55

THE GROWTH OF FISH

IV. THE EFFECT OF FOOD SUPPLY ON THE SCALES OFSALMO IRRIDEUS

BY J. GRAY, F.R.S., AND S. B. SETNA, PH.D.

(Zoological Laboratory, Cambridge.)

(Received 15th April, 1930.)

(With Three Text-figures and Two Plates.)

CERTAIN scales of Salmonoid fish exhibit a series of concentric ridges or circuli,the number of which increases with the size of the whole fish. Each year ofnormal growth is recorded on the scale of a salmon by a concentric band which ismore or less sharply divided into two regions, (i) in which the concentric ridges arerelatively wide apart, (ii) in which the ridges are closer together. It is tolerablycertain that the first region is formed whilst the fish is in the sea, and the secondregion whilst the fish is in estuarine or fresh water; roughly speaking the two regionsmark the summer and winter periods respectively. The factor or factors responsiblefor the difference between winter and summer circuli are not fully understood.There are two possibilities. The variation in width may be dependent on an inherentrhythm upon which external factors may exert little or no control; or the variationmay be due to variations in the external environment of the fish. In view of thehigh economic importance of the facts, curiously little experimental data are availablefor a solution of the problem.

Cutler (1918), working with Pleuronectes platessa and P. flesus, altered experi-mentally the temperature and food supply in the fishes' environment. Fish werekept in "hot" and "cold" tanks, the latter being 50 C. cooler than the former, andat each temperature the fish were fed once a day. The effect of food supply wasdetermined by a comparison of fish fed with excess of food twice a day with fish fedsparingly every other day. Cutler's results, as summarised by Graham (1929),were as follows:

Table I.

Length increment in cm.Sclerite numberSclerite width in n (average)

Tanks

Control

O"I9 ±29±*

Hot

0410 ±112 ±i

Cold

049±i8±£

Abundant

0713 ±3IO±I

Scanty

0-38±f9±i

56 J. GRAY and S. B. SETNA

These data suggest that high temperature increases the sclerite width withoutinfluencing either the growth rate or the number of the sclerites. Abundantfeeding, on the other hand, increases the growth rate and the number of sclerites,without marked effect on the width. Cutler's observations are not readily harmonisedwith those of Thompson (1923), Dannevig (1925) and Graham (1929), since theseauthors found a marked correlation between sclerite width and growth rate. In astate of nature, there can be little doubtthat the growth rate of fish during the summeris greater than that during the winter. If the sclerite width is associated withgrowth rate, it follows that wide sclerites will be formed in summer and narrowsclerites in winter; at the same time the controlling factor might either be tempera-ture (Cutler, 1918) or food supply (Thompson, 1923). The most satisfactory way ofattacking the problem is by the observation of fish under controlled conditions oftemperature and food supply. For this purpose trout form a satisfactory material,they can readily be reared in captivity and the concentric ridges on the scales areusually well defined.

The experiments here described were designed as a direct test of the effect offood supply on the width of the circuli of Salmo irrideus; no attempt was made tokeep the temperature constant, although of course it remained the same for eachsample of fish under observation. The work was carried out at the Midland Fishery,Nailsworth, Gloucestershire; to the manager of the farm, Mr F. Stevens, we oweour sincere thanks for valuable co-operation and help.

It is significant to note, at the outset, that in no case which we have examined dothe scales of rainbow trout, which are fed by hand continuously throughout theyear, show any well-defined summer or winter zones (see PI. II, figs. 1, 2). Thisfact seems to eliminate the suggestion that the periodicity of circulus width foundin other members of the Salmonoid family (when under natural conditions) is dueto an inherent rhythm over which the environment has no control. It also suggeststhat temperature alone is not invariably a decisive factor.

For the present experiment, fifty rainbow trout {Salmo irrideus) were takenfrom the yearling class on July 5th, 1928. These fish were approximately 20 cm.long. Twenty-five of these fish were placed in a concrete tank (16 ft. x 6 ft. x 6 ft.),whilst the remainder were kept in a similar tank below the first. The water supply tothe two tanks was derived from the surface of a lake measuring about an acre. Theamount of water that passed through the experimental tanks was 250 gallons perminute. The top tank represented the starved tank. The fish in this tank were notfed, but maintained themselves on the plankton available in the water. Althoughthe amount of food the fish thus captured was undoubtedly far below their maximumrequirements, they showed no symptoms of unhealthiness throughout the period ofexperiment. Early in December 1928, the water entering the scanty tank was madeto pass through two fine screens, so that the amount of natural foods that passed intothe tank was still further reduced. The fish in the lower tank were fed twice dailywith as much food as the fish would eat. They were given a diet of meat (raw andcooked) together with biscuit and fish meals. This tank was well stocked withnatural foods (shrimps and snails).

The Growth of Fish 57

The water flowing through both experimental tanks varied in temperatureaccording to the season of the year, although the extremes for the monthly averages(Table II) were not as great as those to which fish are often exposed under naturalconditions. The daily temperatures were recorded; the maximum being 630 F.and the minimum 34° F. The monthly averages were as follows:

Table II.

1928

JulyAugustSeptemberOctoberNovemberDecember

°F .

56-148-24 6 050-04 7 0446

1929

JanuaryFebruaryMarchAprilMay

° F .

44-043°45-44 6 051-0

For an examination of the scales, Winge's (1915) method was employed, the scalebeing mounted, on a microscope slide, in glycerine. An eyepiece micrometer wasfocussed on the centre of the scale and the number of ridges in the direction of theanterior longitudinal radius read off, together with the distances apart of successiveridges. The chart shows the total number of ridges and the variations in spacing ofthe ridges in the anterior quadrant. The scales for examination were removedin each case from the same region (shoulder), and the extent to which they weremagnified was the same throughout. The fish were placed in the tanks on July 5th,1928; the first scales were taken on September 18th, 1928. Scales were removedfrom fish selected at random from each tank. Charts were prepared and represen-tative scales were preserved in 10 per cent, formalin. Material of this type wascollected at monthly intervals, care being taken to avoid undue disturbance to theother fish in the tanks. Individuals used for scale examination were not replaced inthe tanks.

In order that an experiment of this type should yield useful results it is essentialthat growth should occur at a measurable rate in each tank. If the amount of foodpresent in the scanty tank falls below a critical level, the fish will not grow since theavailable food is all required for maintenance: on the other hand, the food supplymust be definitely lower than in the tank in which food is abundant. Howevercarefully the conditions are controlled, there is always a marked variation in theability of individual fish to grow on artificial or natural diets, and this variation isaccentuated when food is scarce. The twenty-five fish placed in the abundant tankincreased in length from approximately 20 cm. in July 1928 to 30 cm. in November1928, and to 33 cm. in March 1929. These fish under normal hatchery conditionswould have reached an average length of 29 cm., although a significant amount ofvariation might be expected. It is, however, quite clear that an abundance of foodin the experimental tank resulted in a very rapid growth rate. In the scanty tank, onthe other hand, it is impossible to give even approximately comparable figures. Thefish under these conditions are best divided into three categories: (i) those whichgrew comparatively steadily and attained in February 1929 a length of 26-5 cm.;

58 J. GRAY and S. B. SETNA

(ii) fish which grew very much more slowly; (iii) fish which showed little or noincrease in size, particularly during the latter months of the experiment. Markeddifferences of this type might well be expected, and probably indicate a variation inthe ability of the fish to obtain the food available.

An examination of selected scales revealed quite definite data. PI. II, fig. i, showsa scale typical of the fish as placed in the tanks in July 1928; PI. II, fig. 2, shows a scalefrom a fish reared under hatchery conditions precisely similar to those of fig. 1, butkilled on January 15th, 1929. These two scales may be regarded as typical of fishreared under standard conditions of feeding. It will be noted that, although thelatter fish was two years old, the scale exhibits no well-marked seasonal variation inthe spacing of its ridges; the spacing tends to increase towards the periphery of thescale, in spite of the fact that these rings were formed during the winter months.The contrast between these scales and some of those obtained from fish fed withabundant food is quite definite. A definite percentage of scales removed from theabundantly fed fish at approximately monthly intervals from September 1928 toMarch 1929 show that the peripheral rings are markedly wider apart than thosenearer to the centre of the scale, and are clearly wider than those characteristic ofstandard hatchery conditions. PI. I l l , figs. 6,7,8, and Text-fig. 1 are typical records ofsuch scales from the hand-fed fish. It is, of course, difficult to determine preciselythose ridges which were laid down after the period of abundant feeding began, but thechange from normal width to wider widths is usually fairly abrupt and can be safelyassumed to represent the period of rapid growth under the experimental conditions.

widthin n

5°4540353°252 0

151 0

Total

Table III. Distribution of circulus width for peripheral circuli.

Number of circuli measured on each scale: 20

Abundance of

A

35

I2.

2 0

B

1

812

b2

2 0

c

3b1

42

4

2 0

A.M.=

D

21

b344

2 0

food

E

5552

3

2 0

= 35 ±8

F

1

391

312

20

Total

81337132 0

' 91 0

00

1 2 0

A

1

4751

2

2 0

Scarcity of food

B1 C,

1

1 210 74 34 51

2

20 20

A.M. =

2

5 24 72 55 41 21

20 20

=26 ±6

Fi

121

3841

2 0

Total

.5

16362 22l8

61 2 0

Taking the outer twenty ridges on each selected scale as revealed by the Wingecharts, the variation can be expressed by the graph in Text-fig. 2. It will be notedthat, although the total number of fish observed was small, the effect of the foodsupply upon the spacing of the ridges is sufficiently clearly marked to leave littleor no doubt of the conclusion to be drawn, or of the fact that wide rings can be laiddown in winter months. In order to compare these results with those obtained

The Growth of Fish 59i i i I i i i i

B

C

D WV\

G

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 11 irText-fig, i. Curves of scales showing the successive widths of circulus from measurements of in-dividuals kept in the "abundant" tank. Each minor subdivision of the ordinates represents 5/1;each subdivision of the base line indicates a circulus.

6o J. GRAY and S. B. SETNA

from the "scanty" tank it is necessary to select from the latter each of the specifictypes mentioned on p. 58. Firstly, we may consider the scales from a fish whichgrew steadily on the reduced food supply. PI. I l l , fig. 9, is a typical scale of such a fishkilled on February 12th, 1929, when it had attained a length of 26-5 cm. With oneexception the distance between successive ridges are all less than 40 ft, the averagewidth being approximately 22 /*. It will be noted that the peripheral rings, on theright side of the scale, are markedly narrower than the average. The scales of fish(from the scanty tank) which grew more slowly exhibit the same phenomenon,viz. the peripheral rings are narrow, and are of the order of 20 /x or less (see Text-figs. 2 and 3 and PI. II, figs. 3, 4, 5). It will also be noted that the outer rings on thescales of slowly growing fish are often incomplete, and are more irregular in formthan those characteristic of well-fed individuals.

401-

30

20

10

Scanty food U-Abundantfood

10 15 20 25 30 35Width of ring in /t

40 45 50 55

Text-fig. 2. Showing the distribution of concentric rings of varying widths at the periphery of fishfed with abundant and scanty food respectively.

Although the population concerned is not as large as might be desired, thefacts seem fairly clear, (i) Abundant food can effect an increased growth rate, andduring this period the ring width in some scales is increased, (ii) The formation ofwide rings can occur during the winter, (iii) Scarcity of food entails a reduction ofring width. It is also noticeable that several of the fish in the abundant tank spawnedduring the winter, but the fact is not recorded by any disturbance of ring formation.

The results of the present experiments obviously differ from those obtained byCutler (1918), but are in closer harmony with those of Thompson (1923), Dannevig(1925) and Graham (1929), all of whom recorded a correlation between growth rateand sclerite width. It should not be inferred, however, that temperature is withoutits effect. Hathaway (1927) has shown that the ability of fish to feed at low tempera-

The Growth of Fish 61

"ures is markedly less than at higher temperatures; in other words, although foodmay be present in abundance, the amount actually absorbed may be greatly reducedat a low temperature, and in this way the growth rate will be affected. In addition,temperature may affect the growth rate in another way. The food which is actually

J I I i I I I I I I I I I I I I I I I I I I I I I I I r r r TTT i i i MIL

G

i i i

Text-fig. 3. Curves of scales showing the successive widths of the concentric rings from measure-ments of individuals kept in the " starved " tank. Each subdivision of the ordinates represents 5/x.

absorbed by the fish is utilised in two ways, firstly for the maintenance of existingtissues, and secondly for the formation of new tissue. If a fish absorbs a unit quantityof food (a) at a low temperature, we may suppose that a definite fraction (xj) isrequired for maintenance, leaving the remainder (a — xx) for the production of newtissue. If the temperature be raised, the rate of metabolism increases so that Xi is

62 J. GRAY and S. B. SETNA

increased—to x2—leaving a smaller proportion (a — x2) for the purposes of growth.As shown by Gray (1928) for the embryonic cycle of the trout, the effect of hightemperatures is to produce larger organisms for each standard diet, although thetime required for their growth is increased. As far as one can see, under naturalconditions, the growth of post-embryonic trout will be influenced by temperaturein several ways: (i) a higher temperature may induce a more rapid formation ofnutritive organisms—and hence increase the quantity of food available; (ii) it willincrease the capacity of the fish to capture the food; (iii) it will increase the rate atwhich the food is converted into new tissue; (iv) it will decrease the proportion ofacquired food which is available for growth. The net result will depend on theequilibrium which exists between these various effects.

SUMMARY.

1. Salmo irrideus fed continuously throughout the year exhibit on their scalesno seasonal periodicity in the distance apart of their concentric ridges or rings.

2. Similar fish fed with abundant food form on a proportion of their scalesabnormally wide rings even during the winter months.

3. Fish fed with limited diet develop abnormally narrow rings.4. The width of the rings is probably ciosely associated with growth rate.

BIBLIOGRAPHY.CUTLER, D. W. (1918). Journ. Mar. Biol. Assoc. 2, 470.DANNEVIG, A. (1925). Rep. Norwegian Fish. Invest. 3, 6.GRAHAM, M. (1929). Fishery Investigations, Ser. 2, 2.GRAY, J. (1928). Brit. Journ. Exp. Biol. 6, 125.HATHAWAY, E. S. (1927). Ecology, 8.THOMPSON, H. (1923). Fisheries, Scotland, Set. Invest. 5.WINGE (1915). Medd. Komm. Havunsdersegelser Fisk. 4, 8.

EXPLANATION OF PLATES.

PLATE II.

FIG. 1. Scale characteristic of a fish placed in the experimental tanks in July 1928. Length of fish,20 cm.

FIG. 2. Scale of a fish of the same age as experimental fish but fed under standard hatchery conditions.Fish killed on January 15th, 1929. Length of fish, 29 cm.

FIG. 3. Scale of a fish removed from scanty food conditions on September 18th, 1928. Length offish, 23 cm.

FIG. 4. Scale of a fish removed from scanty food conditions on December 15th, 1928. Lengthoffish, 25-8 cm.

FIG. 5- Similar to the above, but killed on February 12th, 1929. Length of fish, 202 cm.

PLATE III.

FIG. 6. Scale of a fish fed on abundant food from July 1928 until September 18th, 1928. Length offish, 30 cm.

FIG. 7. Similar to Fig. 6, but killed on November 17th, 1928. Length of fish, 325 cm.FIG. 8. Similar to Figs. 6 and 7, but killed on March 12th, 1929. Length of fish, 32-5 cm.FIG. 9. Scale of a fish which grew steadily on scanty diet from July 1928 to February 12th, 1929.

Length of fish, 26-5 cm.

JOURNAL OF EXPERIMENTAL BIOLOGY. VOL. VIII, PLATE II.

Fig. i. Fig. 2.

Fig- 3-

Fig- 5-

J. GRAY AND S. B. SETNA—THE GROWTH OF FISH (pp.55-62).

JOURNAL OF EXPERIMENTAL BIOLOGY. VOL. VIII, PLATE III.

Fig. 6. Fig. 7.

Fig. 9.

J. GRAY AND S. B. SETNA.—THE GROWTH OF FISH (pp. 55-62).