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Wild and hatchery-reared brown trout, Salmo trutta, differ in smolt related characteristics during parr–smolt transformation
Aquaculture 167 Ž1998. 53–65
Wild and hatchery-reared brown trout, Salmo trutta, differ in smolt related characteristics during parr–smolt transformation Kristina Sundell a
a,)
, Claes Dellefors b, Bjorn ¨ Th. Bjornsson ¨
a
Fish Endocrinology Laboratory, Department of Zoology, Goteborg UniÕersity, Box 463, SE-405 30, ¨ Goteborg, Sweden ¨ b Department of Zoology, Goteborg UniÕersity, Box 463, SE-405 30, Goteborg, Sweden ¨ ¨ Accepted 24 April 1998
Abstract Morphological changes during parr–smolt transformation are generally less apparent in hatchery-reared than wild salmonids. The aim of the present study was to investigate possible differences between wild and hatchery-reared brown trout in regard to physiological characteristics during smoltification. Plasma growth hormone levels, hypoosmoregulatory ability, gill Naq, Kq-ATPase activity and condition factor were compared between wild and hatchery-reared fish from the same river stock, in two different streams on the Swedish coast. Plasma growth hormone levels were consistently higher in wild compared with hatchery-reared trout, and the growth hormone levels increased in wild fish from one of the streams after a 24 h seawater challenge test. At the time of parr–smolt transformation, there was a peak in gill Naq, Kq-ATPase activity, which coincided with the lowest plasma sodium levels. Wild fish possessed consistently higher gill Naq, Kq-ATPase activity and lower plasma sodium levels compared with hatchery-reared fish. The condition factor of wild fish decreased throughout the smoltification period, in both river strains, whereas the hatchery-reared fish had consistently high condition factor. It is concluded that the artificial environment of hatchery-reared anadromous brown trout can depress the natural parr–smolt transformation, and that this may adversely affect the success of seawater migration and long-term survival of the fish. q 1998 Elsevier Science B.V. All rights reserved. Keywords: Smoltification; Plasma growth hormone levels; Naq, Kq-ATPase activity; Seawater challenge test; Migration patterns; Teleost
)
Corresponding author. Tel.: q46-31-7733671; Fax: q46-31-7733807; E-mail: [email protected]
0044-8486r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 9 8 . 0 0 2 8 0 - 4
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1. Introduction Brown trout Ž Salmo trutta. show a wide variation in morphology and life history. In anadromous populations, often termed sea trout, males frequently mature as parr, and the age of smoltification as well as first spawning varies greatly both within and between populations ŽL’Abee-Lund et al., 1989.. ´ Ž . Jensen 1968 and Berg and Jonsson Ž1989. reported a 30–40% survival rate from smolt migration to first spawning, and a more than 50% survival rate for repeat spawners in wild brown trout strains from two Norwegian rivers. The proportion of smolts, and the number and age-composition of spawners indicate a similar population composition of wild brown trout in the stream Norumsan ˚ in SW Sweden ŽC. Dellefors, . unpublished data . Available information for hatchery-produced smolts indicates that these have a lower survival rate. In Scandinavia, total recapture rates of hatchery-produced anadromous trout vary from 0% to 20% ŽJonsson et al., 1994; Anon, 1995.. In Sweden, such recapture rates are three times higher in streams emerging into the Baltic Sea Žaverage 7.5%; n s 132. as in those emerging on Swedish west coast Žaverage 2.5%; n s 15. ŽAnon, 1995.. Furthermore, the brown trout migrating into the southern parts of the Baltic sea show a higher growth rate and a larger size at sexual maturity than do the strains migrating out on the Swedish west coast, entering the Atlantic Kattegatt. The recapture rates from hatchery releases depend, among other things, on the performance of the fish during the parr–smolt transformation. This process includes physiological, morphological and behavioral changes which must be temporally synchronized to produce functional smolts. The coordination of the developmental processes is governed by environmental cues such as photoperiod, temperature and water flow ŽHoar, 1976, 1988; Folmar and Dickoff, 1980; Wedemeyer et al., 1980; McCormick and Saunders, 1987; Boeuf, 1993; Bjornsson et al., 1995.. The absence of these ¨ cues or distress that suppresses their response may lead to unsuccessful smoltification, which reduces long-term survival rates and thus, reduces the return rates and the reproductive success ŽMoran ´ et al., 1991.. One of the questions addressed in this study is if the generally lower recapture rates of hatchery-released trout compared with wild trout, can be explained by an incomplete smoltification, as a result of the artificial hatchery environment. The other question addressed is if there are differences in the development of hypoosmoregulatory ability between two anadromous brown trout strains, which have different life histories in terms of feeding and migration pattern ŽSvardsson and Fagerstrom, ¨ ¨ 1982; Aro, 1989.. Therefore, hatchery-raised smolts, were compared with naturally produced smolts, in two streams, one entering the Baltic Sea and the other entering the Atlantic Kattegatt. The comparisons were made with respect to development of seawater tolerance, levels of plasma growth hormone ŽGH., gill Naq, Kq-ATPase activity and condition factor during the parr–smolt transformation. In addition, the migration tendencies of the hatchery-released trout were recorded.
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2. Materials and methods 2.1. Fish 2.1.1. Stream Nybroan ˚ 2.1.1.1. Study site and population data. Stream Nybroan ˚ is located in the Southernmost part of Sweden Ž56862X N, 13880X E.. It is supplied by spring water and has a drainage area of 313 km2 and a yearly mean discharge of about 4 m3rs. The stream is very rich in nutrients and has a high conductivity Ž64 mSrm.. The salinity in the Baltic Sea outside the river is about 8‰. A trap run by the local sport fishing society ŽYSS; Ystadortens Fiskevard ˚ och . is located 3 km from the outlet. The trap catches all downstreamSportfiskeforening ¨ and upstream-migrating trout, except at extreme floods. The trap is in use from mid-April to the beginning of June catching smolts and from late August to the beginning of January catching spawners. The smolt age of stream Nybroan ˚ trout is one or two years ŽEklov ¨ and Olsson, 1994. and the average number of natural smolts recorded per year Ž1979–1990. is 2708, ranging from 410 to 6643. The corresponding number of ascending spawners is 1384, ranging from 307 to 3965, with a female:male ratio of 61:39% Ž n s 16 614. and a mean weight of 2.46 kg and 2.18 kg for females and males, respectively Žunpublished data by YSS.. 2.1.1.2. Rearing and releasing. Ascending spawners were caught in the trap and fertilized eggs were transferred to the Linderod ¨ hatchery, a small hatchery specializing in enhancement of local strains of salmonids, 50 km north of the trap, where the juveniles were raised. During the first year, the trout were raised in square 1 m2 indoor tanks and subjected to natural light conditions. During the second year, until release, the trout were kept in covered, circular, 25 m2 concrete tanks with simulated natural photoperiod. The fish were reared under an ad libitum feeding regime and in spring water from the same source as supplies stream Nybroan ˚ with a temperature minimum of 48C in winter and a maximum of 188C in summer. On April 27th, 1989, 300 fish were tagged with Carlin-tags, and released 9 days later 4 km upstream of the trap. This procedure was repeated in 1990 and 1991 when the release dates were April 15th and May 8th and the released numbers of fish were 493 and 446, respectively. 2.1.2. Stream Norumsan ˚ 2.1.2.1. Study site and population data. Stream Norumsan ˚ is located in SW Sweden Ž58803X N, 11849X E. has a drainage area of 12 km2 and a yearly mean discharge of 0.2 m3rs. The stream is rich in nutrients and has a conductivity of 28 mSrm. The ocean salinity outside the stream is about 22‰. Outgoing smolts are caught in a trap situated 400 m from the mouth of the stream. The trap catches all smolt sized trout Ž) 90 mm., except during extreme floods. The smolt age is mainly 2 years. On average Ž1983–1991, 1993., 1533 smolts have been
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caught each year, with annual catch ranging from 306 to 3750. Ascending spawners are not counted as the trap only catches downstream migrants. However, 641 adult upstream migrants have been caught by electric fishing in the years 1991–1994. Of these, 59% were females with a mean weight of 674 g and 41% were males with a mean weight of 424 g. 2.1.2.2. Rearing and releasing. On October 17, 1988, sea-run spawners were caught by electric fishing. The fertilized eggs were transferred to a hatchery in Trollhattan, 50 km ¨ to the north of the stream. This hatchery is run by the Swedish Agricultural Society and is used for local stocking of trout and salmon. The water used in the hatchery originates from Gota ¨ alv, ¨ a river situated in the same region as the experimental stream. The fish were raised under standard rearing conditions with simulated natural photoperiod and ambient water temperature Ž0.5–208C. in square 4 m2 tanks. Trout were released on March 8th and May 2nd 1990, each release consisting of 283 fish. The fish were divided into two categories based on size; fish larger Ž n s 153. or smaller Ž n s 130. than average Žs 183 mm.. The four groups were differently marked with alcyian blue at the base of the caudal fin, and then released 3 km upstream of the trap ŽDellefors and Faremo, 1988.. 2.2. Experimental procedures 2.2.1. Fish handling Wild brown trout were caught by electric fishing. Sampling dates for the two streams are presented in Table 1. The selected size in each stream represented the dominating smolt size, i.e., the selected trout from stream Nybroan ˚ were mainly 1 year old Ž80%. and the trout from stream Norumsan ˚ were 2 years old Ž100%.. The age was assessed by scale reading. The hatchery-reared fish were netted randomly from their rearing tanks. From hereon, both categories of fish were identically handled. The fish were transported in aerated tanks to Goteborg University, and placed in 1 m3 concrete tanks supplied with ¨ partly recirculating freshwater at 108C. All fish were allowed a three-day recovery period before the start of the experiments.
Table 1 The sampling dates and mean length"S.E.M. Ž ns 20., of wild and hatchery-reared brown trout, in stream Nybroan ˚ and stream Norumsan, ˚ respectively Stream Nybroan ˚ Dates Ž1989.
13r4 5r5 16r5 5r6
Stream Norumsan ˚ Total length Žmm. Wild
Hatchery-reared
129.1 Ž6.3. 165.9 Ž6.5. 166.2 Ž3.2. 152.4 Ž4.4.
169.3 Ž3.4. 171.4 Ž3.8. 174.1 Ž3.6. 185.5 Ž3.1.
Dates Ž1990.
Total length Žmm. Wild
Hatchery-reared
12r3 3r4 17r4 8r5 21r5
146.0 Ž4.1. 143.9 Ž2.5. 148.8 Ž3.9. 139.3 Ž2.8. 144.8 Ž3.6.
193.0 Ž6.2. 193.4 Ž3.7. 196.9 Ž5.9. 194.1 Ž3.4. 202.5 Ž5.0.
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2.2.2. Seawater challenge tests Seawater adaptability was assessed using a 24-h seawater challenge test procedure Žafter Blackburn and Clarke, 1987.. Ten fish from each group Žwild and hatchery-reared., were transferred to aerated 50 l aquaria with seawater Ž29‰. at a temperature of 118C. Similarly, ten fish of each category were transferred to 50 l aquaria with fresh water at a temperature of 118C to serve as controls. 2.2.3. Condition factor (CF) Immediately after the seawater challenge test, the control fish Žtransferred from FW to FW for 24 h. were killed by a blow to the head, length Ž L. measured from the tip of the snout to the outer lobe of the tail and weight ŽW . recorded. CF was calculated as 100 WrL3. The mean length" S.E.M. are presented in Table 1. 2.2.4. Blood and tissue sampling For analyses of plasma sodium levels and plasma growth hormone ŽGH. levels, blood was collected from the caudal vein using heparinized syringes. The blood was immediately centrifuged, the plasma frozen and stored at y808C until further analyses. For the determination of gill Naq, Kq-ATPase activity, the gill arches were removed, rinsed and placed in SEI-buffer Ž300 mM sucrose, 20 mM Na 2 EDTA, 50 mM imidazole, pH 7.3. on ice. The primary filaments were removed just above the base of the gill arch, and placed in 800 ml ice-cold SEI-buffer, frozen immediately in liquid nitrogen and stored at y808C until analysis. 2.3. Analyses 2.3.1. Plasma sodium The plasma sodium levels were measured using a flame emission spectrophotometer ŽTurner 510.. 2.3.2. Plasma growth hormone Plasma GH levels were analyzed using a double-antibody sGH RIA following the general protocol of Bolton et al. Ž1986.. Native sGH was used for standards, resulting in a certain overestimation of the absolute levels compared with the later use of recombinant sGH as standards Žcf. Bjornsson et al., 1994.. ¨ 2.3.3. Gill Na q, K q-ATPase actiÕity The gill samples were thawed approximately 5 min prior to being assayed. The buffer was removed and replaced by 700 ml ice-cold SEI-buffer with 0.1% Na-deoxycholate. The samples were then homogenized in a ground-glass homogenizer, the homogenates
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centrifuged at 4500 = g for 30 s, and the supernatant removed and assayed for Naq, Kq-ATPase activity following the kinetic method of McCormick and Bern Ž1989.. The Naq, Kq-ATPase analyses were carried out on material from the Norumsa˚ strain only. 2.3.4. Statistics The condition factor was analysed using two-factorial ANOVA with category Žwild vs. hatchery-reared. and date as orthogonal factors ŽUnderwood, 1997.. All physiological parameters Žplasma sodium levels, plasma growth hormone levels and gill Naq, Kq-ATPase activity. were analysed using three-factorial ANOVA with category, date and salinity as orthogonal factors. In cases where the ANOVA showed significant differences within one factor or interactions between factors, multiple comparisons between means were made using the SNK-test ŽUnderwood, 1997..
3. Results 3.1. Smolt migration In stream Nybroan, ˚ eight descendants of the hatchery-released fish Ž2.7%. were recaptured in the trap in 1989. This was much less than reported for 1990 and 1991 when 19% and 20% were caught, respectively ŽC. Dellefors, unpublished data.. In stream Norumsan, ˚ a total of 9 trout Ž1.6%. were caught in the trap in 1990. Of these, five smolts came from the first, and four from the second hatchery release. Eight out of nine fish had been larger than average size at release. Migration patterns of wild smolts in stream Nybroan ˚ and stream Norumsan, ˚ respectively, are shown in Fig. 1. 3.2. Condition factor (CF) In stream Nybroan ˚ the CF of wild trout decreased throughout the spring Ž p - 0.05; Fig. 2.. The same pattern was indicated in the Norumsa˚ strain but no significant
Fig. 1. Number of wild migrating smolts captured in traps ŽA. placed three km from the outlet of stream Nybroan, ˚ and ŽB. placed 400 m from the outlet of stream Norumsan. ˚
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Fig. 2. Condition factors of wild Ž^. and hatchery-reared Ž`. brown trout during parr–smolt transformation in ŽA. Stream Nybroan ˚ and ŽB. Stream Norumsan. ˚ Each point represents the mean"S.E.M. of 10 fish.
differences between dates were obtained in the ANOVA. The hatchery-reared trout, on the other hand, had almost unchanged CF over time, which were consistently higher than that of the wild fish in both streams Ž p - 0.05; Fig. 2.. 3.3. Seawater challenge test The transfer of fish to seawater for 24 h increased the plasma sodium levels Ž p - 0.05. of both wild and hatchery-reared fish in the two streams. However, the hatchery-reared trout had consistently higher plasma sodium levels Ž p - 0.05. than the corresponding wild individuals ŽFig. 3.. In stream Nybroan, ˚ the plasma sodium levels were higher at the first sampling point Žbeginning of April. than at sampling points 3 and 4 Žmid-May and beginning of June. but lower than at sampling point 2 Žbeginning of May. for both wild and hatchery-reared fish challenged to seawater for 24 h Ždate
Fig. 3. Plasma sodium levels of wild Ž^, '. and hatchery-reared Ž`, v . brown trout during parr–smolt transformation in ŽA. Stream Nybroan ˚ and ŽB. Stream Norumsan. ˚ Open symbols represent the control groups, transferred from FW to FW, whereas filled symbols represent groups transferred from FW to SW for 24 h. Each point represents the mean"S.E.M. of 10 fish.
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Fig. 4. Plasma growth hormone ŽGH. levels of wild Ž^, '. and hatchery-reared Ž`, v . brown trout during parr–smolt transformation in ŽA. Stream Nybroan ˚ and ŽB. Stream Norumsan. ˚ Open symbols represent the control groups, transferred from FW to FW, whereas filled symbols represent groups transferred from FW to SW for 24 h. Each point represents the mean"S.E.M. of 10 fish.
2 ) 1 ) 3 and 4; p - 0.05.. For the control fish Žtransferred to FW. there were no differences in plasma sodium levels with time among the wild fish, whereas the hatchery-reared fish showed higher plasma sodium levels at sampling point 2 than at the other sampling points Ž p - 0.05; Fig. 3A.. No differences in plasma sodium levels with time could be demonstrated by the post-hoc testing in stream Norumsan ˚ ŽFig. 3B.. 3.4. Plasma growth hormone (GH) Plasma GH levels were higher in wild trout compared with hatchery-reared trout Ž p - 0.05. from both stream Nybroan ˚ and stream Norumsan ˚ ŽFig. 4.. The ANOVA revealed no differences over time in either of the two strains. However, a tendency
Fig. 5. Gill Naq, Kq-ATPase activities of wild Ž^, '. and hatchery-reared Ž`, v . brown trout during parr–smolt transformation in Stream Norumsan. ˚ Open symbols represent the control groups, transferred from FW to FW, whereas filled symbols represent groups transferred from FW to SW for 24 h. Each point represents the mean"S.E.M. of 10 fish.
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towards increased plasma GH levels from mid-April throughout the study is indicated in both strains ŽFig. 4.. Plasma GH levels increased in wild fish from stream Norumsan ˚ after seawater challenge test Ž p - 0.05; Fig. 4B.. This was not seen in the hatchery-reared fish ŽFig. 4B. nor in any of the fish from stream Nybroan ˚ ŽFig. 4A.. 3.5. Gill Na q, K q-ATPase actiÕity, Norumsa˚ strain The wild trout displayed changes in gill Naq, Kq-ATPase activity throughout the sampling period, with higher activity in mid-March, followed by a decrease in early April. Thereafter, the activity increased again in mid-April and May Žsampling points 1, 4 and 5 ) 2 and 3; p - 0.05., coinciding with the smolt run ŽFig. 5.. The gill Naq, Kq-ATPase activity was consistently higher in wild trout compared with hatchery-reared fish Ž p - 0.05., and there were no differences between fish exposed to seawater challenge tests compared with the control trout ŽFig. 5..
4. Discussion The wild brown trout of both the Nybroan ˚ and the Norumsan ˚ strains exhibited parr–smolt transformation patterns well in agreement with other studies on smolting salmonids ŽMcCormick and Saunders, 1987; Bjornsson et al., 1989, 1995; Boeuf et al., ¨ 1989; Prunet et al., 1989; Schmitz et al., 1994.. They reached a maximum in hypoosmoregulatory ability concomitant with a decrease in condition factor and a tendency for elevated plasma GH levels, towards the peak of the smolt run. In both strains, the hatchery-reared brown trout showed less developed smolt-related characters than the corresponding wild trout. The hatchery-reared fish had lower hypoosmoregulatory ability, demonstrated by higher plasma sodium levels after a 24 h seawater challenge test and lower gill Naq, Kq-ATPase activity. Furthermore, the hatchery-reared trout had lower plasma GH levels, without any marked elevations during the parr–smolt transformation, together with high and unchanging condition factor. A similar pattern has been shown for Atlantic salmon where there were no changes in plasma GH levels of hatchery-reared fish, during the parr–smolt transformation, whereas wild smolts showed a remarkable increase in GH levels ŽMcCormick and Bjornsson, ¨ 1994.. In addition, the migration tendency of the hatchery-reared trout was weak. In stream Norumsan, ˚ the migrating fraction was 1.6% as compared with the estimated 60% in the natural population ŽBohlin et al., 1986.. Thus, the present comparisons between wild and hatchery-reared anadromous brown trout suggest that an artificial rearing environment can depress the natural parr–smolt transformation patterns and inhibit the downstream migration behaviour of the fish. Since the hatchery-reared fish, from both streams, were subjected to essentially the same conditions regarding water chemistry, temperature and photoperiod as the wild fish, it is likely that other rearing conditions are affecting the parr–smolt transformation. The artificial confinement of fish at high densities in rearing tanks, suppresses the natural territorial behavior of juvenile salmonids
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and imposes schooling behaviour from early life stages. The feeding regimes of salmonid hatcheries are normally geared towards maximal or near-maximal growth which is exemplified by the size difference between wild and hatchery-reared fish in the present study. Furthermore, the fish are regularly supplied with dry food of uniform size and shape given at the surface. These hatchery conditions differ radically from those usually encountered in the wild. It is therefore tempting to speculate that these aspects of the rearing process, which cause substantial proximal changes in behavior and growth patterns of the fish, may partly be responsible for the suppressed parr–smolt transformation of the hatchery-reared fish in the present study, and may ultimately be responsible for the decreased migratory success and long-term survival. This is supported by data showing altered foraging behaviour of hatchery-reared Atlantic salmon parr in the wild ŽSosiak et al., 1979., and differences in anti-predator behaviour between wild and hatchery-reared juvenile brown trout ŽJohnsson et al., 1996.. The trout in stream Nybroan ˚ showed a variation in hypoosmoregulatory ability with time. Both wild and hatchery-reared trout displayed high plasma sodium levels at the beginning of April, the levels peaked at the beginning of May, and then reached a minimum in mid-May and beginning of June, concomitant with the smolt-run. No such variation in plasma sodium levels with time could be demonstrated among the fish in stream Norumsan. ˚ However, the gill Naq, Kq-ATPase activity, of the trout in stream Norumsan, ˚ increased towards the end of the study concomitant with the smolt-run, which indicates that there was an improvement in the hypoosmoregulatory ability also of these fish. Direct comparisons among different species, strains, streams and years are difficult due to differences in, e.g., environmental and climatic conditions. However, the two strains of brown trout examined in the present study represent two different life history strategies, which may help to explain the presented data. The trout in stream Nybroan, ˚ as well as other strains in SouthEast Sweden, are large at sexual maturity and migrate over long distances ŽSvardsson and Fagerstrom, ¨ ¨ 1982; Aro, 1989., whereas the trout in stream Norumsan ˚ seem to be similar to the Norwegian stocks of brown trout, with smaller size at sexual maturity and a short seawater migration ŽL’Abee-Lund et al., ´ 1989.. Thus, in regard to their life histories, the brown trout of the Nybroa˚ strain appear more similar to the Atlantic salmon Ž S. salar ., than to Scandinavian brown trout in general ŽL’Abee-Lund et al., 1989.. Tanguy et al. Ž1994. identified morphological and ´ physiological characters associated with smolting in hatchery-reared resident and anadromous brown trout, and anadromous Atlantic salmon. They concluded that the parr–smolt transformation is most developed in Atlantic salmon, less developed in anadromous brown trout, and lacking in resident trout Žsee also Soivio et al., 1989.. In the present study, the brown trout from the Nybroa˚ strain showed more pronounced smolt characters regarding all physiological parameters measured, compared with the Norumsa˚ strain. Thus, brown trout strains of southeast Sweden, with life history similar to the Atlantic salmon, probably also resemble that species, in their physiological smolt characteristics, more than they resemble other anadromous brown trout populations. This is further supported by the tendency for elevated plasma GH levels of wild brown trout from the Nybroa˚ strain which is in accordance with previous data reported for Atlantic salmon ŽBjornsson et al., 1989, 1995; Boeuf et al., 1989; Prunet et al., 1989; Stefansson ¨ et al., 1991; McCormick et al., 1995., whereas the plasma GH profiles measured in the
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Norumsa˚ strain more resemble the pattern demonstrated for wild anadromous brown trout from the river Orne in Normandy ŽTanguy et al., 1994.. In the stream Norumsan, ˚ the timing of smolt migration and seawater adaptability vary considerably between years ŽBohlin et al., 1993; Dellefors, 1996.. In 1990, the temperature in this stream was unusually high in early spring Žmid-March. and decreased again in early April, a temperature pattern which prolonged the migration period ŽBohlin et al., 1993.. During the parr–smolt transformation of Atlantic salmon, two groups of fish were subjected either to ambient temperature Žranging from 18C, in February, to 128C, in May. or to 108C. In that study, the high temperature group showed increased gill Naq, Kq-ATPase activity, already in February, while the group reared at ambient Žlower. temperature did not show such an increase. This difference in gill Naq, Kq-ATPase activity was sustained until the beginning of April when the ambient temperature had increased to approximately 68C ŽS.D. McCormick pers. com... Thus, the high temperature in mid-March, in the present study, may explain the unexpectedly high gill Naq, Kq-ATPase activity measured at that time. When the water temperature decreased again in beginning of April, so did the gill Naq, Kq-ATPase activity. From April, there was a pattern of normal temperature increase together with an increase in gill Naq, Kq-ATPase activity, which is similar to other salmonids during spring parr–smolt transformation ŽBjornsson et al., 1989; Boeuf et al., 1989; Prunet et al., 1989; Nance et al., 1990; ¨ Tanguy et al., 1994; McCormick et al., 1995.. No difference in gill Naq, Kq-ATPase activity was demonstrated between the brown trout exposed to seawater for 24 h compared with the fish retained in FW. Even though environmental salinity is a cue well known to increase chloride cell number as well as gill Naq, Kq-ATPase activity in most teleost species examined Žsee McCormick and Saunders, 1987; McCormick, 1995., the present study supports earlier data on brown trout and other salmonids that 24 h of seawater exposure is not long enough time to increase gill Naq, Kq-ATPase activity ŽBoeuf et al., 1989; Madsen and Naamansen, 1989; McCormick et al., 1989; Madsen, 1990; Almendras et al., 1993; Berge et al., 1994.. The present study demonstrates that hatchery-reared brown trout can show disturbances in their parr–smolt transformation compared with wild brown trout of the same strains. Furthermore, the study suggests that the pattern of physiological and behavioral Žmigratory. events taking place during the parr–smolt transformation of anadromous salmonids are not only dependent on the species, but may be strongly modified by the life history of the individual. Thus, conclusions concerning inter- and intra-specific differences in smoltification, especially those that are based on studies of hatchery-reared fish, must be viewed with caution, and more studies concerning the differences between hatchery-reared and wild salmonids are needed.
Acknowledgements We would like to thank Mr. Goran Persson at Ystadsortens Fiskevard ¨ ˚ och Sportfiskeforening for sharing their records about the fish caught in the trap of stream ¨ Nybroan. ˚ We thank Ulo Faremo for his help in fish handling and sampling, and Gunilla
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¨ Eriksson and IngaMaj Orbom for excellent technical assistance. This study was supported by the Swedish Council for Forestry and Agricultural Research and the C.F. Lundstrom ¨ Foundation. References Almendras, J.M.E., Prunet, P., Boeuf, G., 1993. Response of a non-migratory stock of brown trout, Salmo trutta, to ovine growth hormone treatment and seawater exposure. Aquaculture 114, 169–179. Anon, 1995. Laxforskningsinstitutet, ŽSwedish Salmon Research Institute.. Sammanstallningar over ¨ ¨ markningsforsok Summary of returns from releases of tagged sea trout, 1980–1993. ¨ ¨ ¨ med havsoringungar. ¨ Aro, E., 1989. A review of fish migration patterns in the Baltic. Rapp. P.-v. Reun. ´ Cons. int. Explor. Mer. 190, 72–96. Berg, O.K., Jonsson, B., 1989. Growth and survival rates of the anadromous trout Ž Salmo trutta L.. from the Vardnes river, northern Norway. Env. Biol. Fish 29, 145–154. ˚ Berg, A., Fyhn, H.J., Barnung, T., Hansen, T., Stefansson, S.O., 1994. Development of salinity Berge, A.I., tolerance in underyearling smolts of Atlantic salmon Ž Salmo salar . reared under different photoperiods. Can. J. Fish. Aquat. Sci. 52, 243–251. Bjornsson, B.Th., Young, G., Lin, R.J., Deftos, L.J., Bern, H.A., 1989. Smoltification and seawater adaptation ¨ in coho salmon Ž Oncorhynchus kisutch.: Plasma calcium regulation, osmoregulation and calcitonin. Gen. Comp. Endocrinol. 74, 346–354. Bjornsson, B.Th., Taranger, G.L., Hansen, T., Stefansson, S.O., Haux, C., 1994. The interrelation between ¨ photoperiod, growth hormone and sexual maturation of adult Atlantic salmon Ž Salmo salar .. Gen. Comp. Endocrinol. 93, 70–81. Bjornsson, B.Th., Stefansson, S.O., Hansen, T., 1995. Photoperiod regulation of plasma growth hormone ¨ levels during parr–smolt transformation of Atlantic salmon: implications for hypoosmoregulatory ability and growth. Gen. Comp. Endocrinol. 100, 73–82. Blackburn, J., Clarke, W.C., 1987. Revised procedure for the 24 hour seawater challenge test to measure seawater adaptability of juvenile salmonids. Can. Tech. Rep. Fish. Aquat. Sci., No. 1515, 35 pp. Boeuf, G., Le Bail, P.Y., Prunet, P., 1989. Growth hormone and thyroid hormones during Atlantic salmon, Salmo salar L., smolting, and after transfer to seawater. Aquaculture 82, 257–268. Boeuf, G., 1993. Salmonid smolting: a pre-adaptation to oceanic environment. In: Rankin, J.C., Jensen, F.B. ŽEds.., Fish Ecophysiology. Chapman & Hall, London, pp. 106–135. Bohlin, T., Dellefors, C., Faremo, U., 1986. Early sexual maturation of male sea trout and salmon—an evolutionary model and some practical implications. Rep. Inst. Freshw. Res. Drottningholm 63, 17–25. Bohlin, T., Dellefors, C., Faremo, U., 1993. Timing of sea-run brown trout Ž Salmo trutta. smolt migration: effects of climatic variation. Can. J. Fish. Aquat. Sci. 50, 1132–1136. Bolton, J.P., Takahashi, H., Kawauchi, H., Kubota, J., Hirano, T., 1986. Development and validation of a salmon growth hormone radioimmunoassay. Gen. Comp. Endocrinol. 62, 230–238. Dellefors, C., 1996. Smoltification and sea migration in wild and hatchery-reared brown trout, Salmo trutta. PhD Dissertation, Department of Zoology, Goteborg University. ¨ Dellefors, C., Faremo, U., 1988. Early sexual maturation in males of wild sea trout, Salmo trutta L., inhibits smoltification. J. Fish. Biol. 33, 741–749. Eklov, Lan. Lan. ¨ A., Olsson, I., 1994. Havsoringaar ¨ ˚ i Malmohus ¨ ¨ Sea trout streams in Malmohus ¨ ¨ Meddelande 94r9 Lansstyrelsen i Malmohus Lan. ¨ ¨ ¨ In Swedish. Folmar, L.C., Dickoff, W.W., 1980. The parr–smolt transformation Žsmoltification. and seawater adaptation in salmonids. A review of selected literature. Aquaculture 21, 1–37. Hoar, W.S., 1976. Smolt transformation: evolution, behavior and physiology. J. Fish. Res. Brd. Can. 33, 1233–1252. Hoar, W.S., 1988. The physiology of smolting salmonids. In: Hoar, W.S., Randall, D.J. ŽEds.., Fish Physiology, Vol. XI, Part B. Academic Press, San Diego, pp. 275–343. Jensen, K.W., 1968. Sea trout Ž Salmo trutta L.. of the river Istra, western Norway. Rep. Inst. Freshw. Res. Drottningholm 48, 187–213.
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Johnsson, J.I., Pettersson, E., Jonsson, E., Bjornsson, B.Th., Jarvi, T., 1996. Domestication and growth ¨ ¨ ¨ hormone alter antipredator behaviour in juvenile brown trout Salmo trutta. Can. J. Fish Aquat. Sci. 53, 1546–1554. Jonsson, N., Jonsson, B., Hansen, L.P., Aass, P., 1994. Effects of seawater-acclimatization and release sites on survival of hatchery-reared brown trout Salmo trutta. J. Fish. Biol. 44, 973–981. L’Abee-Lund, J.H., Jonnson, B., Jenssen, A.J., Saettem, L.M., Heggberget, T.G., Johnsen, B.O., Naesje, T.F., ´ 1989. Latitude variation in life history characteristics of sea-run migrant brown trout Salmo trutta. J. Anim. Ecol. 58, 525–542. Madsen, S.S., 1990. Enhanced hypoosmoregulatory response to growth hormone after cortisol treatment in immature rainbow trout Salmo gairdneri. Fish Physiol. Biochem. 8, 271–279. Madsen, S.S., Naamansen, E.T., 1989. Plasma ionic regulation and gill NaqrKq-ATPase changes during rapid SW-transfer of rainbow trout Ž Salmo gairdneri .: time course and its seasonal variation. J. Fish Physiol. 34, 829–840. McCormick, S.D., 1995. Hormonal control of gill Naq, Kq-ATPase and Chloride cell function. In: Wood, C.M., Shuttleworth, T.J. ŽEds.., Cellular and Molecular Approaches to Fish Ionic Regulation, 285–316. McCormick, S.D., Saunders, R.L., 1987. Preparatory physiological adaptations for marine life salmonids: osmoregulation, growth and metabolism. Am. Fish Soc. Symp. 1, 211–229. McCormick, S.D., Bern, H.A., 1989. In vitro stimulation of Naq, Kq-ATPase activity and ouabain binding by cortisol in coho salmon gill. Am. J. Physiol. 256, R707–R715. McCormick, S.D., Bjornsson, B.Th., 1994. Physiological and hormonal differences among Atlantic parr and ¨ smolts reared in the wild, and hatchery smolts. Aquaculture 121, 235–244. McCormick, S.D., Moyes, C.D., Ballantyne, J.S., 1989. Influence of salinity on energetics of gill and kidney of Atlantic salmon Ž Salmo salar .. Fish Physiol. Biochem. 6, 243–254. McCormick, S.D., Bjornsson, B.Th., Sheridan, M., Eilertson, C., Carey, J.B., O’Dea, M., 1995. Increased ¨ daylength stimulates plasma growth hormone and gill Naq, Kq-ATPase in Atlantic salmon Ž Salmo salar .. J. Comp. Physiol. B 165, 245–254. Moran, E., Izquierdo, J., 1991. Failure of a stocking policy, of hatchery-re´ P., Pendes, ´ A.M., Garcia-Vazquez, ´ ared brown trout, Salmo trutta L., in Asturias, Spain, detected using LDH-5 a genetic marker. J. Fish Biol. 39, 117–121, Suppl. A. Nance, J.-M., Bornancin, M., Sola, F., Boeuf, G., Dutil, J.-D., 1990. Study of transbranchial Naq exchange in Salmo salar smolts and post-smolts directly transferred to seawater. Comp. Biochem. Physiol. 96A, 303–308. Prunet, P., Boeuf, G., Bolton, J.P., Young, G., 1989. Smoltification and seawater adaptation in Atlantic salmon Ž Salmo salar .: plasma prolactin, growth hormone and thyroid hormones. Gen. Comp. Endocrinol. 74, 355–364. Schmitz, M., Berglund, I., Lundqvist, H., Bjornsson, B.Th., 1994. Growth hormone response to seawater ¨ challenge in Atlantic salmon Salmo salar, during parr–smolt transformation. Aquaculture 121, 209–221. Soivio, A., Muona, M., Virtanen, E., 1989. Smolting of two populations of Salmo trutta. Aquaculture 82, 147–153. Sosiak, A.J., Randall, R.G., McKenzie, J.A., 1979. Feeding by hatchery-reared and wild Atlantic salmon Ž Salmo salar . parr in streams. J. Fish. Res. Board Can. 36, 1408–1412. Stefansson, S.O., Bjornsson, B.Th., Hansen, T., Haux, C., Taranger, G.L., Saunders, R.L., 1991. Growth, ¨ parr-smolt transformation, and changes in growth hormone of Atlantic salmon Ž Salmo salar . reared under different photoperiods. Can. J. Fish. Aquat. 48, 2100–2108. ˚ 1982. Adaptive differences in long-distance migration of some trout Ž Salmo Svardsson, G., Fagerstrom, ¨ ¨ A., trutta. stocks. Rep. Inst. Freshw. Res. Drottningholm. 60, 51–80. Tanguy, J.M., Ombredane, D., Bagliniere, ` J.L., Prunet, P., 1994. Aspects of parr–smolt transformation in anadromous and resident forms of brown trout Ž Salmo trutta. in comparison with Atlantic salmon Ž Salmo salar .. Aquaculture 121, 51–63. Underwood, A.J., 1997. Experiments in Ecology. Cambridge Univ. Press, Cambridge. Wedemeyer, G.A., Saunders, R.L., Clark, W.C., 1980. Environmental factors affecting smoltification and early marine survival of anadromous salmonids. Mar. Fish. Rev. 42, 1–14.
Wild and hatchery-reared brown trout, Salmo trutta, differ in smolt related characteristics during parr–smolt transformation Kristina Sundell a
a,)
, Claes Dellefors b, Bjorn ¨ Th. Bjornsson ¨
a
Fish Endocrinology Laboratory, Department of Zoology, Goteborg UniÕersity, Box 463, SE-405 30, ¨ Goteborg, Sweden ¨ b Department of Zoology, Goteborg UniÕersity, Box 463, SE-405 30, Goteborg, Sweden ¨ ¨ Accepted 24 April 1998
Abstract Morphological changes during parr–smolt transformation are generally less apparent in hatchery-reared than wild salmonids. The aim of the present study was to investigate possible differences between wild and hatchery-reared brown trout in regard to physiological characteristics during smoltification. Plasma growth hormone levels, hypoosmoregulatory ability, gill Naq, Kq-ATPase activity and condition factor were compared between wild and hatchery-reared fish from the same river stock, in two different streams on the Swedish coast. Plasma growth hormone levels were consistently higher in wild compared with hatchery-reared trout, and the growth hormone levels increased in wild fish from one of the streams after a 24 h seawater challenge test. At the time of parr–smolt transformation, there was a peak in gill Naq, Kq-ATPase activity, which coincided with the lowest plasma sodium levels. Wild fish possessed consistently higher gill Naq, Kq-ATPase activity and lower plasma sodium levels compared with hatchery-reared fish. The condition factor of wild fish decreased throughout the smoltification period, in both river strains, whereas the hatchery-reared fish had consistently high condition factor. It is concluded that the artificial environment of hatchery-reared anadromous brown trout can depress the natural parr–smolt transformation, and that this may adversely affect the success of seawater migration and long-term survival of the fish. q 1998 Elsevier Science B.V. All rights reserved. Keywords: Smoltification; Plasma growth hormone levels; Naq, Kq-ATPase activity; Seawater challenge test; Migration patterns; Teleost
)
Corresponding author. Tel.: q46-31-7733671; Fax: q46-31-7733807; E-mail: [email protected]
0044-8486r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 Ž 9 8 . 0 0 2 8 0 - 4
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1. Introduction Brown trout Ž Salmo trutta. show a wide variation in morphology and life history. In anadromous populations, often termed sea trout, males frequently mature as parr, and the age of smoltification as well as first spawning varies greatly both within and between populations ŽL’Abee-Lund et al., 1989.. ´ Ž . Jensen 1968 and Berg and Jonsson Ž1989. reported a 30–40% survival rate from smolt migration to first spawning, and a more than 50% survival rate for repeat spawners in wild brown trout strains from two Norwegian rivers. The proportion of smolts, and the number and age-composition of spawners indicate a similar population composition of wild brown trout in the stream Norumsan ˚ in SW Sweden ŽC. Dellefors, . unpublished data . Available information for hatchery-produced smolts indicates that these have a lower survival rate. In Scandinavia, total recapture rates of hatchery-produced anadromous trout vary from 0% to 20% ŽJonsson et al., 1994; Anon, 1995.. In Sweden, such recapture rates are three times higher in streams emerging into the Baltic Sea Žaverage 7.5%; n s 132. as in those emerging on Swedish west coast Žaverage 2.5%; n s 15. ŽAnon, 1995.. Furthermore, the brown trout migrating into the southern parts of the Baltic sea show a higher growth rate and a larger size at sexual maturity than do the strains migrating out on the Swedish west coast, entering the Atlantic Kattegatt. The recapture rates from hatchery releases depend, among other things, on the performance of the fish during the parr–smolt transformation. This process includes physiological, morphological and behavioral changes which must be temporally synchronized to produce functional smolts. The coordination of the developmental processes is governed by environmental cues such as photoperiod, temperature and water flow ŽHoar, 1976, 1988; Folmar and Dickoff, 1980; Wedemeyer et al., 1980; McCormick and Saunders, 1987; Boeuf, 1993; Bjornsson et al., 1995.. The absence of these ¨ cues or distress that suppresses their response may lead to unsuccessful smoltification, which reduces long-term survival rates and thus, reduces the return rates and the reproductive success ŽMoran ´ et al., 1991.. One of the questions addressed in this study is if the generally lower recapture rates of hatchery-released trout compared with wild trout, can be explained by an incomplete smoltification, as a result of the artificial hatchery environment. The other question addressed is if there are differences in the development of hypoosmoregulatory ability between two anadromous brown trout strains, which have different life histories in terms of feeding and migration pattern ŽSvardsson and Fagerstrom, ¨ ¨ 1982; Aro, 1989.. Therefore, hatchery-raised smolts, were compared with naturally produced smolts, in two streams, one entering the Baltic Sea and the other entering the Atlantic Kattegatt. The comparisons were made with respect to development of seawater tolerance, levels of plasma growth hormone ŽGH., gill Naq, Kq-ATPase activity and condition factor during the parr–smolt transformation. In addition, the migration tendencies of the hatchery-released trout were recorded.
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2. Materials and methods 2.1. Fish 2.1.1. Stream Nybroan ˚ 2.1.1.1. Study site and population data. Stream Nybroan ˚ is located in the Southernmost part of Sweden Ž56862X N, 13880X E.. It is supplied by spring water and has a drainage area of 313 km2 and a yearly mean discharge of about 4 m3rs. The stream is very rich in nutrients and has a high conductivity Ž64 mSrm.. The salinity in the Baltic Sea outside the river is about 8‰. A trap run by the local sport fishing society ŽYSS; Ystadortens Fiskevard ˚ och . is located 3 km from the outlet. The trap catches all downstreamSportfiskeforening ¨ and upstream-migrating trout, except at extreme floods. The trap is in use from mid-April to the beginning of June catching smolts and from late August to the beginning of January catching spawners. The smolt age of stream Nybroan ˚ trout is one or two years ŽEklov ¨ and Olsson, 1994. and the average number of natural smolts recorded per year Ž1979–1990. is 2708, ranging from 410 to 6643. The corresponding number of ascending spawners is 1384, ranging from 307 to 3965, with a female:male ratio of 61:39% Ž n s 16 614. and a mean weight of 2.46 kg and 2.18 kg for females and males, respectively Žunpublished data by YSS.. 2.1.1.2. Rearing and releasing. Ascending spawners were caught in the trap and fertilized eggs were transferred to the Linderod ¨ hatchery, a small hatchery specializing in enhancement of local strains of salmonids, 50 km north of the trap, where the juveniles were raised. During the first year, the trout were raised in square 1 m2 indoor tanks and subjected to natural light conditions. During the second year, until release, the trout were kept in covered, circular, 25 m2 concrete tanks with simulated natural photoperiod. The fish were reared under an ad libitum feeding regime and in spring water from the same source as supplies stream Nybroan ˚ with a temperature minimum of 48C in winter and a maximum of 188C in summer. On April 27th, 1989, 300 fish were tagged with Carlin-tags, and released 9 days later 4 km upstream of the trap. This procedure was repeated in 1990 and 1991 when the release dates were April 15th and May 8th and the released numbers of fish were 493 and 446, respectively. 2.1.2. Stream Norumsan ˚ 2.1.2.1. Study site and population data. Stream Norumsan ˚ is located in SW Sweden Ž58803X N, 11849X E. has a drainage area of 12 km2 and a yearly mean discharge of 0.2 m3rs. The stream is rich in nutrients and has a conductivity of 28 mSrm. The ocean salinity outside the stream is about 22‰. Outgoing smolts are caught in a trap situated 400 m from the mouth of the stream. The trap catches all smolt sized trout Ž) 90 mm., except during extreme floods. The smolt age is mainly 2 years. On average Ž1983–1991, 1993., 1533 smolts have been
K. Sundell et al.r Aquaculture 167 (1998) 53–65
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caught each year, with annual catch ranging from 306 to 3750. Ascending spawners are not counted as the trap only catches downstream migrants. However, 641 adult upstream migrants have been caught by electric fishing in the years 1991–1994. Of these, 59% were females with a mean weight of 674 g and 41% were males with a mean weight of 424 g. 2.1.2.2. Rearing and releasing. On October 17, 1988, sea-run spawners were caught by electric fishing. The fertilized eggs were transferred to a hatchery in Trollhattan, 50 km ¨ to the north of the stream. This hatchery is run by the Swedish Agricultural Society and is used for local stocking of trout and salmon. The water used in the hatchery originates from Gota ¨ alv, ¨ a river situated in the same region as the experimental stream. The fish were raised under standard rearing conditions with simulated natural photoperiod and ambient water temperature Ž0.5–208C. in square 4 m2 tanks. Trout were released on March 8th and May 2nd 1990, each release consisting of 283 fish. The fish were divided into two categories based on size; fish larger Ž n s 153. or smaller Ž n s 130. than average Žs 183 mm.. The four groups were differently marked with alcyian blue at the base of the caudal fin, and then released 3 km upstream of the trap ŽDellefors and Faremo, 1988.. 2.2. Experimental procedures 2.2.1. Fish handling Wild brown trout were caught by electric fishing. Sampling dates for the two streams are presented in Table 1. The selected size in each stream represented the dominating smolt size, i.e., the selected trout from stream Nybroan ˚ were mainly 1 year old Ž80%. and the trout from stream Norumsan ˚ were 2 years old Ž100%.. The age was assessed by scale reading. The hatchery-reared fish were netted randomly from their rearing tanks. From hereon, both categories of fish were identically handled. The fish were transported in aerated tanks to Goteborg University, and placed in 1 m3 concrete tanks supplied with ¨ partly recirculating freshwater at 108C. All fish were allowed a three-day recovery period before the start of the experiments.
Table 1 The sampling dates and mean length"S.E.M. Ž ns 20., of wild and hatchery-reared brown trout, in stream Nybroan ˚ and stream Norumsan, ˚ respectively Stream Nybroan ˚ Dates Ž1989.
13r4 5r5 16r5 5r6
Stream Norumsan ˚ Total length Žmm. Wild
Hatchery-reared
129.1 Ž6.3. 165.9 Ž6.5. 166.2 Ž3.2. 152.4 Ž4.4.
169.3 Ž3.4. 171.4 Ž3.8. 174.1 Ž3.6. 185.5 Ž3.1.
Dates Ž1990.
Total length Žmm. Wild
Hatchery-reared
12r3 3r4 17r4 8r5 21r5
146.0 Ž4.1. 143.9 Ž2.5. 148.8 Ž3.9. 139.3 Ž2.8. 144.8 Ž3.6.
193.0 Ž6.2. 193.4 Ž3.7. 196.9 Ž5.9. 194.1 Ž3.4. 202.5 Ž5.0.
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2.2.2. Seawater challenge tests Seawater adaptability was assessed using a 24-h seawater challenge test procedure Žafter Blackburn and Clarke, 1987.. Ten fish from each group Žwild and hatchery-reared., were transferred to aerated 50 l aquaria with seawater Ž29‰. at a temperature of 118C. Similarly, ten fish of each category were transferred to 50 l aquaria with fresh water at a temperature of 118C to serve as controls. 2.2.3. Condition factor (CF) Immediately after the seawater challenge test, the control fish Žtransferred from FW to FW for 24 h. were killed by a blow to the head, length Ž L. measured from the tip of the snout to the outer lobe of the tail and weight ŽW . recorded. CF was calculated as 100 WrL3. The mean length" S.E.M. are presented in Table 1. 2.2.4. Blood and tissue sampling For analyses of plasma sodium levels and plasma growth hormone ŽGH. levels, blood was collected from the caudal vein using heparinized syringes. The blood was immediately centrifuged, the plasma frozen and stored at y808C until further analyses. For the determination of gill Naq, Kq-ATPase activity, the gill arches were removed, rinsed and placed in SEI-buffer Ž300 mM sucrose, 20 mM Na 2 EDTA, 50 mM imidazole, pH 7.3. on ice. The primary filaments were removed just above the base of the gill arch, and placed in 800 ml ice-cold SEI-buffer, frozen immediately in liquid nitrogen and stored at y808C until analysis. 2.3. Analyses 2.3.1. Plasma sodium The plasma sodium levels were measured using a flame emission spectrophotometer ŽTurner 510.. 2.3.2. Plasma growth hormone Plasma GH levels were analyzed using a double-antibody sGH RIA following the general protocol of Bolton et al. Ž1986.. Native sGH was used for standards, resulting in a certain overestimation of the absolute levels compared with the later use of recombinant sGH as standards Žcf. Bjornsson et al., 1994.. ¨ 2.3.3. Gill Na q, K q-ATPase actiÕity The gill samples were thawed approximately 5 min prior to being assayed. The buffer was removed and replaced by 700 ml ice-cold SEI-buffer with 0.1% Na-deoxycholate. The samples were then homogenized in a ground-glass homogenizer, the homogenates
58
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centrifuged at 4500 = g for 30 s, and the supernatant removed and assayed for Naq, Kq-ATPase activity following the kinetic method of McCormick and Bern Ž1989.. The Naq, Kq-ATPase analyses were carried out on material from the Norumsa˚ strain only. 2.3.4. Statistics The condition factor was analysed using two-factorial ANOVA with category Žwild vs. hatchery-reared. and date as orthogonal factors ŽUnderwood, 1997.. All physiological parameters Žplasma sodium levels, plasma growth hormone levels and gill Naq, Kq-ATPase activity. were analysed using three-factorial ANOVA with category, date and salinity as orthogonal factors. In cases where the ANOVA showed significant differences within one factor or interactions between factors, multiple comparisons between means were made using the SNK-test ŽUnderwood, 1997..
3. Results 3.1. Smolt migration In stream Nybroan, ˚ eight descendants of the hatchery-released fish Ž2.7%. were recaptured in the trap in 1989. This was much less than reported for 1990 and 1991 when 19% and 20% were caught, respectively ŽC. Dellefors, unpublished data.. In stream Norumsan, ˚ a total of 9 trout Ž1.6%. were caught in the trap in 1990. Of these, five smolts came from the first, and four from the second hatchery release. Eight out of nine fish had been larger than average size at release. Migration patterns of wild smolts in stream Nybroan ˚ and stream Norumsan, ˚ respectively, are shown in Fig. 1. 3.2. Condition factor (CF) In stream Nybroan ˚ the CF of wild trout decreased throughout the spring Ž p - 0.05; Fig. 2.. The same pattern was indicated in the Norumsa˚ strain but no significant
Fig. 1. Number of wild migrating smolts captured in traps ŽA. placed three km from the outlet of stream Nybroan, ˚ and ŽB. placed 400 m from the outlet of stream Norumsan. ˚
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59
Fig. 2. Condition factors of wild Ž^. and hatchery-reared Ž`. brown trout during parr–smolt transformation in ŽA. Stream Nybroan ˚ and ŽB. Stream Norumsan. ˚ Each point represents the mean"S.E.M. of 10 fish.
differences between dates were obtained in the ANOVA. The hatchery-reared trout, on the other hand, had almost unchanged CF over time, which were consistently higher than that of the wild fish in both streams Ž p - 0.05; Fig. 2.. 3.3. Seawater challenge test The transfer of fish to seawater for 24 h increased the plasma sodium levels Ž p - 0.05. of both wild and hatchery-reared fish in the two streams. However, the hatchery-reared trout had consistently higher plasma sodium levels Ž p - 0.05. than the corresponding wild individuals ŽFig. 3.. In stream Nybroan, ˚ the plasma sodium levels were higher at the first sampling point Žbeginning of April. than at sampling points 3 and 4 Žmid-May and beginning of June. but lower than at sampling point 2 Žbeginning of May. for both wild and hatchery-reared fish challenged to seawater for 24 h Ždate
Fig. 3. Plasma sodium levels of wild Ž^, '. and hatchery-reared Ž`, v . brown trout during parr–smolt transformation in ŽA. Stream Nybroan ˚ and ŽB. Stream Norumsan. ˚ Open symbols represent the control groups, transferred from FW to FW, whereas filled symbols represent groups transferred from FW to SW for 24 h. Each point represents the mean"S.E.M. of 10 fish.
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Fig. 4. Plasma growth hormone ŽGH. levels of wild Ž^, '. and hatchery-reared Ž`, v . brown trout during parr–smolt transformation in ŽA. Stream Nybroan ˚ and ŽB. Stream Norumsan. ˚ Open symbols represent the control groups, transferred from FW to FW, whereas filled symbols represent groups transferred from FW to SW for 24 h. Each point represents the mean"S.E.M. of 10 fish.
2 ) 1 ) 3 and 4; p - 0.05.. For the control fish Žtransferred to FW. there were no differences in plasma sodium levels with time among the wild fish, whereas the hatchery-reared fish showed higher plasma sodium levels at sampling point 2 than at the other sampling points Ž p - 0.05; Fig. 3A.. No differences in plasma sodium levels with time could be demonstrated by the post-hoc testing in stream Norumsan ˚ ŽFig. 3B.. 3.4. Plasma growth hormone (GH) Plasma GH levels were higher in wild trout compared with hatchery-reared trout Ž p - 0.05. from both stream Nybroan ˚ and stream Norumsan ˚ ŽFig. 4.. The ANOVA revealed no differences over time in either of the two strains. However, a tendency
Fig. 5. Gill Naq, Kq-ATPase activities of wild Ž^, '. and hatchery-reared Ž`, v . brown trout during parr–smolt transformation in Stream Norumsan. ˚ Open symbols represent the control groups, transferred from FW to FW, whereas filled symbols represent groups transferred from FW to SW for 24 h. Each point represents the mean"S.E.M. of 10 fish.
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towards increased plasma GH levels from mid-April throughout the study is indicated in both strains ŽFig. 4.. Plasma GH levels increased in wild fish from stream Norumsan ˚ after seawater challenge test Ž p - 0.05; Fig. 4B.. This was not seen in the hatchery-reared fish ŽFig. 4B. nor in any of the fish from stream Nybroan ˚ ŽFig. 4A.. 3.5. Gill Na q, K q-ATPase actiÕity, Norumsa˚ strain The wild trout displayed changes in gill Naq, Kq-ATPase activity throughout the sampling period, with higher activity in mid-March, followed by a decrease in early April. Thereafter, the activity increased again in mid-April and May Žsampling points 1, 4 and 5 ) 2 and 3; p - 0.05., coinciding with the smolt run ŽFig. 5.. The gill Naq, Kq-ATPase activity was consistently higher in wild trout compared with hatchery-reared fish Ž p - 0.05., and there were no differences between fish exposed to seawater challenge tests compared with the control trout ŽFig. 5..
4. Discussion The wild brown trout of both the Nybroan ˚ and the Norumsan ˚ strains exhibited parr–smolt transformation patterns well in agreement with other studies on smolting salmonids ŽMcCormick and Saunders, 1987; Bjornsson et al., 1989, 1995; Boeuf et al., ¨ 1989; Prunet et al., 1989; Schmitz et al., 1994.. They reached a maximum in hypoosmoregulatory ability concomitant with a decrease in condition factor and a tendency for elevated plasma GH levels, towards the peak of the smolt run. In both strains, the hatchery-reared brown trout showed less developed smolt-related characters than the corresponding wild trout. The hatchery-reared fish had lower hypoosmoregulatory ability, demonstrated by higher plasma sodium levels after a 24 h seawater challenge test and lower gill Naq, Kq-ATPase activity. Furthermore, the hatchery-reared trout had lower plasma GH levels, without any marked elevations during the parr–smolt transformation, together with high and unchanging condition factor. A similar pattern has been shown for Atlantic salmon where there were no changes in plasma GH levels of hatchery-reared fish, during the parr–smolt transformation, whereas wild smolts showed a remarkable increase in GH levels ŽMcCormick and Bjornsson, ¨ 1994.. In addition, the migration tendency of the hatchery-reared trout was weak. In stream Norumsan, ˚ the migrating fraction was 1.6% as compared with the estimated 60% in the natural population ŽBohlin et al., 1986.. Thus, the present comparisons between wild and hatchery-reared anadromous brown trout suggest that an artificial rearing environment can depress the natural parr–smolt transformation patterns and inhibit the downstream migration behaviour of the fish. Since the hatchery-reared fish, from both streams, were subjected to essentially the same conditions regarding water chemistry, temperature and photoperiod as the wild fish, it is likely that other rearing conditions are affecting the parr–smolt transformation. The artificial confinement of fish at high densities in rearing tanks, suppresses the natural territorial behavior of juvenile salmonids
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and imposes schooling behaviour from early life stages. The feeding regimes of salmonid hatcheries are normally geared towards maximal or near-maximal growth which is exemplified by the size difference between wild and hatchery-reared fish in the present study. Furthermore, the fish are regularly supplied with dry food of uniform size and shape given at the surface. These hatchery conditions differ radically from those usually encountered in the wild. It is therefore tempting to speculate that these aspects of the rearing process, which cause substantial proximal changes in behavior and growth patterns of the fish, may partly be responsible for the suppressed parr–smolt transformation of the hatchery-reared fish in the present study, and may ultimately be responsible for the decreased migratory success and long-term survival. This is supported by data showing altered foraging behaviour of hatchery-reared Atlantic salmon parr in the wild ŽSosiak et al., 1979., and differences in anti-predator behaviour between wild and hatchery-reared juvenile brown trout ŽJohnsson et al., 1996.. The trout in stream Nybroan ˚ showed a variation in hypoosmoregulatory ability with time. Both wild and hatchery-reared trout displayed high plasma sodium levels at the beginning of April, the levels peaked at the beginning of May, and then reached a minimum in mid-May and beginning of June, concomitant with the smolt-run. No such variation in plasma sodium levels with time could be demonstrated among the fish in stream Norumsan. ˚ However, the gill Naq, Kq-ATPase activity, of the trout in stream Norumsan, ˚ increased towards the end of the study concomitant with the smolt-run, which indicates that there was an improvement in the hypoosmoregulatory ability also of these fish. Direct comparisons among different species, strains, streams and years are difficult due to differences in, e.g., environmental and climatic conditions. However, the two strains of brown trout examined in the present study represent two different life history strategies, which may help to explain the presented data. The trout in stream Nybroan, ˚ as well as other strains in SouthEast Sweden, are large at sexual maturity and migrate over long distances ŽSvardsson and Fagerstrom, ¨ ¨ 1982; Aro, 1989., whereas the trout in stream Norumsan ˚ seem to be similar to the Norwegian stocks of brown trout, with smaller size at sexual maturity and a short seawater migration ŽL’Abee-Lund et al., ´ 1989.. Thus, in regard to their life histories, the brown trout of the Nybroa˚ strain appear more similar to the Atlantic salmon Ž S. salar ., than to Scandinavian brown trout in general ŽL’Abee-Lund et al., 1989.. Tanguy et al. Ž1994. identified morphological and ´ physiological characters associated with smolting in hatchery-reared resident and anadromous brown trout, and anadromous Atlantic salmon. They concluded that the parr–smolt transformation is most developed in Atlantic salmon, less developed in anadromous brown trout, and lacking in resident trout Žsee also Soivio et al., 1989.. In the present study, the brown trout from the Nybroa˚ strain showed more pronounced smolt characters regarding all physiological parameters measured, compared with the Norumsa˚ strain. Thus, brown trout strains of southeast Sweden, with life history similar to the Atlantic salmon, probably also resemble that species, in their physiological smolt characteristics, more than they resemble other anadromous brown trout populations. This is further supported by the tendency for elevated plasma GH levels of wild brown trout from the Nybroa˚ strain which is in accordance with previous data reported for Atlantic salmon ŽBjornsson et al., 1989, 1995; Boeuf et al., 1989; Prunet et al., 1989; Stefansson ¨ et al., 1991; McCormick et al., 1995., whereas the plasma GH profiles measured in the
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Norumsa˚ strain more resemble the pattern demonstrated for wild anadromous brown trout from the river Orne in Normandy ŽTanguy et al., 1994.. In the stream Norumsan, ˚ the timing of smolt migration and seawater adaptability vary considerably between years ŽBohlin et al., 1993; Dellefors, 1996.. In 1990, the temperature in this stream was unusually high in early spring Žmid-March. and decreased again in early April, a temperature pattern which prolonged the migration period ŽBohlin et al., 1993.. During the parr–smolt transformation of Atlantic salmon, two groups of fish were subjected either to ambient temperature Žranging from 18C, in February, to 128C, in May. or to 108C. In that study, the high temperature group showed increased gill Naq, Kq-ATPase activity, already in February, while the group reared at ambient Žlower. temperature did not show such an increase. This difference in gill Naq, Kq-ATPase activity was sustained until the beginning of April when the ambient temperature had increased to approximately 68C ŽS.D. McCormick pers. com... Thus, the high temperature in mid-March, in the present study, may explain the unexpectedly high gill Naq, Kq-ATPase activity measured at that time. When the water temperature decreased again in beginning of April, so did the gill Naq, Kq-ATPase activity. From April, there was a pattern of normal temperature increase together with an increase in gill Naq, Kq-ATPase activity, which is similar to other salmonids during spring parr–smolt transformation ŽBjornsson et al., 1989; Boeuf et al., 1989; Prunet et al., 1989; Nance et al., 1990; ¨ Tanguy et al., 1994; McCormick et al., 1995.. No difference in gill Naq, Kq-ATPase activity was demonstrated between the brown trout exposed to seawater for 24 h compared with the fish retained in FW. Even though environmental salinity is a cue well known to increase chloride cell number as well as gill Naq, Kq-ATPase activity in most teleost species examined Žsee McCormick and Saunders, 1987; McCormick, 1995., the present study supports earlier data on brown trout and other salmonids that 24 h of seawater exposure is not long enough time to increase gill Naq, Kq-ATPase activity ŽBoeuf et al., 1989; Madsen and Naamansen, 1989; McCormick et al., 1989; Madsen, 1990; Almendras et al., 1993; Berge et al., 1994.. The present study demonstrates that hatchery-reared brown trout can show disturbances in their parr–smolt transformation compared with wild brown trout of the same strains. Furthermore, the study suggests that the pattern of physiological and behavioral Žmigratory. events taking place during the parr–smolt transformation of anadromous salmonids are not only dependent on the species, but may be strongly modified by the life history of the individual. Thus, conclusions concerning inter- and intra-specific differences in smoltification, especially those that are based on studies of hatchery-reared fish, must be viewed with caution, and more studies concerning the differences between hatchery-reared and wild salmonids are needed.
Acknowledgements We would like to thank Mr. Goran Persson at Ystadsortens Fiskevard ¨ ˚ och Sportfiskeforening for sharing their records about the fish caught in the trap of stream ¨ Nybroan. ˚ We thank Ulo Faremo for his help in fish handling and sampling, and Gunilla
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¨ Eriksson and IngaMaj Orbom for excellent technical assistance. This study was supported by the Swedish Council for Forestry and Agricultural Research and the C.F. Lundstrom ¨ Foundation. References Almendras, J.M.E., Prunet, P., Boeuf, G., 1993. Response of a non-migratory stock of brown trout, Salmo trutta, to ovine growth hormone treatment and seawater exposure. Aquaculture 114, 169–179. Anon, 1995. Laxforskningsinstitutet, ŽSwedish Salmon Research Institute.. Sammanstallningar over ¨ ¨ markningsforsok Summary of returns from releases of tagged sea trout, 1980–1993. ¨ ¨ ¨ med havsoringungar. ¨ Aro, E., 1989. A review of fish migration patterns in the Baltic. Rapp. P.-v. Reun. ´ Cons. int. Explor. Mer. 190, 72–96. Berg, O.K., Jonsson, B., 1989. Growth and survival rates of the anadromous trout Ž Salmo trutta L.. from the Vardnes river, northern Norway. Env. Biol. Fish 29, 145–154. ˚ Berg, A., Fyhn, H.J., Barnung, T., Hansen, T., Stefansson, S.O., 1994. Development of salinity Berge, A.I., tolerance in underyearling smolts of Atlantic salmon Ž Salmo salar . reared under different photoperiods. Can. J. Fish. Aquat. Sci. 52, 243–251. Bjornsson, B.Th., Young, G., Lin, R.J., Deftos, L.J., Bern, H.A., 1989. Smoltification and seawater adaptation ¨ in coho salmon Ž Oncorhynchus kisutch.: Plasma calcium regulation, osmoregulation and calcitonin. Gen. Comp. Endocrinol. 74, 346–354. Bjornsson, B.Th., Taranger, G.L., Hansen, T., Stefansson, S.O., Haux, C., 1994. The interrelation between ¨ photoperiod, growth hormone and sexual maturation of adult Atlantic salmon Ž Salmo salar .. Gen. Comp. Endocrinol. 93, 70–81. Bjornsson, B.Th., Stefansson, S.O., Hansen, T., 1995. Photoperiod regulation of plasma growth hormone ¨ levels during parr–smolt transformation of Atlantic salmon: implications for hypoosmoregulatory ability and growth. Gen. Comp. Endocrinol. 100, 73–82. Blackburn, J., Clarke, W.C., 1987. Revised procedure for the 24 hour seawater challenge test to measure seawater adaptability of juvenile salmonids. Can. Tech. Rep. Fish. Aquat. Sci., No. 1515, 35 pp. Boeuf, G., Le Bail, P.Y., Prunet, P., 1989. Growth hormone and thyroid hormones during Atlantic salmon, Salmo salar L., smolting, and after transfer to seawater. Aquaculture 82, 257–268. Boeuf, G., 1993. Salmonid smolting: a pre-adaptation to oceanic environment. In: Rankin, J.C., Jensen, F.B. ŽEds.., Fish Ecophysiology. Chapman & Hall, London, pp. 106–135. Bohlin, T., Dellefors, C., Faremo, U., 1986. Early sexual maturation of male sea trout and salmon—an evolutionary model and some practical implications. Rep. Inst. Freshw. Res. Drottningholm 63, 17–25. Bohlin, T., Dellefors, C., Faremo, U., 1993. Timing of sea-run brown trout Ž Salmo trutta. smolt migration: effects of climatic variation. Can. J. Fish. Aquat. Sci. 50, 1132–1136. Bolton, J.P., Takahashi, H., Kawauchi, H., Kubota, J., Hirano, T., 1986. Development and validation of a salmon growth hormone radioimmunoassay. Gen. Comp. Endocrinol. 62, 230–238. Dellefors, C., 1996. Smoltification and sea migration in wild and hatchery-reared brown trout, Salmo trutta. PhD Dissertation, Department of Zoology, Goteborg University. ¨ Dellefors, C., Faremo, U., 1988. Early sexual maturation in males of wild sea trout, Salmo trutta L., inhibits smoltification. J. Fish. Biol. 33, 741–749. Eklov, Lan. Lan. ¨ A., Olsson, I., 1994. Havsoringaar ¨ ˚ i Malmohus ¨ ¨ Sea trout streams in Malmohus ¨ ¨ Meddelande 94r9 Lansstyrelsen i Malmohus Lan. ¨ ¨ ¨ In Swedish. Folmar, L.C., Dickoff, W.W., 1980. The parr–smolt transformation Žsmoltification. and seawater adaptation in salmonids. A review of selected literature. Aquaculture 21, 1–37. Hoar, W.S., 1976. Smolt transformation: evolution, behavior and physiology. J. Fish. Res. Brd. Can. 33, 1233–1252. Hoar, W.S., 1988. The physiology of smolting salmonids. In: Hoar, W.S., Randall, D.J. ŽEds.., Fish Physiology, Vol. XI, Part B. Academic Press, San Diego, pp. 275–343. Jensen, K.W., 1968. Sea trout Ž Salmo trutta L.. of the river Istra, western Norway. Rep. Inst. Freshw. Res. Drottningholm 48, 187–213.
K. Sundell et al.r Aquaculture 167 (1998) 53–65
65
Johnsson, J.I., Pettersson, E., Jonsson, E., Bjornsson, B.Th., Jarvi, T., 1996. Domestication and growth ¨ ¨ ¨ hormone alter antipredator behaviour in juvenile brown trout Salmo trutta. Can. J. Fish Aquat. Sci. 53, 1546–1554. Jonsson, N., Jonsson, B., Hansen, L.P., Aass, P., 1994. Effects of seawater-acclimatization and release sites on survival of hatchery-reared brown trout Salmo trutta. J. Fish. Biol. 44, 973–981. L’Abee-Lund, J.H., Jonnson, B., Jenssen, A.J., Saettem, L.M., Heggberget, T.G., Johnsen, B.O., Naesje, T.F., ´ 1989. Latitude variation in life history characteristics of sea-run migrant brown trout Salmo trutta. J. Anim. Ecol. 58, 525–542. Madsen, S.S., 1990. Enhanced hypoosmoregulatory response to growth hormone after cortisol treatment in immature rainbow trout Salmo gairdneri. Fish Physiol. Biochem. 8, 271–279. Madsen, S.S., Naamansen, E.T., 1989. Plasma ionic regulation and gill NaqrKq-ATPase changes during rapid SW-transfer of rainbow trout Ž Salmo gairdneri .: time course and its seasonal variation. J. Fish Physiol. 34, 829–840. McCormick, S.D., 1995. Hormonal control of gill Naq, Kq-ATPase and Chloride cell function. In: Wood, C.M., Shuttleworth, T.J. ŽEds.., Cellular and Molecular Approaches to Fish Ionic Regulation, 285–316. McCormick, S.D., Saunders, R.L., 1987. Preparatory physiological adaptations for marine life salmonids: osmoregulation, growth and metabolism. Am. Fish Soc. Symp. 1, 211–229. McCormick, S.D., Bern, H.A., 1989. In vitro stimulation of Naq, Kq-ATPase activity and ouabain binding by cortisol in coho salmon gill. Am. J. Physiol. 256, R707–R715. McCormick, S.D., Bjornsson, B.Th., 1994. Physiological and hormonal differences among Atlantic parr and ¨ smolts reared in the wild, and hatchery smolts. Aquaculture 121, 235–244. McCormick, S.D., Moyes, C.D., Ballantyne, J.S., 1989. Influence of salinity on energetics of gill and kidney of Atlantic salmon Ž Salmo salar .. Fish Physiol. Biochem. 6, 243–254. McCormick, S.D., Bjornsson, B.Th., Sheridan, M., Eilertson, C., Carey, J.B., O’Dea, M., 1995. Increased ¨ daylength stimulates plasma growth hormone and gill Naq, Kq-ATPase in Atlantic salmon Ž Salmo salar .. J. Comp. Physiol. B 165, 245–254. Moran, E., Izquierdo, J., 1991. Failure of a stocking policy, of hatchery-re´ P., Pendes, ´ A.M., Garcia-Vazquez, ´ ared brown trout, Salmo trutta L., in Asturias, Spain, detected using LDH-5 a genetic marker. J. Fish Biol. 39, 117–121, Suppl. A. Nance, J.-M., Bornancin, M., Sola, F., Boeuf, G., Dutil, J.-D., 1990. Study of transbranchial Naq exchange in Salmo salar smolts and post-smolts directly transferred to seawater. Comp. Biochem. Physiol. 96A, 303–308. Prunet, P., Boeuf, G., Bolton, J.P., Young, G., 1989. Smoltification and seawater adaptation in Atlantic salmon Ž Salmo salar .: plasma prolactin, growth hormone and thyroid hormones. Gen. Comp. Endocrinol. 74, 355–364. Schmitz, M., Berglund, I., Lundqvist, H., Bjornsson, B.Th., 1994. Growth hormone response to seawater ¨ challenge in Atlantic salmon Salmo salar, during parr–smolt transformation. Aquaculture 121, 209–221. Soivio, A., Muona, M., Virtanen, E., 1989. Smolting of two populations of Salmo trutta. Aquaculture 82, 147–153. Sosiak, A.J., Randall, R.G., McKenzie, J.A., 1979. Feeding by hatchery-reared and wild Atlantic salmon Ž Salmo salar . parr in streams. J. Fish. Res. Board Can. 36, 1408–1412. Stefansson, S.O., Bjornsson, B.Th., Hansen, T., Haux, C., Taranger, G.L., Saunders, R.L., 1991. Growth, ¨ parr-smolt transformation, and changes in growth hormone of Atlantic salmon Ž Salmo salar . reared under different photoperiods. Can. J. Fish. Aquat. 48, 2100–2108. ˚ 1982. Adaptive differences in long-distance migration of some trout Ž Salmo Svardsson, G., Fagerstrom, ¨ ¨ A., trutta. stocks. Rep. Inst. Freshw. Res. Drottningholm. 60, 51–80. Tanguy, J.M., Ombredane, D., Bagliniere, ` J.L., Prunet, P., 1994. Aspects of parr–smolt transformation in anadromous and resident forms of brown trout Ž Salmo trutta. in comparison with Atlantic salmon Ž Salmo salar .. Aquaculture 121, 51–63. Underwood, A.J., 1997. Experiments in Ecology. Cambridge Univ. Press, Cambridge. Wedemeyer, G.A., Saunders, R.L., Clark, W.C., 1980. Environmental factors affecting smoltification and early marine survival of anadromous salmonids. Mar. Fish. Rev. 42, 1–14.