Growth and feeding responses of a hatchery population of brown trout (Salmo trutta L.) at low temperatures

Ecology of Freshwater Fish 1997: 6: 116-121 Printed in Denmark All rights reserved

Copyrinht Q Marnksaaard 1997

ECOLOGY OF FRESHWATER FISH

ISSN 0906-6691

Short communication

Growth and feeding responses of a hatchery population of brown trout (Salmo trutta L.) at low temperatures Koskela J, Pirhonen J, Jobling M. Growth and feeding responses of a hatchery population of brown trout (Sulrno trutta L.) at low temperatures. Ecology of Freshwater Fish 1997: 6: 116-121. 0 Munksgaard, 1997

Abstract - Feed intake, specific growth rate and changes in body composition were studied in age 1+ (140-190 g) brown trout (Sulmo truttu L.) reared at three temperatures (2,4 and 6OC) under continuous light conditions. Feed intake increased from 35.7 kJ-kg-'.day-' at 2°C to 95.7 kJ.kg-'.day-' at 6"C, and the growth rate increased from 0.19%.day-' to 0.42%.day-' over the same temperature range. The estimated lower temperature limits for feeding and growth were slightly above OOC. For all groups of fish, the majority (about 75%) of the weight gain comprised water and protein, but lipid deposition tended to increase with increasing temperature. The deposition of lipid ac- counted for about 50% of the body energy gain at all temperatures.

Un resumen en espaiiol se incluye detrais del texto principal de este articulo.

J. Koskela', J. Pirhonen', M. Jobling* 'Finnish Game and Fisheries Research Institute, Laukaa Fisheries Research and Aquaculture, Valkola, Finland, 'NFH, University of Tromss, Norway

Key words: Salmo frutta; growth; temperature J. Koskela, Finnish Game and Fisheries Research Institute, Laukaa Fisheries Research and Aquaculture, FIN-41360 Valkola, Finland Accepted for publication May 6,1996

Introduction

Exposure to the long and cold winters at northern latitudes has marked effects on the growth of aquatic fauna. For fish, decreasing the water temperature below the optimum results in reduced feed intake and growth. Eventually both feeding and growth cease in the lower part of the temperature tolerance range (Brett 1979; Elliott 198 1; Jobling 1994).

Wild brown trout (Sulrno truttu L.) have been observed to forage at temperatures close to zero (Cun- jak & Power 1987; Forseth et al. 1992; Heggenes et al. 1993), and in the laboratory, brown trout may continue to feed at temperatures of 2 4 ° C (Elliott 1975a; Jensen & Berg 1993). Successful food acqui- sition does not necessarily lead to an increase in body weight if energy intake is low, because most of the energy is used to maintain vital functions and little is available for growth. Thus, despite active foraging at low temperatures, growth of wild brown trout has been reported to be insignificant during

winter (Mortensen 1985; Cunjak & Power 1987), and the lower thermal limits for growth may be as high as 6 6 ° C (Wingfield 1940; Elliott 1975b; El- liott, Hurley & Fryer 1995).

Salmonids are often reared in hatcheries for stock enhancement purposes, and in Finland most hatchery-reared brown trout are released into natural water bodies at the age of I+ or 2+. In this study we examined the effects of low water temperatures on feed intake, growth and body composition of hatchery-reared juvenile brown trout in an attempt to estimate the lower thermal limits for feeding and growth.

Material and methods

The experiment was carried out between 19 January 1993 and 24 March 1993 at the Laukaa Research Station of the Finnish Game and Fisheries Research Institute (62"30'N, 26"E). The fish used were age I+ hatchery-reared brown trout of the Rautalampi strain, derived from broodstock held at the research

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Growth of brown trout at low temperatures

and 8.5; Jencons Ltd.) followed by compression into pellets and re-drying at 4045°C. Standard curves were then prepared by X-raying known weights of the marked feed and counting the numbers of ballotinis present. Thus, the amount of ballotini in a unit mass of feed could be calculated for later estimation of feed intake by the fish. All feeds were stored at 5°C prior to use. Feed intake measurements were made by providing the marked feed during an evening and the subsequent morning feeding period, followed immediately by anaesthetizing the fish (MS-222), X-raying (Siemens Nanodor X-ray ma- chine; Agfa Structurix D7 film), weighing to the nearest 0.1 g and measurement of total length to the nearest 0.1 cm. X-ray plates were then developed and the amounts of feed consumed by the individual fish estimated from the numbers of ballotinis present in the gastrointestinal tract.

All the results relating to feed intake and growth were calculated from the data collected from the tagged individuals. Growth rates (SGR), in terms of weight and length, were calculated according to the formula:

SGR=[(ln X,-In XJt] x 100, where X, is the weight or length of the fish at the start of, X, is the weight or length at the end of, and t (63 days) is the duration of, the experiment. Condition factor was calculated as (W/L3) x 100, where W is fish weight in g and L is the total length in cm.

At the end of the 63-day experiment, samples of 10 fish per tank were taken for the analysis of chemical composition. Samples were first dried for 24 h at 105°C and then ground to a fine powder. Sub- samples were then taken for the analysis of lipid (by petroleum etherlether extraction), protein (as Kjeldahl-N x 6.25), ash (remains following bomb calorimetry) and energy content (by adiabatic bomb calorimetry).

Statistical analyses were performed using SYS- TAT statistical software (SYSTAT 1992), with pos- sible differences among treatments being tested using a nested ANOVA model (Sokal & Rohlf 1981). Homogeneity of variances was examined using Bar- tlett's test, and the Lilliefors' method was used to test for normality (SYSTAT 1992). The Tukey- Kramer test was used to make post hoc comparisons between sample means, and P=0.05 was taken as the level of significance. Relationships between selected variables were examined using least-squares regression analysis.

station. Brown trout of the Rautalampi strain are those that are most commonly used for stocking natural water bodies in Finland. The fish were reared in 36-mz tanks with approximately 4000 fish per tank, and the fish were exposed to natural photoperiod and ambient water temperatures. During the 2 months prior to the start of the experiment the water temperature was within the range 1-2°C. Six weeks prior to the start of the experiment, fish weighing between 135 and 165 g were selected from a larger population and the selected fish were then individu- ally tagged by injecting a PIT tag (DestrodIDI) into the body cavity. Following tagging, the adipose fin of the fish was removed. This was done to aid in the identification of the fish that were to be followed throughout the growth experiment. A sample of 10 fish was taken at the start of the experiment for the analysis of initial body composition.

Acclimatization to the experimental conditions commenced 3 weeks prior to the start of the experiment. Nine groups of fish, each comprising 28 tagged and 22 untagged trout, were established in 1.7-m2 hatchery tanks (volume: 0.35 m3), giving triplicate groups of fish for each temperature treatment. Temperature was gradually increased from ambient to the test temperature over a 24-h period. Water temperatures of 2, 4 and 6°C were obtained by the heating, cooling, mixing and aeration of the stock water supply prior to distribution to the rear- ing tanks. Daily temperature recordings made during the experiment showed that temperatures were maintained with an accuracy of kO.2"C. Water flow to the tanks was maintained at 10 l.min-', and this was sufficient to maintain a circumferential current. The fish tended to direct themselves against the di- rection of the water flow and maintained station. The fish were exposed to continuous illumination provided by artificial overhead lighting (50 lux at the water surface). The fish were fed twice per day on commercial dry pellet feed (Ewos Forelli Export 4 mm; analyzed composition energy 25 kJ.g-', protein 50.1% and lipid 23.4%), with feed being dis- tributed by belt feeders for 2 h during the early morning and 2 h during the evening. The observa- tion of waste feed on the bottom of the tanks sug- gested that the fish were being fed in excess.

Feed intake was measured using an X-radiographic technique (Talbot & Higgins 1983; Jobling et al. 1993) at the start of the experiment and at 3- week intervals thereafter. Thus, there were 4 feed intake measurements for each tank of fish, and means of these measurements were used as the estimate of feed consumption. Diets used for feed intake measurement were prepared from the normal feed by grinding, homogenization and incorporation of known quantities of X-ray dense ballotini (size 7

Results

There was no mortality during the course of the experiment, and growth data were collected for all of the tagged fish. A small number of X-ray plates

117

Koskela et al. Table 1. Initial and final wet weights, total lengths and condition factors of brown trout (Salmo trutta L.) reared at different temperatures. Data are presented as meanskstandard deviations (n=3). Values within columns that are denoted by different superscripts are significantly different from each other.

Initial Final

Temperature "C Wet weight g Total length cm Condition factor Wet weight g Total length cm Condition factor

2 142.8+3.3a 24.1kO. 1 6a 1 .03k0.03a 161 .7k5.ga 24.4k0.09a 178.2+_2.4b 24.7H0.06h 4 1 44.0i.0.7a 24.0k0.05a 1 .04i.0.00a

6 145.0f2.9a 24.1 +0.05a 1 .04k0.0Zd 189.5f4.7b 25.2+0.1OC 1.18f0.02b

1.1 2t0.03a 1 . 1 8kO .02b

Table 2. The initial and final body composition (YO ww) of brown trout (Salmo hutfa L.). Data are given as meanskstandard deviations (n=3). Initial samples represent the mean values of 10 fish. Final values within columns that are denoted by different superscripts are significantly different from each other.

Temperature "C Water Protein % Lipid % Ash % Energy k J q '

Initial 75.0k1.1 15.9k0.3 7.1k0.9 2.li.O.2 7.0k0.4 Final 2 72.6k1 .Oa 16.8+0.5a 8.1 i.0.7a 2.2kO.la 8.4f0.3a

4 70.0k2.6a 17.8fl .Za 9.4k1 .4a 2.2+0.1a 8.4?0.8a 6 68.2i.0.9b 18.8+0.6b 10.2*0.3b 2.3k0.0a 9,OfO ,3

could not be read, and this led to loss of feed intake data for some fish (4-5 per treatment).

The feed intake of the brown trout increased from 1.43 g.kg-'.day-' (mean of 3 tanks) at 2°C to 2.02 g-kg-'.day-' at 4°C and 3.83 g.kg-'-day-' at 6°C. The corresponding values in terms of energy were 35.7 kJ.kg-'.day-', 50.7 k.l.kg-'.day-' and 95.7 kJ . kg-'. day-' at 2 , 4 and 6"C, respectively. The feed intake was significantly greater at 6°C than at the two lower temperatures, and the relationship between water temperature (T"C) and feed intake (FI g . kg-' .day-') was described by the following linear regression:

FI=0.601 (f0.233) x T+0.025 (R2=0.81; P=O.OOl)

The intersection of the regression line with the x-axis may be used as an estimate of the lower thermal limit for feeding. On this basis, feeding of the juvenile brown trout would be predicted to be maintained until water temperature fell to approximately zero.

Initial wet weights, total lengths and condition factors did not differ among treatment groups (Table 1). In all of the temperature treatments final condition factors (CF) were significantly higher than initial CFs. There were also significant differences in the final CFs among treatments, final CFs being significantly greater at 4°C and 6°C than at 2°C (Table 1). There was a significant effect of temperature on growth, leading to significant differences in final sizes of the fish (Table 1). Fish reared at 6°C were longer than those reared at both 4 and 2"C, and the total lengths of the brown trout held at 4°C were significantly greater than those of the fish at 2°C. At

the end of the experiment, the fish reared at 6°C and at 4°C were significantly heavier than those reared at the lowest temperature (Table 1).

Specific growth rates for both weight (SGR,) and length (SGR,) increased with increasing temperature (Fig. 1); SGRlV from 0.19 to 0.42% day-', and SGRL from 0.02 to 0.07% day-', as water temperature increased from 2 to 6°C. The influence of increasing temperature (TC) on SGRs for both weight and length could be described by simple linear relationships:

SGRw=0.056(H.009) x T+0.093 (R2=0.96; P=O.001)

and

SGRL=0.013(f0.002) x T-0.006 (R'z0.93; P=O.OOl)

The intersections of the regression lines with the x- axis provide estimates for the lower thermal limits for growth in weight and length, respectively. SGR, is predicted to fall to zero at water temperatures below O"C, whereas increase in length would cease at a temperature of approximately 0.6"C.

The percentage of water decreased and the percentages of lipid and protein increased during the course of the experiment. The relative changes in composition were most marked for the fish held at 6°C (Table 2), and by the end of the experiment these fish had the highest lipid and protein concen- trations and the lowest percentage water, whereas the fish held at 2°C had the highest percentages of body water and the lowest protein and lipid concen-

118


u c

2 4 6 Temperature "C

Fig. 1. Specific growth rates in terms of wet weight (0) and length (0) for brown trout reared at different temperatures.

trations. The overall trend was towards an inverse relationship between percentage body water and percentage protein and lipid (Table 2). Data relating to changes in the relative proportions of various bio- chemical components cannot provide a complete picture of changes in body composition, nor are they sufficient to give information about the composition of the weight gain. To obtain a complete picture of the patterns of energy deposition that occur during growth, it is necessary to combine information about weight changes with that obtained from the analysis of the proximate composition of the body tissues. The results given in Tables 1 and 2 have been combined to calculate the absolute amounts of each analyzed major component (water, protein, lipid and ash) present in the bodies of the fish at the start and end of the experiment (Fig. 2A). The weights of all major components increased in all treatment groups during the course of the experiment, with the increases in the weights of body water and protein being most pronounced (Fig. 2A). Together, water and protein were found to comprise 74-78% of the weight gain in fish in all treatment groups, whereas the contribution of lipid to weight gain tended to increase with increasing temperature (2°C: 16%; 4°C: 19%; 6°C: 21%).

The data on weight and body composition changes are presented in terms of energy deposition in Fig. 2B. Total body energy content was calculated from the results of bomb calorimetry presented in Table 2, whereas the contributions of protein and lipid were estimated by multiplying the weights of each component by the a propriate calorific coeffi-

1994)). There was reasonable agreement between the estimates of energy contents based on proximate composition data and those derived from bomb calorimetry of the body tissues, with differences be-

cient (protein: 23.6 kJg P ; lipid: 38 kJg' (Jobling

250

200

150 I M .- p 100

50

0

1800

1200 e 2d

2 5

600

0

(A) 0 Water W Lipid

KY Protein Ash

Initial 2°C 4oc 6°C

U (B) LI Protein Lipid

Initial 2°C 4oc 6OC

Fig. 2. A. Initial and final body weights of brown trout reared at three different temperatures, and the body content of the major constituents (water, protein, lipid and ash). B. Contributions of protein and lipid to the total body energy content of brown trout reared at different temperatures (see text for details of calcula- tions).

tween the totals probably being largely due to the contribution of carbohydrate to the total body energy content. For fish held at 2OC, the energy gain was almost equally divided between protein energy (PE, 106 kJ) and lipid energy (LE, 112 kJ). As temperature increased, increasing amounts of both protein and lipid energy were deposited (4°C: PE, 208 kJ, LE, 250 kl; 6°C: PE, 295 kJ, LE 341 kJ), but the relative contribution of lipid remained similar irre- spective of temperature (LE:total energy gain: 2"C, 0.49; 4 ° C 0.5 1; 6OC, 0.50).

Discussion

The fish continued to feed at 2"C, and it was estimated that feeding would be maintained as temperatures approached zero. The results of other studies also show that brown trout forage at low temperature. For example, both Cunjak & Power (1987) and Heggenes et al. (1993) reported that wild brown trout continued feeding throughout the winter even when water temperatures approached zero. In cap-

119

Koskela et al.

tive brown trout, feeding has been observed at 3.8"C (Elliott 1975a) and 2°C (Jensen & Berg 1993).

As has been reported in many other feeding and growth studies on fish (Brett 1979; Jobling 1994), temperature was found to influence the feed intake of brown trout, and there was almost a threefold increase in consumption as temperature increased from 2°C to 6°C. The feed intake recorded in our experiment was, in terms of energy, from two (at 6°C) to four (at 2°C) times higher than that predicted by the feed intake model developed by Elliott (1976a). These differences could be the result of differences in the protocols used in the different experiments. Holding fish in groups and feeding a high- energy diet by means of automatic feeders (present experiment) may have provided the fish with better feeding and growth conditions than keeping single fish in tanks and feeding them several times per day by hand (Elliott's experiment). The possibility that the differences arose because the fish used in the two studies differed in nutritional status, or were of different genetic stock cannot be excluded.

In our experiment we exposed the fish to continuous light. There is little information about the effects of light conditions on behavior of brown trout, but Heggenes et al. (1993) found that small trout (<25 cm) were seldom active during daylight hours in the winter, whereas larger trout (25-60 cm) were active both during the night and day. Similarly, Grif- fith & Smith (1993) reported that juvenile brown trout were predominantly night-active during the winter months. Young Atlantic salmon (Salrno salar L.) have been shown to be mainly night-active at low temperatures (Fraser et al. 1995). If this is also the case for brown trout (Griffith & Smith 1993), our results might underestimate the potential appe- tite and growth of fish at low temperatures.

Brown trout in all groups were able to consume sufficient feed to maintain positive rates of growth (Fig. 1), and the lower threshold for growth was estimated to be approximately 0-0.6"C. This differs from the results of earlier studies, in which the lower thermal limits for growth have been reported to be 3.6-6°C (Wingfield 1940; Elliott 1975b; Elliott et al. 1995). Also the growth rates of our fish were appreciably higher at 4 and 6°C than those reported for brown trout by Elliott and co-workers (Elliott 1975b; Elliott et al. 1995). The difference in growth limits and growth rates between studies is obviously related to differences in feed intake; our fish ate more than did those in previous studies, and, conse- quently, they had more energy available for anabolic processes and could grow faster at any given temperature.

Cunjak & Power (1987) reported that the condition of wild brown trout (5-250 g) declined during

the early part of the winter and then remained stable until spring. This contrasts with the observations made in this study in which condition increased with time (Table 1). An increase in CF is generally assumed to reflect an improvement in nutritional status, whereas a decline in CF may be related to malnutrition but can also be associated with seasonal anorexia (Tveiten et a]. 1996) or with ontoge- netic changes such as the parr-smolt transformation or maturation (Weatherley & Gill 1987; Wootton 1990).

Lipids in wild brown trout may be mobilized during the winter months because the percentage body lipid has been found to decrease during the early winter (Cunjak 1988). This could arise because of limited food availability, or possibly as a result of a self-imposed anorexia under conditions in which there may be risk of predation (Bull et al. 1996). In laboratory populations, on the other hand, percentage body lipid has been found to remain stable at low temperatures (Elliott 1976b). In our study the fish in all temperature groups increased in both total (Fig. 2A), and percentage body lipid (Table 2). Thus, there was no evidence of a marked mobiliza- tion of lipids in any treatment group, and approximately half of the energy gain was due to the deposition of lipid (Fig. 2B). The deposition of lipid stores is influenced by several factors, but there is a general trend for percentage body lipid to increase with increasing fish size and with increasing feed supply. Any increase in the percentage of lipid is usually accompanied by a decrease in percentage body water (Reinitz 1983; Jobling 1994; Shearer 1994). The results of the present study are in general in accordance with this: the fish held at 6"C, which had the highest relative lipid content at the end of the study (Table 2), were those that had consumed the most food and had gained the most in body weight (Table 1, Fig. 2) and they were also the fish that had the lowest percentage body water (Table 2).

Our results show that hatchery-reared brown trout are well adapted to survive under low temperature conditions. The fish were able to consume sufficient food to maintain positive rates of growth, increase condition factor and deposit lipid stores even at the lowest test temperature. The finding that the relative contribution of lipid to energy gain was similar at all three test temperatures may indicate that temperatures as low as 2°C may not be particularly stressful to brown trout raised in the hatchery environment.

Resumen

1. Hemos estudiado la ingesti6n de alimento, la tasa de crecimiento especifico y 10s cambios en la composicidn corporal

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de truchas de edad 1+ (14CL190 g) criadas a tres temperaturas diferentes (2,4 y 6°C) bajo condiciones continuas de luz. 2. La ingesti6n de alimento aumentd desde 35.7 k J . k g - ' d a 2°C hasta 95.7 kJ.kg-'.d-'a 6"C, y la tasa de crecimiento aumentd desde 0.19% 6' hasta 0.42% d-' en el mismo rango de temperatura. Los limites menores de temperatura estimados para la ingestidn de alimento y el crecimiento fueron ligera- mente superiores a 0°C. 3. Hemos constatado que para todos 10s grupos de peces la mayor parte del aumento de peso (aprox. un 75%), se debi6 a1 agua y las proteinas, aunque 10s dephitos de grasa tendieron a aumentar a1 aumentar la temperatura. Para todas las temperaturas, la acumulaci6n de lipidos representa aprox. 50% de la ener- gia corporal ganada.

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Growth and feeding responses of a hatchery population of brown trout (Salmo trutta L.) at low temperatures