Tolerance and Resistance to Thermal Stress in Juvenile Atlantic Salmon, Salmo Salar

Freshwater Biology {\99l) 25. 61-70

Tolerance and resistance to thermal stress in juvenile Atlantic salmon, Salmo salar

i. M. ELLIOTT Natural Environment Research Council, Institute of Freshwater Ecology. Windermere Laboratory, U.K.

SUMMARY. L The chief objective was to construct a thermal tolerance polygon for juvenile Atlantic salmon. Salmo satarV.., using fish from four groups and two populations: two age groups from one population {(!+, 1+ parr from River Leven). two size groups from the other population (slow and fast growing 1+ parr from River Lune). 2. Fish were acclimated to constant temperatures of 5, 10. 15, 20. 25 and 27^: then the temperature was raised or lowered at 1"C h"' to determine the upper and lower limits for feeding and survival over 10 min. 100 min. HKK) min and 7 days. As they were not significantly different between the four groups of fish, values at each acclimation temperature were pooled to provide arithmetic means (with SE) for the thermal tolerance polygon. 3. Incipient lethal levels (survival over 7 days) defined a tolerance zone within which salmon lived for a considerable time; upper mean incipient values increased with increasing acclimation temperature to reach a maximum of 27.8±O.2°C. lower mean incipient values were below 0°C and were therefore undetermined at acclimation temperatures <20°C but increased at higher acclimation temperatures to 2.2±0.4''C. Resistance to thermal stress outside the tolerance zone was a function of time; the ultimate lethal level (sunival for 10 min) increased with acclimation temperature to a maximum of 33^ whilst the minimum value remained close to 0°C. Temperature limits for feeding increased slightly with acclimation temperature to upper and lower mean values of 22.5±0.3''C and 7.0±0.3°C. 4. In spite of different methodologies, values in the present investigation are similar to those obtained in previous, less comprehensive studies in the laboratory. They also agree with fieldobsenationson the temperature limits for feeding and survival. Thermal tolerance polygons are now available for eight species of salmonids and show that the highest temperature limits for feeding and survival are those recorded for juvenile Atlantic salmon.

Correspondence: Dr J. M. Eilioll. NERC Introduction Insiituic of Freshwater Ecolog>. The Windermere . LnK.r^itoty. Far Sawrcy. Ambles.de. Cumhria. LA22 F. E. J. Fry and his co-workers pioneered ihe OLP. use of thermal tolerance polygons to summarize 61 62 J. M. Elliott the temperature limits for fish (see reviews by remain in fresh water for at least 2 years before Fry, 1947. 1967. 1971; Brelt. 1956, 1970; Elliott, smoltifying, whilst the fast-growers were prob- 1981. 1982). Such polygons provide a useful ably fish that would smoltify at 1 year old (see method for comparisons between species but. review by Thorpe, 1989). unfortunately, the detailed information re- ITie experiments with Leven salmon were quired to construct such a polygon is lacking for performed in constant-temperature tanks de- most species. Amongst the salmonids. thermal scribed in detail by Swift (1961). Each tank tolerance polygons are now available for pink, contained about I(X) I of water that was stirred chum, sockeye. coho and chinook salmon and aerated by compressed air (oxygen concen- {Oncorhynchusgorbuscha) (Walbaum), O. keta tration in water >85% saturation) and main- (Walbaum), O. nerka (Walbaum). O. kisutch tained within ±0.1—0.2^0 of a constant (Walbaum). O. tshawytscha (Walbaum)) (Brett, temperature. The tanks were covered with 1952. 1956), for Ameriean brook trout transparent polyethylene so that there was (Satvetimis fontinalis (Mitchill)) (Fry. Hart & natural illumination with a light intensity at the Walker, 1946), and for brown trout {Salmo water surface of c. 100 lux during the day. trutta L.) (Elliott, 1981). One surprising Experiments with Lune salmon were performed omission is the Atlantic salmon {Salmo salar in similar tanks except that water of a constant L.) and, therefore, the chief purpose of the temperature circulated through all the tanks. present investigation is to construct a thermal Young salmon of similar size were acclimated tolerance polygon for juveniles of this species. to the same constant temperature (either 5. 10. Some intraspeeific comparisons are also feas- 15, 20. 25 or 27''C) for 2 weeks with one fish in ible because the young salmon used in the ex- each tank. Water temperature was then raised periments were from two populations (Rivers at about TC h~' to a final temperature of either Leven and Lune), from different age-groups 20, 22, 24. 26, 28, 30. 32 or 34°C. An additional (0+ and 1+ parr) for the Leven population, final temperature of 36"C was used for acclim- and from slow and fast-growing groups of 1 + ation temperatures of 25''C and 27"C. The rale parr for the Lune population. Values obtained of temperature increase was similar to mean in the present investigation are also compared rates of change in upland salmonid streams but with those obtained in previous, less extensive rates as high as 2.2-2.5°C h ' occasionally laboratory experiments and with those observed occur (Macan, 1958; Crisp & Le Cren, 1970; directly in the field. J. M. Elliott, unpublished). Two fish were kept at the acclimation temperature throughout the experiment and served as controls. Freshly Materials and Methods killed Gammarus pulex L. were fed to the fish. Salmon were reared from freshly fertilized eggs The survival and feeding rates of the young taken from fish on their spawning migration in salmon were recorded every 10 min for the first the River Leven in South Cumbria and the 100 min, every 100 min for the period 100— River Lune in North Lancashire. Eggs were 1000 min and every KKKI min for the period incubated and young fish reared in a hatchery 1000-10.080 min (7 days). Records were kept on the shore of Windermere (for methods, see of the highest temperature for normal feeding Pickering. Griffiths & Pottinger. 1987: Pickering and survival over 10 min, 100 min, IO(M) min & Pottinger. 1988). Experiments with Leven and 7 days at each acclimation temperature. salmon were performed in autumn on under- The experiment was repeated with different fish yearling fish (0+ parr with a mean length of 5 cm to provide five (Leven fish) or three (Lune fish) and mean live weight of 1.5 g), and in spring on replicates for each size group of salmon at each I-year-olds(l+ parrwithamean length of 10cm acclimation temperature. and mean weight of II g). Experiments with A similar experimental procedure was used Lune salmon were performed in spring on I- to determine lower temperature limits for feed- year-olds (1+ parr) that were either slow- ing and survival. The acclimation temperatures growing parr (mean length of 6.0 cm. mean live were5.10,15.20and25°C, and the temperature weight of l.y g) or fast-growing parr (mean was lowered at atiout TC h ' to final values of length of 10.2 cm, mean weight of 11.0 g). The 0, 2, 4, 6, 8, IOT: (not 6, 8, lOX for acclimation slow-growers were probably salmon that would temperature of 5°C). It was difficult to maintain Thennat utterance in .salmon 63

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o '• ' I «• = I I . .1 I I r S-r- u o CO rO (M 64 J. M. Elliott the temperature at 2°C or less and iced waler avoided whenever possible to ensure that few had lo be added lo maintain a temperature near lish died during Ihc experiments. irc. Thermal stress due lo decreasing temperature produced a cessation of feeding and sudden bursts of activity followed by a state of coma. Results Once a fish was in the latter state, it was trans- When the young salmon were affected by in- ferred to slightly warmer water nnd usually creasing temperature, their stress response recovered. The stress response was more rapid progressed through three phases. The first ex- with decreasing than with increasing ternal indications of abnormal behaviour were a temperature. reluctance to feed, sudden bursts of activity The highest and lowest temperatures tor feed- with frequent collisions with the tank sides, ing and survival over 7 days, l()0() min, 1(X) min rolling and pitching, defecation and rapid venti- and 10 min were expressed as mean values latory movements. In the second phase, the fish (with SE). As these were not significantly dif- became quiescent with short bursts of weak ferent (F>(i.{)5 for all paired /-tests) for the swimming, it changed colour rapidly and in- four size groups of salmon at each acclimation creased its ventilatory movements. Movements temperature

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10 15 20 25 30 Acclimoiion temperotufe CC) FIG. 2. Thermal Uilcrancc polygon for juvenile Atliintic siilmon, showing the feeding zone, tolerance zone, incipient lethal level (iur\'ival over "^ d;iys). ultimate ILMIKII level (survival over 1(1 min) and intermediate levels (survival over KKM} min, UX) min); eaeli point is the arithmetic mean of sixteen values (see Table I). Tliermal tolerance in salmon 65 combined to provide overall arithmetic means lations, different age groups and different size with standard errors (Table 1) and these were groups, the upper and lower temperature limits used to construct a thermal tolerance polygon for feeding and sur\'ival are probably applicable (Fig. 2). to Atlantic salmon parr from other populations. Acclimation temperatures markedly affected the mean values for survival (Fig. 2. Table 1). Some salmon that survived for 7 days were kept Discussion at the same temperature for up to I month and it was therefore concluded that mean tempera- Comparison with previous laboratory studies on tures for survival over 7 days were the "incipient thermal tolerance lethal levels' that define the temperature toler- There are two broad categories of exper- ance zone within which the fish can live for a imental methods used to investigate thermal considerable time (all tielinitions follow the ter- toleranee in fish. In the lirst group, a critical mini)It)gy of Fry. 1947. 1971). Upper incipient thermal maximum is determined by raising the lethal temperatures increased linearly with in- temperature at a constant rate from the aeclini- creasing acclimation temperature to reach a ation level, then recording the temperature at maximum valueof 27.S:^0.2°C (Fig. 2, Table 1). which the fish first exhibits signs of stress before The lower incipient lethal temperature eould entering the zone of thermal resistance, and not be determined at aeeiimation temperatures tinally recording the lethal maximum at which below 2(rC because it was obviously below the death oeeurs. In the second group, the (ish are freezing point of water. It increased slightly to kept at an acclimation temperature and then I .()±().3X and 2.2. ±0.4T at higher acclimation abruptly transferred to a higher constant tem- temperatures of 20T and 25'^C, respeetively. perature, this process being repeated until Upper mean values for survival over 10 min, a critical higher temperature is found. Both KM) min and KKK) min followed a pattern similar groups have their supporters and critics (see to that for the incipietit lethal temperatures and Fry. 1947, 1967, 1971; Hutchison, 1976: Becker were within the "zone of thermal resistance' & Genoway. 1979; Elliott, 1981). and a recon- outside the tolerance zone and between ciliation of the two methods is provided by the incipient and ultimate lethal temperatures Kilgour & McCauley (1986). (Fig. 2). The latter was estimated by the tem- Acclimation temperature is a common vari- per;(ture for survival over 10 min and reached a able to both groups, but the effects of rate of maxitnum value of 33°C. The lower ultimate change in temperature are included in the lirst lethal temperature was less than OT because all but not the second group. Methods iu the second fish survived for at least 10 min and KXt min at group also have the disadvantage that the fish (fC. are subjected to handling stress when they are The salmon did not feed at acclimation tem- transferred from the acclimation temperature peratures of 25''C and 27''C. The upper mean to the final temperature. The salmon in the temperature for feeding was 22.5±().3''C, and present investigation were not subject to the the lower limit increased from 3.8±0.2"C at an additional stresses of handling and food depri- acclimation temperature of 5°C to 7.(!=:((..^"C at vation because preliminary experiments showed acclimation temperatures of 15°C or higher that the young salmon refused to feed for (Fig. 2). Although lish did not feed initially at 2-6 days after handling. Differences in exper- 25°^. they commenced feeding as the tempera- imental technique must therefore be taken into ture was reduced to about l(rC atid then eeased consideration when making comparisons with feeding again between 6 and H°C. As cessation previous studies. of feeding will have an important effect on the Four previous studies provide data that can growth and ultimately the survival of the fish, it be compared with those for upper temperature must be considered y thermal stress response limits in the present study (Table 1. note that within the toleranee zone. acclimation temperatures are given in parenth- The thermal tolerance polygon (Fig. 2) pro- eses where they differ slightly from those used vides il sueeinet summary of the results of this in the present study). Bishai (1960) kept salmon investigation. As no significant differences could alevins at 6°C and then slowly raised the water be found between fish from different popu- temperature to critical values thai were only 66 J. M. Elliott

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rit h g 52 "-- |2 Q es t CQ — s Z — — Thermal tolerance in salmon 67 slightly lower than those in the present study (Tahie la). Alevins were also acclimated at WC and 2()°C, then abruptly transferred to higher temperatures to obtain a critical temperature of 23°C that was well below those in the present study, probably because of different experimental techniques (see above). Using methods similar to those of the present study. Spaas (1960) acclimated salmon alevins. 0+ parr and 1+ parr to 'room temperature" (I5-2()'"'C?). thensiowly increased the temperature lo obtain the lethal values. These are similar to those in the present study (Table lb) but suggest a slight increase in upper temperature limits with the age of the fish, a conclusion that was not supported for (f+ and I + parr in the present study. It is still possible, however, that alevins may have a lower temperature threshold 10 15 20 25 30 Acclimation temperature CC) than parr. FIG. 3. Comparison of thermal tolerance polygons Lethal temperatures for salmon smolts in the (only for incipient lelhal level) for brown trout, laboratory (Alabaster. l%7) were lower than Salmo truita (Ellioit. 1981). American hrtwk trout. those for parr in the present study (Table Ic), Salvehnus foniinalis (Fry et al.. 1946) and Allaniic perhaps because there are differences in the salmon parr, Salmo salar (present study). thermal tolerance of parr and smolts. or because the smolts were suddenly transferred to the test tank at the higher temperature. Finally, values .SK3"C- for Salmo trutta, (Elliott, 1981) and 45(1- obtained for salmon parr (Garside. 1^73) were 529°C^ for five Oncorhynchus spp, (Brett. 1952, very similar to those in the present study 1956). Therefore, the highest known tempera- (Table Id), even though the fish in the earlier ture limits for feeding and survival in the Family study were subjected to a sudden increase in Salmonidae are those recorded for Atlantic temperature. It is therefore concluded thai, in salmon parr. spite of the problems of different methodologies, values for Atlantic salmon parr in the present investigation are generally similar to Temperature requirements for Atlantic salmon those obtained in previous, less comprehensive in the field studies. Little is known about the upper temperature As mentioned in the introduction, thermal limits for survival of Atlantic salmon in the tolerance polygons provide not only a succinct field. Returning adults migrated through the summary of the temperature requirements of a Thames estuary during August when water species, but also a useful method of comparison temperatures were never lower than 19''C and between species. This is well illustrated by com- often exceeded 22°C with cKcasional values over paring the thermal tolerance of Atlantic salmon 2n (Alabaster & Cough, 1986). Huntsman parr with that of brown trout and American (1942) found that freshly run grilse in a Canadian brook trout (Fig. 3). The temperature tolerance river died at 29.5-30.5''C whilst parr died at of young salmon is clearly greater than that of higher temperatures of 32.9-33.8°C. The latter the other species with upper temperature limits values are similar to those of the present study about yC higher than those for brown trout. A in which the ultimate lethal level for salmon useful index of thermal tolerance is provided by parr was 3()-33°C and the incipient lethal leve! the area of the tolerance zone, usually expressed was25-28*'C. both levels being about 3''C' higher as °C squared. The value of TOST" for young than those of 26-3()°C and 22-25''C for brown Atlantic salmon is much higher than that re- trout (Elliott. 1981). corded for other salmonid species; values being More is known about the lower temperature 62.SX'" for Salvelinus fontinalis (fry etal.. 1946), limits for feeding and growth in the field. Allen 68 /. M. Elliott

(1940. 1941) found that young Atlantic salmon in streams and rivers. Brown trout will be less in the Rivers Eden (north-west England) and affected by low temperatures because they cease Thurso (north Scotland) reduced or stopped feeding in the range 0-4°C whereas salmon feeding below TQ'. and he later concluded cease feeding in the range 0-7°C depending (Allen, 1969) that juvenile salmon growth upon the acclimation temperature. In contrast, was negligible below TC Young salmon in a higher temperatures will favour Atlantic salmon Scottish stream remained inactive and concealed because they do not cease feeding until 21.6- at temperatures below 6-7°C (Gardiner & 22,5°C, whereas brown trout cease feeding at Geddes. 1980), but other workers conclude that aboui 19T (Elliott, 1981). Although the lower inactivity occurs below 9T (Gibson. 1978; limits for survival are usually below {fC for Rimmer, Paim & Saunders. 1983). The lower both speeies. thermal stress commences at a threshold for growth has been given as 7°C higher temperature for salmon (25-28°C) than (Symons, 1979: Evans, Rice &Chadwick, 1985), for brown trout (22-25''C depending upon 6°C (Power, 1969), 5.6^ (Lee & Power, 1976) acclimation temperature). and 6.3-7.4°C (Jensen & Johnsen, 1986; 1 hese difference.s indicate that small changes Jensen, Johnsen & Saskgard. 1989). An even in water temperature due to human activities lower temperature of 0.9''C for feeding has been (e.g. river regulation, afforestation, climate reported for juveniles in a hatchery (Higgins & change) could favour one speeies at the expense Talbot, 1985). t)f the other. The results of the present investi- The present investigation has shown that the gation on salmon and the previous study on lower temperature for feeding Is usually 7°C but trout therefore have important implications for decreases with acclimation temperature. As the conservation and management of both non-feeding salmon parr will not grow, these species. values are probably also the lower limits for growth. The value of TC agrees with most of the field observations and the slightly lower Acknowledgments values in some field studies could be explained I wish to thank Mrs P. A. Tullett. Mrs. D. J. by lower acclimation temperatures, as demon- Stephenson, Mrs J. Pollard and J. D. Allonby strated in the present study. The lower tem- for all their assistance in this work which was perature limits are therefore not constant but financed by the Natural Environment Research decrease with decreasing acclimation tempera- Council. ture from a maximum value oiTC to a minimum of 4°C. These values are about yc higher than the corresponding values for brown trout References (Elliott. 1981). Little is known about the optimum tempera- Alabaster J.S. (1967) The survival of salmon [Salmo %alar L.) and sea trout (S. irutta L., in fresh and tures for growth in young Atlantic salmon in the saline water at high temperatures. Water Research. field, but laboratory studies indicate that they I, 717-730. are in the range l6-19°C(e.g. Siginevich. 1967; Alabaster J.S. & Gough P.J. (1986) The dissolved Dwyer & Piper, 1987; Wankowski & Thorpe, oxygeti and temperature requirements of Atlantic 1979; Peterson & Martin-Robichaud. 1989). salmon, Salmo satar L., in the Thames Esttiary. Journal of Fish Biology, 29, 613-621. This is higher than the optimum range of 13- Allen K.R. (194fl) Studies on the biology of the early 14°C for brown trout (Elliott. 1973). indicating stages of the salmoti {Salmo salar). 1. Growth in once again that the temperature requirements the River Eden. Journal of Animal Ecologv, 9. 1- for Atlantic salmon are at least TC higher than 23. those for brown trout. Allen K.R. (1941) Studies on the biology of the early stages of the salmon (Salmo salar). 3. Growth in The rather limited field data support the gen- the Thurso river system, Caithness. Journal of eral conclusion that amongst the salmonids, Animal F.cology. 10, 273-295. Atlantic salmon parr have the highest tempera- Allen K.R (1969) Limi'tations on production in sal- ture requirements for survival, feeding and monid populations in streams. Salmon and Trout in Streams (Ed. T. G. Northcotc), pp. 3- IS. Univer- growth. Perhaps the most striking contrast is sity of British Columbia. Vancouver, B.C. the yc difference between salmon and brown Beeker CD. & Genoway R.G. (1979) Evaluation of trout because these species are often sympatrie the eritical thermal maximum for determining Tfiermal tolerance in salmon 69

thermal tolerance of freshwater fish, Environmental Higgins P.J. & Talbtit C", (1985) Growth and feeding Biology ofFhhe.s, 4. 245-2^6. in juvenile Atlantic salmon (Salmo .salar L.). Bishai H.M. (lyWI) Upper lethal lemperaiurcs for Niitrttion and Feeding in Fish (Eds C.B. Cowcy, lar\al salmonids. Journal dti Conscil. 25. 129- 133. A.M. Mackie & J. G. Bell), pp. 243-263. Brett J.R. (1952) Temperature tolerance in young Academic Press. London. Pacific salmon, genus Oncorhynchus. Journal of Huntsman A.G. (1942) Death of salmon and trout the Fisheries Research Board of Canada. 9. with high temperature. Journal of the Fisheries 265-323. Research Board of Canada. 5. 485-501. Brett J.R. (1956) Some principles in the thermal Hutchison V.H. (I97(i) Factors influencing thermal requirements of tishcs. Qiiarierlv Review- of tolerances of individual organisms. Thermal Biology. 31. 75-S7. Flcology, Vol. ll (Eds G. W. Esch & R. M. Brett JR. (1970) Environmental factors. 1. Tempera- McFarlane),pp. 10-26, ERDA Symposium Series, ture Marine Ecology. Vol. I (Ed. O. Kinne). Springfield. Va. pp. 513-560. John Wiley. London. Jensen A.J. & Johnsen B.O. (1986) Different adap- Crisp D.T. & Lc Crcn E.D. (1970) The temperature tation strategies of Atlantic salmon (Salmo salar) of three different small streams in north west |M)ptilations Io extreme climaies with special reier- England. Hvdrohiologia. SS, 305-323. cnce to some cold Norwegian rivers. Canadian Dwyer W.P. & Piper R.G. (1987) Atlantic salmon Journal of Fisheries and Aquatic Sciences, 43, growth efficiency as affected by temperature. 980-984. Progressive Fish Culturist. 49. 57-59. Jensen A.J., Johnsen B.O. &. Saksgard L. (1989) Elliott J.M. (1975) The growth rate of brown irout Temperature requirements in Atlantic salmon (Salmo iruita L.) fed on maximum rations. Journal (Salmo mlar). brown trout {Salmo truna), and of Animal Ecology, 44, 805-821. Arctic Char {Salvelinus alpinits) from hatching to Elliott J.M. (I98I) Some aspects of thermal stress on initial feeding cotnparcd with geographic distri- freshwater tclcdsts. Stress and Fish (Ed. bution. Canadian Journal of Fisheries and Aquatic A. D. Pickering), pp. 209-245 Academic Press, .Sciences. 46, 786-789. London. Kilgour D.M. & McCauley R.W. (1986) Reconciling Ellioti J.M. (1982) The effects of temperature and the two methods of measuring upper lethal tem- ration si^e on the growth and energetics of sal- peratures in fishes. Environmental Biology of tnonids in captivity. Comparative Biochemistrvand Fishes, 17. 281-290. Physiology. 73B. 81-91. Lee R.L.G. & Power G. (1976) Atlantic salmon Evans G.T.. Rice J.C. & Chadwick E.M.P. (1985) (Salmo salar) of the Leaf River. Ungava Bay. Patterns of growth and smolling of Atlantic asimon Journal of (he Fisheries Research Board of Canada, ISalmo salar) parr in a southwestern Newfoundland 33,2616-2621. river. Canadian Journal of Fisheries and Aquatic Macan T.T. (1958) The temperature of a small stony iciCTifCi. 42. 539-543. stream. Hvdrobiologia, 12. 89-106. Fr>- F.E.J. (1947) Effects of the environment on Peterson R.H. & Martin-Robichaud D.J. (1989) First animal activity, ilmversity of Toronto Studies tn feeding of Atlantic salmon {Salmo salar L.) fr>' as Biology Series .5.5, Publications of the Ontario influenced by temperature regime. Aqtiaculture, Fi.\heries Re.search Laboratory, 68, 5-62. 78. 35-53. Fr>- F.E.J. (1967) Responses ol* vertebrate poikilo- Pickering A.D.. Griffiihs R & Pottinger T.d. (1987) therms to temperature. Thermohiology {Eii. A. H. A comparison ot the effects of overhead eover on Rose), pp. 375-409. Academic Press. U>ndon. the growth, survival and haematology of juvenile Fr>' F.E.J. (1971) The effect of environmental factors Atlantic salmon, Salmo salar. L.. brown trout on the physiology of fish. Fish Physiology. Vol. Salmo trutta L., and rainbow trout. Salmo gairdneri VI (Eds W.S. Ht'tar & D.J. Randall), pp. 1-98. Richardson. Aquaculture. 66. 109-124. Academic Press, London. Pickering A.D. & Pottinger TG. (1988) Lympho- Fr>' F.E.J., Hart J.S. & Walker K.F. (1946) Lethal cytopcnia and the overwinter sur\ival of Atlantic temperature relations for a sample of young salmon parr, Salmo salar L. Journal of Fish Biology. speckled trout. Sahelinus fontinalis. University of 32. 689-697. Toronto Studies tn Biology Series 5J, Publications Power G. (1989) The salmon of Ungava Bay. Arctic of the Ontario Fisheries Research Laboratory, 66, Instintte of North America. Technical Paper, 11, 9-35. Gardiner W.R. & Geddes P. (1980) The influence Rimmer D.M., Paim V. & Saunders R.L. (1983) of body composition on ihe survival of juvenile Autumnal habitat shift of juvenile Atlantic salmon salmon. Hydrobiologia, 69, 67-72. {Salmo sular) in a small river. Canadian Journal of Garside ET. (1973) Ultimate upper lethal tempera- Fisheries and Aquatic Sciences. 40. 671-680. ture of Atlantic salmon Salmo salar L. Canadian Siginevich G.F. {19f>7) Nature of the relationship Journal of Zoolofiy. 51. 898-900. between increase in size of Baltic salmon fry and Gibson R.J. (1978) The behaviourof juvenile Atlantic the water temperature. Gidrolnologic Zhurnal, 3. salmon {Salmo salar) and brcok troul {Snivelinus A^~^^ {Fisheries Research Hoard of Canada Trans- foniinatis) with regard to temperature and lo water lation Series. No. 952, 1-14). vclocily. Transactions of the American Fi.sheries Spaas J.T (1960) Contribution to Ihe comparative Society. 107. 703-712. physiology and genetics of the European 70 J, M. Elliott

salmonidae. III. Temperature resistance at differ- Thorpe J.E. (1989) Developmental variation in sal- ent ages. Hydrohiologia, 15. 78-88. munid populations. Journal of Fish Biology, 35 Swift D.R. (1961) The annual growth-rate cycle in (Supp. A), 295-303. brown trout (Salmo trutta Linn.) and its cause. Wankowski J.W.J. & Thorpe J.E. (1979) The role of Journal of E.\perimental Biology. 38. 595-604. food particle size in the growth of juvenile Atlantic SymonsP.E. (1979) Estimated escapement of Atlantic salmon {Salmo salar L.). Journul of Fish Biology, salmon {Salmo salar) for maximum smolt pro- 14,351-370. duction in rivers of different productivity. Journal of the Fisheries Research Board of Canada, 36, (Manuscript accepted II June 1990) 132-140.