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Fitness-related effects of growth investment in brown trout under field ... Uppsala University, S-752 36 Uppsala, Sweden and ‡Institute of Freshwater Research,.
Journal of Fish Biology (2000) 57, 326–336 doi:10.1006/jfbi.2000.1305, available online at http://www.idealibrary.com on

Fitness-related effects of growth investment in brown trout under field and hatchery conditions J. I. J*¶, E. J¨ *, E. P†, T. J¨ ‡  B. T. B¨ * *Department of Zoology, Go¨teborg University, Box 463, SE-405 30 Go¨teborg, Sweden; †Laboratory of Streamwater Ecology, National Board of Fisheries, S-810 70 A } lvkarleby, Sweden and Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University, S-752 36 Uppsala, Sweden and ‡Institute of Freshwater Research, S-170 11 Drottningholm, Sweden and Department of Zoology, Stockholm University, S-106 91 Stockholm, Sweden (Received 2 December 1999, Accepted 20 March 2000) The mortality of brown trout Salmo trutta over winter in a near-natural stream was not significantly increased by growth hormone (GH) treatment, but lipid reserves were lower in GH-treated fish. As GH-treated trout grew faster than controls, GH appears to promote growth at the expense of investment in maintenance. However, the growth promoting effect of GH was much more pronounced in the hatchery than in the stream, suggesting that the pay-off associated with increased growth investment is higher under hatchery conditions with unrestricted food supply than in the wild, where food availability is limited.  2000 The Fisheries Society of the British Isles

Key words: ecology; growth hormone; Salmo trutta; selection; trade-off.

INTRODUCTION In mammals, growth hormone (GH) promotes tissue growth by increasing the rate of cell differentiation and growth (Steele & Evock-Clover, 1993), and available evidence indicates a similar role for GH in salmonid fish (Bjo¨rnsson, 1997). Through these actions, GH increases the metabolic demands, which may result in increased experience of hunger. Consistent with this hypothesis, GH treatment increases growth rate, appetite, aggression and competitive ability (Johnsson & Bjo¨rnsson, 1994; Jo¨nsson et al., 1996, 1998). This suggests that the potential for the GH system to promote faster growth is underutilized. In many animal species, body size is correlated positively with fitness (Roff, 1992), especially in animals with indeterminate growth patterns like fish (Huntingford & Turner, 1987). Larger dominant individuals get prior access to food and territories (Riechert, 1998) and are also generally less susceptible to predation (Werner et al., 1983). Moreover, body size is correlated positively with reproductive success in both males and females of many species (Wootton, 1990; Fleming, 1996). As exogenously administered GH promotes growth, the question arises why the endogenous growth regulatory system is not set to promote maximal growth. Several explanations are possible. Firstly, predation is an ¶Author to whom correspondence [email protected]

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 2000 The Fisheries Society of the British Isles

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important factor driving evolution and structuring populations (Lima & Dill, 1990; Persson et al., 1997). Because GH treatment reduces behavioural responses to predation risk in salmonids in laboratory experiments (Johnsson et al., 1996; Jo¨ nsson et al., 1996), increased GH secretion may result in increased mortality from predation under natural conditions. Moreover, increased endocrine growth stimulation could reduce the probability of surviving harsh periods with low food availability, for instance during winter, by increasing allocation to growth at the expense of declining energy reserves (Sibly & Calow, 1986; Bull et al., 1996; Arendt, 1997). Indeed, laboratory studies have shown that GH treatment reduces lipid content in salmonids (Leatherland & Nuti, 1981; Sheridan, 1986; Weatherley & Gill, 1987; O’Connor et al., 1993). Secondly, the abundance and type of food available varies both spatially and temporally, whereas such variation is absent or reduced in domestic environments (Kohane & Parsons, 1989), where a constantly high supply of food is the rule. Moreover, generally live prey should be more difficult to catch than food pellets. Thus, the increased energetic needs associated with high GH stimulation may not be met under natural conditions. If so, additional GH should be more beneficial for growth in the hatchery environment than in natural streams. Recently developed sustained-release GH formulations allowed these hypotheses to be addressed in a long-term over-winter experiment, where the performance of GH-treated and control brown trout Salmo trutta L., juveniles was compared in two different environments: a near-natural stream section and a standard hatchery rearing tank. MATERIALS AND METHODS The study was carried out from September 1997 to March 1998 at the Fishery Research Station in A } lvkarleby, Sweden, on underyearling (0+) offspring of wild sea trout (four males and four females) from the River Dala¨ lven. Prior to the start of the study the experimental fish were reared at the hatchery according to normal practice. The length and area of the experimental stream in A } lvkarleby is 110 m and 345 m2, respectively, with Wolf traps at both the upper and the lower end. The Wolf trap is a concrete structure through which all water in the stream runs. A system of stainless gratings leads the fish to a collection tank. No trout fry can escape the stream, nor can any competitive or predatory fish invade the system. The stream consists of four pools interspaced by three riffle sections (Fig. 1). During the study, the water flow was 150 l s 1. The ambient temperature regime during the study is given in Fig. 2. The 200 fish used in the study were starved for 24 h before they were sampled from the hatchery tank on 18 September. Each individual was anaesthetized (2-phenoxyethanol, 0·5 ml l 1) and body wet weight (w1) and fork length (l1) were recorded. A small incision was made in the dorsal body wall with a scalpel, whereupon a PIT tag was inserted into the peritoneal cavity to allow individual identification. Then, half of the fish received recombinant bovine growth hormone (rbGH) in a sustained-release GH formulation (Posilac, Monsanto Company), while the other half received excipient only. The gel-like formulation was injected as a depot into the peritoneal cavity through the same incision, using a positive-displacement pipette (Microman 25, Gilson). The volume was 1 l g 1 fish and the GH dose was 0·3 mg rbGH g 1 fish. The fish were allowed to recover from treatment overnight in a flow-through aquarium. The next morning, 75 GH-treated and 75 control trout were released, equally distributed among the four pools in the experimental stream. The density of parr in the stream was 43 individuals (100 m2) 1, which is within the range of natural trout densities in the region (T. Ja¨ rvi, pers. obs.). These fish had access only to the naturally occurring

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Inlet Pool 1

Bridge Run 1

Pool 2

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Pool 3 Bridge

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Pool 4

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F. 1. Schematic view of the experimental stream in A } lvkarleby.

food. For information on important prey taxa in the stream, see Johnsson et al. (1999). The remaining 25 GH-treated and 25 control trout were transferred to an 800-l hatchery tank (120·4 m) supplied with river water at ambient temperature (Fig. 2) and simulated natural photoperiod. These fish were given food pellets (Astra-Ewos) equivalent to 2% of body weight per day throughout the experiment and their weight and length

Temperature (°C)

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13 12 11 10 9 8 7 6 5 4 3 2 1 0 Sep. 1997

Oct. 1997

Nov. 1997

Dec. 1997

Jan. 1998

Feb. 1998

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F. 2. Water temperature during the experiment.

were measured every 30 days. Thus, the performance of four treatment groups could be compared: (i) control trout in the stream (CS); (ii) GH-treated trout in the stream (GHS); (iii) Control trout in the hatchery (CH); (iv) GH-treated trout in the hatchery (GHH). During the study, the two Wolf traps were checked daily. No fish were caught in the downstream trap and only four (three control and one GH-treated trout) in the upstream trap. Signs of predators were noted also. Mink Mustela vison and herons Ardea cinerea, and their traces were frequently observed. As recaptured fish generally were in good physical condition and migration was prevented by the traps, we assumed that predation was the main cause of mortality in the study. On 25 March, the stream was drained slowly and the fish were caught carefully by hand-netting (for details on the sampling method, see Johnsson et al., 1999). Each recovered fish was scanned with a PIT-tag reader for identity. Then the fish were transported back to the hatchery and allowed to recover from the capture overnight in a flow-through aquarium. The following day all experimental fish from the stream and hatchery were killed with a blow to the head whereupon weight (w2) and fork length (l2) were determined and blood was sampled from the caudal vessels using a heparinized syringe. Plasma was obtained by centrifugation (5000 g, 3 min) and stored at 80 C for subsequent GH analysis and the carcass was stored at 80 C until subsequent lipid analysis and dry : wet weight ratio measurement. For dry and wet weight analyses, a cut was made from the base of the dorsal fin down to the middle of the abdomen and a piece of muscle removed that had the same width as the dorsal fin. The muscle pieces were weighed, dried at 60 C for 3 days and weighed again to the nearest 0·001 g. Endogenous plasma growth hormone levels were measured using a salmon GH-radioimmunoassay (Bjo¨ rnsson et al., 1994). Lipid content of muscle and liver was analysed by subjecting 0·5–1 g tissue pieces to homogenization and methanol/chloroform extraction. The chloroform phase was then transferred to preweighed tubes, the chloroform evaporated under nitrogen, the tubes re-weighed, and the lipid content calculated as % weight of the tissue analysed. Specific growth rates for weight (Gw) and length (Gl) were calculated as 100[log (w2*w11) or log (l2*l11)](d2 d1) 1 where (d2 d1) is measurement interval in days (Ricker, 1979). Condition factor (CF) was estimated as (100w*l 3) for both initial and final size. For the analyses of growth and condition factor a two-way ANOVA (adjusting for unequal sample size) was conducted with the independent class variables treatment (C or GH) and environment (S or H) and their interaction. As previous studies have found positive correlations between size and lipid levels and between size and dry : wet weight ratio (Elliott, 1976), these variables were analysed with a two-way ANCOVA, with initial

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T I. Size measurements and final endogenous GH levels (mean..) in control (C) and GH-treated (GH) brown trout reared in a stream or hatchery environment

Initial weight (g) Initial length (cm) Initial CF Final weight Final length Endogenous GH (ng ml 1)

C/stream

GH/stream

C/hatchery

GH/hatchery

9·22 (0·39)a 9·20 (0·12)a 1·13 (0·01)a 14·97 (0·80)a 11·36 (0·20)a 1·38 (0·28)a

8·31 (0·35)a 8·95 (0·12)a 1·11 (0·01)a 15·25 (1·00)a 11·75 (0·23)a 1·34 (0·30)a

7·85 (0·55)a 8·80 (0·19)a 1·12 (0·02)a 18·84 (1·55)a 11·94 (0·28)a 0·48 (0·08)b

8·77 (0·54)a 9·12 (0·18)a 1·12 (0·01)a 35·31 (1·91)b 14·37 (0·25)b 0·42 (0·17)b

Means paired by the same superscript are not significantly different at the 0·05 level (Tukey multiple comparison test).

length added as a covariate (Wilkinson, 1989). Fish were used as primary sample units (for a recent discussion, see Bart et al., 1998).

RESULTS The mortality in the experimental stream did not differ significantly between GHS trout (48%) and CS trout (36%) (21 =2·2, P=0·14), nor did initial weight, length or condition factor (P>0·05 in all cases; Table I). Surviving trout (GHS and CS trout combined) were larger initially than trout that died during the experiment [initial weight (mean..)=10·03·4 g v. 7·62·6 g, respectively; t=4·8, P