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Temperature Tolerance in Young Pacific Salmon,
Genus Oncorhynchusl
BY J. R. BRETT
• Pacific Biological Station, and
Department of Zoology, L""niversity of Toronto
(Received for publication Septenzber 19, 1951)
Introduction
Acknowledgeme.<ts
:;\Iaterials
:\Iethods
Results .
Upper limits of temperature tolerance
Lower limits oi temperature tolerance
Preferrerl temperatures
Comparison of temperature resistance
Zones of thermal tolerance
Discussion and Conclusions
Time and temperature
CONTENTS
Comparison with some other salmonoids
Some ecological relations
Summary
References
App~ndix I. Statistical procedure
Appendix II. Table:; IV-XIV
ABSTRACT
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315
Lethal limits of high and low temperatures were determined for the young of fiye species of
Pacific salmon, the spring (Oncorlr:yncht~s ts!tawytscha), the pink (0. go.~busclta), the sockeye (0.
ne•ka), the churn (0. kl'ia) and the coho (0. kisutch).
For acclimation temperatures ranging from 5o to 24°C. significan~ rlifferences between sr.:dt:::>
in their resistance to high temperatures was obtained. The spring and cono were most resistant.
The pink and churn salmon were least resistant, and the sockeye was distinguishable from the
latter two by greater resistance for pt'Olonged exposure to high temperatures. ;{o species could
tolerate temperatures exceeding 25.1 °C. when exposed for one week.
A fanning~out of the opercula was shown to be directly correlated with the onset of death from a
low temperature. By use of this criterion mixed le~hal effects at low itm~peraturcs were demonstra-
ted and found to be influenced by the size of the fish and by the salinity of the watet'. None of the
species could with:;tand temperatures lower than 4°C. when acclimated to 20°C. and above. When
taken from holding troughs as low as 5°C., coho and sockeye could not tolerate long exposure
(four daysJ to 0°C. -·---
tBased upon portions of a thesis accepted by the Faculty of Graduate Studies, t"niversity of
To1·onto, in partial fulfilment of the requirements for the degree of Doetor of Philosophy.
fi. F.tSH. RL~S. ao··.· C.-\~ .• 9 tU), Hl5;}
[}rinted in Canada. :J
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· In a vertical gradient little difference in preferred tE'mperature was observed, either between
spectes or for different acclimation temperatures. The 12° to l4°C. stratum was the region of
great~st concentration.
Specific <!iifferences in temperature responses are in keeping with taxonomic and ecological
diEtinctions.
INTRODUCTION
No ACTIVITY of an animal escapes the effect of temperature. Distribution, develop-
ment, propagation and mere existence, each is influenced strongly in some
manner by temperature. This influence must · 'e met and surmounted eitht•r
through resistance or adaptation, external avoidance or. internal control. It is
known that the upper and lower limits of temperature-tolerance in fish arc
extended through both adaptation and resistanc~ ~Fry, 1947a), and the varying
degrees of these t\\'O attributes sepa~ately and collectively distinguish :he species
in this respect. By conducting experiments on tolerance to high and to low
temperatures among the young of the five North American species of Pacific
salmon, the relative abilities of these species to cope w::h extremes of temperature
have been des(.ribed in the following analysis.
Among earlier experiments, interest in the ability of fish to survive tempera-
tures in the region of the freezing point of water and slightly below was expres:ed
by Regnard (1895). In 1899, Maurel and Lagriffe while invetJcigating both upper
and lower levels of temperature-tolerance, chiefly in fresh-water fish, concluded
that these species were better adapted for resisting low than high temperatures.
Later investigators, dealing mainly with mort;:~lity froo. high temperatures, ex-
pressed the resistance in t:erms of the tem;_:.,erature reat:l.::d before death when
heated at a constant rate (Huntsman and Sparks, 1924)r or averaged either the
times to death (Loeb and \Vasteneys, 1912) or the number of fish dead following
a given exposure (Hathaway, 1927) at various constant temperatures. This
quantitative expression of temperature-tolerance has been developed to provide
a more inclusive treatment, borrowing from the methods of pharmacological
·procedure ~oncerning dosage-mortality (Fry er; al., 1946).
The phe~1omenon of thermal adaptation in relation to previous temperature
history provides the organism with greater scope for environmentdl experience.
The term "acclimation" has been used. to describe this effec~, although "acclima·
tization" is apparently synonomous (Doudoroff, 1942; Heilbrunn, 1943; Brett.
:!~44). The importance of temperature-acclimation in nature and in experimental
work has been stressed with significant emphasis (Doudoroff, 1945; Fry, 1947a),
By working systematically with ,different temperature-acclimations the variou.s
levels of both upper and lower thermal tolerance can be determined within sufft-
cient statistical limits to permit accurate prediction. The development of precise
methods of physiologtcal me:asurement has set the stage for physiological
description.
The close taxonomic relation of the Pacific salmons, genus Ortcorhynclw.s,
(l'viilne, 1948) coupled with faidy distinct ecofogical habits, provides interest Hl
the affinities whkh might be revealed by a rigorous analysis of their temperature·
tolerances. Similar work on other ::salmonoids is mounting (Fry et al,. 19·10;
-
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Fry, 1947b~
attributes on
the role of t
animals \Vill
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both directe · ·
wide variety · • ~l has been the ,.
The matli
of Dr. D. B. ~·
The expel·
logy whi. ch i.s .. ·. of Lands and !
ment of Lant
labor.a tory a1.1"
fish by 1\ilessti
measnre to th~
fhe salmt
Pacific Biologq
of Fisheries, \\
tional shipmet3
The Fish'
extended leav .
tance. It is a
SouRcE
The five
America were
Each lot ,
insulated box,··
Successful shi
TAULE I. The
Species
l. Spring
2. Pink
3. Sockeye
4. Chum
5. Coho
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267
Fry, 1947b; Graham, 1949). vVith the gradual recording of such physiological
attributes on a comparable basis within and between taxonomic groups of fishes,
the role of temperature in the ecology, and possibly in the evolution, of these
animals will become increasingly apparent.
ACKNOWLEDGMENTS
I am greatly indebted to Dr. F. E. J. Fry who has for a number of years
both directed and stimulated research on temperature relations in fish. His
wide variety of interests and knowledge in the problems of experimental biology
has been the source <:t <t wealth of suggestions and .?.. constant inspiration.
The rnathematica1 analysis of the data has bee.~: •;.m.der the helpful guidance
of Dr. D. B. DeLury of the Ontario Research Foundation.
The experiments were conducted in the Laboratory for Experimental Limno-
logy which is operated jointly by the University of Toronto and the Department
of Lands -nd Forests, located at the Southern Research Station of the Depart-
ment of Lar'ds and Forests, 1\llaple, Ontario. The excellent facilities of the
laboratory and the attention devoted to feeding and maintaining the stocks of
fish by 1t1essrs. D. Cucin, G. 'Stolfa and \V. Sanderson contributed in a large
measure to the successful execution of the research.
The salmon eggs were obtained through the courtesy of i\1r. F. );eave,
Pacific Biological Station, British Columbia, and of Mr. C. H. Ellis, Department
of Fisheries, \Vashington. They have each responded to urgent pleas for addi-
tional shipments when transp~rtation problems resulted in minor catastrophies.
The Fisheries Research Board of Canada has not only seen fit to grant
extended leave of absence to the author, but has al!1o given him financial assis-
tance. It is a pleasure to acknowledge this support.
l\IATERTALS
SOURCE
The five species of Pacific salmon common to the west coast of Xorth
America wete obtained as eyed eggs from three hatcheries (Table I).
Each lot of approximately two thousand eggs was shipped in a fiberglass-
insulated box, pa~ked with ice and perforated to permit air exchange for the eggs.
Successful shipment by air was possible if not more than thirty-six to forty-eight
TABLE I. The hatchery locations and-dates of fertiliz.ng, shipping~. J 50 per cent hatch for
the five species o(Pacific salmon.
Species Hatchery Fertilized Shipped 50% Hatch -
1. Spring Dungeness, \Vash. 30/8/49 20/10/4H . 9/11/40
2. Pink " .. 28/9/49 7/12/49 12/12/49
a. Sockeye Issaquah, " l0/10/·19 25/11/411 6/1/50
4. Chum ~ile Creek, B.C. 28/10/-19 7/1/50 4/2i50
5. Coho " " " 14/11/49 7/1/5C 27jl/50
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Fry, 1947b; Graham; 1949). \Vith the gradual recording of such physiological
attributes on a comparable basis within and between taxonomic groups of fishes,
the role of temperature in the ecology, and possibly in the evolution, of these
animals will become increasingly apparent.
ACKNOWLEDGMENTS
I am greatly indebted to Dr. F. E. J. Fry who has for a number of years
both directed and stimulated research on temperature relations in fish. His
wide variety of interests and knowledge in the problems of expel·imental biology
has been the source of a wealth of suggestions and a constant inspiration. ·
The mathematical analysis of the data has been under the helpful guidance
of Dr. D. B. DeLury of the Ontario Research Foundation.
The experiments \Vere conducted in the Laboratory for Experimental Limno-
log-; which is operated jointly by the University of Toronto and the Department
of Lands and Forests, located at the Southern Research Station of the Depart-
ment of lands and Forests, lVIaple, Ontario. The excellent facilities of the
laboratory and the attention devoted to feeding and maintaining the stocks of
fish by lVIessrs. D. Cucin, G. 'Stolfa and \V. Sanderson contributed in a large
measure to the succPssful execution of the research.
The salmon eggs \vere obtained through the courtesy of :VIr. F. ~eave,
Pacific Biological Station, British Columbia, and of Mr. C. H. Ellis, Department
of Fisheries, \Vashington. They hc:ve each responded to urgent pleas for addi-
tional shipments when transp~rtation problem.., resulted in minor catastrophies.
The Fisheries Research Board of Canada has not only seen fit to grant
extended leave of ahsence to the author, but has also given him financial assis-
tance. It is a pleasure to acknowledge this support.
MATERIALS
SOURCE
The five speCies of Pacific salmon common to the west coast of X orth
America were obtained as eyed eggs fro-n three hatcheries \Table I).
Each lot of approximately two thousand eggs was shipped in a fiberglass-
insulated box, packed with ice and perforated to permit air exchange for the eggs.
Successful shipment by air was possible if not more than thirty-six to forty-eight
TABLE I. The hatchery locations and-dates of fertilizing, shipping and 50 per cent hatch for
the five species o(Pacific salmon.
Species Hatchery Fertilized Shipped 50~:·(; Hatch -
1. Spring Dungeness, \\'ash. 30/8/49 20/10/-!!> 9/11/49 .
2. Pink ,, II 28/9/49 7/12/49 12/12/49
3. Sockeye Issaquah, lt 10/10/-19 25/11/49 6/1/50
4. Chum ~ile Creek, B.C. 28/10/49 7/1/50 4/2/50
5. Coho " II " 14/11/49 7/1/50 27/1/50
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268
hours elapsed between packing and receiving . .An initial mortality not exceerling-
2 per cent inevitably followed the handling necest:itated by shipment. \Yith thi~
excep..:ion, egg losses from other causes were exceptio!lally 1ow in all cases where
subsequent experiments were performed.
FEEDING AND CARE OF YOUNG
The transition stage from alevin to free-swimming, feeding fry is a precarious
one for young salmonids. The habit of feeding must be d·~veloped and encouraged,
usually by frequent presentation of small particles of food. By directing a jet of
water into a small aluminum screened basket containing finely groum' heef or
hog livet=, adequate dispersal of thP food over periods of 15 to 20 minut~3, four
times daily, was achieved. This routine was maintained for the first month of
feeding, followed by reduction in feeding frequency and n. change of diet, mainly
in accordance with fish-cultural procedures for salmon currently practised in
\Vashington State (Burrows, no date). The diet selected was a slight modification
of one reported by h~l.is (1948) which had been found to give best growth and
least mortality for young spring salmon when tested on a variety of diets. .\
mixture of 50 per cent beef or hog liver together with -!:8 rer cent grourtd '1fish-
pack" (haddock and cod fillet waste) and ) per cent yeast was provided, up to
the second month, followed by a reduction in liver w 30 per cent for the balance
of the experimental period.
:Mortality in the stock tanks with a constaq_t temperature of 8.8° ± 0. r;o
was virtually negligible. No prophylactic treatments were introduced. At higher
temperatures, 20°C. and above, up to 5 per cent mortality \vas observed in all
species, and irrfrequent treatments (t\vo to tlu·ee times per month) with a 1 :4,000
solution of Roccal were applied (Burrows). Two cases where disease became
significant '"ere encountered; one with five-month-old chum salmon, from a single
tank, which necessitated discarding the remaining fish as well as one series of
obviously discordant data; the other, with three-month-old sockeye, raised by
stages to 24°C. and apparently incapable of deriving adequate nutrition from
their diet at such an elevated temperature.
The pH of the well water supply~ng the laboratory was 7.3 with total
solids amounting to 254.3 parts per million (Table II).
RETAINING TROUGHS
The retaining troughs were each supplied with running water tapped from
bot-and cold-water sources of relatively constant temperature and pressure.
Adjustment of these with regular inspection permitted setting the temperature
of a trough (above 9°C.) to within ± 0.1 °C. of any desired temperature. esunllr
two, sometimes three, sp~cies were cultured in a divided trough.
P.elmv 9.°C. a refrigeration unit reduced the temperature in a single holding
tank in which the five species were retained separately in cages of fine aluminum
w.ire screening. Thus, different levels of temperature-acclimation were ·readily
obtained with a high degree of accuracy and constn,ney.
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SIZE A~D A~\ l.rniforn~~·
was maintain.
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ensure abu nd
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The tim~ :f ~.about two 11.
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TAEi:..E ll. ::\1\neral constituent-: of the water supply
used in these experiments, as reported by
the Chief Provincial Analyst, Sept. 24:, 1947.
Total solids
_-\lkalinity
Total hardness
Iron and Aluminum (o:\ides)
Iron
Calcium
:\Iagnesium
Potassium and Sodium
Sulphates
Chlorides
*As carbonate of lime.
parts per million
25±.3
202.0*
1!;';1. 0*
4. 7
0.2
89.5
14.1
36.8
45.1
13.0
269
SIZE AND AGE OF EXPER~:-tENTAL FISH
Uniformity of conditions in every feature of tne history of the young fish
was maintained as far as possible. Keerir1!!, them in the same or similar troughs,
at the same temperature, and presentinf ·~ue same diet in sufficient quantity to
ensure abundance, were the first precautions. The variations in response to
subsequent high or low temperatures might then be considered as attributable
to specific differences only.
The time for commencing experiments was set at thr. -e months after hatching
(about two months after f~eding commenced), and the"1 continued for an addi-
tional two to three months 1 The fish from highGr temperatures were used first.
The knO\vledge that the young chum and pink salmen move to salt water early
in their first year motivated making comparison of the species i~., the very you·Jg
stages.
TABLE III. ~lean fork-lengths, weight" and agee of the salraon fry
used in temperature-tolerr=~.::e tests.
Species
Spring
Pink
Sockeye
Chum
Coho
Spring
Sockeye
Ch\tm
Coho
Lenglh (em.) W~ight (g.)
Cpper temperature tolerance
4.44 ±0.40
3.81 :±0.29
4.49 ± 0.84:
5.44 ± 0.89
4. 78 ± 0.60
1.03 ± 0.27
o.zo ± 0.15
0.87 ± 0.45
1..62 ± 1.03
1.37 ± 0.62
Lower temperature :tolerance
4. 72 ± 0.4~
4.50 ± 0.53
5.09 ± 0.51
4.83 ± 0.45
Age (months)
3.6
3.~
4.7
4.0
5.2
7.7
5.8
5.2
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In Table III mean fork-lengths and "-eights (vrith standard deviations) and
the average age from hatching of all samples used in the temperature-toieranre
tests are compiled. No weights are included tor the fish used in low-temperature
tests. These samples \Yere not removed from the lethal tanks until some tilile
after death. and water absorption had affecten thtir weight.
LETHAL BATHS
The lethal baths, six,in number and measuring 22 inches square by 11 inches
deep (Figure 1) were each constructed of galvanized iron coated inside with
aluminum paint and adapted for use in either upper or lower thermal-tolerance
tests. The addition of complete insulation with fiberglass of one-inch thickness
was of value in reducing temperature variation to a minimrm. Thermostatically
controlled, 120-watt heater-coils in pyrex tubing count~rbalanced a steady loss
of heat, mainly from aerat;0n and from aver} slmv exchange of wat;.:;rf equal to
the volume of the tank every twenty-four hours. In the low-temperature Iethals
the heat loss was augmented by the additibn of a layer of crushed ice, partitioned
off on three sidt.' of the tank by a removable galvanized iron sheet. A standardized
r .Gl"RE 1. Apparatus for determining upper and lower le..:hal tempemtures being assembled.
Two units, one with four, th"! other with two lethal baths are shown ·vith connections for thermal
control, aerattion and water exchange. (Photograph by Mr. W. P. I<ice.J
never
high 1
<:oncernmg-
variously •
:~n inches h
t ivcly. Pla
romplete t
the bottom
hol~, the
F~GURE 2,
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271
thermome,er calibrated in intervals of 0.1°C. was used throughout all experi-
ments. Ofttn no ~etectable change in the tank temperatures was apparent and,
in general, variation did not exceed a range of more than 0.1 °C. from any set level.
Under maximum loads of fish per tank (40) oxygen concentrations ,.,ere
nevt~" reduced below 93 per cent saturation (5.24 cc. 0:/L, 26.5°C.) in tests on
high lethals, and not below 81 per cent (6.91 cc. 02/1., G.0°C.) in low-lethal
experiments.
PREFERRED-TEMPER.:\..TURE TA~KS
Two preferred-temperature tanks were used in a limited series of experiments
concerning the .region most frequented in a vertical temperature gradient by
variously acclimated salmon fry. These tanks, illustrated in Figure 2, stand
36 inches high, with length and width measurements of 36 and 20 inches respec-
tively. Plate glass facings held in angle iron edging and bolted to the main frame
complete the outer structure. \Vater, usually of low temperature, is introduced at
the bottom through a metal tube perforated uniformly over its length with small
holes, the displaced \Vater being drained off at the top. A coiled copper tube
FrGURE 2. A preferendum tank davided into ten tells by white cord for recording of fish positions
Under low illumination. Thermometers are situated in the front nght of f'ach cell. A faint outline
-of the coiled copper tube for carrying hct water is visible within the tank.
A~~~Tf'lllllt.Mif ··•••
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forming-a closed system conducts hot water in a downward spiral around the
inside p,~riphery of the tank in contradirection t\) the rising "cold fro!lt". By
adjusting the temperature and rate of flow of the introduced cold water as well
as that of the hot water ·within the copper coil, any desired tempera cure gradient
can be obtained.
l\IETHODS
The approach to the problem of describing the temperature-tolerance of
young Pacific salmon has been to hold samples of each species at different non-
lethal temperatures but otherwise similar conditions. These variously accl~mated
samples were later tested for their tolerance to high and to low temperatures,
ranging from rapidly lethal to sublethal levels. The data were treated graphically
or mathematically to distinguish such differences as might occur.
The application of these methods are considered below.
..:\CCLUlATION
As early as 1895 Davenport and Castle reported on the "acclimatization oi
organisms to high temperature", and threads of this principle have been variously
w·oven around the theme of temperature relations in fish by Loeb and \.Vasteneys
(1912), Hathaway (1927), Binet and l\Iorin(l934), Sumner and Doudoroff (1938),
and more generally by \Veigmann (1929, 1930, 1936), Ogle and ~Iills (1933),
Heilbrunn (1943), and others. Yet a great deal of experimental \Vork has been
done \vithout adequate regard for the conditioning effects of temperature in the
past-history of animals. A study of changes in heat-tolerance for the goldfish,
Carassius auratus, from both low (4°C.) and moderately high (20°C.) temperature-
acclimations (Brett, 1946) led to the general conclusion that rate of acclimation
was related to metabolic rate. Thus, at low temperatures, acclimation proceeded
at a slow rate but incre:tsed to a very rapid rate at high temperatures, probably
in geometric progression. Conversely the loss of acclimation to any level of tem-
perature was a comparatively slow process under most conditions.
The thermal history for the egg, alevin and early fry stage for each of the
salmon species was 8.8°C. with very little variation. \Vhen the fry were about
two months old the process of moving ther::-t through a series of temperature-
acclimations was initiated. The ·minimttm standards set for acclimation from the
holding-trough temperature of 8.8°C. to any one of the following temperatures
were:
'I' -oc"" 0 i) •
To l0°C.
To 20°C.
To 23°C.(or 2-!°C.)
4 weeks at 5°C.
3 weeks at l0°C'.
3 weeks at l;)°C.
1 week at 15°C.t 2 weeks at 20°C.
1 week at l5°C., 1 week at 20°C.,
1 week at 23"~"'
Repetition of sQme of the upper Iethal~t:emperature experiments after one
and even five months' lapse of time without further change in acclimation gave
no significant change in heat-tolerance.
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inclicatcd
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live specie ..
next ;n linl
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about 40 1\\
obtained ii\: ,.
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Each l
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chosen by p~
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by dosP. ins
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of an asym
various tem
fry from 10
1937) that
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The first species to be investigated was the spring salmon. Preliminary tests
indicated that a maximum acclimation temperature without significant loss in
the holding troughs was close to 24°C. This was later substantiated by success-
fully culturing over 200 young spring salmon at 2·eC., at which temperature
they proved to be very active and to be good feeders, but had reduced growth
rate when compared with groups from lower temperatures, particularly those
from 15°C. A level of 2-±°C. was introduced, therefore, as the highest standard
acclimation temperature for all species. By chance one of the most hardy of the
five species had been used to set the standard for the others. The pink salmon,
next in line by age for progressive acclimation to 24°C., fed poorly. Immediate
lethal-temperature experiments following minimum acclimation standards for
24°C. showed a breaking away fro~ the usuaf temperature-time mortality curve
after prolonged exposure to a temperature of 24.5°C. Extrapolation of this
divergent trend indicated that 2-!°C. bordered on 50 per cent lethality for pro-
longed exposure. Evidence of the unsatisfactory nature of such a high acclimation
temperature was convincing in the sockeye fry. The latter species, while apparently
lTl.Ore resistant than the pink salmon, showed a complete aversion to feeding in
about 40 per cent of cases which later appe.:'lred as typical "pin heads", often
obtained in hatcheries when young fish do not develop the feeding habit (al-
though at an equable temperature). The growth of the remainder was curtailed
~lmost completely and their activity was quite apparently reduced. Conse-
quently, the acclimation temperature was lowered to 23°C. for the sockeye, the
chum and the coho. Insufficient numbers of spring and pink salmon remained to
provide comparison at the ne\v acclimation level.
r·PPER LETHAL TE11:PERATURE
The method of lethal-temperature determination as conducted by· Fry and
associates has remained basically consistent from its inception (Brett, 1941),
with the marked exception of the duration of exposure to given temperatures
which produce some but not complete mor.tality. The analysis and interpretation
of the data have changed and expanded considerably (see Fry et al, 1942; Brett,
1944; Doudoroff, 19-!5; Fry et al, 19-±G; Fry, 1947a; Hart, 1947, HH9). \Vithout
tracing the history of these changes, a discussion of the present treatment of
temperature data and the current terminology used to describe the-observations
IS necessary ..
Each lethal bath is regulated to a constant t~r.tperatur~:; aimost exactly
0.5°C. different from the temperature of an adjacent bath and appropriately
chosen by preliminary tests to span the conditions from rapid to slO\v, partial, or
non-lethal temperature effects. Records of the times to death for all fish are kept
by close inspection. These latter have been called the resistance tint.es which, if
plotted graphically on normaL axes in order of occurrence, take on the appearance
of an asymmetrical S-curve. A series of such curves can be plotted, inc:luding the
various temperatures investigated, as has been done for a sample of spring salmon
fry from l0°C. acclimation in Figure 3a. It has been demonstrated (Bliss, 1935a,
1937) that many dosage-mortality curves can be resolved into straight-tine
;{
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274
relations if the proper derivative of time is applied and the variation of ·
response is normally distributed within the sample. By converting the axes into
probability units as one variable (order of death) and logarithm of time as the
other variable (time to death) a linear progression of points is frequently obtained
(Figure 3b). The application of this principle to lethal··temperature experiments
with fish was shown to be quite appropriate by Fry et al. (1S46). The hundreds of
observations which have since been made on many species of fish (Hart, 19-1-7.
1949; present paper) and found to adhere closely to the above interpretation
have added convincingly to the validity of the relation. The normalitv of the
distributbn permits application of standarrl. statistical treatments. In ~ddition
the mean, median and mode, all coincide in a normal distribution, so the descrip-
tive value of the single figure (50 per cent puint) is evident.
From each lethal-temperature experiment a series of median resistance times
may be plotted for the corresponding levels of temperature, in the manner of
Figure 4a. It is apparent that for every state of acclimation the possibility of a
series of such points exists. Thus, an overall picture of the effect of temperature
can be constructed. Conveniently enough these curves, in the case of high-
temperature tolerance, can be resoln~d into straight liaes by using the logarithm
of time against temperature (Figure 4/;1). A distinct break in the semilogarithmic
·plot, not otherwise evident, occurs at a progressively earlier point of time in the
lines for lower levels of acclimatitJn (usually below 20° to 15°C. for Pacific salmon).
The discovery of thi8 break (Fry et al., 1946) and its variable occurrence with
acclimation was most significant and has constituted the main difference in
experimental procedure from that of earlier investigations. The definition of
lethal temperature h3.s been that temperature at w·hich 50 per cent of the population
is dead after inde.finite exposure. The stumbling block in the past has been the
duration of the experimental test. Doudoroff (1945) questioned the 14-hour p~riod
used by Fry et al. (1942) and shortened to 12 hours by Brett (1944). The answer,
as indicated above, was provided when breaks in the resistance time-temperature
relations showed that mortality from temperature as a primary cause had ceased.
The duration, even as long as the seven-day period used for Pacific salmC':l
should be govern~d by this factor since it varies for different species and different
acclimations, As long as the resistance times continue to be finite the fish arc
considered to b~ in a zvne of resisfa1tce. Beyond this lies the zone of tolera11ce
(Fry, 1947a).
At one acclimation there are any number of resistance times but only one
lethal temperature. To distinguish indices derived from high-and low-temper;l-
ture experiments the terms ·upper and lower lethal tem~eratures are applit..J
respectively.
LOWER LETHAL TEMPERATURE
Temperatures distributed from 0°C. (0.1 o ± 0.1 °C.) to 7°C. at one degree
intervals were used in lower lethal-temperature determinations. Olle or tv.to in·
stances of experiments at fractional degrees are ~eportedf but the use of 20 fish
per tank fmm a limited total sample preclwded crrrying the investigation to a
finer point.
-
~ PM .p
from high
cessation of
romplete loss
Often no
lethal-tern
from a large
t.•quabh~
h:u been
~ample of
I 042; Brett,
operations in
Close in
death the
rhilled fish
reveries, a co
highly signi
correlation r
almost enti
long, 3 inches
sa.nples for
test tempera
rt>gardless of
taitwr was
container
mort ali tics,
(similar to u
pattern wh
•1ny further
experiments
line of
I
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1'
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I
L r-
1
l
(
I
..
_,......_ _ _.....-..n ....... ~-----------·--. ~c
275
There seems to be relatively little trouble in deciding when a fish has died
from high temperature, except in a few instances (Brett, 1944; Hart, 1949). A
cessation of rec;:piratory movements and muscular contraction accompanied by
romplete loss of response to stimuli have been regarded as quite decisive criteria.
Often no reference concerning such end points is included in reports on upper
lethal-temperature experiments. A check on 180 Pacific salmor., including all
species, by removing the fish to a lower temperature immediately after "death''
was recorded, resulted in no recoveries. On the other hand the depressing effects
of low temperatures, producing a type of "suspended animation", have been the
source of considerable trouble in establishing satisfactory criteria of death from
this cause. Usually groups of fish at a single low temperature have been removed
from a large sample and tested for mortality by immersion in water of a more
equable temperature, the recoveries being noted over the first 24 hours. This
has been performed at intervals throughout the ~xperiment, or, when only a small
sample of fish was available, at the end of a given exposure time (Fry et al.,
1942; Brett, 1944). The lack of a more direct criterion of death has restricted
operations in this field.
Close inspection of Pacific salmon revealed that with the approach of cold-
death the characteristically immobile and closely compressed opercula of the
chilled fish commence to fan out perceptibly. By systematically recording this
symptom before removal of each sample to a testing tank (at l2°C.) for re-
coveries, a comparison of the ''predicted" and "actual" mortalities was made. A
highly significant correlation between the two was obtained (coefficient of
correlation r = + .90, P.o1 = .37), the cases o non-agreement being scattered
almost entirely on the side of greater "actual'' mortality. Unpredicted recovery
was virtually non-existent. Consequently, the resistance times could be tabluated
from direct observation of the fish in the lethal baths as in the upper lethal
experiments, and the median resistance times plotted for different degrees of low
temperature, a system hitherto not em?loyed in low temperature work.
In practice, lots of ten fish 'vere placed in small plastic cylinders (6 inches
long. 3 inches in diameter) capped at either end with plastic screening. Two such
samples for each species from a given acclimation were inspected at each of the
test temperatures. vVhen the number of predicted dead in the first cylinder-
regardless of the number dead in the second, had reached 50 per cent, the con,
tainer was removed to running water at l2°C. The treatment of the second
container varied in order to test the prediction value over a gre:ater range of
mortalities, but usually contained estimated deaths of between 50 and 100 per
cent. The number of actual dead was recorded 24 hours later and excluded all
fish shmving perceptible activity--rarely a questionable category.
The median resistance times, determined by plotting the order of death
(similar to upper temperature· resistance), when transposed to a graph follow a
pattern which has not been possible to convert into a more convenient form by
any further resolution of the data. A solution [or the problem of duration in the
experiments on effects of high mperature was presented. Following the same
~
line of reasoning, though not <-apparent in this case, a flattening-out of the
curves to become asymptopic with the time axis. is indicative of continued, pro-
-
\
l
I
l
l
r
t r
I
l
I
r
r
. .
longed survival of the sample under the corresponding temperature conditions.
This latter inflection occurs by at least 5,000 minutes (three and a half days) in
practic::tlly all cases, and considerably earlier for the higher acclimations. Conse-
quently, a limit of 5,500 minutes was set for the duration of alllow-temnerature ..
work.
A further use of the lethal temperature to delineate the biokinetic range of
fishes has been illustrated by the construction of a trapezium relating upper and
lower lethal temperatures to acclimation tempet·ature (Fry et al., 19-i2, and later
references). For every stage of acclimation there is a corresponding lethal tem-
perature. In the upper temperature region the lethal and acclimation tempera-
. tures approach each other, finally providing an ultimate upper lethal temperature
(Fry et al., 1946) beyond 'vhich no extension of temperature-tolerance is possible
for the species as we kno·w it. Such relations for the Pacific salmon have be• n
illustrated in Figures 20 to 2-1.
PREFERRED TEMPERATURE
The specific aim of the investigation was to work out in some detail the
limits of tolerance; it was also possible to carry out research on temperature
selection but of a preliminary nature and consequently presented as such.
l\rieasurements of the aggregatio~. of fish in horizontal temperature gradients
have been conducted effectively by Doudoroff (1938) and Sullivan (19-HJ).
Empfiasis must be placed on the horizontal nature of these gradients since
vertical gradients were employed for the Pacific salmon. One highly significant
difference is apparent, namely, that a gravity gradient is inextricably involved
in a vertical tank. It has been customary to reduce as far as possible all interfering
factors when recording the responses of an organism to a gradient of a given
identity. The methods employed in the present instance were to habituate ten
previously acclimated fry to feeding freely in the preferendum tank for one week
at the same acclimation temperature. No other control was instituted. Lh·c
Daphnia regularly introduced with finely ground food, and slowly swept around
the tank by ~urrents produced through .'.eration, served to scatter the ftsh in an
irregular manner throughout the tank, Lighting during the haLituation period
was from overhead 1.10-watt bt.tlbs and from sunlight through side windows
(Figure 2). .
On the day of an experiment, feeding was reduced (excessively fed fish tencl
to sink to the bottom when inactive) and only between 10 p.m. and midni~~t
were observation'; on distribution in a temperature gradient recorded. At thts
time lighting, sufficient only to re;,:-ord positi\ms accurately, was produced by
two 3-candle-power sources, placed 35 to 40 inches on either side of a middle
point of the tank Any defi!nce of territory which had been exhibited under fu!l
illumination was never displayed in the gr£atly reduced lighting of an exp:n· ·
ment. The distribution in various thermal gradients was then noted by counung
the number in each cell of known temperature.
..
in rcspon
These
the five
.txes, a
acdima
during
The 1
tTable-
\':1:.; been
mortalit)
The
the lcvell
par~\llel
~\·rk·s of
that for
<ttT\ima
times for
n-sultcd
(•quailed
st•rvc><l r
by Fry
or lesser
!',\)C<'lCS
ll·ngth ~
.wt·limat
1Co
mcnt of
1
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I)
1:
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..... ,
277
STATISTICAL TREAT'.IENT
The various sources of variability in response to extremes of temperature
and the statistical treatment of the data are presented in Appendix I. ::\'Iost of
the calculations were made by the method of analysis of variance.1
RESULTS
The actual levels of tolerance to extremes of temperature and the differences
in response among the five species have constituted the main theme of study.
These are presented by dealing with one aspect of temperature and considering
the five species collectively under each heading.
"CPPER LUHTS {,tF TEMPERA.TURE TOLERANCE
SPRING SAJ ... ~ION. Upper limits of temperature-tolerance include the resistance
times and lethal temperatures for each acclimation. A typical series of mortality
times at different test temperatures has been depicted in Figure 3a on normal
axes, and on probit and logarithmic axes in Figure 39 for young spring salmon
acclimated to l0°C. At 24.0°C. and below no deaths were recorded for that sample
during the 10,000-minute (one week) duration of the experiment (Table IV).
The lethal temperature therefore lies somewhere between 24.0° aP'.:!.. ~4.5°C.
(Table XI). In the latter graph the mean of the logarithms of the times to death
has been calculated. The very close approximation ot the median and mean
mortality times is apparent and in agreemet't with the findings of Fry eta!., 194G.
The median times to death have bef:'n plotted further in Figure 4a, illustrating
the levelling-off of the median resistance times at lower temperatures to become
parallel \vith the time axis. In Figure 4b the resolution of these data into a linear
series of points has been achieved. The line A-B drawn almost at right angles to
that for the median resistance times for 5°, 10° and l5°C. acclimations denotes
the po;nts of time at which continuation of the experiment provides no change in
results (up to 1-0,000 minutes). Although the resistance times of the higher
acclimated fish (20° and 24°C.) showed an increased t0lerance at comparable
times for periods of 1,000 minutes (about 17 hours) and less, continued exposure
resulted in continued mottality to a level of death (line B-C) which fi.nallv
equalled that of the lower acclimation of l5°C. This phenom~non has been ob-
served repeatedly over the higher levels of acclimation fc.r every species studied
by Fry et al., (1942, 1946) and Hart (Hl-4:7, 19-!9). It is a characteristic, to a greater
or lesser extent, of all the species considered in the following presentation.
PINK SAL"!\!ON. The pink salmon were decidedly the most diffirult of the five
species to handle in fresh water after the first month of feeding, and for their
length showed the least \Vcight (Table III). The difficulties experienred in
arclimating this species to 24°C. were noted em·li~r. Their intolerance to a tem-
perature as high as 24.0°C. is also apparent in the distribution of their resistance
1Complete tables of data are included in a Ph.D. thesis, 1951, in the libraries of the Depart-
ment of Zoology, University of Toronto, and the Pacific Biological Station, Xanaimo, B.C.
l ~~
l I : ( ' I : I
' l· I
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't' ~ 1
''1 : L r
! : .... ,. .. ' :~ l '" r ! !
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278 ,-, ;· 7 • I
90 r-. • • •
26·0° I I 25·5° j 25•0° .. y. \." .. / j/ I I 70 • • ;· •
I I I ~ • •
0 I I I· <
"' 0 50 • r • -50 "lo Morfali!y
I /· .J ... • ( • z I I w
0
a::
w • • • ;· n. I I I • • • fl
I J /. I
10 /:!. /~ • I / I
_j
0 200 400 1,000
TIME TO DEATH MINUTES
FIGURE 3a: Times to death at different lethaltest temperatures amdng young spring
salmon acclimated to 10°C. Plotted on arithmetric axes.
l 90 I •
I
I •
255"1 ~ I I
0
"'
tJ
w
0
... z
~! j w
()
a::
w
• Q.
) u j I \ . ~ .~
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260'1
70 • I
50 I
I
30
10.
i
;:
"' I
10 100
TIME
{
t
ro DEATH
•
Minutu
X: Geometric mean
tesistance time.
FIGURE 3b. Times to death at different lethaltest temperatures among young spring
salmon acclimated to l0°C, Plotted on probit X logarithmic axes, Calculated geometric
mean resistance times coincide with the· median resistance times (at probit 5.0) •
f :~
r-~------
. _ ... rr~~n1Uillu:rlJ•••~ iW &44 • *"""
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FIGURE
28 I
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t,) i • I·
t.l 26.
a::
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a::
t.l
II.
:!
w 24 ...
.. ~
FtGURE 4
acclimated
~
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278
0
<(
U.l
0
.... z
U.l
0
u:.
1&.1
II.
0
<
11..1
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·-z
11..1
0
a:
1.1.1
0..
90
70
!50
30
10
90
70
50
30
10.
l 7 ;· 7 I • • • •
26·0· I I 255· /25·0° 24·0 \... ../ j/ I I • r.; r •
I I I • Cl • •
I I I· I • • • --50°/o Mortality
I I. /· • • I I I • • ) ;· I I I • • • • I J /. I //. /. • / I
0
FIGURE 3a.•
10
200 400 6()0 l;JOO
TIME TO DEATH MINUTES
Times to death at different lethaltest temperatures among young spring
salmon acclimated to lV°C. Plotted on arithmetric axes.
I I • •
no·.f 25·5· I •
.I • I I
i •
f I • " I .. •
/·
• • /~J
IQO
TIME T'O
I •
25{)"' • I • I • I •
1 •
I •
I
'·· I
DEATH
.I
.. ..l
I • 1
;:
• I • I • I
LJ.
t,ooo
M :nutes
X: Geometric m•an
reshlance lima.
Fr:tURE 3b. Times to death ut different lethaltest temperatures among young spring
salmon acclimated to 10°C, Plotted on probit X logarithmic axes. Calculated geometric
tnean resistance tknes coincide with the·. .,.;.b.n resistan('e times (at pro bit 5.0).
r '''c-~-.::-:~-.::: ~~JIIo ... T.
:·
1
1
•
24
22
t.
FIGURE ~b.
acclimated
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.,
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. '
...,.
. . . . ·:. ' .. ; .'" . . -. . . . . ...... .
!-
~ 28 oe \\
(,) . , ~·\. Acclimaticn temp.
w
a:
;:)
1-
<
a:
w
IL
!E , ...
1-
~~""'· 24° \\ ~
261-0• 0~·--~ \. -------0 ---~--
1 \ " -o/15~ --h> 0 ~
I \ •o• • 0 .,/'
I ~--------------·--------------------24 •
\
•
• \
• 50 \ ~ •
22 !-
II I I I I I
0 2 4 6 8 10
T I M E TO 5 0._,• M 0 R TALl T Y 1,000 Minuh;,
FIGU...,.& 4a. Median resistance times to high temperatures among young spring ::.almon
acciimated to temperatures indicated. Plotted on arithmetric axes.
2'8-
..; •
2 2.
-----·----------------------------------------~
Acclimation TtmiJ.
z••......._
it
~ ·~
2 o•
·~
10".......... -...........__. •
<>-~-9 ~ ~.~ . ~.......... • 9 ••
5" "-.. ~ ""' '()-~ ,e_------~---•,.E
•" .o-I ·~ ,;---------.-----
• I "v~----------------A
TIME TO 50% MORTALlTY -Mlnultl
279
FIGURE 4b. Median resistance times to high temperatures among young spring salmon
acclimated to temperatures indicated. Plotted on arithmetric X logarithmic axes. (See text
for further explanation.)
-
IIIII A
•: I
~ . . l
"",r
..
~
. ~~:...:.:~_:._-· · ---·· ·iiru:+Ce~
.......
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280
times following a minimum period of acclimation to this level of temperature
(Table IV). After 2,000 minutes' exposure to 25.5°, 25.0° and 2-1.5°C., no increase
in their tolerance over that for 20°C. acclimated s<?mples was obtained.
The results for lower acclimations (Figure 5) were in accordance with general
expectations except for the 5°C. group. ~Iortality was so rapid in leth;:tl tanks
with tempeqt.tures of 22.5° and 23.0°C. that it was decided to test the majority
of the remainder of a limited sample at 21.0° and 19.0°C. Only four fish finally
u . L
I
ILl 26-
a:
::>
1-
c( ' a: r--
w I ~ I
w 24 -· .... I I_
22-
Acctlmatio" Temp.
TIME TO 50"1'• MORTALITY -Minutes
FIGT:RE 5. :\Iedian resistance times to high,temperatures among young pink: salmon
acclimated to temperatures indicated. The encircled point for 5°C, acclimated p:inks
denotes the use of four fish instead of the normal ten in other points.
remained for an intermediate test at 22.0°C. The reliability of these cbta is
therefor~ not as great as that for the more orderly points of higher acclimations.
socKEYE .?AL~roN. Sockeye salmon, although held at a maximum acclimtttion
of 23°C. (thus 1 °C', lower than the highest for pink salmon), also showed an
inherent intolerance for such levels of temperature as 2-1.0°C. and 2-1.5°C. after
prolonged exposure (Table IV, Figure()). Howev~, of the five species, the sockeye
are probably the best adapted to fresh water, often spending two years in lakes
before migrating seaward. A completely fresh-water subspecies is also commonly
reported (Oythond, 1030). The responses of the young sockeye to high ternpera-
tures were quite similar in pattern to those of a fresh-water species of Salmonidac.
SalveUnus fontinalis (F'ry et al., 19-10). The lines connecting median resistanrc
times for acclimations of 20°C. and below are fairly regularly spaced and are not
significantly different in slope to be <li~tinguished as not parallel (Table X).
,,
1
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mately
u .
w.
a:
::> ...
<C
a:
ILl
Ei
... ,
"" I
CHC,
in. Table
for expe
1,000 mi
in life al
Chit1 an
after 9,0
half the
· to 2-1: °C ..
COif_'
the stoc
ted som
...i;.
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tu[i
ease
• I
I
. ' t
281
The apparent variation in slope for the l5°C. acclimated group is not beyond
what might be expected from chance. This has been derived from a consideration
of the total data mustered in the tables of analysis of variance (Tables VI to X).
As a result,.in this instance only, the line for the l5°C. acclimation has not been
drawn by inspection as the best straight line for the plotted points, but as the
most likely relation to be expected on the basis of the total data, that is, approxi-
mately parallel.
t A'<limolioo Torno.
281-
1
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L
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W2GI--
c:: I
::l :
1-
"' l
0:: .:--
UJ 1
Q. i
~ 241-
1-I ~
22L
I
to•
s•
-o-I
"'-. I ;t----------·1
.I I -------------1
lt,.... _ ____;t.....__...J_...L-LI _t_l _t_! ..LI url __ .t__.._j_J_I I I l I I l i Ill!
10 100 1,000 10,000
TIME TO 50"1~ MORTALITY -Minutes
FtGt:RE 6. ).ledian resistance times to high temperatures among young sockeye saimon
acclimated to temperatures indicated. A somewhat lowered re::.i::.tance among the 23°
and 20°C. acclimated groups for prolonged exposure to 24.5°C., below the expected level,
is indicated by the dotted line on the extreme right-hand side.
CHUM SAL1ION. The results of experiments with chum salmon are recorded
in Table VII and Figure 9. This species showed the greatest amount of variability
for experiments in which the mean resistance time approached or exceeded
1,000 minutes. Like the pink salmon, the chum normally move to sea quite early
in life although some have been maintained in fresh water up to two years by
Chirt and Kuroda (1935). Acclimation to 23°C. was quite successful. However,
after 9,000 minutes' (6 days') exposure to 2-1:°C. in a temperature-tolerance test,
half the sample had died, ~onfirrning the impossibility of aedimating this species
·to 24°C.
COHO SA.L~[ON. An accident in the early history of the coho salmon eliminated
the stock of eggs held in one of two troughs. This loss, while unselective 1 necessita~
ted some curtailment in the programme of study. At the time of experimentation
4 ,hOt ... ,...
I.
~ .
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282
28
22 -
10
FIGURE 7.
Acclimcticn Tamp.
I I II !Ill
100 1,000 10,000
TIME TO 50"h MORTAL!TY -Minuln
Median resistance times to high temperatures among young chum salmon
acclimated to temperatures indicated.
Acclimation Temp.
I u..I __ _,____,_--1-_,LJ I I I I
10 100
TIME TO !10"1• MORTALITY -Mlnutu
FIGCRE 8. ~ledian resistance times to high temperatures among young coho salmon
acclimated to temperatures indicated.
---
I
l
1
f • 1,
l
~
i •
I
t
J
I
with upper}
coho were .
the spring f.
permit morl
' In retrosp
between c
temperatu.
Ther
PROLO
high temp
5°C. Thes ~
exposure \VI.
In this res1
sockeye re
l
salmon, it· conditions~~
tures have~{
one week)\
The results'
Figures 9 al
3,000 minu
that for th
first day (t
period a rj
chum salm ·
dir~ction oj
penmentat1
LOWER LL
SPRING·
lethal level
species amt
with 50 ped
total of 20 ·
times at 5
of removin.
checking''
a single tes .
mortality. j
No siz~
on heat-told
ever, were ;1
such that tl
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was on han.
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283
with upper lethal temperatures, ic was apparent that at higher acclimations the
coho were conforming very closely to the reaction times already determined for
the spring salmon. The remaining tests in this series were therefore bypassed to
permit more intensive investigation in the relatively unexplored low-lethal range.
In retrospect this was perhaps unfortunate as it now appears that a difference
between coho and spring salmon, where such occurs, is present in their high-
temperature tolerance from low acclimations.
The results for the coho appear in Table IV and Figure 8 .
PROLONGED EXPOSURE. An experiment concerning long-term exposure to
high temperatures was performed with sockeye and chum salmon acclimate(l to
5°C. These fish do not feed readily at critical high temperatures, so prolonged
exposure would inevitably cause death from malnutrition. if from no other cause.
In this respect the two species are alike. Since they differ in mig1atory habits, the
sockeye remaining in fresh water usually for at least one year longer than chum
salmon~ it is quite possible that they d11ier in ability to tolerate fresh-water
conditions (cf. Hoar and Bell, 1950). So far, few experiments with high tempera-
tures have involved exposure times in excess of 10,000 minutes (approximately
one week), particularly for fish from acclimation temperatures below l5°C.
The results for 30,000 minutes' exposure for these two species are recorded in
Figures 9 and 10. The sockeye typically showed no additional mortalities beyond
3,000 minutes. The pattern of mortality in the chum salmon was very similar to
that for the sockeye, with no further deaths. recorded between the end of the
first day (1,440 minutes) and the end of a week (10,080 minutes). Beyond this
period a rather unexpected but orderly progress of mortality appeared in the
chum salmon samples. Speculation as to the cause of death might be made in the
direction of the relative intolerance of this species to fresh water; rurther ex-
perimentation is desirable.
LowER LIMITS OF TEMPERATURE ToLERANCE
SPRING SAL:MON. The method of determining the resistance times at low-
lethal levels of temperature usually involved two samples of ten fish of the same
species and acclimation for each test temperature. The removal of one sample
with 50 per cent predicted dead changed each test :Jefore completion from a
total of 20 to a total of 10 subjects, hence the plotting of the individual resistance
times at 5 per cent intervals changed to 10 per cent intervals follo\ving the time
of removing the first sample. The slight inconvenience involved \Vas a result of
checking "predicted" against "actual" dead. In this manner all mortalities from
a single test temperature could be plotted in determining the time to 50 per cent
mortality.
No size effect in Pacific salmon of the same age was demonstrated from data.
on heat-tolerance (Table XIII). Results of experiments on cold-tolerance, how-
ever, were strongly suggestive of a size influence. The method employed was not
such that the individual fish, once dead, could be later identified when the whole
sample was removed from a lethal bath. A group of fish, some living, some dead,
'Was on hand. By considering only those rases in which at least three hut not
&StAt
. .
, ~ , ~: . '"'P • , , ~ . . : , . " . "' .. '
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90 0 . /--------------j
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~ ·I ;· w ( the first, o 0 •
50 and was fo • 0 I 1-24·0° I 23·o·f the metho
2: • w I -------------remainder.·
0 30 • 0 n
a: l j { recorded o, w ~
a.. size factor~. I . / • firmatm;:. ~
10 r 0 comparat1
l I I 21·0° None die stitute the{ -------------l Prelil" I
! had been i f I
100 1,000 10,000 2-:1:0 and 2 \ I
TIME TO 0 EATH -M inutea ti with upperl I FrGt:RE 9. Times to death at various high temperatures among young sockeye salmon
acclimated to 5°C. a3d tested for 30,000 minutes (approximately three weeks). I
l
l
90 /. I tempe I 0. 0 ;· I of death.
I I
!'' 0 • 0 '
70 I l
0 • 0 l I
c( I l w
0 0 L
!50 • i I 1-··l l • 0 2t·o·J standing z 22/ I l w 23·0·
0 30 • 0 stopped. a: j· I w •
10. I 10 I l -! I I temperatu
Even 10c-(
I (three day
100 1,000 10,000 those ta I
The I TIME TO 0 EATH -Mloutu I nounced
FrGrRE 10. Times to death at various high temperatures among young chum salmon low tern l
acclimated to 5°C. and tested for 30,000 minutes (approximately three weeks). I I
l
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285
more than seven had succumbed, comparison of the sizes among all specimens
sho,ved nearly twice as many living fish above the mean length for the total
sample as dead fish. Since the measurements were made some time after death,
weights were pot taken. The mean lengths and standard errors of the two groups
were: living = 5.00 ± 0.046 em., dead = 4.75 ± 0.043 em. The data show a
statistically significant difference (Table XIV).
Evidence was procured for t'~.VO separate lethal effects of low temperature:
the first, occurring only at the lowest temperatures, was very rapid and decisive,
and was follmved by a second series of deaths after considerable delay. Owing to
the methods employed, the first mortalities could not be sorted out from the
remainder. They constituted a relatively small fraction of the total dead. Fn-
recorded observation at the time of an experiment revealed an apparently distinct
size factor in this primary phase of death, the smallest fish dying first. Con-
firmatory experiments will be required for adequate proof. The presence of t,hese
comparatively smaller fish in the samples of dead fish recorded above may con-
stitute the main source of difference between the two major group~.
Preliminary tests with spring salmon, before the system of predicting death
had been instituted, were performed at 0.5°C. intervals from 0° to 3°C. (Figure 11,
24° and 20°C. acclimations; Table V.) The reasoning, derived from experience
with upper lethal experiments, was fa.IIacious in part since the range of low tem-
peratures causing death for 24°C. acclimated salmon was almost twice as great,
within the same t!.~·ne limits (covering 6 rather than 3 degrees C.). The doubly
"expensive" technique of closely spaced temperature tests coupled with sampling
for dead t 1 ·roughout the experiment was replaced by the predicting system for
tests at 1 °C. interval in the remaining cases reported for the spring salmon.
The median resistance times follow a rather varied relation '\vit!l increasing
temperature (Figure 11), and are apparently complicated by more than one cause
of death. The sigmoid shape of the curves is one characteristic which persists
throughout the remaining species, particularly at higher acclimations.
PINK SAL~ION. Although a few preliminary tests were made with l0°C. ac-
climated pink salmon, 5}/2 months old, mortality in the fresh-water holding
troughs appeared during the last two weeks in sufficient proportions to signify
some intolerance to these conditions. 3mall samples were incapable of y.,·ith-
standing 5°C, Attempts to continue work with this species in fresh water w-ere
stopped.
SOCKEYE SAL1ION. The inability of Pacific salmon to tolerate sudden im-
mersion in· low temperatures was well exemplified in the work with young sockeye
salmon. For survival in nature the necessity for this species to acclimate to low
temperatures is emphasized by the results illustrated in Figure 12 (Table V).
Even l0°C. acclimated samples succumhed to 2° and 3°C. within 4,000 minutes'
(three days') exposure, and~ temperature of 0°C. caused some mortality amongst
those taken from holding tanks at 5°C.
The sigmoid pattern of the resistance time-temperature curves is most pro-
nounced among the sockeye. An initial period of rapidly increasing resistance to
low temperature (for 20° to l0°C. acclimation) is followed by relatively little
,_
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286
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Acclimation
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TIME TO 50~. MORTALITY -1,000 Minutu
5
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t
FIGURE 11. l\tfedian.resistance times to low temperatures among young spring salmon
acclimated to temperatures indicated. Arrows signify tests at temperatures which caused
less than 50 per cent death for 5,500 minutes• exposure if placed above the line, or greater
than 50 per cent by the time indicated if below the line.
B
Acclimation t
T!!mp.
6
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TIMe TO sc•;. MORT ALIT'/-1,000 Minutes
FIGURE 12. Median resistance times to low temperatures among young sockeye ~mlmon
acclimated to temperatures indicated. Arrows used as stated in Figure 11.
-
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287
change in resistance for two and three degrees' increase in temperature. No
mortality occurs within a degree or so above this latter zone even for a considerably
increased exposure time. The presence of this "break" at an exposure time of at
least 4,000 minutes for fish acclimated to l0°C. and higher (usually occurring at
test temperatures of 2°C. and above) supports the overall experimental time of
5,500 minutes for lower lethal-temperature determinations.
CH1Thf. SALMON. The greatest difference in response to low temperatures was
e.xhibited by the chum salmon from different acclimations (Table V, Figure 13).
\Vhen taken from 23°C. and put at 7°C., 50 per cent mortality occurred by
4,000 minutes. From l0°C., however, mortality at 0°C. was observed only toward
the very end of the imposed test time. This was somewhat surprising in view of
the scant but indicative findings on the intolerance discovered for the pink
salmon, t0. which the chums appear to be most closely related (Milne, 1948).
COHO SALMON. The data and curves m~·strating the median resistance times
to low temperatures for coho salmon appear in Table V and Figure 14. The sig-
nificant mortality among members of this species at 0°C. when acclimated to
as low as 5°C. demonstrates how confined the coho are to temperatures above
the freezing point of water. In general their reactions show the same trends as in
the other Pacific salmon.
MIXED LETHAL EFFECTS. Brief rr.ention was made of two distinct responses
observed while studying the lethal effects of low temperatures. The presence of
very rapid mortalities in CO'ltr~st with delayed lethal effects, either between.
tiamples at slightly different temperatures, or within samples at given critical
temperatures, was apparent from even superficial examination. Doudoroff (1942)
observed somewhat similar phenomena among young greenfish, Girella nigricans,
and distinguished between "primary chill-coma" and "secondary c\ill-coma".
He records that "The initial shock was not manifest until several seconds after
transfer to the low temperature, and apparently was not due to stimulation of the
cutaneous sense organs, but was produced only when the low temperature had
penetrated internally, probably to the central nervous system. Accordingly, it
was more delayed in large specimens than in small ones". The discovery of a
satisfactory criterion of cold-death :J.mong the Pacific salmon permitted a more
critical study of the time-temperature-acclimation relations for death. Results for
sockeye salmon will be presented, being more extensive but not unique. By plot-
ting the data on probability X logarithmic paper it was possible to discriminate
clearly between the two trerl~;:: of death. From 23°C. acclimation (Figure 15a),
1 °C. caused rapid death for all individuals (as presumably would lower tempera-
tures); 2° to 3°C. spHt th€ samples into rapid anci delayed deaths as shown;
4° to 6°C. resulted in only delayed deaths; above 6°C., less than 50 per cent
mortality was obtained. From 20°C. acclimation (Figure 15b) 0°C. caused rapid
mortality; 0.5°C. divided the sample into the two types of death; l°C. and above
caused delayed to no mortality. From l5°C. acclimation (Figure 1.5c) one case
of mortality was observed for a lethal-test temperature of 0°C. followed by de-
layed to no mortality at higher temperatures. The time to 50 per cent. mortality
is consequently affected by per cent occurrence of ''primary" cold-deaths within
the sample and by the size of the fish which chance to be present in that sample.
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288
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TIME TO 50c/• MORTALITY-1,000 Minutes
FIGCRE 13. :Median resistance times to low temperatures among young chum salmon
acclimated to temperatures indicated, Arrows used as stated in Figure 11.
u •
4
Acclimation
Temp.
""
t
----·---------------'
l
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t
10~-----,
.~~~---~~~---~:-.~ l 2 3 4
TIME TO 50% MORTALITY -1,000 Minutu
FIGCRE U. :\Iedian r~sistance times to low temperatures among young coho salmon
acclimated to temperatures indicated. Arrows used as stated in Figure 11.
···--~,.-...
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DEATH Minutes
FIGUREr l5a. Times to death at various low temperatures a-nang young sockeye salmon acclima-
ted to 23°C. Plotted on probit X logarithmic axes.
90
I .I I we. • I
70 I .. o·o··::. ···y • c ../ .
~ e'/ w • c I I • 50 • • ... l z •• • ;· • ~ 30
a: • w ,
11.
10
10 tOO 1,000 10,000
TIME TO OE ATB Mln1.1tu
Ftol;RE 15b. Times to death at various low temperatures among young sockeye'salmon ncclima-
ted to 20°C. Plotted on probit X logarithmic axes.
I. ,_"'-~··--•,r-··-~ : ...... -.. -......... _ .. ,.--
"~ ,,
, , • ' .&iUfjljglflj@!liL;ti-~t '*' r
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10 100 1,000 10,000
TIME TO DEATH -MintJfea
FIGURE l5c. Times to death at various low temperatures among young sockeye salmon acclima·
ted to l5°C. Plotted on probit X logarithrroic axes.
A reason for greater variability in cold-temperature resistance and the variety
of inflections making up ::he median resistance time-temperature curves can be
attributed partly to these causes.
The work of Doudoroff (1942, 1945) was suggestive of an osmoregulatory
problem in the delayecl cold-deaths, possibly acting as an accessory lethal factor.
To test the hypothe-~;1s, a preliminary experiment using two groups of 20°C·
acclimated sockeye, one in fresh water and the other in Atlantic sea water diluted
to 9.9 parts per thousand, was performed at comparable low temperatures
(Figure 16). Both rapid and delayed ~old-deaths were observed at 0.2°C without
significant differ-ence in response within the two media. At 0. 7°C. an indication
of greater resistance amon~ the last surviving members in the saline solution
was present. At 3.2°C. a decided increase in the resistance was observed but not
to the point of eliminating death from low temperature in part of the sample.
Two conclusions can be drawn from this experiment. At the lowest lethal
levels of temperature a medium of salt water (slightly hypertonic) does not
alter the course of death from that observed in fresh water. Such a medium does,
however, reduce the lethal effects of low temperature for delayed cold-deat~
when resistance times exceed 1,001) minutes (about 17 31ours). From these tt
would seem that three causes for death are involved: one, a very rapid agent
usually effective within 60 minutes of exposure, a second, not so rapid in action,
and a third which is re!ated to osmotic balance.
-·
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FIGURE lJ
acclimatedl
(slig.ltly h
The
osmotics
and Hoa
~\tlantic
These fin
lethal ten
agent at
from hig ·
involved
SPRI.-
of preferr
lined und
surfaces,
demonstr
0
of the ide
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0-Frtsh Wahr
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w I/~ I
0 30
a:
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c.
10 /~ o1,-~l /3·2·~/
10
TIME TO PEATH Minutea
FIGURE 16. Times to death at various iow temperatures for samples of young sockeye salmon
acclimated to 20°C. and tested in fresh water and in sea water diluted to 9.9 parts per thousand
(slightly hypertonic). Where a difference in :~sponse was apparent a broken line has been used for
the salt-water data.
The observation that size appears to have some bearing on resistance to
osmotic stress was reported by \Vilder (1944) for sea-nm speckled trout. Huntsman
and Hoar (1940) using salinities of 20 and 28 parts per thousand concluded that
Atlantic salmon parr "as they increase in size become more resistant to sea water".
These findings in conjunction with the size effect among Pacific salmon at low
lethal temperatures support the possibility of an osmotic factor acting as a lethal
agent at low temperatures. Conversely the lack of any size relation in deaths
. from high temperatures might be taken to indicate other than osmotic factors
involved in these mortalities.
PREFERRED TEMPERATURES
Sl.'RING SALMON. Some of the inherent problems concerning the determination
of preferred temperatures for fish in a vertical temperature gradient were out-
lit-led under 41 lVIethods''. The presence of other gradients (gravity, distance from ·
surfaces, etc.), if impossible to remove or control, must be ac<..ounted for by
demonstrating the supression of these irt relation to preference for some level
<>f the identity under investigation. By changing the position of the temperature
gradient within the tank, without altering other relations, it was oossible to . .
demonstrate the selective aggregation of spring salmon in the r.egion of 12° to
'
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292
13°C. (acclimation of 20°C.) despite a highly significant difference in their position
within the tank. This distribution in space, varied yet remaining relatively constant
with respect to temperature, has been depicted for this species in Figure 17. An att-
empt has been made to conform to the relative dimensions of the tank and distribut-
ion of the fish, such that the figure presents a "graphical picture's in every sense of
the word.
z
0
U)
>
c
X
ao 60 40 20 o 20 40 60 ao
FREQUf;NCY
FIGURE 17. Frequency distribution of young spring salmon acclima-
ted to 20°C. in three successive temperature gradients, using the same
tank. The calculated preferred temperatures are noted for each distribution.
i
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I
A few observations which apply to all the species are of significance. -:\o
matter what the gradient, even reaching the lethal level, the fish wo.uld make
feeding excursions to the surface if the appropriate movements of the investigator~
which always accompanied feeding, were made. On some, although infrequ<.>nt,
occasions, under the routine procedure of !ow illumination and night-time rc-. J
cording, no selected temperatures could be determined. Activity of the fish was
too great, being more limited by the surfaces of the tank than by any other rc·
cognizable feature. No suggestion to account for the increased "excitability" on
these particular occasions can be advanced. Adequate feeding and unifonr·r
quiet conditions were always observed prior to introducing a temperatun ..
gradient. A natural "expJoring'' activity is a characteristic of the group.
-
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for ac :
~peciesi
tole~arf
spCC'IC
obscrv'
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and in
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tl
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(4 :
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differcn
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an· lima
nmside
Sp
analysi.
1 Refer
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293
PINK, SOCKEYE~ CE:t!"t AND COHO SALMON. The distribution in various tem-
perature gradient~ as inmcated by the preferrc,; -:emperatures (mean and mode)
for acclimations, mostly includiq:; 10°, 15° a11rl 20°C. in the Pacific salmon
species, are presented in the gra.ph.s used to display the zones of temperature
tolerance (Figures 20 to 2.:1:). The vr:.rl.ation in ;:esponse between the different
species was not sufficient to warr~nt dealing with them separately. Some general
observations can be made.
Despite considerable difference in temperature-al:climation, amounting to
li5°C., comparatively little difference in preferred temp:crature \Yas ob~erved
t::.1>.periment1.!ly. On the average no greater difference than 3°C. (11 o to l-!°C.)
~·:a~ displayed between means, and the region of greatest preference lay in the
12° to l4°C. stratum. The pink salmon from 20°C. acclimation constituted the
only case in ·vvhich a preferred temperature as high as 17.7°C. was observed. The
general avoidance of temperatures above l5°C. for all species, in $lpite of acclima-
tion to thib level .:1nd to 20° and 2-!°C., was very markeci. A tendency to show
greater dispf;rsal in the fish from higher acclimations is suggested by the some-
what larger standard deviations for these samples.
Only a record of the mode was availab!e for 5°C. acclimated sockeye on
final analysis. Unfortunately no more supporting data are on hand.
C0:\1PAR!SON OF TEMPERATURE RESISTANCE
RESISTANCE TIM~~ TO HIGH TE:~IPERA.TURES. The extent to which acclimation
affects the resistance times to high temperatures ·within each species and the
levels of toleran ..;e characteristic of each species have been p_resented graphically
and in tabular hrm. If comparison is to be maJe a variety of questions may be
posed:
(1) HO\v do these species differ in their resistance times at differe!lt levels of
a1.Tlimation?
(2) If a difference exists, is it a matter of a differe1tce in s1ope (rate of change
of resistance time with temperature), a difference in overall level of temperature
resistance, or a difference in both slope and level? •
(3) vVhat measure of difft:rence can be quoted and with what statistical
significance?
(J: Can the postulated straight-line relation bet\veen the logarithm of .\~e
median t~sistance time and temperature be justified? ·
Each of t.hese que,tions can he answered by the method of analysis of
variance (AIJpendix I) which permits a sorting out of the sources of specific
difference from those resulting from sample variability coupled with interaction
uf the factors of acclimation, lethal test temperature and resistance time. Three
basic comparisons can be made involving two of the variates-species, lethals1 or
acclimation.s2-in as many cases as exist in terms of the third. Thes}! are now
con~idered:
Species X lethals, for three levels of acclimation. The results from three
analysis-of-va~iance tables (Table VI) demonstrate a highly significant differem·e
1 Refers to lethal test temperatures. ~ Refern to acclimatmn temperatures.
4A
'"'h~
. ·' ;
it
1
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l r
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I l
f
l
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. . ~
,. • . . . ~ .. ,~ ' -~ 0
I . . v , -·· . " ,, --
.J ... ~~·-~~~-~C\¢~••V·>H·'·1····
294
between species (P < .01) which increases with lower levels of acclimation,
that is, at a lower level of acclimation temperature for a comparable treatment of
lethal temperature the difference is more distinct. This is the crucial test. Figures
l8a and b illustrate this relation. A further analysis to determine 1vhich species
are contributing to the difference is considered later. As might be exp._cted, the
0 •
LIJ
cC
j ...
~
a:
LIJ
Q.
:IE
LLI ... 21
I I Ill
100 1,000 10,000
TIME TO 50% MORTALITY -Minutes
FIGURE 18a, Comparative median resistance times to high temperatures among young Pacific
salmon acclimated to 20°C. Lines have been drawn for the most and least tolerant species.
u •
22
FlGURE 18b.
•
y-Piok -' -====-=
"'--Chum -f
I II II I
1,000
TIME TO 50% MORTALITY Mlnutu
Comparat~~'c median resistance times to high tempera 1~ures among young Pacific
salmon acclimated to 15°C,
J
'•-····~-~--··--;-·~--'"" -·~-···~--.~···---•• ·: •' .. ••···•····~·••oe····~•····-·""' •·••
"' .. o . ·i'1~MI18ii'i.Wilillullliiill~~ ... it:l. --
\
I
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!
differences f
arc also highl
Species
is a case in ,,.,.
lethal levels i
results in Ta
crease at }0\\'
as that for a
lower levels
If a lethal
have little
<'On trast, t
that will best
Letltals
of-variance
com pari sons.
temperatures.
in each of
'{<
spedcs, the S<l:,
the others ( ,
.tpparent fron
It is poss
s pedes X let It
icspvnse amo
levels of tern
lethality, red
of the three fi,
the interactio ·
3.0, and is su
rpecies X letlz
A further
may be attribf. ,
in the first an<j
the total sum ,
extract each
(Fisher and Y
for single deg
and can be c
Such a search
findings from·,
made by use o
<'<Hion of the
(1) Nosi,
exists betwce
(2) Spri:~ '
from that of c
-
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--al:n,
1ent of
, i~'es
,·P ·. es
•. , d, the
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mt~"' ·r~:,r ..•. :~· .. · ..
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295
differences for all species in their response to different lethal test temperatures
are also highly significant. "
Species X acclimat·ions, for four levels of lethal test temperature. This
is a case in which the lumping of resistance times of three accJimations for single
lethal levels is used to distinguish between species. It can be concluded from the
results in Table VII that between species at each lethal level, and with some in-
crease at lower levels, there is a consistent significant difference, yet not as great
as that for a series of 1ethals at one acclimation. The increasing significance at
lower levels of lethal temperature is inherent in the study of temperature effects.
If a lethal temperature approaching that for boiling water were used, it would
have little consequence what species or acclimation characterized the fish. In
contrast, therefore, it is the temperatures which just cause distinct mortality
that will best demonstrate specific and acclimation differences.
Letlwls X acclimations, for different species. These five "4 X 3" analysis-
of-variance tables (computed in Table VIII) complete the series of first-order
comparisons. In essence they s!gnify what has already been stated, namely, that
temperatures of both acclimation and iethal level have highly significant effects
in f!ach of the species (former tables only applied to the group as a whole). One
species, the sockeye (P < .05), does n0t show the same degree of significance as
the others (P < .Oi). There is a greater variability in this species \v-hich is
apparent from the diversity in the points plotted in Figure 6.
It is possible to dmw up a table of second-order comparison, for example,
species X lethals X acclimations. The v~ry fact of a difference in temperature-
response among the species which resulted in the use of somewhat different lethal
levels of temperature, to bridge the c.uses from non-lethality to fairly rapid
lethality, reduces this table for like comparisons below a feasible size. A survey
of the three first-order tables, however, reveals that the error term, signified by
the i:nt~raction component in each table, lies mainly bet'..veen values of 1.0 and
3.0, and is sufficiently consistent to support the view that the interaction of
species X lethals X acclimations would also be con.3istent throughout the relation.
A further step involves assigning the particular amount of ·variation which
may be attributed to each independent comparison (degrees of freedom). Thus,
in the first analysis concerning species X lethals at .20°C. acclimation (Tnble VI),
the to1 al sum of squares was 1249.02 with 29 degrees of freedom. It 1s possible to
extract t:ach independent comparison by the use of appropriate multipliers
(Fisher and Yates, 1948; see Appendix). Since these are then the sums of squares
for single degrees of freedom they also equal the mean square or variance (s 2 ;
and can be compared for significance directly with the "error" by an F test.
Such a searching analysis has been carried out in this particular case only. The
findings from it con~erning the species X lethals, and the statements already
made by use of d1e more generalized analysis tables submitted, permit the appli-
cation of the following conclusions to the whole problem (consult Table IX):
(1) No significant difference in response to upper lethal levels of temperature
exists between spring and coho salmon (acclir:tated to i0°C. and above).
(2) Spring and coho salmon show a highly significant difference in response
from that of either sockeyet pink or chum.'
-
.. -.::;:o ..
..
L%2ZJt
1
I
!
I·
I
I
I
296
(3) Pink and chum salmon show a barely significant difference from each
other, but not'from sockeye in either case.
(4) There is a very highly significant "linear fitness" of the logarithmic re-
lation for these data which accounts for 98 per cent of the variance; the balance
can be attributed to curvature.
Of the total 29 degrees of freedom, 20 were assigned to the "error" com-
ponent (Table VI). This component is constituted of the variability of the
organisms resulting in slight deviations from the postulated relation and their
interaction (lethals X species), plus the variations due to experimental procedure
which can never be entirely eliminated. By the same method of using appropriate
multipliers, 20 separate components each representing one degree of freedom
were obtained. A study of these p: <·vided no value \Yhich in itself was signi-
ficantly different from that to be expected from the variability of the material.
Consequently it can be concluded that:
(5) The slopes of the lines relating rosistance time to temperature for the
five species are not significantly different (acclimations 10° to 20°C.) and
(6) The same relation can be applied to each species with equal confidence,
differing only in the temperature level at which this relation exists.
RESISTANCE TIMES TO LOW TE1iPERA.TURES. The constancy of relations in
the upper temperature levels is in contrast to that for lower temperatures. ~o
systematic testing of the latter data is possible from present knowledge of the
subject. A graphical presentation of some of the responses among the young
Pacific sumon taken from the same acclimation temperatures (Figure 19a
and b) serves to illustrate this phenomenon. A fair similarity in pattern for 23°C.
acclimated species becomes progr~gsively more variable with decreasing acclima-
tion. The chum salmon 1 which at first seemed to be among the most sensitive
judging from high acclimations, were the ieastsensitive from an acclimation of l0°C.
The spring salmon were consistently the most sensitive to the lowest tem-
peratures (0°C.), but showed a rapid increase in resistance at slightly higher
temperatures.
A striking intolerance to low 1emperatures characterizes all five species.
Further study in this field of temperature-responses will be necessary to clarify
some of the complexity which has appeared in these findings. The possible in-
fluence of size has been pointed out. The mean fork-lengths of the fish used are
reported in Table III.
ZONES OF THERMAL TOLERANCE
The· concept of a zone of thermal tolt>rance bounded by upper and lower
incipient lethal temperatures for the greatest possible ra,nge of temperature-
acclimation, and terminated by ultimate lethal temperatutes, was advanced by
Fry et al. (1942) .for the goldfish. The freezing point of water limited the minimum
acclimation to 0°C. for fresh-water fish. By construction of a trapezium relating
these confining temperatures, calculation of the area of the zone of tolerance in
"degrees Centigrade squared" gave quantitat~ve expression for an otherwise
quaHtative description. Various species of fish have since been des.cribed in this ,
i ~
l •
\
I
l
~
I
f
FIGURE 19a.
salmon
6
<.i
•
w
a:
::1 ....
o( 4 a:
w
a.
2 ..,
1-
2
l
J
•
f
I
'lh
uc re-
f
I
t
4
I
4
f
w a::
;;) ....
< a::
w
c.
:::!!
t:r ....
297
--::=:==========:..-:-:-::. Sprino -• Chum - o
0 t
• ----------------Sockeye-&
' ~ Coho -~
• 0 ;------·-
.Vi"J ·o n·
ott____.o ______._--.....1--_.__--.J-..-_____.
0 2 3 4
TI':4E TO 50"/e MORTALITY-1,000 Minutes
FrGURE 19a. Comparative median resistance times to low temperatures among young Pacific
salmon acclimated to 23°C. Arrows used as stated in Figure 11.
+ "
6
0
.....
a::
;;)
1-
< 4 0:
w
Q,
~Chum -o
t Sockeye·&
~ ·-··················· ••••••• Coho -~ w ....
Sprino -•
2
0
TIME TO 50% MCRTALITY-1,000 Minutes
FtGt ~ 19b. Comparative median resistance times to low temperatures among young Pacific
salmon acclimated to l5°C, Arrows used as stated in Figure 11.
' I
·-···---··---.. -------. --~ '1
:.; • \
-~---'"~--~~~· ~~-
\
l
I
I
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!
\
l
I
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L r-
\
l
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l
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t
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!'
·'
298
fashion (Brett, 1944; Fry et al., 1946; Hart, 1947, 1949), all conforming within
slight variations to the original pattern for the goldfish. An increasing acclimation
temperature has always resulted in an increasing lethal temperature in some
fractional proportion. The construction of a diagonal iine at an angle of 45° to
the axes (Figure 20) has provided a ready means of determining the ultimate
upper iethal temperature, since this line represents the locus of all points for
which lethal temperature equals acclimation temperature. CharacteristicalJy, for
upper incipient lethal temperatures, no spedes has been found to exploit the
, full possibility suggested .bY e.xtrapolation of th1s linear relation (between upper
lethal temperature and acclimation temperature), always dropping short as a
result of uniform intolerance at the highest acclimations, providing a "plateau"
in a graphical presentation. Although the resistance time to a high temperature
may be lengthened through higher acclimation, it was pointed out that this re~
sistance is finite and the lethal temperature remains unaltered for the relation
designated by the "plateau';. These relations are illustrated iP '~igures 20 to 24
for the Pacific salmon. Some new aspects,· cliff ering from the nor 1t1al trapezium,
are apparent. The lethal-temperature points are not always best represented by a
straight line, particularly in the lower lethal bracket. A high degree of sensitivity
to low temperatures among the Pacific salmon almost confines these species to
acclimation temperatures above 0°C. Some death at this level was observed
among 5°C. acclimated samples (Table XII). In a preliminary acclimation
culture of spring salmon at aoc., high mortality occurred in the presence of
healthy sockeye, chum and coho salmon of the same temperature histol\y. This
intolerance of the springs might account for the rapid falling away of the upper
lethal temperature for low acclimations, which is not apparent for the coho
salmon, so similar in other respects.
The spring and coho salmon had the greatest tolerance and were practically
identical in area (529 and 528 degrees C. squared respectively). The sockeye were
i~termediate (5()5 degrees C. squared) and the chum salmon least (468 degrees C.
squared). The line relating upper lethal temperature to acclimation temperature
for the pink salmon was very similar to th.at for the chum salmon Th~ apparent
intolerance of the pinks to low· temperatures would restrict their zone of tolerance
even more than in the case of the chums, placing them lowest in order of eury-
theqnal relations. \Vith the possible exception of the pink salmon, and notwith-
standing the variable nature of the lines relating lower lethal temperature to
acclimation temperature, most of the difference in areas is a result of difference
in upper lethal temperature.
DISCUSSION AND CONCLUSIONS
TIME AND TEMPERATURE
Division of response to extremes of temperature into zones" of tolerance and
resistance, previously set forth for other fishes, has been appropriate for similar
distinctions among the Pacific salmon. Although the pattern of resistance to low
temperatures was quite di(ferent from that for high temperatures, the same
factors of tolerance and resistance were equally applicable.
-
I
l
f
the .. ,. ....... '"' .......
These ha
and Beleh
"there are .·
due to the
Ft
pr
wi
c
\\"
extremes of
whit·h an o
tern pcratu r ·
chnractcris
in tlucnecd , ·
when the r
s~tmple at
which no m
hns been e.1·
tur. cs (h.igh .• .. · .. • <:an be dete .
'
•
I
I
I
~0 I
\na.
·; for
..
.. 'J.t,ure
'he~· , J I
,;l.il .
~ _.
··~
·¥~ry-:fntl : ... r .
~fe .~ ence
l
I
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1
1
~
() l -~.1..~.---...L
299
Heilbrunn (1943) has compiled a considerable number of records concerning
the temperature at which thermal death occurs in a wide variety of organisms.
These have been taken largely from reviews by Kanitz (1915), Uvarov (1931),
and Belehradek (1935). In criticism of these data Heilbrunn (p. 420) comments
"there are very fe·wr useful records of heat (or cold) death temperatures. This is
clue to the fact that many authors have neglected the time factor". Death from
w
a:
~ ...
4
a:
w
Q.
:E
w ...
0
.t:! -..
..1
~ .. .. .. • -.., ..
Q.
0
25
= 5 ..
..1 .. .. • 0
..1
0 5 10 20 25 •c.
ACCLIMATION TEMPERATURE
FIGPRE 20. Thermal tolerance for young spring salmon in fresh water. The
preferred temperatures are represented by a central point for the mean,
with limits for one standard deviation dotted above and below. The degree
Centigrade in which the mode occurred is represented by a s01id vertical line.
Where an experiment was performed but resulted in less than 50 per cent
mortality a "V" has been inserted.
extremes of temperature is not just dependent on a threshold level below or above
which an organism either lives or dies, but may be considered a resultant of both
temperature clnd expo~ure time. At each lethal level of temperature there is a
characteristic rate of dying (rate of mortification, Fry et al., 194G) which may be
influenced within limits by acclimation. A threshold level is appi ;ached, however,
when the rate of dying approaches zero, as in the case calculated for half the
sample at the incipient le~hal temperature. Consideration of the time beyond
which no more mortality may be expected from tempei·ature as a primary cause
has been extended in the present study for low lethal temperatures. Tempera-
tures (high or low) which would not cause mcrtality, regardless of acclimation,
can be determined from the zone of tolerance. Very similar limits can also be set
-
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f ~
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:li
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1: •' I:
1i
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~
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1 J
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t ' l
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!
l
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1··.·
I
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300
&~ -0
~ .,.. ..
...1
... ·---·----·-· ---·------...
Ci. zo a.
:;) Il
1
15--
"0 .. ... ... .. -Il .. ...
0.. i
/
0
ACCLIMATION TEMPERATURE
FIGURE 21. Thermal tolerance for young pink salmon. No !ower lethal
experiments were performed. Preferred temperatures plotted as in
Figure 20.
~c.
0
.s: -.;
...1
.------------;t··-1
--·-----... ---... .. ... 20 <>.
~
w
a:
:;) 15 yl! ! ... "0
"' .. 1~
a: ... . ...
w .. . i -a. ..
2 ~ 10~ I
1.1.1
1-\ I , ,
•I
0 s: 5
./ -.,.~·-..
..J .-------_ ..
.. ., L, . !;
0
..J
0 5 10 15 20 25
ACCI.!MATICN TEMPERATURE
FIGURE 22. Thermal tolerance for young sockeye salmon.
temperatures plotted as in Figure 20.
•c.
Preferred
,. .
,)··.·~ ·.:]l ..
,• :~:;
--... ~
a.
2'
w
1-
\
\
Ftm'
I
I
t
I
r
I' v•
•
( f .. , l ;,
I
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L
l
l
l
\
J
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I
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w
a:
::»
~
<
a:
o.J
Q.
:E
IIi ...
" J:: -o;
..1
"' • .. ..
"' -• .. :g.
" £ -• ..1 .. ..
~
0
..1
---
15
10
5
0
__ o
li:---··-----·---
T
/It It l! ! ..t
/
.~ ~·
+ __J!
s-ICi 15 20
ACCLIMATION TEMPI;RATURE
25 •c.
FIGURE 23. Thermal tolerance for young chum salmon. Preferred t~m
peratures and "V" plotted as in I<'igure 20.
ILl
a:
::» ...
< a:
ILl
0.
:E
ILl ...
0
.<:: -..
..1
"0 .. .. .. .. -~
~
0..
;;
.c;
;
..1 .. .. .,
0
-'
5
I 5 10 15 20 25 •c.
AC CLJMATION iEI.IPER ATUR E
FIGURE 24. Thermal tolerance for yottng coho salmon. Preferred tem-
f , perature plotted as in Figure 20. ·
:. i
'J
' ' '~
., ,. ·.· ·.;J· ~' ,. ~.~',
.,
" ..... ~-. -·-··········-····~ ....... ., . ., .. -·-··· ·r ..
t --1
. I
301
'· .
~·
t r
I
l.
l
r·
l
l
I
!
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j
l
[
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.~,.
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~~~ ' ' ~\ \
302
by examining the resistance times for various acclimation temperatures as in
Figilre 25 for sockeye ~~lmon. The points be:F.md which no more deaths are likely
to occur have been h.dicated by a dotted line. Thus, temperatures between
go and 21 ~c. are unliL 2ly to catwe death among sockeye no matter what the
acclimai:ion, nor what the exposure time. The higher or lower the temperature is
above 0r below these limits, the longer the test time necessary to determine the
lethal temperature. A somewhat different series of ~ethal temperatures would
have br-'.;fi quoted if no experiments had been continued beyond 24 hours (1,440
min,) for both upper and lower lethal levels.
Future experhnents on temperature-tolerance will continue to add to our
knO\vledge of the factors affecting temperature relations in fish. In the investiga-
tion of Pacific salmon, emphasis has been placed on uniform treatment of ail
samples such that, although the methods and later analyses may change, the
differences set forth should remain unaltered. One limitation should be pointed
out. The results apply to the stocks of salmon from which the eggs were collected
(Table I) and may therefore be traced back to comparatively few females. The
possibiJity of variation both within and between local stocks cannot be disregarded.
COliPARISON \YITH SOlfE OTHER S.-\L~fONOIDS
The resistance times for six species of salmonoids determined for samples
acclimated to 20°C. have been plotted in Figure 26 (from Fry, 1947b; present
paper). Data for only two of the species of Oncorhynchus are included. These two,
the spring salmon (0. tschawytscha) and the chum salmon (0. keta) wtre res-
pectively the most and least resistant to the same test temperatures; the re-
maining three ·species occur at intermediate positions (Figure 18). It will be
seen that the two species of Salmo occupy positions distinct both from each
other and from the ~emaining species. Salmo salar, the Atlantic salmon, is the
most resistant of the salmonoid group. The members of the Pacific salmon species
lie in a compact series intermediate between Salmo and Cristivomer, while
Salvelintts fontinalis approaches the resistance of Salmo trutta at the highest test
temperatures (28.0° and 28.5°(',) but drops below it for lower temperatures,
falling within the range for Oncorhynchus. Except for the speckled trout (Salve/in us
fontinalis), no further comparisons are \Varranted until more experimental data
are obtained. A marked difference in the lower lethal relations between the
speckled trout and the Pacific salmon exists, sufficient to suggest a qualitative
difference rather than a purely quantitative one. The former was found to be
resistant to low temperatures by Fry et al., (104G) who report that the lower
lethal temperature "was only just above 0°C. when the acclimation temperature
was 2-eC''. This results in a comparatively large zone of tolerance (025 units:
exceeding that for Pacific salmon which ranged from 408 to 520 units.
SOME ECOLOGICAL RELATIONS
Limits of tolerance to extremes of temperature among young Pacific salmon
have been determined, Significant differences exist, \Vhether these differences
are sufficient to account for some of the distinctive habits which characterize
the different species is a matter of conjecture.
1
I
i
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r
t
-• i t
\
30
28
22
20
0
• 19
""' a::
;::) ._
<t
a::
""' c.
:::e
w
1-
16
14
12
10
6
4
Fmt:RE 25.
Broken lin~s .
.I
~.
l
\
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t
f
l
l
i
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! :
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r ...... . (::' "" . ' --. . .
• L.:;. *~,,.. .. :.,, .. ~ , •••• '~ '' )-o'' ..:.
r
I
he
ll<J
.tcw
;r~
al.-
he
~o~~
D .
1 xes : ::1
~~
~~~
ch
hf•
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·He
, :!St
es~
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~ta
'·h~ ' ' ' ' ~ Vt
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303
D oys
28
t\il; • Acclimation Temp.
26~, 12 '-:._--:_--:::,'Jil::•-~'.,___ ..................... -··-···-···-·------··-~-:--···-@). _ _g~~~:--
24 .\~ --.. -~·----.----------------
\ ....___ . ..-· 10° \ @-,.·-------------------
·........__ ••.•. -·· 50 ..,.. ________________________ _
22 ./" •.. ··
.........
20
(.)
0 18
w
a:
:J
1-
16
<t 14
a:
w
a.
':E
w
1-
12
10
Ac c lim ati on Tern p.
8 ·····-·················
-.... .,
6
4
/
?···.-.. ------23° ··. .........
•... ... ... , I .. 2 0
21 ;· ·· .... \.
~ . '
0 1___... I • ./-.o/, ' I \. _s_o-1---~--~---~'------~
I 2. 3 4 5 6 8 9 10
TIME TO 50% MORTALITY-1,000 Mlnutes
FIGURE 25. ';.\1edian times to death at high and low temperatures for young sockeye.
Broken lines indicate levels of temperature causing little ot· no mortality for continued
exposure. Dotted lines join the appt·oximate points of inflection.
pt;,
-~--
fl
I
I
I
11
304
Young sockeye are usually lake-dwellers, frequenting the open water and
subsurface regions, probably in the cooler temperatures in the vicinity of the
thermocline (Ricker, 1937). During the summer they are rarely seen or caught
in the shallow, littoral zones oi the lake (Brett and McConnell, 1950) where
young coho, shown to have a higher temperature-resistance~ may b~ found on
occasion in abundance. The sockeye migrate in the spring of the year shortly
after the ice has left more northern lakes, or following rising spring temperatures
~0~
• • 0 ..
w
a:
::::»
1-
<t
a:
IIJ
a.
~ 26 I&J
1-
~
Salvelinus fontinalls~~ -..'::~--~oe-......_-.... e Salmo solar ~,.,-............. ~ ' .......... 1--•il........,_ 0 •
....... " .......................... "' ~~'--.... ,,::·b--·~-
0 i ..... A ........ ..... .....
Cristivomer namayce--'-... ...............
o '-......._ -A .... .._oncorhynchus tschowytscha
..... ..... .... ---........... • ---1:!. ... ..... -
o ............... 1o Jo. kisutch
......._ '-... O.c;~orbuscha \:'.t..._ 0. nerlla
Oncorhynchus keto
10
TIME TO 50'Y• MORTALITY -Minutes
FIGURE 26. 1Iedian resistance times for different salmonoids acclimated to 20°C. Data for
other than Oncorhynchus from Fry (1947).
in such a lake as Cultus which may remain uopen" throughout the year (Foerster,
1937). Termination of the migration is closely correlated with ascending surface
temperatures and the presence .of a well established epilimnion which Foerster
(1937) points out may form a temperature block. Coho continue to migrate
dmwnstream after sockeye have ceased to move.
Young pink and churr usually do not experience warm lake or river waters.
Their migration to sea almost immediately after hatching in the spring of the
year eliminates any such high-temperature experience at this stage of life. Their
intolerance to fresh water would probably be more pronounced at higher tem-
peratures. The limited success of Chin and Kuroda (1935) in holding churn salmon
in fresh water beyond one year depended in part on low temperatures. The
interaction of thermal and osmotic stresses requires investigation.
The spring salmon, although a first year migrant to sea, may be found
during the summer in streams and rivers, and is more like the coho in this res-
( --
siderati
bt! the
This grou
made on
Five
spring
nerka),
other, but
(4)
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(5)
the five
(6)
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ures
305
pect. These two species were the most tolerant to high temperatures. The problem
of their rektive abilities to remain active at high and low temperatures must
remain unanswered· for the present. Observations, both field and laboratory,
indicate-a greater ability to feed and sport (jumping, darting, etc.) in ·warm
waters among the spring and coho than.arnong the remaining three species.
On the basis of morphological studies, rates of growth and life history con-
siderations, Milne (1948) concluded that the pink and chum salmon appeared to
be the most specialized, and the spring and coho probably the most prir.nitive.
This grouping of the species within the genus is in accord with distinctions
made on the basis of temperature-tolerance.
SU::\Il\IARY
Five species of Pacific salmon are found in North American w·aters, the
spring (Oncorh)!_nchus tschawytscha), the pink (0. gorbuscha), the sockeye (0.
nerka), the chum (0. keta) and the coho (0. kisutch). Young of these species,
averaging 4 to 5 em. in length and 1 gm. in weight, were used in a series of ex-
periments concerning toleranee to high and to low temperatures.
Two months after hatching, each stock of .fish was divided into five groups
for acclimation to 5°, 10°, 15°,20° and 23°C. (24°C. in spring and pink); acclima-
tion and lethal .. temperature experiments continued throughout the following
f: ·r months. Resistance times were determined at intervals of 0.5°C. for high
_nperatures and L0°C. for low temperatures (0.0°C. and above). Upper lethal
temperatures were calculated for exposures of 10,000 minutes (one week) and
lower lethals for exposures of 5,500 minutes (approxi"mately four days).
RESISTANCE TO HIGH TEMPERATURES. A statistical analysis, using the methods
of analysis of variance for test temperatures ranging from 24.5° to 27.5°C. and
acclimations of 10° to 20°C., for all species, led to the following conclusions:
(1) No significant difference in response to upper lethal levels of temperature
exists between spring and coho salmon.
(2) Spring and coho salmon show a highly significant difference in response
from that of either sockeye1 pink or chum (P < .01).
(3) Pink and chum salmon show a barely significant difference from each
other, but not from sockeye in either case (P = .05).
(4) There is a very highly significant (P < .01) linear fit of the logarithmic
relation for these data (logarithm of the median time to death in relation to the
temperature causing that death).
(5) The slopes of the lines relating log resistance time to temperature for
the five species are not significantly different.
(6) The same relation can be applied to each species with equal ~..·onfidcnce,
differing only in the temperature level at which this relation exists.
The ultimate upper lethal temperatures for each species were: spring-
2i5.10C., coho-25.0°C., sockeye-24.4°C., pink-23.9°C., chum-23.8°C.
CRITERION OF DEATH AT LOW TE;<.tPERATURES, It was discovered that with
the approach of death from a low temperature. the opercula commence to fan out
perceptibly:This creterion was shown to be significant when compared with data
WW:·~
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, .
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I
l
306
from re(ryvery tests at warmer temperatures. Thus, the individual times to death
al: ~:h·en low temperatures could be recorded and median resistance times
det.:.ri'i:~~ned wr each sample.
RESISTANCE TO LOW TE).lPERATURES. The relation ')etween resistance time
to low. temperature and the level of that temperature has not been resolved into
a simple equation as has been the case for heat-tolerance relations. A variable
but usually sigmoid to double sigmoid pattern characterized the curves ,vhen
plotted on normal axes. An initial period of rapidly increasing resistance to low
te11,perature was followed by relatively little change in resistance for two and.
three degrees increas~ in temperature (15° to 23°C. acclimation). Xo mortality
usually occurred within a degree or so above this latter zone for a considerably
increased exposure time up to 5,500 minutes.
· The young salmon were very sensitive to low temperatures. Among the four
species tested, the coho and sockeye salmon could not tolerate long exposure (four
days) to 0°C. even when taken from holding temperatures as low as 5°C.
The lower lethal temperatures for the highest acclimation, 23°C., were:
spring-7.4°C., coho-6A°C.l sockeye-6.7°C.-, chum-7.~°C.
1HXED LETHAL EFFECT OF LOW TE~!PER.-\.TURES. From acclimation tempera-
tures of 20°C. and above, mixed responses were noted in the lethal baths. A
rapid death of all fish occurred at the lowest temperatures. Temperatures slightly
above this level caused rapid death in part of the sampie followed by a long
dday and then death of the remainder. Temperatures somewhat higher, yet still
low enough to cause death, did so only after prolonged exposure. By plotting the
data on probability X logarithmic paper it was possible to discriminate clearly
between the two trends of death. Exposure to the same low temperatures in
lethal baths containing 9.9%0 sea water instead of fresh \Vater (slightly hyper-
tonic) resulted in partially increased tolerance among sockeye salmon.
It therefore appears that three causes for death may be involved: one, a
very rapid agent usually effecdve 'vi thin GO minutes of exposure, a· second: not so
rapid in action, and a third which is related to osmotic balanc·e.
SIZE EFFECT. Xo significant difference in the size of the first and last fish
to die from high temperatures was present. For death from low temperatures,
however, the size distribution of the dead fish from samples in which 30 to 50 per
cent of the fish died showed a significantly lower :nean length than in the balance
of living fifh. The earlier death among smaller fish appeared to be IJartly the
result of grnater susceptibility to "rapid" cold-death.
ZONES OF THERMAL TOLERANCE. The zones of thermal tolerance were con-
structed graphically and the areas calculated in units of degrees Centigrade
squared. The high degree of sensitivity to low tcmperrt.tures, almost conftning
these species to acclimation temperatures above 0°C., results in a comparatively
low thermal tolerance rating. The spring and coho were almost identical, with
529 and 528 units respectively; the sockeye was ne:<t with 505 unitsj followed by
the chum with 4G8 units. Lacking low lethal-tempe~ature data, the pink aalmmt
cannot be included, but one preliminary experiment suggested a lower resistance
than in the chum s3.lmon, and consequently a smaller zone of tolerance. Even
;:: .aw
the
arclim
CO.
t•mpha~.
hy pre~
n:fiista
than i ·
is mor
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)
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the pint ... ~
taxono1
i
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Ul3
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307
the most tolerant of the Pacific salmon was considerably below the speckled
trout Salvelinus fontinaHs, with a calculated area of G25 ·units.
PREFERRED TEMPERA.TURES. Comparatively little difference in preferred
temperature was recorded experimentally, either between species or for differences
in acclimation amounting to l5°C. in some instances. On the average, no greater
difference than 3°C. (le to l4°C.) was displayed behveen means from different
acclimations. The region of greatest preference lay in the 12° to l4°C. stratum.
Cm.lPARISON OF TE~IPERA.TURE TOLER.\NCE. In making comparisuns, most
empl1asis was placed on the resistance times to high temperatures. Experiments
by previous investigators .., ... ith other salmono\ds demonstrate a greater heat
resistance in two species of Salmo and lesser resistance in Crisli'vvmer namaycush
than in the Oncorhynchus group (all acclimated to 20°C.). Sai?Jelinus fontindis
is mo1 e resistant to temperatures of 27°C. and above than any of the Pacific
sahi'On; however, below t~.is level, the generic distinction does not apply.
G ~NERAL CONCLUSIONS. The species of Pacific salmon are comparative!~·
stenothermal. An intolerance to low temperatures particularly restncts their
biokinetic range. For prolonged exposurf: (up to one week) to high temperatures
the spring and coho salmon 'vere most resistant, the sockeye intermediate anti
the pink and chum salmon least resistant. These differenc~"s are in keeping with
ta.-:onoii1ic conclusions and certain ecological distinctions.
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\W
~11.' :/ .
! .
---·--···--·. ···-----···--·----·--"!
' ? ,t y
l
~~· ---~
:..~
308
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-
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309
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---