size range

      The largest of the salmoniform fishes are members of the family Salmonidae and include the Pacific king salmon (chinook salmon) (Onchorhynchus tshawytscha) and the Danube and Siberian huchen (Hucho hucho), both of which are known to attain a weight of 50 kilograms (110 pounds) or more. The North American muskellunge (Esox masquinongy), a member of the pike family, also approaches this size. The majority of the salmoniform species, however, are small. Most of the deep-sea species do not exceed 150 millimetres (six inches) in length, and many at maturity are no more than 25 to 50 millimetres (one to two inches) long. The largest of the marine salmoniforms is one of the lancet fishes (lancet fish) (family Alepisauridae); this species may reach a maximum length of 2.1 metres (about 7 feet). The lancet fish has an elongated body with tremendously enlarged, dagger-like teeth, a fragile sail-like dorsal fin, and a soft, flaccid body. Occasionally a lancet fish migrates from the ocean depths to the surface and may be caught by a fisherman or found washed up on a beach. Lancet fishes, like other deep-sea salmoniforms, are so highly modified that the relationships to trout and salmon are not obvious. A basic salmoniform feature, however—the small, fleshy adipose (fatty) fin that is situated between the dorsal fin and the tail—is found on both trouts and lancet fishes and has been inherited from a very ancient, but common, ancestor.

      Most salmoniform species, including the smaller forms, are predacious fishes. Many peculiar modifications have been evolved by the small species of marine salmoniforms to allow them to capture and consume prey sometimes as large as themselves. Some of these lilliputian monsters appear to be mostly head and jaws, all out of proportion to the soft, gelatin-like body. The lack of a neck in fishes limits the mobility of the head and jaws; remarkable adaptations increase the flexibility of the head and allow a great enlargement of the mouth opening to engulf prey quickly. Several deep-sea salmoniforms lack bone on the anterior portion of the vertebral column, increasing the flexibility of the head and jaws.

Distribution and abundance

      Salmoniform fishes are found in fresh water on all continents and in all of the oceans of the world. Various representatives of the trout, pike, and smelt families are indigenous to the cooler fresh waters of the Northern Hemisphere. Species of the family Salmonidae inhabit the colder waters of North America, from tributaries of the Arctic Ocean to tributaries of the Gulf of California in northwestern Mexico; in Europe and Asia, a comparable distribution is found, from the Arctic Ocean to the Atlas Mountains in North Africa and to the island of Taiwan. One member of the family, the Arctic char (Salvelinus alpinus), is the most northerly occurring of any freshwater fish. The development of an anadromous life cycle—spawning in fresh water but migrating to the sea for feeding and maturation—has allowed species of trout and salmon to extend their range greatly, particularly into fresh waters of glaciated regions after the glaciers recede and waters become inhabitable. The use of marine invasion routes allows a rapid expansion in the distribution of a species into new areas, often inaccessible to other species completely restricted to a freshwater life cycle. Species of the family Salmonidae are clearly the dominant fishes of the recently glaciated fresh waters of the Northern Hemisphere.

      The pike and its allies (family Esocidae) have a distribution somewhat similar to the Salmonidae; however, their range extends neither so far north nor so far south. The pikes are completely restricted to fresh water throughout their life cycle; however, the distribution of the northern pike (Esox lucius) in Europe, Asia, and North America is one of the broadest distributional patterns of any fish species. Such a distribution must have been achieved when direct freshwater connections existed between the present major drainage basins and between Asia and North America. The smelts (smelt) of the family Osmeridae are small fishes of Europe, Asia, and North America. Some smelts are permanent freshwater inhabitants, but the distribution of freshwater smelts is associated with relatively recent geological events; most smelts are anadromous or marine. No smelt species has penetrated far enough inland to establish a broad distribution in fresh water comparable to that of the salmonid fishes. The other salmoniform fishes with anadromous and freshwater species in the Northern Hemisphere are members of the Far Eastern families Plecoglossidae and Salangidae. In the Southern Hemisphere, salmoniform fishes that are ecologically similar to the trouts and smelts are encountered in the fresh waters of southern Africa, southern South America, Australia, New Zealand, and Tasmania. These fishes are classified in the families Galaxiidae, Retropinnidae, Aplochitonidae, and Prototroctidae (of the suborder Galaxioidei). The galaxioid fishes are typically small (measuring only 100 to 300 millimetres [four to 12 inches]) marine and freshwater fishes. The family Galaxiidae contains the most species (about 35) and has the broadest distribution—in Africa, South America, Australia, New Zealand, and Tasmania. The smeltlike fishes of the family Retropinnidae comprise about six species native to Australia, New Zealand, and Tasmania. The family Aplochitonidae consists of three species in southern South America and a larva-like (neotenic) species in Tasmania. The Prototroctidae has two, troutlike species in Australia and New Zealand. Various species of Salmonidae, particularly the North American rainbow trout (Salmo gairdneri) and the European brown trout (S. trutta), have been widely introduced and successfully established in suitable waters in Africa, South America, Australia and New Zealand. When introduced into lakes with abundant food fishes but previously lacking large predator fishes, the introduced trout flourish, growing rapidly to a large size. In certain lakes in Australia and New Zealand, famed for their trophy-sized trout, the trout feed avidly on their distant relatives, species of the Retropinnidae and Galaxiidae.

      The remaining 25 or more families of Salmoniformes, with about 800 species, are entirely marine, typically middepth and deep-sea fishes (deep-sea fish). Representatives are found in all oceans and all depths, but in temperate and tropical waters major concentrations occur at depths of 200 to 2,000 metres (about 650 to 6,500 feet). The tremendous abundance attained by some populations of these marine salmoniforms has become evident only with the advent of modern sonar equipment, which has detected aggregations many square kilometres in extent.

Importance

      The economic significance of the trouts and salmons both as sporting fishes and as commercial (commercial fishing) products is well-known. Governments invest heavily to maintain and increase the production of trout and salmon; hundreds of millions of trout and salmon are hatched, reared, and stocked each year for sport and commerce. In fact, a large private industry has developed—particularly in Denmark, Japan, and the United States—to supply trout to markets and restaurants. With the problems of increased human population and the demands made on rivers by industry and agriculture, the challenge of perpetuating and increasing the abundance of salmon and trout has become a serious one for fisheries scientists.

      The demand for trout as a sport fish far exceeds the supply in heavily populated regions. This situation, particularly in the United States, has resulted in a massive program by state and federal agencies to raise trout to acceptable size and to stock them in heavily fished waters. Such an artificial abundance, however, is a poor substitute for natural trout fishing.

      Except for the pikes, the remaining freshwater salmoniforms are too small or too rare to be significant sport fish, but most are considered excellent food fish. The oceanic salmoniforms have little direct importance to man; because of their tremendous abundance, however, they form a vital link in the food chain of the oceans, providing forage for valuable predator species such as the tuna. Many of the deep-sea salmoniforms undertake daily vertical migrations (migration), rising toward the surface layer of the ocean at night for feeding. This vertical migration exposes them to predation by larger fishes and functions in the recycling of energy in the ocean by elevating energy accumulated in the lower depths (in the bodies of the small salmoniforms) and making it available to large predators in the upper zones.

Natural history

Life cycle and reproduction

      Virtually every type of life cycle and mode of reproduction known for fishes is exhibited by some salmoniform fishes. These life cycles range from passage of the entire life-span in the confines of a small pond or stream to migrations encompassing thousands of kilometres from a stream to the ocean and back to the stream. Some species have a direct development stage from the egg, hatching as miniature adults, ready to fend for themselves. Most deep-sea marine species have larval stages, drastically different from the adult. Some larvae have eyes attached to long stalks from the head. Most salmoniform species consist of males and females, but several deep-sea groups are hermaphrodites (hermaphroditism), a single individual having functional testes and ovaries. Evidently, in the darkness of the ocean depths, it is advantageous for an individual to function both as male and female.

      The life cycles of salmons and trouts have been intensively studied because of the economic importance of salmonid fishes. Factual information the life cycle and reproduction is used to settle disputes between nations regarding the origin of salmon caught in the open ocean and for the intelligent management of the resource.

      The life cycle and reproduction of the deep-sea salmoniforms, however, are little known except for interpretations gained from examination of a few specimens and collection of eggs and larvae. Eggs and larvae of many of the marine species have not yet been found.

      Among the salmoniform fishes, only the pike family (Esocidae) and the mudminnow family (Umbridae) are completely restricted to fresh water throughout their life cycle. All other families that have freshwater representatives contain some species that enter the marine environment for growth and maturation, returning to fresh water to spawn. One species of the family Galaxiidae has a catadromous life cycle—spawning takes place in a marine environment, and the young migrate to fresh water to mature. All of the oceanic salmoniforms are completely marine throughout their life cycle.

      The families Salmonidae and Osmeridae demonstrate a transition between freshwater and marine life cycles. All species of salmonids spawn in fresh water, but the Pacific pink salmon (Onchorhynchus gorbuscha) has reduced the freshwater stage to the spawning migration and incubation of the eggs. As soon as the eggs hatch and the yolk sac is absorbed, the pink salmon fry migrate to sea. Some pink salmon may even spawn in the intertidal zone at the mouths of small streams, virtually eliminating the freshwater stage in the life cycle altogether. Other species of the family Salmonidae, such as the lake char, or lake trout (Salvelinus namaycush), the graylings (Thymallus), and many of the whitefishes (Coregonus), have completely freshwater life cycles. Interestingly, life cycles may differ among closely related species or even between populations of the same species; for example, rainbow trout that go to sea and return as large, silvery individuals are called steelhead trout. A single river system may contain local resident populations of small rainbow trout—maturing, spawning, and completing a life cycle within 100 metres (about 300 feet) of the site of their birth—as well as anadromous steelhead rainbow trout that have returned from the ocean after a two- or three-year journey spanning several thousand kilometres. Evidently the heritable differences that govern the type of life cycle in trouts—anadromous or freshwater—are slight. It has been demonstrated that offspring (animal breeding) from anadromous parents can be used to establish populations in completely landlocked environments, and that the progeny of nonanadromous parents may go to sea if given the opportunity.

      Reproductive behaviour, the type and size of the eggs (egg) laid, and the amount of parental care have been developed in each species by the process of natural selection. In an evolutionary sense, spawning success is ultimately judged by the number of mature adults resulting from any spawning act. If the eggs and larvae are exposed to a harsh and perilous environment, there is a selective advantage for a female to produce fewer but larger eggs and to provide some extra measure of protection for the developing embryos. Cold, swift rivers with sparse food, typically utilized by salmons and trouts for spawning, undoubtedly have been a major selective force in the evolution of large eggs (four to eight millimetres [roughly ⁵/₃₂ to ⁵/₁₆ inch] in diameter) and of nest-building behaviour in the trouts and salmons.

      A large egg with a large yolk to supply food to the developing embryo allows for direct development—that is, the young hatch in an advanced stage, resembling a miniature adult. In more benign environments, such as lakes and the ocean, most salmoniform fishes produce smaller but more numerous eggs, and hatching takes place when the larvae are only partially developed. In many species the larvae are quite unlike the adult form and undergo a rather striking transformation (metamorphosis). Eggs of all freshwater spawning salmoniform fishes are heavier than water (demersal eggs) and develop on or in the bottom of a stream or lake. Marine species typically have pelagic (free drifting) eggs and larvae; the eggs are of neutral buoyancy and thus drift with the currents in the surface layer of the ocean. The eggs and larvae of many deep-sea salmoniforms have not yet been described, and in some species the eggs and larvae may be associated with the ocean bottom.

      As far as known, all salmoniform fishes lay eggs and have external fertilization (oviparous fishes). In several of the deep-sea salmoniform families, in which hermaphroditism is common, it is not known if the species are self-fertilizing.

      Some of the deep-sea salmoniforms have luminescent (bioluminescence) organs, one of the functions of which probably is sexual recognition. In the lantern fishes (lantern fish) (Myctophoidei), the light organs are arranged in distinctive patterns that distinguish males and females of a species.

Behaviour and locomotion

      Only the freshwater salmoniform fishes can be studied in any detail by direct observation. Most of what is known about the deep-sea species is based on preserved specimens, and, for most species, behaviour and locomotion can only be surmised from an examination of the morphology and anatomy.

      The generalized body form of trout and salmon is characteristic of active, swift-moving fishes. A trim, fusiform body, powerful caudal (tail) muscles, and a well-developed tail combine to propel the fish against strong currents with a minimum of resistance. These features also give the trout or salmon the ability to leap barrier falls as high as three metres (10 feet) or more.

      Predatory fishes that dart out to grasp their prey are exemplified by the pike, in which the dorsal fin is situated posteriorly on the body to act more as a rudder than a keel. The pikelike body form has been evolved independently many times among predatory fishes such as the barracuda (Sphyraena sphyraena, of the order Perciformes). Among the deep-sea salmoniforms, however, certain predatory species are sedentary and have only weak swimming ability. Such fish remain immobile until unsuspecting prey ventures close enough to be grasped. Some evidently use a luminous lure to attract their prey.

      A peculiar type of locomotion is encountered among the barracudinas (family Paralepididae), marine salmoniforms of the suborder Myctophoidei. The barracudina swims in a vertical plane, darting up and down with the head oriented downward.

      The behaviour of a fish toward other members of its species can be highly variable. Often, predator species are territorial and aggressive, whereas plankton-feeding species typically form schools and do not function normally unless they are close to other members of their species. Although behaviour patterns are largely innate and species-specific, striking differences occur between closely related species. pink salmon fry, on hatching, seek each other and form schools prior to seaward migration. The young of the coho, or silver salmon (Onchorhynchus kisutch), however, establish territories and aggressively attack other young cohos that invade their territory. This difference in aggressive behaviour is associated with the longer period of freshwater life and limited food supply experienced by the coho salmon.

      One fascinating aspect of the behaviour of trout and salmon is their homing instinct—i.e., the ability to return to the stream of their birth after migrating thousands of kilometres in the ocean for one to three years. Homing to the site of birth for reproduction is apparently a rather universal trait among the Salmonidae. Trout, char, and whitefishes in lakes segregate into discrete populations during the spawning season, each at a specific site.

      It is now generally accepted that the sense of smell plays the major role in guiding an anadromous trout or salmon to its precise natal stream once it enters a river drainage from the ocean. How it finds the mouth of the river system leading to the natal stream from the open ocean is not yet understood; celestial navigation and detection of fields of gravity by some unknown means have been hypothesized. Several senses besides smell may be used to locate the natal stream. cutthroat trout (Salmo clarki) in Yellowstone Lake, Wyoming, have been found to be able to return to their spawning stream after experimental blocking of the senses of smell and sight.

      Homing behaviour has allowed the development of discrete populations among anadromous species of salmon and trout. Different life-history characteristics can be maintained because different populations segregate for spawning, and individuals of a population spawn (animal breeding) only with each other, perpetuating hereditary traits. In major river systems such as the Columbia and Fraser in North America, one species may include several distinct races, each having different life cycles; such a situation greatly complicates the management of a species.

Ecology

      As with other aspects of the biology of salmoniform fishes, the ecology of species of the family Salmonidae is best known. All species of salmonid fishes evolved in clear, cold water, and they thus require pure, well-oxygenated, cold water; for this reason salmonid fishes are the first species (indicator species) to suffer when water quality is degraded. Other freshwater salmoniforms, although not quite so sensitive to water quality as the salmonid fishes, are also susceptible to the inimical effects of man-induced environmental degradation.

      Most salmoniform fishes are predators, feeding on other fish and large invertebrates. The process of evolution, however, works to modify and adapt species for certain ecological specializations in order to exploit a variety of food resources. In the lakes of the Northern Hemisphere, several whitefish species (Coregonus) are comparable, ecologically, to the herrings in the ocean. Such whitefishes, which are often called freshwater herrings, cruise the open water of lakes, filtering out minute organisms by straining the water through a fine mesh of gill rakers—minute bony elements attached to the gill arches. The sheefish, or inconnu (Stenodus leucichthys), a large, predatory whitefish of the Arctic, demonstrates that evolution for ecological adaptation is occasionally reversible: the adults feed on other fish and have evolved a pikelike body shape and large, powerful jaws, the development of teeth taking precedence over that of the gill rakers; the sheefish is quite unlike the typical whitefish from which it has evolved.

      There probably has been strong selection for freshwater salmoniforms to utilize the marine environment for feeding. All groups except the esocoid fishes (pike family and related groups) have species that migrate to the ocean for feeding. This presents a problem of osmotic regulation in waters of different salinities. The physiology of most fishes is fixed for life in fresh water or in the sea, but most of the freshwater salmoniforms are able to live in the sea because they can excrete excess salts through cells in the gills. They also possess well-developed kidneys, which, in the freshwater environment, handle the excess of water that diffuses into their blood via the gills.

      Little is known of the ecology of the wholly marine salmoniforms. They may be ecologically grouped by the depths that they inhabit and by their feeding preference. Those found in the twilight zone of the ocean (200–1,000 metres [650–3,300 feet]) consist of plankton feeders and predators. The plankton feeders typically are more active and have a more fully developed and functional swim bladder than is typical of the predatory forms.

      Because virtually all primary food production in the oceans takes place in the upper, sunlit layer, the deep-sea fishes live in a food-poor environment. At first, it may seem contradictory that they are able to maintain such numerical abundance; certain features of the biology of the deep-sea salmoniforms, however, allow them to attain great numbers. The body of the typical oceanic salmoniform is feebly developed, appearing to consist of little more than gelatinous material. The skeleton and muscles are reduced, so that little energy is needed to maintain the body. Many of the deep-sea species make nightly migrations (migration) to the food-rich surface zone for feeding. The species inhabiting the deepest parts of the ocean must depend on a food supply that filters down from above. This food is concentrated in a narrow bottom layer (the benthic zone), with the result that the benthic species may attain a relatively high abundance.

Form and function

Features of the generalized salmoniform

External characteristics

      The tremendous range of structural diversity found in salmoniform fishes has already been mentioned. Comparisons of some of the extreme morphological and physiological modifications with a generalized, standard type can be useful in understanding the evolutionary trends leading to certain specializations. A trout of the genus Salmo, such as a rainbow trout or brown trout, can serve as a “standard” for the form and function of salmoniform fishes. The nonspecialized morphology and physiology of a typical trout species allow it to utilize diverse ecological niches during its life. A trout's diet consists of a variety of organisms, and its habitat may vary from small streams, large rivers, or lakes to the ocean. The body and fins are streamlined and symmetrical; the body is covered with small, smooth (cycloid) scales; the fins are formed from soft supporting rays, without spines. A small, fleshy adipose fin is located between the dorsal fin and the tail. The dorsal fin is located midway along the body on the dorsal surface. On the ventral surface, the paired pectoral fins are directly posterior to the head, the paired pelvic (or ventral) fins are directly beneath the dorsal fin, and the single anal fin is positioned beneath the adipose fin. The well-developed tail (caudal fin) connotes a powerful swimming ability. The presence, absence, rearrangement in position, and modifications in size, shape, and function of the various fins are characteristic of the numerous families of Salmoniformes.

Digestive system

      The structures associated with feeding and digestion denote the diversity in a trout's diet. The mouth is fairly large with moderate development of nonspecialized teeth on the jaws and on several bones within the mouth. An adult trout can capture and consume a fish about one-quarter its own length without undue difficulty. Feeding on invertebrate organisms, as small as a few millimetres (perhaps ¹/₄ inch) in length, is facilitated by the gill rakers on the surface of the gill arches; they strain small organisms from a stream of water passing over the gills and funnel them to the esophagus. The well-defined muscular stomach opens by a valve into the intestine. A series of fingerlike appendages opens off of the intestine immediately posterior to the stomach. These appendages, called pyloric ceca, secrete enzymes and provide additional digestive areas to the intestine. Among closely related species of the family Salmonidae, there is a tendency for the more predacious species to have more numerous pyloric ceca. Generalizations relating pyloric cecal development to diet cannot be extended, however, to other fishes. The highly predacious pikes of the genus Esox completely lack pyloric ceca, whereas the algae-eating ayu (Plecoglossus altivelis, family Plecoglossidae) probably has more numerous ceca than any other fish, up to 400 or more.

Sense organs

      Because vision is important in the life of a trout, the eyes are well developed; the retina possesses both rods (for vision in dim light) and cones (for perceiving more acute images and for colour vision). The sense of smell is also highly developed.

      The lateral line nervous system functions as a pressure receptor and a direction finder for objects that move, such as another fish. The lateral line might be considered as a remote sense of touch; it does not, however, function in hearing low-frequency sound waves as was once believed. It has been demonstrated that sound waves are well below the threshold necessary to stimulate the lateral line cells. In trout, the lateral line consists of a series of connected sensory cells (neuromasts) with tiny, hairlike projections. These cells are embedded under the scales along the midline of the body and open to the surface through pores in the scales. An extension of the lateral line system on the head consists of a ramification of sensory canals. In some deep-sea salmoniforms living in the absence of the effects of sunlight, other senses are needed to compensate for vision in perceiving the environment, and the neuromast sensory cells may be exposed on raised papillae, thus increasing their sensitivity.

      The swim bladder (or air bladder) has a hydrostatic function, adjusting internal pressure to maintain a weightless condition of neutral buoyancy at various depths. The trouts have a primitive type of swim bladder with a connecting duct from the bladder to the esophagus. The duct is an evolutionary holdover from an ancestor in which the swim bladder was mainly an accessory respiratory organ. Many salmoniform fishes lack the duct, and several deep-sea marine species lack a swim bladder altogether.

Departures from the generalized body plan

      From the primitive body plan exemplified by the trouts, it is possible to derive all of the specialized body types of other salmoniform fishes by the elimination of some structures and by the modification, exaggeration, and rearrangement of others.

      The pike is an example of a specialized predator whose diet, after the first year of life, consists almost entirely of other fishes. Its success depends on how effectively it captures and consumes other fishes, and its whole morphology and physiology are directed toward this end. A pike has an elongated body with a large head and large, powerful jaws. Its mouth is armed with large, canine-like teeth that can handle large prey. Patches of teeth on the gill arches replace the typical gill rakers. Vision is the primary sense used by pike to detect and capture prey. The visual centre of the brain (optic lobe) is more highly developed than are the centres of smell (olfactory lobes). The eyes have a high proportion of cones to rods in their retinas and are positioned to provide partial binocular vision (i.e., the eyes are aimed in the same direction), sighting down grooves on the snout to aim at moving prey. The body form and position of the fins are specialized for swift, darting movements. The dorsal fin is placed posteriorly, over the anal fin, and, as is typical of other salmoniform fishes with posteriorly oriented dorsal fins, the adipose fin is absent.

      The most extraordinary modifications in the basic salmoniform body plan are found among the marine species of the middepths and great depths of the ocean. The more striking adaptations include luminous organs, eyes specialized to function in dim light, feeding adaptations allowing some predatory species to kill and eat a fish as large as themselves, and drastic departures in body shape and fin development.

      Bioluminescence, the production of chemical light by living organisms, is widespread in nature. Among vertebrate animals, only marine fishes have light organs. Light organs (or photophores (photophore)) are encountered in many diverse groups of fish. These structures apparently have been evolved independently several times in different groups of fish. It is believed that light organs of fish have evolved from mucous cells of the skin. Salmoniform fishes, particularly species in the suborders Stomiatoidei and Myctophoidei, have developed some elaborate and highly complex light-producing systems. Some structures have lenses, reflectors, and eyelid-like shades. In addition to light cells on the sides of the body, luminous tissue may be found on the head, around the eyes, on fin rays and barbels, and on the ventral surface; in the myctophoid family Paralepididae, an internal duct makes the whole fish glow. The great diversity in the type and position of light organs suggests that they must serve different functions in the groups possessing them. In the family Searsiidae (suborder Alepocephaloidei), a large sac on the shoulder emits a display resembling a shower of sparks when the fish is disturbed. Such a structure probably is a defensive mechanism. Light organs on the head may help in locating food, and those on elongated dorsal fin rays or chin barbels may lure prey. Sexual recognition and territorial behaviour are other suggested functions. Although not all marine salmoniform fishes have light organs, the latter are typically found in species that spend most of their life in the lower twilight and upper dark zones of the ocean. The effects of sunlight essentially disappear at about 700 metres (2,300 feet); the maximum abundance of luminous fishes occurs at about 800 metres (2,600 feet).

      There are some parallels in the development of eyes and light organs in fishes correlated with the depth at which the species lives. Perhaps the most sensitive of all vertebrate eyes is found in fishes inhabiting the dim twilight zone of the ocean; the eyes, specialized to function at very low light intensity, may be greatly enlarged. The retina typically consists entirely of rods with golden pigment to increase sensitivity to blue light of the light spectrum (the last part of the visual light spectrum to be filtered out in water). Another adaptation found in some marine salmoniforms for concentrating weak light is tubular eyes. Fish with tubular eyes appear to be wearing exaggerated goggles. Tubular eyes are aimed in the same direction (binocular vision) and may be directed straight ahead or directly upward. Two sets of retinas are associated with tubular eyes, one on the side of the shaft and one in the normal position at the base. The two sets of retinas function to enlarge the field of vision. A most unusual modification of the eyes is found in the myctophoid genus Ipnops (family Ipnopidae), which appears to be eyeless; however, a thin, transparent bony plate on top of the head covers a mass of retinal cells. Evidently such an eye functions to perceive faint luminescence (bioluminescence) at great depths. Larval stages of a few salmoniforms have eyes extended out from the body on stalks, which are resorbed when the eyes assume a normal position during metamorphosis.

      Some grotesque fishes are found among the predatory stomiatoids and myctophoids. The teeth may be developed into tremendously enlarged fangs, which may be likened to daggers, spears, or sabres. The gape of the jaws is sufficiently large to engulf a prey as large as the predator. Stomiatoid predators have a peculiar modification of the anterior vertebral column, which remains unossified, resulting in a flexible jointlike mechanism allowing the head to snap back and enlarge the gape. To allow the swallowing of large prey, the body is soft, distensible, and usually lacks scales; the stomach is highly elastic.

Evolution and classification

Evolutionarily important taxonomic characters

      Studies of the skeletal system (osteology) and comparative anatomy have produced most of the information used in the classification of salmoniform fishes. At present, however, the taxonomy of Salmoniformes is not well defined because no character or group of characters is exclusive to salmoniform fishes, and little consistent difference in characters occurs among the suborders.

      The fishes grouped in Salmoniformes possess a mosaic of primitive characters from which it is possible to derive most of the more advanced orders of teleostean (teleost) fishes. Both evaluation of the hypothetical evolutionary branching sequences to denote relationships and judgment concerning the primitive or derived (advanced) state of a character are based on an evolutionary principle that a structure lost or highly modified during evolution will never be re-evolved in its original condition; for example, the adipose fin, the mesocoracoid bone of the pectoral skeleton, and teeth on the maxillary bone of the jaw are considered to be primitive salmoniform characters. The absence of these characters represents an advancement; evolutionary lines that have lost these features therefore could not have been ancestral to fishes that possess one or more of these characters. No family of Salmoniformes has all of the primitive characters, but the families Salmonidae and Osmeridae have most of them.

      The primitive dentition pattern of the ancestral salmoniform would be with teeth on the premaxilla and maxilla (bones of the upper jaw) and on the dentary bone of the lower jaw, with the maxilla clearly dominant over the premaxilla in forming the gape of the upper jaw. Inside the mouth, on the upper surface, teeth would be on palatine and pterygoid bones on each side and on the median vomerine bone. On the lower surface of the mouth, teeth would cover the tongue and occur on a plate overlying the basibranchial bones (between the gill arches). Many separate lines of salmoniforms show evolutionary advancement for the loss of teeth and the dominance of the premaxilla over the maxilla, with loss of teeth on the maxilla.

      The primitive structure of the pectoral girdle, associated with the ventral position of the pectoral fin, consists of an additional supporting bone—the mesocoracoid. The advanced condition, related to a more dorsally positioned pectoral fin, is the loss of the mesocoracoid.

      The primitive salmoniform condition of the caudal skeleton has three separate vertebral centra (the centrum is the main body of the vertebra) and associated bony elements functioning in support of the bony plates (hypural plates), which form the base of the tail. Such a structure is a vestige of the upturned tail (heterocercal tail) characteristic of a more primitive stage of fish evolution. Other such vestiges found in some salmoniform fishes include abdominal pores (minute ducts from the body cavity to the exterior), remnants of a preteleostean type of intestine (spiral valve), and the absence of oviducts in females. Evolution in several salmoniform lines has reduced by fusion the three supporting caudal vertebrae to two or, more commonly, one. The primitive type of salmoniform swim bladder is connected to the esophagus by a duct. The absence of the duct or absence of the swim bladder is the advanced state. The primitive salmoniform had pyloric ceca on the intestine—a variable trait among living species. The light organs of some marine salmoniforms are an advanced character and are considered to be derived from mucous cells.

Annotated classification

      The classification presented here is based on that of P.H. Greenwood et al., with some modifications incorporated from more recent publications. These alterations consist of transferring the family Salangidae from the suborder Galaxioidei to the suborder Salmonoidei, placing the family Bathylaconidae in the suborder Alepocephaloidei (eliminating the suborder Bathylaconoidei), and the recognition of two additional families: Prototroctidae (in the suborder Galaxioidei) and Searsiidae (in the suborder Alepocephaloidei).

Order Salmoniformes

 A diverse group of fishes with a mosaic of primitive characters. Typically fusiform or elongated predatory fishes. Adipose fin usually present; dorsal fin and pelvic fins typically placed midway along body; fin rays without true spines; pectoral fin generally in ventral position. Scales, if present, typically smooth (cycloid). Light organs present in several marine families. Caudal skeleton with 1 to 3 vertebral centra functioning in support of tail. Fossils from Cretaceous.

      Suborder Salmonoidei

 About 100 species; 10–150 cm (4 to 60 in.) long: freshwater, anadromous, or marine; Northern Hemisphere. Adipose present in all species; swim bladder with open duct; maxilla dominant over premaxilla in upper jaw; no light organs; intestine with pyloric ceca (except Salangidae); tail support on 3 distinct vertebral centra in Salmonidae, fused into single element in other families. Suborder includes the families Salmonidae (including Coregonidae and Thymallidae), salmons, trouts, chars; Osmeridae, smelts; Plecoglossidae, ayu; and Salangidae, icefishes.

      Suborder Galaxioidei

 About 50 species; 7.5–40 cm (3 to 15³/₄ in.) long; freshwater, anadromous, or catadromous; Southern Hemisphere. Adipose fin absent in Galaxiidae, present in other families; swim bladder with or without duct; relationship of maxilla and premaxilla variable among genera. Light organs absent. Pyloric ceca present or absent. Tail support on 1 or 2 vertebral centra; mesocoracoid bone of pectoral girdle absent; teeth present on mesopterygoid bone in roof of mouth. Suborder contains the families Galaxiidae, no group name; Retropinnidae, New Zealand smelts; Aplochitonidae, South American trouts; and Prototroctidae, New Zealand “grayling.”

      Suborder Esocoidei

 Ten species; 5–150 cm (2 to 60 in.) long; freshwater; Northern Hemisphere. Adipose fin lacking; swim bladder with open duct; maxilla without teeth; pyloric ceca lacking; pectoral girdle without mesocoracoid bone; tail support on 3 separate vertebral centra; 2 sets of paired ethmoid bones on snout region of skull. Suborder includes the families Esocidae, pikes; and Umbridae (including Dalliidae), mudminnows (mudminnow).

      Suborder Argentinoidei

 About 50 species; 3–40 cm (about 1 to 15³/₄ in.) long; marine; worldwide. Adipose fin present on most species; swim bladder without duct or absent entirely; maxilla and premaxilla reduced, without teeth; light organs present in several species; tail support on 2 vertebral centra. Suborder includes the families Argentinidae (including Xenophthalmichthidae and Microstomatidae), argentines; Bathylagidae, deep-sea smelts; and Opisthoproctidae (including Dolichopterygidae, Macropinnidae, Winteridae), barreleyes.

      Suborder Stomiatoidei

 About 350 species; 2.5–45 cm (1 to 17³/₄ in.) long; marine; worldwide. Adipose fin present or absent, some species with both a dorsal and a ventral adipose fin; swim bladder without duct or absent entirely; maxilla the dominant bone of the upper jaw; some species with greatly enlarged, depressable teeth; anterior vertebrae sometimes unossified; light organs present in most families; members of some families with chin barbel, which may be a highly elaborate structure; tail support on single vertebral centrum. Suborder includes families Stomiatidae, scaly dragonfishes; Gonostomatidae, bristlemouths; Sternoptychidae, hatchetfishes; Astronesthidae, snaggletoothed fishes; Melanostomiatidae, scaleless dragonfishes; Chauliodontidae, viperfishes; and Idiacanthidae, black dragonfishes.

      Suborder Alepocephaloidei

 About 120 species; 3–700 cm (about 1 in. to about 23 ft); marine, deep-sea; worldwide. Adipose fin lacking; swim bladder lacking; teeth small; intestine with pyloric ceca. Light organs present in some species (on raised papillae). Tail supported by 3 vertebral centra. Suborder contains the families Alepocephalidae, smoothheads; Bathylaconidae, bony throats; Searsiidae, tubeshoulders; and Bathyprionidae.

      Suborder Myctophoidei

 About 470 species; 2.5–200 cm (1 in. to 6¹/₂ ft) long; marine; worldwide. Adipose fin usually present; swim bladder present in some species, if present, with duct. Premaxilla dominant over maxilla in upper jaw; no mesocoracoid bone in pectoral girdle. Light organs present in all species of family Myctophidae, but absent in species of most other families; tail support on single vertebral centrum. Suborder includes the following 15 families: Myctophidae, lantern fishes; Aulopodidae, thread-sail fishes; Synodontidae, lizard fishes; Harpadontidae, bombay duck; Chlorophthalmidae, green-eyes; Bathypteroidae, spider fishes; Ipnopidae, grid-eye fishes; Paralepididae, barracudinas; Omosudidae, hammerjaw; Alepisauridae, lancet fishes; Anotopteridae, javelin fish; Evermannellidae, sabre-toothed fishes; Scopelosauridae, paperbones; Neoscopelidae, blackchin; Scopelarchidae, pearleyes.

Critical appraisal

      Previous schemes of fish classification have been based mainly on the work of the British ichthyologist C.T. Regan and the Soviet ichthyologist L.S. Berg. Both Regan and Berg grouped most of the generally primitive fishes with soft fin rays and smooth scales in an order with the herring family, Clupeidae. Regan called this order Isospondyli, and Berg used the name Clupeiformes. Such a classification considered Isospondyli or Clupeiformes as the most primitive of the teleostean fishes and as ancestral to all other advanced orders of Teleostei. The work of Greenwood and his colleagues clearly demonstrated that the classifications of Regan and Berg were without evolutionary reality, that the fishes classified as Clupeiformes or Isospondyli, as formerly arranged, were not all derived from a common ancestor but consisted of several unrelated groups. The true herrings (family Clupeidae and their direct derivatives) possess some unique characters, such as the structures involved with the connection of the swim bladder to the inner ear, not found in any other teleostean fishes; the herrings thus are not very likely to have been the progenitors of all other modern teleosts. The order Salmoniformes was created to remove several diverse groups of dubious relationships from the order Clupeiformes; these groups are thus considered as the basal stocks in the evolutionary radiation of teleostean fishes. The order Iniomi of Regan (Scopeliformes of Berg) was placed as a suborder, Myctophoidei, in Salmoniformes. It should be emphasized, however, that this taxonomic revision has added little new knowledge concerning the relationships among the various suborders grouped in Salmoniformes. At present no coherent picture of evolutionary affinities among the suborders and with other orders has emerged. Undoubtedly the present interpretation of Salmoniformes will undergo major revisions in the future both in structure and in its implications regarding the evolutionary links leading to other teleostean orders. Publications by D.E. Rosen and by the British ichthyologist Colin Patterson consider new evidence and a more critical interpretation of previous data; they have separated the suborder Myctophoidei from the Salmoniformes into the order Myctophiformes and have suggested that the suborder Giganturoidei of the order Cetomimiformes should be placed in Salmoniformes. The myctophoid fishes (lantern fish) are well separated from other salmoniforms, having undergone their own evolution at least since Cretaceous times (about 100,000,000 years ago)—fossil records of four families are known from Cretaceous deposits—and recognition of the order Myctophiformes seems justified.

      Hopefully, new evidence will be forthcoming from future studies providing new insights into the evolutionary events that transpired from 50,000,000 to 100,000,000 years ago and resulted in the evolution of the various families and suborders of Salmoniformes. From such evidence, a better understanding of the ancient divergences leading to the bulk of the present teleostean fishes should follow. Ichthyologists may have exploited anatomical characters to the limit of potential information yield, but it is to be expected that new fossil finds of extinct, intermediate groups will yield valuable information.

      New techniques for examining chromosomes and comparing their number, size, shape, and content and for comparing the structure of certain evolutionally stable protein molecules are promising approaches for the interpretation of evolution.

Robert John Behnke

Additional Reading

J.W. Jones, The Salmon (1959); W.E. Frost and M.E. Brown, The Trout (1967), two works with general information on Salmoniformes; J.E. Fitch and R.J. Lavenberg, Deep-Water Teleostean Fishes of California (1968), a book designed for the interested layman, covering many deep-sea Salmoniformes; P.H. Greenwood et al., “Phyletic Studies of Teleostean Fishes with a Provisional Classification of Living Forms,” Bull. Am. Mus. Nat. Hist., 131: 339–455 (1966), created the order Salmoniformes; S.H. Weitzman, “The Origin of the Stomiatoid Fishes with Comments on the Classification of Salmoniform Fishes,” Copeia, pp. 507–540 (1967), created the new suborder Osmeroidei and modified the classification of Greenwood et al. (above); R.M. McDowall, “Relationships of Galaxioid Fishes with A Further Discussion of Salmoniform Classification,” Copeia, pp. 796–824 (1969), suggested further modifications in the classification of Salmoniformes; D.E. Rosen and C. Patterson, “The Structure and Relationships of the Paracanthopterygian Fishes,” Bull. Am. Mus. Nat. Hist., 141:357–474 (1969), a revision of Salmoniformes with new information on early teleostean evolution; C. Patterson, “Two Upper Cretaceous Salmoniform Fishes from the Lebanon,” Bull. Br. Mus. Nat. Hist., Geol., 19:207–296 (1970), provides new information and suggested relationships of primitive salmoniforms; W.A. Gosline, “The Morphology and Systematic Position of the Alepocephaloid Fishes,” Bull. Br. Mus. Nat. Hist., Zool., 18:183–218 (1969), a review of the suborder Alepocephaloidei; J.G. Nielsen and V. Larsen, “Synopsis of the Bathylaconidae (Pisces, Isospondyli) with a New Eastern Pacific Species,” Galathea Rep., 9:221–238 (1968), revises the suborder Bathylaconoidei, family Bathylaconidae in the suborder Alepocephaloidei; N.B. Marshall, “Bathyorion danae, a New Genus and Species of Alepocephaliform Fishes,” Dana Rep., 68:1–10 (1966), a technical paper on the suborder Alepocephaloidei; G.J. Nelson, “Gill Arches of Some Teleostean Fishes of the Families Salangidae and Argentinidae,” Jap. J. Ichthyol., 17:61–66 (1970), another technical article revising the order Salmoniformes; R.J. Behnke, “A New Subgenus and Species of Trout, Salmo (Platysalmo) platycephalus, from Subcentral Turkey, with Comments on the Classification of the Subfamily Salmoninae,” Mitt. Hamb. Zool. Mus. Inst., 66:1–15 (1968), classification of trouts and salmons, and “The Application of Cytogenic and Biochemical Systematics to Phylogenetic Problems in the Family Salmonidae,” Trans. Am. Fish Soc., 99:237–248 (1970), classification of whitefishes, subfamily Coregoninae; Stephen D. Sedgwick, The Salmon Handbook: The Life and Cultivation of Fishes of the Salmon Family (1982); Gary A. Borger, Naturals: A Guide to Food Organisms of the Trout (1980).

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