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A Critical Examination of the Evidence for Physical and Chemical Influences on Fish Migration

1924; The Company of Biologists; Volume: 2; Issue: 1 Linguagem: Inglês

10.1242/jeb.2.1.79

1477-9145

F. E. Chidester,

Fish Ecology and Management Studies

It was because of a series of records prepared in connection with a study of the salt-water minnows that so successfully cope with the salt-marsh mosquitoes of the north (Chidester,. 1916) that the writer was invited in 1919 by the U.S. Commissioner of Fisheries, Dr H. M. Smith, to engage in an attempt at the physics and chemistry of the migrations of fish.The subject is one that several experienced zoologists have refused to follow for any length of time, as it is difficult of field observation, and certainly not one to be solved by laboratory experiments.After several summers of spare time spent in experimental work, amplified by field observations, it has been deemed advisable to survey the literature, and this paper will, it is hoped, aid in crystallising our knowledge of the migrations of anadromous fishes.To a zoologist who is looking for a problem that will eventually have a solution, it is most disconcerting to discover that there is much evidence that fish like the salmon are able to return in an apparently inexplicable manner to the streams where they were bred.We are deeply indebted to Dr C. H. Gilbert of Stanford University for most careful work on fish scales that has shown that salmon return to the river of their nativity for spawning, and that they are even able to locate in that river the spot where they were once fingerlings.Jordan mentions certain observations of Dr Gilbert on the Chinook salmon and Red salmon of the streams near Walla Walla, Washington. Dr Gilbert found that at a point where the salmon have a choice of two streams that come together under a bridge, the Chinooks (king salmon) go up either one of the streams indiscriminately, but the Red salmon (bluebacks) turn always to the stream with a lake.In a recent paper Dr E. E. Prince, Dominion Commissioner of Fisheries, Ottawa, Canada, states (1916) that his previous report—published in 1896 and repeated in 1912—to the effect that "each river has its own race of salmon," is borne out by more recent observations. A dark-fleshed race of Sockeye salmon inhabit a small creek near the Skeena River, and the salmon canners rarely net them as the meat is of a "dark, repulsive colour," although the distance is not great from the waters that furnish the attractive pink salmon of the regular catch.Dr David Starr Jordan is inclined to question whether migration up the parent streams may not be due to the fact that the young fish do not travel far from the mouths of the rivers that gave them birth, and consequently they find the parent waters pouring into the ocean and quite naturally return to them. Jordan also believes that the salmon are not unfailingly true to their native rivers.Jordan has pointed out the fact that salmon do not apparently care about the quality of the water, and that while the Chilcoot River comes from a glacier and the water is milk white with glacial debris, the fish migrate into it. Jordan (1920) also cites a case of apparent attractiveness of lake water.The first lake on the Yukon River, Lake Labarge, is 1800 miles from the mouth of the river. At Boca de Quadra, also a noted salmon stream, is a little stream about ten feet wide and less than a mile long, the outlet of a lake. At the head of the lake it is fed by clear springs. The fish go up the small stream just as they go up the Yukon, although they have only about five miles to go. Their start is accordingly a late one. Jordan does not explain this condition.Further interest in lake-fed streams is aroused when we cite the case (mentioned by Jordan) of observations by J. P. Babcock of the British Columbia Fish Commission (Jordan, 1919). Babcock observed that in the case of water piped from a lake-fed stream across to another stream, the Red salmon gathered around the mouth of the pipe which contained the lake water.The writer cannot refrain from remarking at this juncture that a fish responds to currents of water, and that it is quite likely that the Red salmon would have gathered around almost any non-poisonous fluid of the optimum temperature, providing it came with a little force through a tube.Our knowledge of salmon behaviour has been clearly stated by Dr C. H. Gilbert in a personal letter, in which he answers several questions asked by the writer, and with his permission the answers will be quoted."Dear Sir,—I have no knowledge concerning possible factors governing migrations of fishes, and am thus unable to prepare any discussion of the subject that you may care to use. As regards migration of the salmon, however, there are certain unquestioned facts that must be taken adequately into account by any theory which claims to explain their movements."1. Salmon which are schooling together in the sea on feeding grounds far removed from their final spawning districts, will at the proper time separate and go their own way rather directly to the mouth of the distant stream from which they originated. At the time they separate, it would seem they must assuredly be exposed to identical environmental conditions."2. Salmon ascending a river together will react differently on approaching a given tributary, though again it would seem they must be exposed to the same conditions. There is a fair body of evidence to show that in the main they will re-enter the tributary in which they were hatched."3. In both the above instances, we seem wholly at a loss to suggest any purely external factors which condition and guide the migration, and yet lead to such diverse results when applied to fish of different early history."4. The 'parent-stream theory,' in so far as it has validity, is not a theory in any sense of the term, but a bald statement of fact. The salmon either do, or they do not, return in the main to their parent stream at maturity. We hold that they do, but we are far from claiming that this phrase, which is merely descriptive of their conduct, affords any explanation of it. When the quest is for the causative factors of migration, the 'parent-stream theory' is a confession of ignorance pure and simple. But it seems far more whole some and more hopeful of future results to confess ignorance where ignorance undoubtedly exists, than to set up spurious claims to achievement as is all too frequently done in this field. —Very truly yours,C. H. GILBERT."Such clean cut statements as these backed by the observations of Dr Gilbert and his associates, Mr Henry O'Malley and Mr W. H. Rich (1919), who tagged adult Sockeye salmon and studied their migration, would seem to indicate that we have a long way to go in explaining the factors that influence migration.It may be that we shall have to come to the idea of emanations from the mother, transmitted to the offspring, which serve to guide the fish of a particular race back to their parent stream.It may not be out of place at this juncture to mention the statement of J. O. Snyder, who reported on the return of king salmon (1922).In 1919, 2500 king salmon were marked by removing the adipose and the right ventral fins. They were expected to return to the Klamath River in 1921, on the basis of previous scale data. At that time twenty-three were recaptured. The age calculated from the scales was identical with the known age. The interpretation given is that the fish remained in the river during the first year, and most of them must have been in contact with the same environmental conditions of the sea during the second year. Snyder concludes that associations of individuals formed in youth may continue throughout life.The remaining discussion will instance experiments and observations that show some advance in our knowledge of the determining factors that may in some way influence the migrations of fish.The anadromous fishes migrate past all sorts of obstacles and over bottoms of various types in order to reach favourable spawning grounds.It is the belief of Gurley (1902) that the selection of spawning grounds is by no means a question of chance, but has been determined by the egg type "via natural selection." Gurley mentions the fact that spawning grounds of fishes are mainly of three kinds : mud, weeds and sand, gravel and rock, and that the habits of the fishes in deposition and the physical condition of the eggs have determined the survival of the fishes. One is immediately led to inquire whether the migratory fish do not occasionally become dispersed to new favourable localities for spawning and thereafter establish a race for that particular stream. We must have further observations and records to fully substantiate this statement so frequently given as a fact.Prince has stated (1920) that the eggs and young of but few fishes are found on the sea bottom, and that the majority of marine fishes deposit floating eggs or else spawn inshore. He cites the work of Professor M'lntosh of St Andrews, Scotland, who proved that the eggs of the salmon will not develop in salt water, but become rubbery in consistency.The migration of fishes seems to be unaffected by the character of the bottom, but their spawning places are quite certainly regulated by such factors. Observations of polluted streams prove, however, that fish will spawn in places that were formerly clean but have become so polluted that the eggs are not able to develop.There is no question that the factor of stream pressure is extremely important in connection with the migrations of fish.Chamberlain (1907) writes of the tendency in dry seasons of salmon to tarry inshore in bays and the mouths of small streams, and only to proceed up to their spawning grounds when the floods have come rushing down.Prince (1920) mentions the importance of a down-floating stream, but emphasises the necessity for shallow, clean, gravelly rapids in the case of the salmon, and gives weight to the added fact that the cold waters of the salmon rivers are usually well aerated, since coldness increases the power of the water to absorb gases. Further mention will be made of both of these points.The significant experiments of E. P. Lyon (1904, 1909) performed with the killifish, Fundulus heteroclitus, Linn., the scup, Stenotomus chrysops, Linn., the stickleback, Gasterosteus bispinosus, Walb., and the butterfish, Poronotus tricanthus, Peck., indicate clearly that fish respond to stream pressure through the optic and tactile senses.By an ingenious series of devices, Lyon proved that the fish Fundulus responds to relative motion rather than to a current; that the moving "optical field" is the stimulus, and that in the complete absence of pressure the fish will respond to movement outside glass containers. He concluded that the current only stimulates by moving the fish away from their environment.Blinded fish on the bottom of a long box with open ends (screened with coarse netting) oriented themselves in the sand. Other fish that were blinded and placed in the tideway leading from the eel-pond at Woods Hole, Mass., were quite irregular in their motion until they touched the bottom and then they headed upstream. Even contact with a bit of eel-grass was enough to give them orientation.The general cutaneous nerves were the ones involved.Dr Caswell Grave has emphasised to the writer the supposition that variation in turbidity of the water may therefore be a most important difference in the orientation of the fish to streams, and that debris in the water at the time of floods will serve to accentuate tactile stimuli.Lyon showed that in the case of concentrated streams such as those from a small bore tube or flume, there is sufficient difference in the velocity of the water at the centre and the outside of the stream to furnish the requisite stimuli. In his experiments with fish blinded in one eye, Lyon proved (1909) that they react to currents like the normal fish.The writer found in 1919 and 1920 (Chidester, 1922) that by increasing the stream pressure of fresh water or of toxic substances in solution and presenting them in a trough that was almost parallel to its twin with sea water flowing into a long receiving trough, it was possible to lure killifish (Fundulus heteroclitus, Linn.) into the unfavourable stream. It is quite possible that the idea of intoxication by chemicals, suggested by Shelford, is not always tenable, and that occasionally the fish in his experimental tank moved towards the toxic substances because they were attracted by the force of the entering stream. His control and experimental streams were situated at opposite ends of the tank, with the outlet at the middle.It must of course be recognised that the factors of temperature and oxygen content of the water are significant, but we must also appreciate the fact that just as birds respond to air currents, fish not primarily confined to the bottom respond most definitely to the force of moving water.As pointed out so aptly by Lyon (1904) the fish in rushing torrents orient because of the difference in velocity of the adjacent parts of the stream. In the wider and deeper streams, sight or contact with the bottom or with floating particles in the water furnish the requisite nerve-stimuli.Rutter (1902) has shown that the Chinook salmon run into the rivers against ebb tide, and then, when the tide turns, run out against flood tide. The flood tide is not continuous for so long a time as the ebb tide, and so the fish keep ascending until the tidal movement is replaced by the river current.Nothing could be more striking or more worthy of application to lessons on human behaviour than the fact that weakened and spent salmon go down to the sea tail first, feebly fighting the current.Fish vary considerably in their movements according to light or to darkness. Salmon move both by night and by day. Atkins (1874) mentions the fact that the Atlantic coast salmon spawned at night or on a dark cloudy day. Alewives rest in small pools at night and travel by daylight. Herrings apparently require clear water and a clear sky for their migratory movements.Shad are said to be timid and easily frightened by shadows. M'Donald cites the case (1884) of the shad, and indicates that floods and muddy water arrest their movements.Allen, in discussing the migration of mackerel (Mackerel and Sunshine, Allen, 1909), has pointed out that sunshine produces more of the plant food of Copepoda, such as diatoms and Peridinidæ, and that an abundance of Copepoda offers rich food for the mackerel. He attempted, therefore, to "correlate the average quantity of mackerel per fishing boat taken in May with the total number of hours of sunshine recorded during the first quarter of the year." The effort was unsuccessful, however, and he states that "whilst the 1905 temperature maximum agrees with the maximum total catch of mackerel the temperature of 1903 is accompanied by low catches of mackerel." Fishermen of the Atlantic coast find that they are more successful in catching mackerel on dark days, and according to Mr Ernest Romling of the U.S. Bureau of Fisheries, they believe that this is due to the fact that their scattered bait (chum) is present in the absence of the living Crustacea that appear near the surface on bright days.Reeves has concluded (1919) that the longer wave lengths of light have a physiological or psychological effect upon sunfish (Eupomotis gibbosus, Linn.) and horned-dace (Semotilus atromaculatus, Mitchill) that differs considerably from light of shorter wave length and from white light.The fish in her experiments were trained to respond to food stimulus with the accompaniment of blue light. Then it was tried with red light of brightness approximating that of the blue for the human dark adapted eye. The fish responded about as often to red as to blue at first and then became discriminating and red had to be reduced in intensity.Parker and Larchner studied the responses of Fundulus to white, black, and darkness (1922). They prepared three boxes, one lined with dull white paper and exposed to the light from a 100 watt lamp: the second lined with black paper and similarly exposed to the 100 watt light: and a third, absolutely light-proof. Funduli placed in the light one remained light in colour ; those placed in the dark one remained dark in colour ; but the ones in the light-proof box remained light until removed and then became dark for five minutes, later becoming light again. Temporarily blinded fish also remained light coloured. These experiments, while of no special interest in connection with the problem of fish migration, serve to emphasise the optical factor in behaviour, and to corroborate the work of Sumner and of Mast along the same line.The writer has shown (Chidester, 1923) that Fundulus heteroclitus, Linn., when given a choice of temperature and light combinations, is influenced somewhat by the attractiveness of intense light, and may be attracted towards water that is several degrees warmer than that which is its optimum at that time, without the added factor of light.We must conclude that fish vary in their responses to light so much that it can be stated that some are primarily influenced in their reaction to currents by their optical sense, while others are primarily responsive to turbidity and to powerful stream pressure increased by floating debris.By far the most evidence has been gathered to support the theory that temperature is the primary influence in fish migration.Gurley (1902) has prepared a highly instructive paper discussing the relations between temperature and the other factors in fish migration. He holds that there is probably a temperature-responsive nerve-mechanism. This mechanism would explain why spawning in cooling water is associated with migration from warmer to cooler water.Gurley points out that the time of spawning has been determined by natural selection, and that natural selection has therefore determined the time of migration.To his statement that spring spawning does not necessarily mean spawning in warmer water, the writer most heartily subscribes. In connection with observations on the killifishes of New Jersey (Chidester, 1920), it was observed that the early spring migrants to the marshes came in April when the waters inshore were cooler than they were at the time in the Raritan Bay.Jordan says (Science Sketches, 1888, pp. 51-52) that Blue-back salmon and Humpback salmon ascend only snow-fed streams with sufficient volume to send their waters well out to sea. Gurley adds to this the statement that spring freshets mean heavy spring runs and lighter fall runs. Gurley believes most salmonids to be spawners in cooler water. He states that migration to cooler water favours the development of the gonads. Gurley has also pointed out that the fish probably starts to migrate as the result of a temperature stimulus, then continues in response to the pressure stimulus from currents, and that it runs upstream until the gonads have ripened their products and spawning takes place.Natural selection is the factor that determines the survival of eggs spawned in water of a certain character.Chamberlain claims (1907) that fish leavę cooler water for warmer. He also points out that streams with lakes have a higher temperature in the summer than streams of similar volume without lakes. Certainly in the case of some fish such as the menhaden it would seem that they prefer warmer waters offshore in the summer. They are attracted by water above 10° C., and may even migrate inland until the water reaches a temperature of 23° C. (Goode, 1879).Stevenson (U.S. Fisheries Report, 1898) quotes M'Donald as stating that "warm rains produce vast schools of shad." Floods and muddy water arrest their movements, however.Mr R. A. Goffin and Mr W. L. Howes of the Woods Hole Laboratory of the Bureau of Fisheries record the fact that alewives come into Oyster Pond soon after the ice leaves in the spring when the temperature is not more than 5° C. The swift currents flowing out of the pond cause the fish to rush in great shoals and almost fill the stream. They are travelling from warmer to cooler water.Shelford and Powers showed (1915) that herring are sensitive to temperature differences as small as 0. 2° C.Galtsoff (1923) in a paper on the migration of mackerel in the Black Sea shows that as the temperature decreases the fish press inshore. They are caught in horizontal nets close to the shore. Apparently the fish are not affected by absolute temperature but by the relative temperatures. The same phenomenon occurs when the temperature drops from 24° C. to 21° C. as happens in the drop from 17° C. to 10° C., as observed near Sebastopol. Galtsoff holds that the difference in salinity is not significant, as the same phenomenon occurs in regions of the Black Sea with quite different content of salts.Johnstone (1908) concludes that it is difficult to separate the influences of salinity and temperature, but there is no doubt that temperature is a factor in itself.He believes that there is sufficient evidence to conclude that seasonal migrations of fish are related to seasonal changes in temperature, and cites the work of D'Arcy Thompson, who has correlated the volume of catches made by Aberdeen trawlers with the temperature of the sea on the fishing grounds.Ward (1920) discusses the migration of the Sockeye salmon and finds that the volume and the swiftness of the streams are not apparently determining factors in the selection of one tributary to a stream in preference to another. He further shows that great difference in turbidity is ineffective, and that there is no difference in the apparent chemical character of the waters. The food supply is apparently uniformly poor.Temperature is the factor that he believes of paramount importance, and he subscribes to the theory that the salmon prefers steadily flowing cool water for spawning.Whatever influences may be important for migration besides temperature, the writer holds that we must acknowledge the fact that it bears a most important relation to chemical processes, and thus involves not only the environment of the fish but the metabolism of the body of the animal itself. Even if we decide that the fish has some mysterious sense that man cannot discover, it is quite evident that the temperature of the water will have a pronounced effect on the utilisation of that sense.Fish vary considerably in their habits as respects feeding when they migrate inshore.Young immature fish continually travel from the deep waters of the ocean to the shallower waters of the coast and up into the marshes in search of food. Although several species may be in the same shoal, in general it is found that those travelling together far into the inland streams during the period prior to maturity are of the same species. In the ocean the young of several species will be found together.At the same time that immature minnows come to feed on the teeming insect life of the salt marshes (Chidester, 1916, 1920), one notes that older fish of the same species are migrating inshore primarily for the purpose of spawning.During the period of travel from the deeper waters, there is usually little feeding done by the mature animals that are to spawn in brackish or fresh water. In no fishes is this characteristic more striking than in the salmon.Gurley (1902) believes, and it would seem rightly so, that abstinence from food in fishes is in direct ratio to the length of time required as a minimum and the amount of time available as a maximum, for the species to reach their spawning grounds.Prince holds (1920) that the salmon has never changed its habits but "repairs to the ancestral breeding localities, regardless of the geological and topographical changes wrought in the course of long centuries." He states that the surroundings of the spawning beds have been changed and the former salinity has been changed to freshwater conditions ; but the connecting channels still remain, and the salmon persists in its habit of going to the old spawning locality.Whether we accept this as the explanation of the habits of the salmon or not, we must acknowledge that the fish travels for 2000 miles up the rivers of the Pacific Coast to spawn, and that it fasts during the period after it leaves the ocean for fresh water.Greene (1914) is responsible for a most careful study of the storage of fat in muscular tissue of the salmon. He found that the salmon do not feed in fresh water, no matter how far they travel into it to spawn. The stored fat is apparently the only source of the fats to build up the ovaries, and it also must furnish the energy for muscular activity during the long pilgrimage to suitable spawning grounds.It is stated by other competent observers, however, that certain salmon will seize bait while migrating up the Columbia River.The explanation of the fact that a salmon will seize bait when migrating is probably that while the animal is too strongly impelled towards its spawning grounds to stop for feeding en route, it is quite responsive to the optical stimulus of something that is apparently edible.In the case of fish that spawn inshore, such as the cod, it is stated by Mr R. Hamblin of the U.S. Fisheries Laboratory at Woods Hole, Mass., that although the manuals of fish-culture indicate that they do not eat during the spawning season, both the females and the males will eagerly seize food placed in their detention pools.It is probably safe to conclude that fish that spawn inshore in salt water or brackish water will feed until just before they are to spawn, while those that travel far inland press onward, responding by optical and tactile senses to current stimuli, until their eggs have matured and they must spawn. The distance which any particular race of fish travels before spawning is in all likelihood determined by natural selection, together with the factor of time required for the development of the gonads.It has been shown that the anadromous fishes have blood that is more saline in sea water than it is in fresh water. It has also been found that changing the medium for marine fishes to a less saline one will induce change in their blood. The internal equilibrium of the animal has been preserved by the presence of membranes that are practically impermeable to salts, though permeable to water.Mather (1881) has listed thirty-three species of fishes that can live in both fresh and salt water. Slow acclimatisation permits these animals to range between the two media with impunity.There is great variation in the adaptability of fishes to salt or fresh water, and this adaptability is probably due to an inherited resistance.Sumner (1905, 1906) has studied the effects of changing certain brackish and freshwater fishes to pure fresh water and to water of different degrees of salinity. He mentions changing the young of the Chinook salmon (Onchorhynchus tsawylscha) which weighed from 8 to 30 gms., and which had been reared in fresh water, abruptly to water of a density of 1.013 without any harm, and suggests that a higher salinity would not have injured them.Rutter (1904) found that if the young of Pacific Coast salmon were transferred alternately from sea water of low to high dilution, it was possible gradually to raise the salinity. This reminds us of the gradual change for the fish that must result when it travels with the ebb and flow of the tide before it finally begins the long journey in fresh water. Rutter found that young quinnat salmon were able to live in higher salinities as they grew older, and from 25 per cent, sea water at six days of age they were able at two months to live in almost pure sea water.The age of Fundulus heteroclus embryos was found by Loeb (1894) to be definitely correlated with their ability to survive the addition of different proportions of NaCl to sea water.Bert (1871, 1873, 1883) found that he could gradually acclimatise freshwater fishes to live in water of one-half the salinity of the sea, and that they would survive abrupt transfer to diluted sea water if the proportions were two parts distilled water to one part of sea water. He explained the death of freshwater fishes in salt water by osmotic action on the gills, producing contraction of the capillaries and thus asphyxiation. With scaleless fishes, osmotic action took place over the entire surface of the body.Fredericq (1885) indicated that the gills, while permeable to gases, are almost impermeable to salts of the sea.Bert (1883) mentioned the fact that if mucus was removed from skins of freshwater eels, they were quite susceptible to salt water.Garrey (1905) experimented with Fundulus heteroclitus,, denuding about one-half the body surface of scales from a large number of them. When placed in fresh water, normal sea water, and a mixture of distilled water with an equal quantity of sea water, it was found that the fish survived in the sea water of one-half its normal concentration, but died in the other solutions. Garrey concluded that if the internal and the external media are approximately isotonic, no ill effects result. He holds that injury to the integument furnishes an opportunity for fatal osmotic action.Sumner (1906) was not able to confirm Garrey's work.Trout and other freshwater fishes must be handled with great care when stripped of their spawn.There must be considerable variation in the susceptibility of fishes to injuries, as many salmon arrive at their spawning grounds with bodies "torn by rough stones, gashed by jutting rocks, maimed by jagged and precipitous obstacles, or by falling, time after time, down almost impassable falls" (Prince, 1920).Ringer (1883), working with minnows and goldfish, tried the salts of sodium, potassium, and calcium to discover which were capable of sustaining life longer and found that CaCO2 would sustain life longer than a corresponding quantity of sodium or potassium salts. Combinations of KCl1 Na2CO3, and CaC12 aided materially in supporting life. When fish were placed in solutions in which many fish had previously died, the new lot live