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1183The Journal of Experimental Biology 216, 1183-1190
© 2013. Published by The Company of Biologists Ltd
doi:10.1242/jeb.080556
RESEARCH ARTICLE
Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is
associated with hypoxia tolerance, ventricle size and myoglobin level
Katja Anttila1,*,†, Rashpal S. Dhillon1,*, Elizabeth G. Boulding2, Anthony P. Farrell1,3, Brian D. Glebe4,
Jake A. K. Elliott5, William R. Wolters6 and Patricia M. Schulte1
1
Department of Zoology, 6270 University Boulevard, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4, 2Department
of Integrative Biology, University of Guelph, Guelph, ON, Canada, N1G 2W1, 3Faculty of Land and Food Systems, 2357 Main Mall,
University of British Columbia, Vancouver, BC, Canada, V6T 1Z4, 4Fisheries and Oceans Canada, Aquaculture Division,
St Andrews Biological Station, 531 Brandy Cove Rd, St Andrews, NB, Canada, E5B 2L9, 5Kelly Cove Salmon (KCS),
Division Cooke Aquaculture, 874 Main Street, Blacks Harbour, NB, Canada, E5H 1E6 and 6National Cold Water Marine
Aquaculture Center, 25 Salmon Farm Road, Franklin, ME 04634, USA
*These authors contributed equally to this work
†
Author for correspondence (anttila@zoology.ubc.ca)
SUMMARY
In fishes, performance failure at high temperature is thought to be due to a limitation on oxygen delivery (the theory of oxygen
and capacity limited thermal tolerance, OCLTT), which suggests that thermal tolerance and hypoxia tolerance might be
functionally associated. Here we examined variation in temperature and hypoxia tolerance among 41 families of Atlantic salmon
(Salmo salar), which allowed us to evaluate the association between these two traits. Both temperature and hypoxia tolerance
varied significantly among families and there was a significant positive correlation between critical maximum temperature (CTmax)
and hypoxia tolerance, supporting the OCLTT concept. At the organ and cellular levels, we also discovered support for the OCLTT
concept as relative ventricle mass (RVM) and cardiac myoglobin (Mb) levels both correlated positively with CTmax (R2=0.21,
P<0.001 and R2=0.17, P=0.003, respectively). A large RVM has previously been shown to be associated with high cardiac output,
which might facilitate tissue oxygen supply during elevated oxygen demand at high temperatures, while Mb facilitates the oxygen
transfer from the blood to tissues, especially during hypoxia. The data presented here demonstrate for the first time that RVM and
Mb are correlated with increased upper temperature tolerance in fish. High phenotypic variation between families and greater
similarity among full- and half-siblings suggests that there is substantial standing genetic variation in thermal and hypoxia
tolerance, which could respond to selection either in aquaculture or in response to anthropogenic stressors such as global
climate change.
Key words: critical maximum temperature, enzyme activity, heat shock protein, heritable, oxygen and capacity limited temperature tolerance, heart.
Received 25 September 2012; Accepted 2 December 2012
INTRODUCTION to modify the maximum temperature tolerance and hypoxia tolerance
Models of the earth’s climate predict an increase of 1–7°C in mean of many, but not all, fish species (e.g. Rees et al., 2001; Ford and
global temperature over the next hundred years (e.g. Ficke et al., Beitinger, 2005; Eme and Bennett, 2009; Fu et al., 2011; Petersen
2007). Associated with future increases in global mean temperature, and Gamperl, 2011). For example, salmonids appear to have fairly
the occurrence of extreme climate events is predicted to increase limited capacity for acclimation of these traits as maximum
(e.g. Ficke et al., 2007; Doney et al., 2012). In addition, temperature tolerance changes only a few degrees in response to
eutrophication as a result of anthropogenic effects is already causing acclimation (Elliott, 1991; Baroudy and Elliott, 1994). If
an increased prevalence of aquatic hypoxia in many areas (Diaz, environmental change exceeds the capacity of fish to respond via
2001). Together, changes in water temperature and oxygenation will these mechanisms, selection might act on these traits, allowing
pose a substantial challenge for aquatic organisms including fish. populations to respond via evolutionary adaptation. However, for
When temperature increases beyond the optimum temperature selection to act over ecologically relevant time scales, thermal and
range or oxygen declines below optimal levels, growth, development hypoxia tolerance must be genetically determined and sufficiently
and reproductive capacity decrease and susceptibility to disease variable among individuals to provide the standing genetic variation
increases in fish (Brander, 2007; Pörtner and Knust, 2007). As a on which evolution can act (Boulding and Hay, 2001).
result, changes in climate are predicted to have detrimental effects Unfortunately, little is known about the genetic basis and extent
on fish populations both in nature and in aquaculture settings of inter-individual variation in thermal tolerance or hypoxia
(Brander, 2007). Fish may be capable of adjusting, at least in part, tolerance, and thus the potential for adaptive change in these traits
to these changing environmental variables through phenotypic is difficult to estimate. Temperature-at-death has been shown to be
plasticity in their responses to high temperature and hypoxia. significantly heritable in least killifish (Heterandria formosa)
Acclimation, a form of reversible phenotypic plasticity, is known (Doyle et al., 2011) and mosquitofish (Gambusia holbrooki) (Meffe
THE JOURNAL OF EXPERIMENTAL BIOLOGY
, 1184 The Journal of Experimental Biology 216 (7)
et al., 1995), suggesting that there is a genetic component of were produced from a group of 70 parental fish. Each family had
maximum temperature tolerance and the potential for selection to different dam (i.e. 41 female Atlantic salmon were used to produce
act on this trait at least in some fish species. In rainbow trout the families), but only 29 sires were used; eight sires fertilized eggs
(Oncorhynchus mykiss), the existence of a quantitative trait locus from two different dams (resulting in eight pairs of half-sibling
(QTL) associated with maximum thermal tolerance also suggests a families) and two sires fertilized eggs from three different dams
genetic basis for this trait (Perry et al., 2001). Hypoxia tolerance (resulting in two half-sibling groups of three families each), while
may also be genetically determined, at least in part, in fishes. For the remaining 19 sires were crossed with independent dams
example, hypoxia tolerance has been shown to have significant (resulting in 19 unrelated families). This breeding design allowed
heritability in common carp (Cyprinus carpio) (Nagy et al., 1980). us to estimate the genetic component of the observed phenotypic
Together these data suggest that temperature and hypoxia tolerance variation, and by using independent dams with the same sire to
may have a significant heritable component in fishes, but the capacity generate the half-sibling families (rather than independent sires with
for selection to act on these traits depends in part on whether these the same dam) we are able to exclude maternal effects as a possible
traits are positively or negatively associated. For example, if there cause of similarity in phenotype between half-sibling families. In
is a functional or genetic trade-off between hypoxia tolerance and order to keep track of the family background of the fish, families
thermal tolerance, it would be difficult for selection to were kept in separate tanks at the National Cold Water Marine
simultaneously increase both traits. In contrast, if there is a positive Aquaculture Center (Franklin, ME, USA) until the fork length of
functional or genetic association between the traits, then selection fish exceeded 12cm and fish could be tagged with passive integrated
on one trait will also act positively on the other trait. transponder (PIT) tags. After PIT-tagging, the fish were transferred
There is some theoretical and empirical evidence to suggest that to St Andrews and kept together in common tanks. In order to
thermal tolerance and hypoxia tolerance may be positively partially control for tank effects that might occur before tagging,
associated, at least in some species of fishes (including salmonids). the progeny from each family was divided across two separate tanks.
The theoretical basis for this possibility stems from the concept of Each tank was split to contain two different randomized families.
oxygen and capacity limited thermal tolerance (OCLTT), proposed All tanks were identical flow-through tanks of the type used in
by H. Pörtner (for reviews, see Pörtner and Knust, 2007; Pörtner, aquaculture. The fish were kept at a natural photoperiod (9h:15h
2010). The basis for the concept comes from the early findings of light:dark) and water temperature (4.0±0.1°C) at time of the
Fry (Fry, 1947), who observed that while routine metabolic rate experiments. Fish were fed ad libitum once a day with commercial
increases exponentially with temperature, maximum metabolic rate, feed (Skretting, St Andrews, NB, Canada) and were fasted 24h
after first increasing exponentially with temperature, reaches a before experiments. Treatment of all experimental animals was in
plateau and then starts to decline at high temperatures. The accordance with the approved University of British Columbia animal
temperature at which the maximum aerobic scope (the difference care protocol A07-0288-A002.
between routine and maximum rates) is reached is called the
optimum temperature (Topt). The decline of maximum performance Temperature tolerance experiment
above Topt is suggested to result from mismatch between the demand The temperature tolerance of fish was tested with a critical maximum
for oxygen and the capacity to supply oxygen to tissues (Pörtner temperature (CTmax) protocol that warmed the fish until they
and Knust, 2007; Pörtner, 2010). There is good empirical evidence exhibited sustained loss of equilibrium (LOE) and lost the capacity
supporting the validity of this concept in a variety of fish species, to escape conditions that would eventually lead to death (Beitinger
including salmonids (Farrell, 2009; Eliason et al., 2011). et al., 2000). Briefly, each evening one fish from each family was
Furthermore, Steinhausen with her co-workers (Steinhausen et al., randomly selected and transferred from the rearing tanks into an
2008) observed a failure to increase maximum cardiac output above experimental tank (88l) with constant flow-through freshwater at
Topt, suggesting that limitations at the level of the heart were the the holding temperature (4°C). Two identical setups were used.
cause of limited oxygen supply with increasing temperature. This Because of possible diurnal light cycle effects on temperature
limitation in oxygen supply and constant increase with oxygen tolerance of fish (Bulger, 1984; Healy and Schulte, 2012), all the
demand could lead to functional tissue hypoxia at temperatures experiments were performed between 09:45 and 13:45h for each
beyond Topt (Farrell, 2002), limiting temperature tolerance of the day. After an overnight acclimation period in the experimental tank,
individual. However, at the tissue and molecular levels, less is known the water flow was turned off and the temperature of the water was
about the properties that make some individuals more tolerant than increased at a constant rate of 0.3°Cmin–1 to 22°C, and at a rate of
others and whether these differences support the OCLTT concept. 0.1°Cmin–1 thereafter until the fish exhibited LOE. Water
The objectives of the present study were thus to: (1) determine temperature was controlled with a circulating 1100W heater (1160S,
the extent of variation in temperature and hypoxia tolerance within VWR, Mississauga, ON, Canada) and five submersible aquarium
and between families of Atlantic salmon, (2) determine whether there heaters (100W, Marineland Aquarium Products, Cincinnati, OH,
is a positive association between these traits, and (3) examine USA). Water homogeneity and oxygenation were assured by
variation in physiological organ- and cellular-level factors in these bubbling air vigorously into the tanks, keeping oxygenation level
families that would be hypothesized to account for some of the above 80% saturation throughout the experiments. After a fish lost
tolerance variation, based on the predictions of the OCLTT concept. equilibrium, it was quickly removed from the tank, identified (by
reading the PIT tag) and placed in a recovery tank at the acclimation
MATERIALS AND METHODS temperature. After the experiment, all the fish were lightly
The research was conducted at the Fisheries and Oceans Biological anesthetized with 50p.p.m. MS-222 (Sigma-Aldrich, Oakville, ON,
Station at St Andrews, NB, Canada, with 1+ juvenile Atlantic salmon Canada) buffered with sodium bicarbonate, and the mass and length
(Salmo salar L.) in January 2011 (mean fork length and mass were of the fish were recorded before returning the fish back into the
163.2±0.9mm and 47.9±0.8g, respectively). The fish came from rearing tank. Twelve fish per family were tested for CTmax (total
experimental brood stock maintained at Cooke Aquaculture, Oak 492 fish) and only three mortalities (0.6%) were recorded in the
Bay Hatchery, NB, Canada. Forty-one families of Atlantic salmon days that followed the CTmax determinations.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
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