Exp. Geront. Vol. 13, pp. 125-140.

0531-5565178/0801-0125502.0010

© Pergamon Press Ltd. 1978. Printed in Great Britain.

FISH IN STUDIES OF AGING* A. D. WOODHEAD Brookhaven National Laboratory,Department of Biology,Upton, New York, U.S.A.

(Received 26 August 1977) INTRODUCTION ALTHOUGH Shock (1977) listed 51,893 references related to aging from January 1949 to May 1977, these included few comparative studies other than those made with the laboratory rat, mouse and Drosophila. Indeed, Comfort (1957) has pointed out that "biologists have been surprisingly incurious about the fate which finally overtakes the animals they investigate". There is urgent need both for further comparative studies and for a larger repertoire of documented, short-lived experimental vertebrates. There would seem to be a good rationale for using fish in experimental studies of growth and senescence. The physiological characteristics of mammals impose limits which considerably reduce the spectrum of conditions under which they can be examined. Mammals tend to have few young at each birth, and to obtain adequate data, the young from many births must be used. This leads to fairly high genetic and physiological variability in the experimental stock. For the same reason, sampling throughout the lifespan is restricted, or must encounter increasing variability with larger heterogenous samples. The period of growth is restricted to the earlier part of the lifespan of mammals and final size is closely determined genetically, as is the size at sexual maturity--indeed, the growth pattern of many mammalian species is almost immutable, thus restricting the opportunities for comparison of the interrelations of growth and the aging process. Mammals are warm-blooded and control of homeostasis of their milieu interieur is precise, insulating tkem from changes in their laboratory environment. Finally, most mammals are long lived. These problems apply even more to studies on human subjects. There have been few studies which have set out specifically to investigate the aging process throughout the lifespan of any fish. Comfort's actuarial studies of mortality in populations of guppies, Lebistes reticulatus, are amongst the few exhaustive investigations which have been made, (Comfort, 1960, 1961 a, b). There is, however, a considerable volume of relevant information in papers which have been concerned principally with the growth dynamics of populations of commercially important species. Beverton (1963) has made the point that the response of a population of fish to fishing depends upon three biological characteristics; growth, natural mortality and the size at which the fish enter the fishery. In many cases, the size at which the fish first become exploited is the same as that at which first maturation is reached. This information provides a valuable and detailed background against which to compare experimental studies of growth and aging. In this article, I shall attempt to assemble some of the information obtained from studies of wild fish, which illustrates the flexibility of growth and reproductive responses to environmental changes. Particular emphasis will be given to the effects of food availability and * Research carried out under the auspices of Administration. Contract YOL-CP-50202.

the United States

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space restriction, since these factors have been manipulated in laboratory studies (Comfort, 1960) and might be profitably used again. FISH AS EXPERIMENTAL

ANIMALS

Because of their plasticity in growth and reproductive capacity, fish provide unique opportunities for a wide range of experimental manipulation. Their internal environment varies with the temperature of the external environment and they are sensitive to many other environmental changes. Many fish continue to grow throughout their lives and are able to change their growth rate in relation to changes in their ecological opportunities, particularly changes in feeding, space and temperature. The final size attained by the fish and its longevity also vary with growth rate. Reproductive processes show equal flexibility and vary with growth. The combinations of these growth and aging parameters allow collection of a wide range of data for analysis of their complex interrelationships-which is not the case with mammals. Fish commonly produce large numbers of eggs at any spawning so that an experiment can be made on a single brood, which can be adequately sampled throughout the lifespan. Many teleosts are conveniently short lived, yet there are species which have a well defined postreproductive phase. Finally, the practical and economic considerations of rearing and keeping large numbers of fish throughout their lives are far fewer than those encountered with mammals. Numerous long term field studies of growth have been made by fisheries scientists on particular stocks of commercially important fishes living in fairly restricted geographical areas. For example, in the North Sea, growth data for herring, Clupea harengus, has been collected and analysed for each separate year of growth, from the first to the sixth year of the fish’s life, over a period of thirty years (Iles, 1971b). Similar extensive information is available for many marine and freshwater species throughout the northern temperate and boreal regions. There is no such wealth of data for any other vertebrate class of species living in the wild. An important feature of this field work is that data on the age, the spawning history, and sometimes, the place of origin can be obtained for individual fish. In contrast, for mammals living in the wild, it may be difficult to evaluate the age of an individual, particularly after the animal has attained maturity and has reached its final body size. Seasonal variations in the growth of fish have long been recognized as causing the development of markings upon their bony structures and scales. Because of the annual periodicity of these visible markings, they have been used extensively for the determination of age in fish. Growth rings on scales were employed by Reibisch as early as 1899, and by Lea in 1910 to assess the age of plaice, Pleuronectes platessa, and herring, Clupea harengus, respectively. For some species, the width of the annual growth zone on the scales and otoliths (earstones) has been shown to be approximately proportional to the growth in length of the fish. It is therefore possible, by back-calculation, to estimate the length of the individual fish at earlier stages of its life history (Hickling, 1931; Trout, 1957; Mina, 1967). The scales of the herring, &pea harengus, are well suited for back-calculation of growth (Glenn, 1975), and Iles (1971b) has analyzed scale data for East Anglian stocks of herring in the North Sea to cover growth over a period of nearly 30 years, from 1939 to 1967. After the attainment of sexual maturity, the nature of the markings changes, and spawning (or breeding) rings have been described (Nordeng, 1961). Spawning rings are

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most clearly seen in fish from temperate seas, which spawn annually (Fig. 1). Other characteristics of the markings, such as the appearance and size of the central nucleus have been used to identify particular populations of fish, or sub-groups within a population. Rollefsen (1934) found that the otoliths of the cod, Gadus morhua, from northern Norwegian waters had distinctive markings and Trout (1957) was able to trace the movements in the Barents Sea of cod from different regions. Recently markings of daily growth have been described for otoliths and there is also evidence suggesting two-weekly and monthly cycles occuring within the annual patterns (Panella, 1971). Plainly, much important information about the the details of a fish's life is recorded upon its bony structures. The most commonly used structures for determining the age of fish are the external scales and the otoliths of the inner ear, and thousands are "read" each year by fisheries biologists. Nevertheless, it is not a wholly precise technique, being more of an art than a science, which entails empirical interpretations, even in experienced hands. Graham (1929), Mina (1968), Lamont (1967) and Reay (1972) have discussed the validity and problems of the otolith method for age determination. Blacker (1974) has reviewed new techniques for otolith preparation, so that aging methods can be compared. Direct measurement of the growth rate of fish, obtained by repeated weighings of the same individual at short intervals throughout its lifespan, is the best method for obtaining complete and accurate growth information. This method is restricted to captive populations and data are available for only a very limited number of species. The nearest approach to individual growth measurements of fish in the wild has been obtained from marking experiments, which now number many thousands. Fish are measured on initial capture, released and measured again on recapture, so giving a value for growth during a known time period. This information has been supplemented by length measurements taken from large numbers of individual fish, the successive and frequent sampling of the population allowing an evaluation of its average growth history. GROWTH AND MORTALITY IN FISH One early theory of aging, which has long persisted in the literature, is that senescence is a consequence of growth cessation. The idea that cessation of growth represents a causative factor in the aging of animals appears, at first sight, to fit mammalian systems well. Mammals have a clearly defined lifespan, growing to attain an adult size characteristic of the species, after which growth ceases or declines dramatically and debilities associated with aging begin to appear. Most fish and some reptiles do not fit this pattern. They continue to grow throughout life and do not show a sharp fall in growth rate, nor do they show obvious signs of aging until close to death. Bidder (1932), one of the strongest proponents of this idea, believed that determinate size and aging arose in mammals as a result of their evolution on land and that indeterminate size represented the earlier condition in vertebrates. Fish, with continued growth throughout life and indeterminate size would not therefore exhibit aging, and were potentially immortal. Bidder based his arguments upon his studies with the female plaice, Pleuronectes platessa, which shows continuous slow growth over a long period and no apparent senescence (Fig. 2). Bidder's hypothesis was clearly disproven by Comfort and his associates (Comfort, 1960) who made laboratory studies with populations of guppies, Lebistes retieulatus, to find out whether the mortality rate increased with increasing age. At that time there were few field data on fish mortality available, and no captive population of fish, reptile or amphibian had

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FIG. 2. Some examples of the growth rate of fish (from Beverton and Holt, 1959). been kept under observation for long enough to determine the form of the age-mortality curve. These studies remain the most detailed to have been made. The findings were clear-under all experimental conditions the rate of mortality rose with age. As the environment in which the fish were kept was improved (by better diet or more space), the survival curves progressively changed to approach a rectangular configuration, i.e. more individuals in the population lived for a longer time, but the maximum lifespan for the species was not altered. This work clearly established that fish, like warm-blooded vertebrates, show increasing mortality with age. At the same time they may continue growing, although the growth rate may be slight during the latter phases of the lifespan. Walford and Lui (1964) have given survival curves for populations of the annual fish, Cynolebias adloffi. In this species, there was almost 100% survival of the females until the age of 10 months; thereafter mortality increased, and all of the females were dead by 14 months. The mortality of male fish increased from 6 to 9 months and by 13 months there were no survivors. Accompanying the rise in mortality rate, the fish sho~ed evidence of senility changes including gradual curvature of the spine, clouding of the cornea, exophthalmos and "generally ragged appearance".

Field studies of growth and mortality Examples of the spectrum of growth patterns shown by some common species of fish are given in Fig. 2. Species such as the sturgeon, Acipenser nudiventris, and the female plaice, Pleuronectes platessa, continue to grow throughout life. Indeed, a comparison of their

F~c. I. The otolith of a cod, Gadus morhua from the Barents Sea, showing annual growth rings, denoted by an 'x', and spawning zones, indicated by ' ' Photograph was taken by R. W. Blacker, Fisheries Laboratory, Lowestofl, U.K.

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growth curves with those of many mammals might suggest that there is a fundamental difference between poikilotherms and homiotherms--as Bidder (1932) believed. But this distinction was over emphasized. Very many fish, for example the herring, Clupea harengus, have a limiting size rather than showing unlimited growth, although growth to the limiting size is usually more protracted than the growth of mammals to their specific size. In other species, such as the males of many small tropicals including the guppy, the growth pattern is nearer to the mammalian type, i.e. rapid growth to a specific size, after which growth almost completely ceases. There are relatively few instances in which direct estimates are available of the natural mortality of fish from wild populations, since most stocks are subject to commercial fisheries and differences in natural mortality with age are small compared with mortality due to fishing. Values have been obtained from data collected at times when fishing was suspended, as during wartime, when sampling of the population was begun before fishing started, or when fishing activity was low. These data show that mortality increases throughout the lifespan, although there are considerable differences in the form of the survival curves between species. In some fish, the survival rate is almost linear over the whole of the observed range. For example, in many long-lived fish, such as the sturgeon, Acipenser nudiventris, the perch, Percafluviatilis, the white fish, Coregonus clupeaformis and the female plaice, Pleuronectes platessa, mortality seems to be almost constant at about 5-10~ per year over a considerable span of the life history (Probst ar.d Cooper, 1954; Alto, 1951; LeCren, 1958). For sturgeon older than 30 years, however, the mortality rate increase rapidly. At the other extreme, some fish show a sharp rise in mortality rate at the onset of maturity. This reaches its extreme form in species in which all, or nearly all, of the population die soon after their first spawning. The well-known examples of this so-called "parental death" are the eels, Anguilla spp., the five species of Pacific salmon, Oncorhynchus spp., the Atlantic salmon, Salmo salar, the lampreys, Lampetra spp., and the eapelin, Mallotus villosus. In the majority of these fish, the males suffer complete mortality whilst a number of females may survive to spawn another year. Species showing parental death deserve particular attention in aging studies because of the suggestion that their death may represent accelerated aging. In the course of a few months, or even weeks, the condition of the salmon migrating in fresh water declines dramatically, and the spawning fish is a very poor counterpart of the lively healthy individual that entered the river. Migrating salmon show histological evidence of deterioration of the stomach, liver, spleen, thymus, thyroi& pituitary, kidney and cardiovascular system. The skin and the islets of the pancreas also exhibit hypertrophy and hyperplasia. Some investigators believe that the post-spawning death of the salmon is directly related to greatly elevated levels of circulating adrenocorticosteroids (Robertson et al., 1961) whilst others have related death to elevated gonadal hormones (McBride and Fagerlund, 1973). A study made by Childs and Law (1972) indicates that varying maximum lifespans seen in male fish within a population of Pacific coho salmon (Oncorhynchus kisutch) may reflect differences in their early rate of growth and differentiation. Between thesetwo extreme forms of the survival curve there are many species, over a wide size range, in which the mortality rate increases steadily with age. Analyses of the natural mortality rate of the Pacific herring, Clupea pallasi, throughout its lifespan have been given by Tester (1937) and Taylor (1958). This species provides a good example of an increase in mortality with age, rising from a value of 0.12 from the post-larval stage to one year, to 1.16 to ages 8 and 9 years (see table).

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TABLE 1. THE INCREASE IN NATURAL MORTALITY WITH AGE IN THE PACIFIC HERRING, (FROM TAYLOR,

Age interval Mortality

0-1 0.12

1-2 0.25

2-3 0.38

3-4 0.51

1963) 4-5 0.64

5-6 0.77

6--7 0.90

Clupea pallasi 7-8 1.03

8-9 1.16

A similar pattern of increased mortality with age has been reported by Kennedy (1954) for lake trout, Cristivomer namaycush, by Wohlschlag (1954) for Alaskan whitefish, Leucichthys sardinella, and by Mann (1973) for the roach, Rutilus rutilus. Williams (1967) found the same relationship in four species of freshwater fish from the River Thames, U.K. In summary, a consideration of the growth curves and mortality rates of wild fish suggests that there is no constant and fundamental distinction between their patterns and those seen in mammals. Aging occurs, despite continued growth (Comfort, 1960). There would seem to be no justification for treating the cold-blooded vertebrates as distinct from mammals for studies of growth and senescence.

VARIATIONS IN T H E ONSET OF SEXUAL M A T U R A T I O N W I T H C H A N G E S IN E N V I R O N M E N T A L CONDITIONS It is stated that fish become sexually mature for the first time at a size which is a rather constant proportion of their final length; this value is usually given as close to two-thirds of the final body length. Maturity would, therefore, appear to be correlated with the growth rate. Under good conditions, growth will be rapid and this length attained when the fish is young. Burd (1962) reported that maturity is established in the herring, Clupea harengus, of the southern North Sea at a length of 22 cm, irrespective of age. In the years following World War II, when feeding conditions were good, herring reached this length as early as their second summer of life, or at the latest, during their third summer. Prior to 1939, fish had not reached this size until their fourth or fifth summer. Saville (1963) also reported increased growth in the herring from the Clyde Estuary, Scotland from 1949, and, correspondingly, an earlier onset of sexual maturity. The situation may now be reversing. Since 1964 there seems to have been a decline in the abundance of the copepod, Calanus spp., the principal food of the herring, and there is evidence for a delay in the onset of maturity. Aim (1946, 1959) made an analysis of the relationship between growth and the onset of sexual maturity in populations of perch, Percafluviatilis. He showed that the onset of first maturity depended upon growth and the achievement of a certain body size, but at the same time, maturity also depended upon the fish having attained a minimum age. In any one age group (year-class) those fish which ,a'ere the first to mature were the largest individuals, with the best rate of growth. Fish with a medium growth rate reached maturity later, but by then had attained a larger body size than the earlier maturing fish. Fish which grew poorly became mature even later, and, at maturity, their size was below that of the medium growth rate fish. Svardson (1949) showed the same pattern in a laboratory population of male guppies, Lebistes reticulatus. Maturity was established first in the fastest growing guppies, whilst fish of medium growth rate matured later, but at a larger body size and with larger testes. The slowest growing males were the last to mature, at a smaller size and with smaller testes. Garrod (1959) found that amongst a population of cichlids, Tilapia esculenta, in Lake Victoria those individuals maturing when relatively small had a higher rate of growth than those which matured at a larger size. Parker and Larkin (1959) also reported that faster growing salmon (Salmo and Oncorhynchus spp.,) mature at an earlier age than slower

FISH IN STUDIES OF AGING

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growing fish, although the former group may be smaller in size at the onset of first maturity than later maturing fish. Changes in feeding conditions and the onset of maturity

An improvement in feeding conditions has been shown to hasten the onset on maturity by one year in flounders, Pleuronectes limanda (Kandler, 1932; Gross, 1949), herring, Clupea harengus (Cushing and Burd, 1956) and char, Salvelinus alpinus (Runnstrom, 1951), whereas poor feeding delayed maturity in trout, Salmo trutta, and perch, Perca fluviatilis (McCay et al., 1929; Aim, 1951; Alt, 1973). In the short-lived lake smelt, Osmerus e. eperlanus, changes in the onset of maturity are extremely plastic and in unfavorable years,

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growth and development can be so delayed that the fish do not mature, but in good feeding years, a whole generation may ripen in one year. Maturity is reached by 30--40~ of three year old Caspian roach, Abramis brama when their growth rate is high, but at low rates of growth, only 10-20~o of three year old fish become mature. Similarly, cod, Gadus morhua living in the Baltic may become mature at three years of age, and analyses of the agecomposition of the spawning stock in years of good growth showed that there were 32,°/ of three year old fish amongst the spawners. In years of poor growth, there were only 12-17~ three-year-old fish in the breeding population (Dementjeva, 1964). Changes in the growth rate offish may also result from a reduction in population density under the influence of a fishery--usually effective through reduced competition for available food. This has been recorded for populations of sturgeon, Acipenser spp., herring, Chlpea harengus, Atlantic salmon, Sahno salar and carp, Cyprim~s carpio (Chuganova, 1951; Nikolsky, 1950). The fish then show an increase in mean length at age, accompanied by a fall in the age at which maturity is established. When the older larger fish were removed from populations of brook trout, Sa/velinus fontinalis, by heavy fishing, the younger fish grew more rapidly and matured earlier (Jonson, 1971). The most dramatic and ~apid changes in these parameters are seen in fish populations subjected to heavy fishing after a wartime period of light fishing (Margetts and Holt, 1948; Parrish and Craig, 1963). Simpson (1959) showed a marked changed in the age composition of spawning plaice, Pleuronectes platessa in the North Sea from older age groups to progressively younger fish as the fishery intensified during the years from 1946 to 1950 (Fig. 3).

Space restriction and the onset of maturity The cichlid genus Tilapia is particularly interesting for growth studies, for in densely crowded situations the fish mature and breed at a much smaller size than do fish in the original, non-crowded situations from which they were derived, i.e. the fish "stunt". The stimulus to stunting seems to be associated with physical restriction in a confined environment. Stunted fish are not in poor condition ; in fact they have been noted for their good physical state (Worthington, 1929; Coo, 1966). Generally, the young fish grow rapidly, but after an initial period of rapid growth, the rate slows dramatically and then ceases almost entirely. Ilcs (1971a) found that the initial rate of growth of stunted populations was fi.ve or six times the average value found in normal lake populations of Tilapia. Garrod (1959) recorded that the first years growth rate of a stunted population of T. esculenta in Lake Victoria was higher than any other growth rate known for a lake stock of this species. "Stunting" does not appear to be a simple density-dependent growth factor resulting from competition for food, and it has not been prevented or reversed by increased feeding in either pond or laboratory culture. Stunting is not determined genetically--although the ability to form stunted populations under crowded environmental conditions may be an inherited characteristic. Stunted fish retain the capacity to resume growth wizen they are transferred to uncrowded habitats. Iles (1973) believes that stunting represents an adaptive mechanism which enables Tilapia populations to withstand extremely high mortality rates-due to heavy predation by birds. It is interesting to compare further the growth and maturity rates given by lies (1973) for normal and stunted populations of Tilapia, since these give a clear indication of the enormous flexibility and range of these physiological responses. For example, T. nilotica living in favorable lake conditions may exceed 60 cm in length (Lowe, 1958), although the

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average length reached is about 35 cm. A stunted population of the same species grows only to 17 cm, less than half the maximum length recorded for its parent stock. The smallest of the stunted species. T. grahami, does not exceed 10 cm in length (Coe, 1966). The time of onset of maturity may change to a similar great extent. Thus, the average age at first maturity in normal populations of Tilapia varies from 2 to 4 years (Ben-Tuvia, 1960; Fryer, 1961) and the length of the fish at first maturity is high in relation to final length, since Tilapia normally matures relatively late in its growth history. By contrast, stunted fish can breed at the age of three months (Chimits, 1957) and T. grahami has been found to breed at 2.5 cm, growing to a final size of 10 cm. Chimits (1957) also recorded fish breeding at 9 cm in length in populations in which individual fish reach over 20 cm. A finding which has emerged from these studies of stunted populations is that the early onset of sexual maturity does not necessarily involve a marked decline in somatic growth rate, per se, nor any decline in the capacity for future growth. Stunted fish resume good rates of growth when they are transferred to better environmental conditions, even though maturity is well established. Comfort (1960) found that retarding the growth of female guppies, Lebistes reticulatus by restricting their diet and living space produced small mature fish, rather than chronically immatures, and that on refeeding, or providing more space, rebound growth was fast and nearly isometric.

Temperature and the onset of maturity Temperature does not regulate growth of fish in the wild in a simple, direct fashion and there are indirect effects through food production, length of the growing season, etc. The subject has been discussed by Gerking (1966), and only the broader outlines of the relationship will be given here. There are large regional differences in the growth rate of fish which have been associated with temperature differences (Fig. 4) and with these varying growth rates, the onset o f first 80

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A. D. WOODHEAD

maturity and also longevity may also be changed. The general pattern is that fish living in the south of their range, where temperatures are higher grow faster, mature earlier and have a shorter lifespan than those living in the northern parts of the range. Thus, the North American grayling, Thymallus signifer in Lake Michigan, U.S.A., grows rapidly and has a short lifespan, the oldest fish collected being 6 years of age. Its Arctic subspecies, living in the cold waters of Great Bear Lake, Canada, does not mature until it is five years old and usually lives for about 12 years. The stickleback Gasterosteus aculeatus in the south of France does not live for more than 14--18 months, but in northern latitudes it takes several years alone to reach maturity. There are similar examples within a more limited geographical area. The yellow tailed flounder, Limandaferruginea, in New England waters grows rapidly, matures at two to three years and generally lives to six or seven years. On the Scotian shelf the same species grows more slowly, reaches maturity at five to six years and lives for ten to twelve years (Lux and Nichy, 1969; Scott, 1954; Pitt, 1973). Alt (1973) compared the growth of populations of the inconnu, Stenodus leucichthys, in Alaska. Fish living in the Upper Yukon River had the shortest lifespan, reaching a maximum recorded age of twelve years and a maximum weight of 5.5 kg; sexual maturity was usually established at seven years. In contrast, the slower growing fish from the Kobuk-Selawick river system matured later, and lived for about 18 years, reaching a final weight of about 27 kg.

VARIATIONS IN FECUNDITY WITH ENVIRONMENTAL CONDITIONS Fecundity may act as a regulatory mechanism by means of which the numerical strength of a population is brought into line with the food resources of a body of water. Generally, an improvement in feeding conditions, either by an increase in food supply, a reduction of the population by fishing, or transference to another body of water results in a greater number of eggs laid during the spawning season. When living conditions deteriorate and the growth rate of the fish is reduced, the age at first maturity increases and the fecundity of the fish falls. Thus, when fishing reduced the numbers of Sakhalin herring, Clupea harengus, feeding conditions improved considerably and their fecundity increased. Similarly, the fecundity of the Caspian roach, Rutilus rutilus of 18 cm length increased by 50~ in 1946 when feeding conditions were exceptionally favorable (Chugunova, 1951). When a warm season preceeded spawning, the length and weight of Onega Bay herring increased, along with their relative and absolute fecundity; conversely fecundity decreased after a cold feeding season (Anokhina, 1960, 1963). Anokhina sees decreased fecundity as an adaptation to guarantee survival and subsequent spawning in future years. A considerable number of eggs do not develop fully in carp, Cyprinus carpio, but are resorbed after spawning (up to 35~ of the eggs of older fish). Vasnetzov (quoted by Nikolsky, 1950) has suggested that when there is an improvement in feeding conditions, these eggs may develop normally, increasing fecundity. Large scale degeneration of ovarian eggs has been recorded for a considerable number of species in the wild (Honma, 1959; Honma and Tamura, 1963; Sathyanesav, 1962; Woodhead and Woodhead, 1965; Woodhead and Eilett, 1969) and in some cases, this has been associated with poor environmental conditions. In the cod, Gadus morhua, the growth achieved and the energy reserves laid down during the summer feeding period may be reflected in the number of eggs which are secondarily recruited into the maturation cycle during the autumn (Woodhead and Woodhead, 1965).

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In such ways the physiological requirements of reproduction may be related to the metabolic capacity of the fish. In an unexpected experiment, Menshutkin et al., (1968) demonstrated the efficiency of fecundity variation in response to changes in the environment. They removed a quantity of perch spawn from a lake (some 15-17 million eggs) and accidentally missed some tens of thousands. Six years later, the number of eggs masses laid was only slightly less than originally, when the lake was first stripped. In this respect, it is interesting to find very large annual variations in fecundity in many species of fish. These variations amount to 48~ for plaice, 40~o for long rough dab, 28~ for witch, 25~ for pike, 34~ for herring, 56~ for haddock and the very high value of 250~ for Norway pout (Bagenai, 1973). An improvement in the diet of freshwater fish causing an increase in maternal glowth rate and fecundity, may also result in an increase in egg diameter. When the diet of lake trout, Salvelinus namaycush changed so that their rate of growth improved markedly, egg size as well as egg number increased. Vladykov (1956), Scott (1962) and Fry (1949)found an improvement in both egg size and numbers in freshwater fish when there had been an improvement in feeding. Experimental restriction of the diet of the rainbow trout, Salmo gairdneri did not, however, influence the size of eggs at maturity (Scott, 1964), although observations on natural populations of these fish have shown that there are large variations in egg size. The size of the eggs may determine the spawning success of the navaga, Eleginus navaga living in the White Sea (Anukhina, 1968), where there are large variations in food supply and conditions for fish growth are often marginal. Unfavorable feeding conditions have a negative effect on all biological indices except egg size but when feeding conditions are good, larger numbers of smaller eggs are produced. In other marine species, improved feeding results in more, but smaller eggs, for example in the herring, Clupea harengus (Bridger, 1961). The sea is a variable environment, and it seems that the reproductive responses of fish will be geared to fully exploit the opportunity to multiply, i.e. to produce more eggs, during good years. In this respect, it is interesting to find that fluctuations in the year class strength of the White Sea navaga, in marginal living conditions are only in the order of 10-fold. By contrast, year class fluctuations for the cod, Gadus morhua living in the Barents Sea, where there is a vast feeding area and a much more labile food supply, range from fifty to ninety-fold. SEXUAL DIFFERENCES IN NATURAL MORTALITY In the earlier discussion of mortality rates in fish, no distinction was made between males and females. But sexual differences in natural mortality are commonly seen in all vertebrate classes, including fishes, the males usually showing an increased mortality rate compared with the females of the same species. The cause of this is uncertain. In fish increased male mortality has been associated with earlier onset of maturity--and, resulting from this, a greater committment of energy reserves to reproduction. There is good evidence that this idea is not generally applicable; for example, in the Atlantic salmon, Salmo salar, the female uses up much more energy in spawning migration and reproduction than the male, yet there is a very marked preponderance of females in the survivors after spawning. The higher fishing mortality of male fish in exploited populations may be accounted for, in part, by differences in spawning behavior. Thus male plaice, Pleuronectes platessa, arrive first at the spawning grounds and remain there longer, so that they are accessible to the

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commercial fishery for longer periods. In the same way, differences in spawning behavior may make the males more vulnerable to predation by other animals. The difference in natural mortality, however, is greater than can be accounted for by behavioral differences alone. In a number of species of fish, functional hermaphroditism--the existence of male and female sex within a single individual--is common. Unlike most higher vertebrates, in which sex is determined prior to or at fertilization, as in male or female heterogamy, the genetic basis of sex in fish may be autosomal and sex appears to be more liable relative to the higher vertebrates. Cytologically distinguisable sex chromosomes have been demonstrated only in a few species (including Lebistes), but even in these cases it has been possible to experimentally alter sex chromosome into autosome, and by selective breeding, to elicit phenotypic expression of sex opposite to the genotypic sex (Chan, 1970). Hermaphroditism in fish may be simultaneous (synchronous) or sequential. In sequential protogynous forms, the fish functions first as a female and then as a male, whilst the reverse situation occurs in protandry. Functional hermaphrodism has been reported in five orders offish and reaches a complex and diverse expression in the Order Perciformes, particularly in the porgies, seabasses and wrasses. In such sequential hermaphrodites, individual fish carry the genetic capacity to function both as a complete male and a complete female, and also have the capacity to switch from one sex to the other. The switch mechanism, which shifts development from the currently expressed sex to the latent, temporarily suppressed sex is undefined. Warner and his associates (Warner, 1972; Warner, Ross and Leigh, 1975) have shown that under certain ecological conditions there are distinct advantages afforded by sequential hermaphroditism to the individual, by increasing its reproductive potential relative to that on a non-changing member of the same population. Natural selection appears to operate at the individual, rather than population level. During the course of evolution of sequential hermaphroditism within a population, an average size (and/or age) for the transformation tends to become established. This is the size at which the reproductive potential of the individual will be maximized. Comparisons of the growth, maturity and mortality rates of sequential hermaphrodites with those of non-changing individuals from the same population offer the possibility of resolving some of the speculations concerning the nature of sex differences in mortality. Especially valuable would be a study of those species in which sex expression is unusually labile and in which exogenous factors, rather than endogenous ones, exert a powerful influence on the timing of the sex change. Fricke and Fricke (1977) have recently described socially controlled protandric hermaphroditism in the coral reef fish, Amphiprion, in which the aggressive behavior of the dominant female within the social grouping regulates the production of male fish. By contrast, in populations of the labrid fish, Labroides dimidiatus, a protogynous hermaphrodite, the aggressive behavior of the dominant male within each group suppresses the tendency of females to change sex (Robertson, 1972). Robertson notes the rapidity and ease of such sex changes; in one interrupted reversal a female changed behaviorally into a male, then to a female and back again to a male before successfully completing the change. This all occurred within the period of about two weeks. CONCLUSIONS The case for comparative studies of growth and aging has been strongly presented by Comfort (1960), who has pointed out that such studies could provide test systems in which many aging theories could be initially screened. But in a series of papers summarizing the

FISH IN STUDIES OF ACING

I39

status of aging research (Bioscience, 25, 1975) the non-mammalian vertebrates were mentioned in only two instances, and there was no suggestion that such comparative work might play a role in the future. Despite the initial impetus to experimental studies given by Comfort (1960) and by Walford and his colleagues (1964) in which the value of fish models was clearly demonstrated, there has been little subsequent work. We reiterate the unique advantages of fish for both laboratory and field studies, and point out the wealth of background data which exists on growth, maturation and aging. K o h n (1971) has discussed the problem of whether the evolutionary origins of aging are in processes that restrict growth and the period or reproductive activity. The extent to which these parameters can be integrated and segregated by environmental changes in fish suggests that such comparative studies might give good indications of when aging processes are initiated. Finally, fish are the largest and most diverse class of vertebrates, numbering over 20,000 species (a conservative estimate) and the class provides an enormous spectrum of reproductive mechanisms, size and longevity. Reproductive processes range from ovipatity, through ovo-viviparity to viviparity with all degrees o f parental care. Differences in adult size range from the tiny goby, Mistchthys luzonensis measuring ½ in. to the sturgeons, Acipenser spp., which reach over 15 ft in length. Longevity, similarly, varies from about a year, as in the white goby Latrunculus pellucidus, to over 60 years in the European catfish, Stlurus glonis.

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