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Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids

Environment, antecedents and climate change: lessons from the study of temperature physiology and... The Journal of Experimental Biology 212, 3771-3780 Published by The Company of Biologists 2009 doi:10.1242/jeb.023671 Commentary Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids A. P. Farrell Zoology Department, 6270 University Boulevard, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4 [email protected] Accepted 19 August 2009 Summary Animal distributions are shaped by the environment and antecedents. Here I show how the temperature dependence of aerobic scope (the difference between maximum and minimum rates of oxygen uptake) is a useful tool to examine the fundamental temperature niches of salmonids and perhaps other fishes. Although the concept of aerobic scope has been recognized for over half a century, only recently has sufficient evidence accumulated to provide a mechanistic explanation for the optimal temperature of salmonids. Evidence suggests that heart rate is the primary driver in supplying more oxygen to tissues as demand increases exponentially with temperature. By contrast, capacity functions (i.e. cardiac stroke volume, tissue oxygen extraction and haemoglobin concentration) are exploited only secondarily if at all, with increasing temperature, and then perhaps only at a temperature nearing that which is lethal to resting fish. Ultimately, however, heart rate apparently becomes a weak partner for the cardiorespiratory oxygen cascade when temperature increases above the optimum for aerobic scope. Thus, the upper limit for heart rate may emerge as a valuable, but simple predictor of optimal temperature in active animals, opening the possibility of using biotelemetry of heart rate in field situations to explore properly the full interplay of environmental factors on aerobic scope. An example of an ecological application of these physiological discoveries is provided using the upriver migration of adult sockeye salmon, which have a remarkable fidelity to their spawning areas and appear to have an optimum temperature for aerobic scope that corresponds to the river temperatures experienced by their antecedents. Unfortunately, there is evidence that this potential adaptation is incompatible with the rapid increase in river temperature presently experienced by salmon as a result of climate change. By limiting aerobic scope, river temperatures in excess of the optimum for aerobic scope directly impact upriver spawning migration and hence lifetime fecundity. Thus, use of aerobic scope holds promise for scientists who wish to make predictions on how climate change may influence animal distributions. Key words: thermal niches, optimal temperature, aerobic scope, oxygen uptake, metabolic rate, cardiac output, heart rate, tissue oxygen extraction, oxygen partial pressure, biotelemetry, lifetime fecundity, climate change. Introduction –2°C in Antarctica to +42°C in Lake Magadi, Kenya). Similarly, The study of the physiological and biochemical mechanisms that ~43% of all fish species live in freshwater rather than the vastly set the limits for environmental tolerance, and which in many ways more abundant saline habitats [>99% of the available aquatic distinguish species, is an active area of investigation that has gained habitat (Nelson, 2006)]. Although the foundation for the thermal importance in the current era of climate change. This article is distributions that we see today may seem to reflect an absence focused on the physiological mechanisms that become critical of the requisite genomic machinery, a more circumspect view when fishes, particularly salmonids, approach their upper may be need. For example, Antarctic fishes, which have lived in temperature limits. Furthermore, to address the need for examples a thermally stable environment for many thousands of years, are of how large-scale environmental records of climate are translated now known to be able to thermally acclimate to temperatures at the scale of the organism (Helmuth, 2009), this mechanistic previously thought to be lethal and well above those found in understanding is applied to the river migration of an adult Pacific their present ecological niche (Franklin et al., 2007). Thus, salmon species. observing a stenothermal existence does not necessarily mean My focus on predominantly one group of fishes (the insufficient phenotypic plasticity to tolerate a broader salmonids) and on one environmental variable (temperature) is temperature range. for two reasons. First, this is where data are most abundant. Temperature and aerobic scope Second, a case study of temperature tolerance among fishes is likely to prove extremely fruitful in addressing the more general Temperature has a central role in shaping the distribution of and important question of animal resilience and adaptability to animals. In explaining latitudinal and longitudinal limits of biomes, environmental change. This is because fishes have evolved Shelford’s law of tolerances envisaged a centre of animal around species-specific niches, living in almost every abundance bounded by ‘toleration’ of environmental ‘controlling conceivable aquatic habitat and representing almost half of the factors’ (Fig. 1A). Clearly, the poleward shift in fish distributions earth’s vertebrate species. However, no single fish species with the progressive warming of aquatic habitats (Brander et al., tolerates the entire temperature range exploited by fishes (from 2003; Brander, 2007; Pörtner and Knust, 2007; Dulvy et al., 2008) THE JOURNAL OF EXPERIMENTAL BIOLOGY Toleration 3772 A. P. Farrell Farrell, 2008), illustrating an importance well beyond fishes. Even so, and as shown in the following, our understanding of the Controlling Controlling proximate causes that limit a fish’s aerobic scope beyond its factors factors optimal temperature range remains formative. Centre of abundance The Fry curve for aerobic scope Aerobic scope is derived from measurements of a fish’s minimum ) as a function of and maximum rates of oxygen uptake (V temperature (Fig.1B). The difference between these two rates is aerobic scope, which takes the form of a bell-shaped curve as a Latitude/longitude/temperature function of temperature – a ‘Fry curve’ for aerobic scope (Fig.1C). Simplistically, a Fry curve represents an animal’s capacity for activity as a function of temperature. (standard or basal metabolic rate) represents the 2.5 Minimum V Active metabolic cost to support an animal’s existence in a non-feeding, is directly non-reproducing and non-motile state. Minimum V 2.0 affected by body temperature [thermodynamics (Krogh, 1914)], typically doubling or tripling with a 10°C acute increase in effect; Fig.1B). Minimum V also temperature (termed a Q 10 O 1.5 varies among species (a genetic basis) and with body size [scaling (Schmidt-Nielsen, 1984)]. Standard 0.5 Clearly, life beyond short-term existence requires a capacity to above this minimum level. Energy expenditure for increase V feeding, growth, reproduction and locomotion (used for foraging as well as escape from predators and unfavourable environments) 1.5 . In terms of the temperature dependence of needs an active V , Fry (Fry, 1947; Fry and Hart, 1948) made the crucial active V of exercising goldfish (Carassius observation that maximum V 1.0 auratus) failed to continue increasing with temperature beyond an ). By contrast, standard V of resting fish optimal temperature (T opt O A Fry curve 0.5 continued its exponential increase until temperature approached a for aerobic scope is created by lethal level (Fig.1B). Thus, the T opt to continue increasing with the failure of maximum V temperature. Consequently, because activities such as growth 8 16 24 32 40 depend on aerobic scope, it is not surprisingly that growth rate as Acclimation temperature (°C) a function of temperature has a similar bell-shaped, species-specific Fig.1. The controlling and limiting effects of temperature on animal curve for fishes (Fig. 2B) (Brett, 1971). In fact, fish must eat more distributions, metabolic rate and scope for activity. (A)A schematic just to deal with the exponential increase in standard V . Like representation of Shelford’s law of tolerances (Shelford, 1931). , active V is also species-specific and varies with minimum V O O 2 2 (B)Measurements of standard and active metabolic rates for goldfish as a body size. function of temperature approaching their upper incipient lethal At a critical temperature (T ), aerobic scope is zero and aerobic crit temperature. (C)Aerobic scope (or scope for activity) as a function of activity becomes impossible. Thus, a thermal niche for existence in temperature, which is the difference between the measurements of values (which standard and active metabolic rates shown in B (Fry, 1947). a resting state is bounded by the upper and lower T crit and CT values determined using correspond closely to the CT max min other methods). However, existence without an aerobic scope is represents a more insidious manifestation of the anthropogenic- necessarily short-lived in nature because, besides being an easy driven change in animal distribution that Shelford characterised target for predators, starvation is just a matter of time. nearly 80 years ago (Shelford, 1931). Consequently, an animal’s functional thermal niche is narrower Temperature tolerance at the whole animal level was first given than that bounded by T crit a mechanistic explanation for fishes by Fry (Fry, 1947), who Fry curves are species specific. Differences result from their showed that temperature both controlled and limited their position on the temperature scale (temperature niches), being metabolic rate. To illustrate his ideas, he used scope for activity, centred near 27°C for goldfish and at cooler temperatures (<20°C) which is now termed aerobic or metabolic scope, i.e. the difference for most salmonids (Fig.2A). There are also species differences in . Athletic species such as salmonids have a between standard and active metabolic rates (Fig.1B,C). In doing standard and active V so, Fry recognized that the predictive value of knowing the high aerobic scope, but this does not necessarily translate into a temperature dependence of aerobic scope was considerably greater larger thermal niche. For example, generalists such as goldfish than that of knowing a temperature tolerance range (e.g. critical (Fig.2A) and Fundulus heteroclitus (Fangue et al., 2006) have a and CT ). Indeed, maximum and minimum temperatures; CT low aerobic scope and a broader thermal niche (eurythermal) max min the aerobic scope concept is now being used broadly to examine compared with salmonids. the impacts of the aquatic warming trends and other environmental Scaling up of laboratory-derived aerobic scope data to ecology climate changes on marine ectotherms (Pörtner, 2001; Pörtner, and biogeography will not necessarily be a simple task because 2002; Mark et al., 2002; Pörtner and Knust, 2007; Pörtner and other environmental factors reduce aerobic scope and narrow an THE JOURNAL OF EXPERIMENTAL BIOLOGY Toleration –1 –1 –1 –1 Aerobic scope (ml O kg min ) V (ml O kg min ) 2 O2 2 Animal abundance Ultimate upper incipient lethal temperature Salmon in hot water 3773 9.0 found to lose nearly 50% of their aerobic scope with only a 2°C Gates increase above the average summer temperature (Nilsson et al., sockeye 7.5 2009), and an increase of 3°C compromised growth of spiny- Weaver damselfish (Acanthochromis polyacanthus) (Munday et al., 2008). sockeye 6.0 However, the collapse of aerobic scope at warm temperatures was Chehallis Rainbow coho less evident (Fig.2A) for the bullhead (Ameiurus nebulasa) and trout 4.5 brown trout (Salmo trutta), suggesting that other factors may set thermal tolerance. Lake trout 3.0 Brook Brown bullhead trout The rise and fall of aerobic scope in salmonids 1.5 As temperature increases, exponentially more oxygen must be Brown trout Goldfish delivered to tissues, which is the task of the cardiorespiratory fails to increase beyond T , the system. Since maximum V O opt 010 20 30 40 2 (i.e. the downward trend of a decline in aerobic scope beyond T opt Fry curve) therefore reflects the inability of the maximum 0.08 cardiorespiratory capability to keep pace with these increasing corresponds with a failure Brook trout tissue oxygen demands. By contrast, T crit 0.06 of the resting cardiorespiratory capability to keep pace with increasing tissue oxygen demands. The resultant mismatch between oxygen supply and oxygen demand forces animals to progressively 0.04 switch to anaerobic metabolism to survive (Pörtner, 2001; Bull trout Frederich and Pörtner, 2000), perhaps causing an acceleration of 0.02 cardiorespiratory collapse (Farrell et al., 2008) and the rightward Allopatry skew often seen in Fry curves. At present, cardiorespiratory information pertaining to the collapse of aerobic scope during warming is most abundant for 0 5 10 15 20 25 30 salmonids. The data are examined below within the context of the Acclimation temperature (°C) cardiorespiratory oxygen cascade in order to explore why active does not increase beyond T and why minimum V collapses Fig.2. The influence of temperature on aerobic scope and growth rate. V O opt O 2 2 (A)Fry curves for a range of salmonids and other species (Fry, 1947; Fry, . at T crit 1948; Fry and Hart, 1948; Lee et al., 2003). (B)Growth rates of brook trout and bull trout grown either separately (solid lines with the accompanying Active V and the cardiorespiratory oxygen cascade dashed lines showing the 95% confidence limits) or together (long dashed The cardiorespiratory oxygen cascade conceptualizes the lines grouped by allopatry) (McMahon et al., 2007). movement of oxygen down its partial pressure gradient from a corresponds to the respiratory medium to tissues. Hence, V oxygen flux per unit time through this cascade and oxygen animal’s functional thermal niche (Fry, 1947; Fry, 1971; Brett, diffusion rates are proportional to the relevant oxygen partial 1971; Pörtner and Farrell, 2008; Munday et al., 2009). For example, pressure (P ) gradients. For fish, oxygen diffuses from water aquatic hypoxia, independent of temperature, can reduce aerobic across gill secondary lamellae and binds to haemoglobin (Hb) in scope (Graham, 1949; Gibson and Fry, 1954; Fry, 1971; Brett, red blood cells, which are transported by the circulatory system to 1971) to the extent that feeding and growth are halted, and tissues where oxygen diffuses across the capillary wall and into the development and reproduction are delayed (see Richards et al., cell to be used in mitochondrial respiration (Fig. 3). 2009). Therefore, both hypoxia and hypercapnia are likely to A countercurrent arrangement of blood and water flow at the constrain the breadth and height of a Fry curve (Pörtner and Farrell, secondary lamellae ensures that the arterial blood leaving the gills (Pa ) close to ambient water, and its Hb is almost fully 2008). Furthermore, the aerobic scope for a developing fish may has a P O O 2 2 ) is near not reach its full potential until the cardiorespiratory system is fully saturated, i.e. the oxygen content of arterial blood (Ca developed. Therefore, a family of Fry curves may exist for different maximal. Convection of oxygen to tissues by the arterial system is and cardiac output. Thus, life stages. Behaviour adds further complexity. For example, inter- quantified as the product of Ca for growth (Fig.2B), as seen specific competition can shift the T increasing cardiac output is the only means to internally transport opt in brook trout (Salvelinus fontinalis) when growth was suppressed more oxygen to the tissues, unless stored red blood cells are while competing with bull trout (Salvelinus confluentus), but not released from the spleen to increase Hb concentration [Hb] and (see Gallaugher and Farrell, 1998). Once in tissue vice versa (McMahon et al., 2007). hence Ca An important index that can be derived from a Fry curve is the capillaries, factors such as the architecture of the capillaries, the and T . thermal window, the temperature difference between T presence of myoglobin and lipid droplets in the cytoplasm and the opt crit This thermal window is an index of a species’ resilience to actual location of mitochondria within the cell significantly temperature change. In salmonids, the thermal window for the influence the rate of diffusion of oxygen from the red blood cell to collapse of aerobic scope with warming is just 6–7°C (Fry, 1947; the mitochondria. Farrell et al., 2008), which is a relatively small safety margin in the In a resting fish, increasing tissue oxygen delivery with context of global warming scenarios. Tropical species apparently increasing temperature could simply recruit mechanisms that are have narrow thermal windows too (Hoegh-Guldberg et al., 2007; normally used during exercise. When salmonids exercise at a . For example, Tewksbury et al., 2008) and live close to their T constant temperature, there are increases in gill ventilation (to crit cardinalfishes (Ostorhinchus doederleini and O. cyanosoma) were deliver more water), cardiac output (to transport more oxygen to THE JOURNAL OF EXPERIMENTAL BIOLOGY –1 –1 –1 Aerobic scope (ml O kg min ) Growth (g day ) 2 3774 A. P. Farrell (Clark et al., 2008a). In fact, Pa actually increased in resting Pa 2 (Steinhausen et al., 2008). sockeye salmon warm to T crit data during warming is more complex because Interpreting Ca Increase of potential pH and temperature effects on the Hb–oxygen affinity gill Gills Tissues curve, and because warming has variable effects on blood [Hb] ventilation Increase O (Taylor et al., 1997; Farrell, 1997; Sandblom and Axelsson, 2007). extraction was maintained in resting sockeye salmon warmed Even so, Ca by tissues O as well as in exercising sockeye salmon warmed above T 2 to T crit opt (Steinhausen et al., 2008). By contrast, Ca decreased at T in O crit Increase 2 cardiac output resting rainbow trout (O. mykiss) (Heath and Hughes, 1973) and in resting Chinook salmon (Clark et al., 2008a). The modest decrease Fig. 3. A schematic diagram representing the oxygen cascade for a fish , in the absence of an effect on Pa , in resting Chinook in Ca O O 2 2 during rest (shaded lines and arrows) and swimming (dark lines and salmon probably reflects a decrease in Hb–oxygen affinity rather arrows). The oxygen partial pressure is an arbitrary scale (see text for than a limitation on oxygen diffusion at the gills. details). A limitation in the circulatory system? If a circulatory limitation exists for exercising salmonids during the tissues) and tissue oxygen extraction from blood (Stevens et al., is warming, increases in cardiac output should cease once T opt 1967; Kiceniuk and Jones, 1977). Increased tissue oxygen reached. Indeed, maximum cardiac output in exercising sockeye as extraction can contribute almost as much to the increased V salmon (Brett, 1971; Steinhausen et al., 2008) and rainbow trout cardiac output because resting fish remove only about one third of (Taylor et al., 1996) reached a maximum value at a temperature ) and , as did V . Thus, ultimately as warming the arterial oxygen and so venous oxygen content (Cv well below T O crit O 2 2 (Pv ) can decrease considerably during exercise the potential to increase maximum cardiac output venous blood P approaches T O O opt 2 2 (Fig.3). While all of these exercise-induced cardiorespiratory (as revealed by exercising fish) fails to keep up with the required changes are possible during warming, as shown below, not all of increase in cardiac output in a resting fish (Fig. 4). As a result, them occur when resting fish are warmed up to T because scope for cardiac output does not increase above T crit opt (Fig. 5), swimming effort either declines or stops. When an exercising fish is warmed, it is more a matter of how is even more much the warming increases the rate and force of muscle For resting salmonids, the cardiac limitation at T crit contraction to enhance maximum cardiorespiratory capacity. In obvious. Cardiac arrhythmias and bradycardia often develop at T crit (Heath and Hughes, 1973; Clark et al., 2008a), although their addition, oxygen diffuses at a faster rate, potentially allowing a . Furthermore, the temperature sensitivity of the lower Pv physiological basis has not been studied. Thus, experimental Hb–oxygen binding curve (e.g. Clark et al., 2008a) is such that a evidence points unequivocally towards a cardiac limitation both at of fully saturated in exercising salmonids and at T in resting salmonids. Further rightward shift with warming increases the Pa T O opt crit arterial blood. This also promotes a faster unloading of oxygen at insight into the mechanistic basis of the cardiac response to could decrease during warming without a the tissues. In fact, Cv warming and its limitations comes from an analysis of heart rate (this direct temperature effect is in addition to a decrease in Pv (the rate function) and cardiac stroke volume (the capacity similar benefit from the Root- or Bohr-shifts as tissues release more function). carbon dioxide and H during exercise). The importance of increased heart rate during acute warming is Some fairly simple theoretical predictions can be made using this extremely clear. Warming increases cardiac output solely by conceptual framework, against which existing cardiorespiratory increasing heart rate. This is true for both resting and exercising data on warming in fishes can be compared. The analysis is further salmonids (Sandblom and Axelsson, 2007; Clark et al., 2008a; simplified by asking where the potential limitation might exist Steinhausen et al., 2008), presumably through a direct temperature (gills, circulatory system or tissues), and by focusing on underlying effect on the cardiac pacemaker rate (Randall, 1970). However, for resting fish and at T for exercising mechanisms (at near T because fish have a maximum heart rate (Farrell, 1991) and heart crit opt fish). rate is already elevated by the exercise, the maximum heart rate must be reached at a temperature well below that for resting fish Changes in cardiorespiratory variables with acute warming in (Steinhausen et al., 2008). In fact, the scope for heart rate plummets association with T in exercising salmonids and T in to zero near T (Fig.5). Fred Fry made from its maximum at T opt crit opt crit resting salmonids a similar observation for heart rate in Salvelinus fontinalis alevins A limitation at the gills? (Fig. 6A) (Fry, 1947) and commented that this might reflect the T opt Oxygen is poorly soluble in water. Compounding this, its solubility for the activity of an organ (i.e. the heart)! We now know that Fry’s for the maximum in water decreases ~2% per degree centigrade. Therefore, gill assertion was correct because the T opt ventilation must compensate for the decreased oxygen availability performance of isolated rainbow trout hearts is well below T crit (Fig.6B). and the lower Hb–oxygen affinity, as well as increased tissue oxygen demand as temperature increases. Therefore, a decrease in In contrast to heart rate, cardiac stroke volume appears to be Pa during warming would indicate a clear problem associated thermally insensitive to warming. This is true for resting and with gill oxygen delivery and transfer. However, the data for exercising salmonids (Sandblom and Axelsson, 2007; Clark et al., salmonids are inconsistent on this matter. 2008a; Steinhausen et al., 2008), but it is an especially surprising When exercising adult sockeye salmon (Oncorhynchus nerka) result for resting fish. In fact, it seems paradoxical, given that , Pa was were warmed to a temperature well above T cardiac stroke volume can triple during swimming at constant opt O maintained (Steinhausen et al., 2008). Similar results were found temperature (Stevens et al., 1967; Brett, 1971; Kiceniuk and Jones, in resting Chinook salmon (O. tshawytscha) warmed up to T 1977; Farrell and Jones, 1992; Thorarensen et al., 1996; Gallaugher crit THE JOURNAL OF EXPERIMENTAL BIOLOGY Tissue O extraction –1 (ml O ml blood ) Tissue O extraction –1 (ml O ml blood ) Salmon in hot water 3775 80 50 O2 Heart rate 0.05 15 17 19 21 23 0.10 Temperature (°C) 0.15 16 Fig.5. Changes in scope for oxygen uptake (V ), cardiac output (V ) and O b heart rate (f ) in swimming sockeye salmon during acute warming. Note that although all fish continued swimming in temperatures up to and including 19°C, some fish stopped swimming at higher temperatures and B so the data are only for those that continued to swim (Steinhausen et al., 2008). 40 filling pressure also increased (Sandblom and Axelsson, 2007). , venous However, with further warming to 16°C, which is near T opt blood pressure was unchanged and cardiac stroke volume decreased when heart rate increased further. Although a complete systolic emptying of the ventricle may be a disadvantage with 0 regard to the capacity to increase cardiac stroke volume during warming, it may be more important in ensuring a completely ‘fresh’ 0.05 supply of oxygen enters the lumen of the heart with each heart beat 0.10 20 given oxygen diffusion to the myocardium is driven by a low Pv 0.15 (see Farrell, 2002). The increase in cardiac stroke volume when salmonids swim at a constant temperature is supported by an increase in venous blood pressure (Kiceniuk and Jones, 1977) and by contraction of Fig.4. Cardiac output and tissue oxygen extraction (Ca –Cv ) for 12°C- O O 2 2 locomotory muscles aiding venous return (Farrell et al., 1988). acclimated sockeye salmon either (A) at rest, or (B) swimming continuously at about 70% of maximum swimming speed, while the temperature was There are several potential reasons why warming does not increase –1 acutely increased at 2°Ch and held at the temperature for 1h while cardiac stroke volume any further. There could be physical upper cardiorespiratory measurements were made. All resting fish completed the limits to venous return and end-diastolic volume. Also, increasing temperature challenge and recovered, but above 19°C swimming fish heart rate during warming reduces cardiac filling time and creates began to stop swimming and so progressively fewer are represented at a negative frequency effect on cardiac contraction, both of which higher temperatures. The x–y surface at each temperature represents could constrain cardiac stroke volume (Farrell, 2007). In addition, oxygen uptake (i.e. the product of cardiac output and tissue oxygen extraction), which clearly increases with temperature in resting but not at a time when the heart is working maximally, its extracellular swimming fish above their optimum temperature of around 15°C. Changes environment (the venous blood) becomes acidemic and in cardiac output with temperature are a result of increased heart rate (see (Steinhausen et al., 2008). hyperkalemic, and has a low Pv text) (Steinhausen et al., 2008). Although the negative inotropic effects of these extracellular changes were prevented by adrenergic stimulation of the heart (Driedzic and Gesser, 1994; Nielsen and Gesser, 2001; Hanson et et al., 2001), that this additional capacity for increasing cardiac al., 2006), this adrenergic protection was greatly reduced at 18°C stroke volume is not exploited by resting fish when they are compared with 10°C in rainbow trout (Hanson and Farrell, 2007). (Fig.4). So why is this? warmed to T crit A limitation at the tissues? The difficulty may revolve around the fact that cardiac end- The rate and degree of oxygen diffusion from capillaries to tissues systolic volume is essentially zero in salmonids (Franklin and gradient. These Davie, 1992). This means that, unless venous return and end- is influenced by several factors besides the P diastolic volume are increased first, an increase in cardiac include tissue capillary density, the intracellular mitochondrial contractility cannot increase cardiac stroke volume appreciably location, regional blood flow and red blood cell capillary contact (Sandblom and Axelsson, 2007). Furthermore, there are indications time. Taylor et al. (Taylor et al., 1997) suggested that regional that during warming inadequate venous return may limit cardiac oxygen delivery by convective transport in exercising rainbow trout stroke volume in the first instance. In resting rainbow trout warmed is determined mainly by changes in cardiac output as temperature from 10 to 13°C, cardiac stroke volume was maintained when heart changes, i.e. active peripheral redistribution of blood flow is rate increased because venous blood pressure and mean circulatory modest. Even so, red muscle blood flow during aerobic swimming THE JOURNAL OF EXPERIMENTAL BIOLOGY Temperature (°C) Temperature (°C) –5 –1 –1 Scope for: V (µmol 10 min kg ) –1 –1 –1 V (ml min kg ) Heart rate (min ) –1 –1 Cardiac output (ml min kg ) –1 –1 Cardiac output (ml min kg ) 3776 A. P. Farrell 120 was acidemia and Cv decreased (Clark et al., 2008a). When again remained exercising sockeye salmon were warmed, Pv Sockeye 2 temperature insensitive, albeit it at a lower level compared with resting fish (Steinhausen et al., 2008). This consistent temperature points to a diffusion limitation for oxygen insensitivity of Pv unloading (see Farrell, 2002; Farrell and Clutterham, 2003). Why to the level seen in resting fish warming does not decrease Pv with swimming at a constant temperature is unclear. just prior to T may In resting salmonids, the decrease in Cv O crit Brook trout reflect a desperate situation created by inadequate tissue perfusion. The ability of fish to recover from warming may be informative in this regard. For example, when sockeye salmon and Chinook were –1 and kept at a constant incrementally warmed at 2–4°Ch 0 5 10 15 20 temperature for 1h between temperature steps, the fish recovered Temperature (°C) well at the control temperature and within 1–2h, especially if the heat stress was terminated before cardiac arrhythmias developed (Steinhausen et al., 2008; Clark et al., 2008a). In these experiments, 10 and Chinook salmon decreased sockeye salmon maintained Cv only in association with acidemia at 24°C. By contrast, when Cv ‘opportunistic’ blood samples were taken from resting rainbow 7/7 14/14 –1 ), all but one fish died trout during continuous warming (1.5°Ch 11/13 9/15 and venous blood became depleted of oxygen (Heath and Hughes, 1973). 14/14 What emerges from the above is that the heart becomes a weak link for the cardiorespiratory oxygen cascade when exercising . Although a direct temperature salmonids are warmed above T opt effect on the cardiac pacemaker rate appears to be the predominant 0 5 10 15 20 25 mechanism for improving tissue oxygen transport, a crucial Acclimation temperature (°C) limitation is reached when this rate function reaches its maximum. Fig.6. (A)A comparison of heart rates measured in brook trout alevins (Fry, for exercising fish and at T for This apparently occurs at T opt crit 1947) and adult sockeye salmon (Steinhausen et al., 2008) to illustrate the resting fish. What follows during warming is a sequela of events: convergence of heart rate in resting (lower lines) and active (upper lines) a decrease in scope for heart rate preceding that for cardiac output, fish such that there is no scope for heart rate at T . (B)A composite of the crit which precedes that for aerobic scope (Fig.5). It is also evident that maximum cardiac performance for isolated perfused rainbow trout hearts during warming the contributions of several capacity functions acclimated to different temperature to illustrate that there is a peak performance around 15°C for the heart. Beyond this temperature, an ([Hb], tissue oxygen extraction and cardiac stroke volume) are only increasing number of preparations would fail as indicated by the ratio of small and variable. Why this excess capacity is not exploited when successful/attempted preparations besides each data point (Farrell et al., resting fish are warmed is particularly perplexing and warrants 1988; Keen and Farrell, 1994; Farrell et al., 1996). further study. Beyond salmon was lower at 18°C than at 11°C (Taylor et al., 1997). In addition, The details provided above for salmonids apparently apply more the basal oxygen requirement of white (fast glycolytic) muscle in broadly to other fishes. For example, warming of three species fish increases during warming because it accounts for >50% of showed that like rainbow trout: (1) cardiac output increases body mass and receives 28–50% of routine cardiac output in resting predominantly through increased heart rate, (2) routine heart rate that is species specific, and rainbow trout (Randall and Daxboeck, 1982; Bushnell et al., 1992). shows a plateau or collapse before T crit Indeed, the finding that blood flow to white muscle increased from (3) cardiac stroke volume is temperature insensitive (Fig.7) 40% to 75% of cardiac output at 6°C versus 18°C in resting rainbow (Sandblom and Axelsson, 2007 and references therein). In addition, trout (Barron et al., 1987) clearly reflects a significant elevation of the temperature dependence of Hb–oxygen affinity and the variable . White white muscle oxygen demand relative to whole animal V effects of warming on [Hb] are well known among fishes (Cech et muscle also has a low capillary density (Egginton, 2000), which al., 1976; Gallaugher and Farrell, 1998; Gollock et al., 2006), and increases the likelihood of a diffusion limitation developing for a direct temperature effect on the spontaneous pacemaker rate is oxygen diffusion. recognised for plaice (Pleuronectes platessa) (Harper et al., 1995). Further insight into potential limitations on tissue oxygen Furthermore, in resting Atlantic cod (Gadus morhua), although , heart rate removal during warming is evident from measurements of Cv heart rate and cardiac output both collapsed before CT O max and Pv . For example, Pv and Cv could not decrease if there (at 18°C versus at reached a plateau before cardiac output and V O O O O 2 2 2 2 was a diffusion limitation. In fact, a decrease in Cv is a very 20°C) (Gollock et al., 2006). important mechanism for increasing tissue oxygen extraction The effects of acute warming have been thoroughly studied in during swimming at constant temperature (Fig.4). However, for winter flounder (Pseudopleuronectes americanus) seasonally resting sockeye salmon, warming actually increased Pv and acclimated between 5°C and 18°C (Cech et al., 1975; Cech et al., Cv and tissue oxygen extraction (Fig.4) remained unchanged 1976). After a 5°C warming at each acclimation temperature, an O , was temperature (67–83% per 5°C increment) was always (Steinhausen et al., 2008). Similarly, Pv increase in V O O 2 2 insensitive in resting Chinook salmon, except at 25°C when there accompanied by a nearly equivalent increase heart rate (54–77% THE JOURNAL OF EXPERIMENTAL BIOLOGY Maximum myocardinal –1 –1 Heart rate (min ) power output (mW g ) Tissue O extraction –1 (ml O ml blood ) Tissue O extraction –1 (ml O ml blood ) Salmon in hot water 3777 75 80 Trout Wolfish Cod Flounder 0.01 0.02 0.03 0.75 0.01 0.02 0.50 10 0.03 0.25 0 5 10 15 20 25 30 Fig.8. Cardiac output (V ) and tissue oxygen extraction (Ca –Cv ) for b O O 2 2 Temperature (°C) winter flounder either (A) seasonally acclimated to a temperature, or (B) acutely warmed by 5°C increments from the acclimation temperature. The Fig.7. Changes in cardiorespiratory variables in resting fishes during acute x-y surface at each temperature represents oxygen uptake (the product of warming: a comparison of wolffish, winter flounder and Atlantic cod with V and Ca ), which clearly increases with temperature and either reaches b O rainbow trout. (Data kindly supplied by Dr Kurt Gamperl: wolffish – N. a plateau between acclimation temperatures of 15 and 18°C, or collapses Joaquim and A. K. Gamperl, unpublished; trout – A. K. Gamperl, with an acute increase to 23°C. The greatest contributor to increases in unpublished; Atlantic cod – L. H. Petersen and A. K. Gamperl, unpublished; V is almost always V , which is a result of increased heart rate (see text) O b flounder – P. C. Mendonca and A. K. Gamperl, unpublished.) (Cech et al., 1975; Cech et al., 1976). per 5°C increment). However, with warming from 18°C to a near- environmental factors on aerobic scope to be properly explored. lethal temperature, cardiac output and cardiac stroke volume Accompanying such fieldwork is the need to better understand the , Pa , collapsed even though heart rate increased (Fig. 8). Ca control of heart rate at high temperature and to determine if the O O 2 2 and Pv were all maintained, except for 5°C- and 18°C- Cv heart is operating at its maximum pacemaker rate. O O 2 2 acclimated fish when tissue oxygen extraction increased (Fig.8). Temperature and the river migration of sockeye salmon Heart rate may be a limiting factor during warming in decapod Beyond direct temperature reactions (i.e. acute effects occurring in crustaceans as well. Heart rate is reported to reach a plateau near in various crab species: the spider crab [Maja squinado T minutes to hours considered above), two other time scales can be crit (Frederich and Pörtner, 2000)], the rock crab [Cancer irroratus applied to temperature effects. Thermal adaptation spans (Frederich et al., 2009)] and the kelp crab [Taliepus dentatus generations and occurs at the population level through natural (Storch et al., 2009)]. Cardiac stroke volume was also temperature selection acting on individual variability. The study of heritable insensitive in the kelp crab. Therefore, the upper limit for heart rate factors related to thermal tolerance is in its infancy. Thermal may emerge as a valuable, yet simple predictor of T in active acclimation (or thermal compensation), however, occurs when an opt in resting animals. If this is the case, biotelemetry animals and T individual undertakes physiological and biochemical adjustments crit of heart rate could easily extend this work to field situations (Clark over days to weeks [or perhaps months for Antarctic fishes at near et al., 2008b; Clark et al., 2009), allowing the full interplay of freezing temperatures (Franklin et al., 2007)]. Here, a new THE JOURNAL OF EXPERIMENTAL BIOLOGY Temperature (°C) Temperature (°C) –1 –1 –1 –1 Stroke volume (ml kg ) Heart rate (min ) Cardiac output (ml min kg ) Cardiac output Cardiac output –1 –1 –1 –1 (ml min kg ) (ml min kg ) 3778 A. P. Farrell phenotype emerges from an existing genome as an animal to river temperature above T . In fact, migration success was only opt (at 18–21°C), but acclimates to a new thermal environment. Given the potential for 0–11% when river temperature was near T crit thermal acclimation and adaptation, the obvious question becomes: increased to 77% when the river seasonally cooled to 14°C and near (Farrell et al., 2008). This result suggests that a warm river Do the acute responses to temperature in fishes have any ecological their T opt or evolutionary relevance? In the specific case of adult sockeye temperature limited aerobic scope, and impaired upriver migration salmon that return to the Fraser River, BC, Canada to spawn, the and lifetime fecundity. These warm river temperatures experienced answer is categorically yes. During this return migration, sockeye by Weaver Creek sockeye salmon in 2004, which turned out to be salmon can experience large and rapid temperature changes when record highs, contributed to a catastrophic 70% loss of the they make daily vertical ocean movements prior to river entry and migrating population! exploit deeper, cool water in lakes (Fig. 9). Thermal acclimation Adult sockeye salmon return migrations also provide a Warm acclimation alters thermal tolerance (Fry et al., 1942), fascinating insight into something that is normally difficult to and T . The linkage , T and maximum aerobic scope (Fry and Hart, witness, an ecological significance for T increasing T opt crit opt crit between aerobic scope and lifetime fecundity is obvious for 1948). Warm acclimation, in addition to permitting a higher sockeye salmon because their entire lifetime fitness hinges on a maximum heart rate, also decreases routine heart rate at the level single, precise spawning date that is preceded by an energetic of the pacemaker. This acclimatory change then provides upstream migration lasting up to several weeks. Therefore, to compensation for the limitation that maximum heart rate imposes spawn, they are committed to an upriver migration that periodically on aerobic scope by restoring the scope for heart rate either fully may require their full aerobic scope, with only a sensory imprint (Harper et al., 1995) or partially (Farrell, 1997). However, the for navigation, while developing gonads, without feeding and benefits of temperature acclimation for specialists like salmon are without prior experience of the temperature conditions en route small compared with temperature generalist. For example, CT max for salmon increases by only 2°C over a 15°C acclimation (Hinch et al., 2006). Consequently, if a warm river temperature of 10°C for goldfish reduces aerobic scope, sockeye salmon do not have an option of temperature range versus an increase in CT max postponing reproduction as other fishes might do. In fact, with just over a 30°C acclimation range (Brett, 1956). In fact, routine and 4–6 weeks to live after entering the river, even a slower migration maximum heart rate in 22°C-acclimated sockeye salmon –1 –1 and 106beatsmin , respectively (Brett, 1971)] are could reduce lifetime fecundity. [86beatsmin Using Weaver Creek sockeye salmon as an example and barely different for a 14°C-acclimated fish acutely warmed to 22°C –1 –1 and 106beatsmin (Steinhausen et al., 2008)]. considering only aerobic swimming, upstream migration should be [90beatsmin for aerobic scope) but impossible at favoured at 14.3°C (their T Other documented responses to warm acclimation, such as the opt ) (Lee et al., 2003). As predicted, when adult 20.4°C (their T decrease in cardiac mass (Gamperl and Farrell, 2004) and decrease crit Weaver Creek sockeye salmon were intercepted in 2004, implanted in capillary density the red (slow aerobic) muscle of rainbow trout with biotelemetry devices and released back to the river to follow (Taylor et al., 1996; Egginton, 2000), even seem counterproductive. their subsequent progress, migration success was inversely related Conversely, compensatory decreases in gill epithelial thickness, as seen for other species (Taylor et al., 1997), would be beneficial. Antecedents and concluding remarks Adams River sockeye thermal experience 2006 20 Like a salmon down on the Fraser, swimmin’ with their Shuswap battered fins, Lake Searchin’ for their childhood home, A patch of gravel they knew as their own. Excerpt from ‘The Ballad of Old Tom Jones’ by Barney Bentall The genomic information passed down by antecedents determines an individual’s potential for survival, growth and reproduction. The 11 antecedents of present day Fraser River salmon have passed on their environmental experiences through natural selection for over Lower ~10,000 years since their post-glacial invasion. However, we have Fraser River only ~60 years of reliable archival records of the river temperatures Georgia Strait experienced during recent salmon migrations (Farrell et al., 2008). Nevertheless, remarkably the historic mean and median river migration temperature for Weaver Creek sockeye salmon is 14.5°C 21-Aug 31-Aug 10-Sep 20-Sep 30-Sep 10-Oct 20-Oct is 14.3°C). This observation, combined with the fact that (their T opt and T is only 7.3°C and that the thermal window between T opt crit Fig.9. Hourly temperature recordings from an I-button temperature logger , suggests that thermal acclimation provides little benefit to CT max that was recovered from an Adams River sockeye salmon after is potentially a product of natural selection. If this is the their T implantation in the peritoneal cavity in the Georgia Strait (ocean conditions) opt and a 40-day migration through the Fraser River watershed to its spawning case, one has to question whether or not natural selection among area near the Shuswap Lake, BC, Canada. The highlighted areas sockeye salmon can accommodate the rapid warming trend already represent periods where the fish behaviourally sought out water that was evident for the Fraser River (peak summer temperature has cooler than either the mainstem river or at the surface of lakes. The increased 1.8°C in the past 60 years). general downward trend over time represents seasonal cooling of the If the salmonid genome is too inflexible to adapt to a new T opt watershed, and daily oscillations in temperature can be resolved in the perhaps the genetic determinants of the spawning date are more shallow spawning streams towards the end of the trace. (Data kindly supplied by David Patterson.) flexible. Dangerously high temperatures could then be avoided by THE JOURNAL OF EXPERIMENTAL BIOLOGY Internal hourly temperature (°C) Salmon in hot water 3779 migrating when the river is seasonally cooler (see Keefer et al., Brander, K. M., Blom, G., Borges, M. F., Erzini, K., Hendersen, G., MacKenzie, B. R., Mendes, H., Ribeiro, J., Santos, A. M. P. and Toresen, R. (2003). Changes in 2008), but this may result in a fish encountering other unfavourable fish distribution in the eastern North Atlantic: are we seeing a coherent response to conditions such as faster river flows earlier in the year and an changing temperature. ICES Mar. Sci. Symp. 219, 262-270. Brett, J. R. (1956). Some principles in the thermal requirements of fishes. Q. Rev. inevitable run-on-effect on the timing of larval emergence. Biol. 31, 75-87. Alternatively, warm water could be avoided behaviourally if Brett, J. R. (1971). Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon opportunities exist. Behavioural temperature preferences are (Oncorhynchus nerka). Amer. Zool. 11, 99-113. certainly shown by adult salmon during migration, which include Bushnell, P. G., Jones, D. R. and Farrell, A. P. (1992). The arterial system. In Fish Physiology Vol. 12A (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 89-139. seeking water cooler than their T (Fig.9) to lower V and opt O San Diego: Academic Press. perhaps slow energy depletion, suggest they likely know which Cech, J. J., Jr, Bridges, D. W. and Levigne, J. R. (1975). Cardiovascular responses of the winter flounder, Pseudopleuronectes americanus, to near-lethal temperatures. temperature conditions are best for them. However, opportunities In Respiration of Marine Organisms (ed. J. J. Cech, Jr, D. W. Bridges and D. B. to seek cool refuges are very limited in the Fraser River (Donaldson Horton) pp. 155-162. Proc. Marine Section, First Maine Biomedical Science Symp., Mar. 14-16, 1975. Augusta. The Research Inst. Gulf of Maine (TRIGOM) Publ.: et al., 2009). Without such behavioural responses, the warmer than South Portland. normal river temperatures may force Pacific salmon near the Cech, J. J., Jr, Bridges, D. W., Rowell, D. M. and Balzer, P. J. (1976). Cardiovascular responses of winter flounder, Pseudopleuronectes americanus southern limit of their geographic distribution to follow the fate of (Walbaum), to acute temperature increase. Can. J. Zool. 25, 1383-1388. other species, a heart-breaking (Wang and Overgaard, 2006) Chown, S. L., Jumbam, K. R., Sørensen, J. G. and Terblanche, J. S. (2009). Phenotypic variance, plasticity and heritability estimates of critical thermal limits northward shift in their distribution. The response of tropical coral depend on methodological context. Funct. Ecol. 23, 133-140. reef fish species to climate change could be equally dramatic. Clark, T. D., Sandblom, E., Cox, G. K., Hinch, S. G. and Farrell, A. P. (2008a). In closing, the best, albeit limited data set for a single animal Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha) Amer. J. Physiol. 295, R1631-R1639. group appears to provide a mechanistic understanding for the Fry Clark, T. D., Taylor, B. D., Seymour, R. S., Ellis, D., Buchanan, J., Fitzgibbon, Q. curve. Heart rate, which is the main driver for the increase in V P. and Frappell, P. B. (2008b). Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna. Proc. R. Soc. B 275, 2841- during warming, reaches its maximum rate at T and becomes a opt weak link for the cardiorespiratory oxygen cascade. Shelford Clark, T. D., Hinch, S. G., Taylor, B. D., Frappell, P. B. and Farrell, A. P. (2009). Sex differences in circulatory oxygen transport parameters of sockeye salmon (Shelford, 1931) recognized that ‘Animals are better short-period (Oncorhynchus nerka) on the spawning ground. J. Comp. Physiol. B, 179, 663-671. indicators (of environmental change) than plants’ because animals Donaldson, M. R., Cooke, S. J., Patterson, D. A., Hinch, S. G., Robichaud, D., Hanson, K. C., Olsson, I., Crossin, G. T., English, K. K. and Farrell, A. P. (2009). can potentially move away from unfavourable environments. Limited behavioural thermoregulation by upriver-migrating sockeye salmon However, this behavioural response requires an aerobic scope, (Oncorhynchus nerka) in the lower Fraser River, British Columbia. Can. J. Zool. 87, 480-490. which is both controlled and limited by temperature. Future study Driedzic, W. R. and Gesser, H. (1994). Energy metabolism and contractility in on aerobic scope will continue to inform us of an animal’s ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature. Physiol. Rev. 74, 221-258. fundamental thermal niche. By contrast, a continued focus on Dulvy, N. K., Rogers, S. I., Jennings, S., Stelzenmuller, V., Dye, S. R. and temperature tolerances for resting animals will only inform us of Skjoldal, H. R. (2008). Climate change and deepening of the North Sea fish thermal niche for existence and perhaps create needless worry assemblage: a biotic indicator of warming seas. J. Appl. Ecol. 45, 1029-1039. Egginton, S. (2000). The influence of environmental temperature on microvascular about the precise techniques for such measurements (Chown et al., development in fish. Zoology 102, 164-172. 2009). Fangue, N. A., Hofmeister, M. and Schulte, P. M. (2006). Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J. Exp. Biol. 209, 2859-2872. The Natural Sciences and Engineering Research Council, Canada funds my Farrell, A. P. (1991). From hagfish to tuna: a perspective on cardiac function in fish. research. I am grateful for the expert assistance with artwork provided by Linda Physiol. Zool. 64, 1137-1164. Hanson, Steve Tang and Dustin Farrell, and for the improvements to the Farrell, A. P. (1997). 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Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids

P., Farrell, A.
Journal of Experimental Biology , Volume 212 (23) – Dec 1, 2009
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The Journal of Experimental Biology 212, 3771-3780 Published by The Company of Biologists 2009 doi:10.1242/jeb.023671 Commentary Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids A. P. Farrell Zoology Department, 6270 University Boulevard, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4 [email protected] Accepted 19 August 2009 Summary Animal distributions are shaped by the environment and antecedents. Here I show how the temperature dependence of aerobic scope (the difference between maximum and minimum rates of oxygen uptake) is a useful tool to examine the fundamental temperature niches of salmonids and perhaps other fishes. Although the concept of aerobic scope has been recognized for over half a century, only recently has sufficient evidence accumulated to provide a mechanistic explanation for the optimal temperature of salmonids. Evidence suggests that heart rate is the primary driver in supplying more oxygen to tissues as demand increases exponentially with temperature. By contrast, capacity functions (i.e. cardiac stroke volume, tissue oxygen extraction and haemoglobin concentration) are exploited only secondarily if at all, with increasing temperature, and then perhaps only at a temperature nearing that which is lethal to resting fish. Ultimately, however, heart rate apparently becomes a weak partner for the cardiorespiratory oxygen cascade when temperature increases above the optimum for aerobic scope. Thus, the upper limit for heart rate may emerge as a valuable, but simple predictor of optimal temperature in active animals, opening the possibility of using biotelemetry of heart rate in field situations to explore properly the full interplay of environmental factors on aerobic scope. An example of an ecological application of these physiological discoveries is provided using the upriver migration of adult sockeye salmon, which have a remarkable fidelity to their spawning areas and appear to have an optimum temperature for aerobic scope that corresponds to the river temperatures experienced by their antecedents. Unfortunately, there is evidence that this potential adaptation is incompatible with the rapid increase in river temperature presently experienced by salmon as a result of climate change. By limiting aerobic scope, river temperatures in excess of the optimum for aerobic scope directly impact upriver spawning migration and hence lifetime fecundity. Thus, use of aerobic scope holds promise for scientists who wish to make predictions on how climate change may influence animal distributions. Key words: thermal niches, optimal temperature, aerobic scope, oxygen uptake, metabolic rate, cardiac output, heart rate, tissue oxygen extraction, oxygen partial pressure, biotelemetry, lifetime fecundity, climate change. Introduction –2°C in Antarctica to +42°C in Lake Magadi, Kenya). Similarly, The study of the physiological and biochemical mechanisms that ~43% of all fish species live in freshwater rather than the vastly set the limits for environmental tolerance, and which in many ways more abundant saline habitats [>99% of the available aquatic distinguish species, is an active area of investigation that has gained habitat (Nelson, 2006)]. Although the foundation for the thermal importance in the current era of climate change. This article is distributions that we see today may seem to reflect an absence focused on the physiological mechanisms that become critical of the requisite genomic machinery, a more circumspect view when fishes, particularly salmonids, approach their upper may be need. For example, Antarctic fishes, which have lived in temperature limits. Furthermore, to address the need for examples a thermally stable environment for many thousands of years, are of how large-scale environmental records of climate are translated now known to be able to thermally acclimate to temperatures at the scale of the organism (Helmuth, 2009), this mechanistic previously thought to be lethal and well above those found in understanding is applied to the river migration of an adult Pacific their present ecological niche (Franklin et al., 2007). Thus, salmon species. observing a stenothermal existence does not necessarily mean My focus on predominantly one group of fishes (the insufficient phenotypic plasticity to tolerate a broader salmonids) and on one environmental variable (temperature) is temperature range. for two reasons. First, this is where data are most abundant. Temperature and aerobic scope Second, a case study of temperature tolerance among fishes is likely to prove extremely fruitful in addressing the more general Temperature has a central role in shaping the distribution of and important question of animal resilience and adaptability to animals. In explaining latitudinal and longitudinal limits of biomes, environmental change. This is because fishes have evolved Shelford’s law of tolerances envisaged a centre of animal around species-specific niches, living in almost every abundance bounded by ‘toleration’ of environmental ‘controlling conceivable aquatic habitat and representing almost half of the factors’ (Fig. 1A). Clearly, the poleward shift in fish distributions earth’s vertebrate species. However, no single fish species with the progressive warming of aquatic habitats (Brander et al., tolerates the entire temperature range exploited by fishes (from 2003; Brander, 2007; Pörtner and Knust, 2007; Dulvy et al., 2008) THE JOURNAL OF EXPERIMENTAL BIOLOGY Toleration 3772 A. P. Farrell Farrell, 2008), illustrating an importance well beyond fishes. Even so, and as shown in the following, our understanding of the Controlling Controlling proximate causes that limit a fish’s aerobic scope beyond its factors factors optimal temperature range remains formative. Centre of abundance The Fry curve for aerobic scope Aerobic scope is derived from measurements of a fish’s minimum ) as a function of and maximum rates of oxygen uptake (V temperature (Fig.1B). The difference between these two rates is aerobic scope, which takes the form of a bell-shaped curve as a Latitude/longitude/temperature function of temperature – a ‘Fry curve’ for aerobic scope (Fig.1C). Simplistically, a Fry curve represents an animal’s capacity for activity as a function of temperature. (standard or basal metabolic rate) represents the 2.5 Minimum V Active metabolic cost to support an animal’s existence in a non-feeding, is directly non-reproducing and non-motile state. Minimum V 2.0 affected by body temperature [thermodynamics (Krogh, 1914)], typically doubling or tripling with a 10°C acute increase in effect; Fig.1B). Minimum V also temperature (termed a Q 10 O 1.5 varies among species (a genetic basis) and with body size [scaling (Schmidt-Nielsen, 1984)]. Standard 0.5 Clearly, life beyond short-term existence requires a capacity to above this minimum level. Energy expenditure for increase V feeding, growth, reproduction and locomotion (used for foraging as well as escape from predators and unfavourable environments) 1.5 . In terms of the temperature dependence of needs an active V , Fry (Fry, 1947; Fry and Hart, 1948) made the crucial active V of exercising goldfish (Carassius observation that maximum V 1.0 auratus) failed to continue increasing with temperature beyond an ). By contrast, standard V of resting fish optimal temperature (T opt O A Fry curve 0.5 continued its exponential increase until temperature approached a for aerobic scope is created by lethal level (Fig.1B). Thus, the T opt to continue increasing with the failure of maximum V temperature. Consequently, because activities such as growth 8 16 24 32 40 depend on aerobic scope, it is not surprisingly that growth rate as Acclimation temperature (°C) a function of temperature has a similar bell-shaped, species-specific Fig.1. The controlling and limiting effects of temperature on animal curve for fishes (Fig. 2B) (Brett, 1971). In fact, fish must eat more distributions, metabolic rate and scope for activity. (A)A schematic just to deal with the exponential increase in standard V . Like representation of Shelford’s law of tolerances (Shelford, 1931). , active V is also species-specific and varies with minimum V O O 2 2 (B)Measurements of standard and active metabolic rates for goldfish as a body size. function of temperature approaching their upper incipient lethal At a critical temperature (T ), aerobic scope is zero and aerobic crit temperature. (C)Aerobic scope (or scope for activity) as a function of activity becomes impossible. Thus, a thermal niche for existence in temperature, which is the difference between the measurements of values (which standard and active metabolic rates shown in B (Fry, 1947). a resting state is bounded by the upper and lower T crit and CT values determined using correspond closely to the CT max min other methods). However, existence without an aerobic scope is represents a more insidious manifestation of the anthropogenic- necessarily short-lived in nature because, besides being an easy driven change in animal distribution that Shelford characterised target for predators, starvation is just a matter of time. nearly 80 years ago (Shelford, 1931). Consequently, an animal’s functional thermal niche is narrower Temperature tolerance at the whole animal level was first given than that bounded by T crit a mechanistic explanation for fishes by Fry (Fry, 1947), who Fry curves are species specific. Differences result from their showed that temperature both controlled and limited their position on the temperature scale (temperature niches), being metabolic rate. To illustrate his ideas, he used scope for activity, centred near 27°C for goldfish and at cooler temperatures (<20°C) which is now termed aerobic or metabolic scope, i.e. the difference for most salmonids (Fig.2A). There are also species differences in . Athletic species such as salmonids have a between standard and active metabolic rates (Fig.1B,C). In doing standard and active V so, Fry recognized that the predictive value of knowing the high aerobic scope, but this does not necessarily translate into a temperature dependence of aerobic scope was considerably greater larger thermal niche. For example, generalists such as goldfish than that of knowing a temperature tolerance range (e.g. critical (Fig.2A) and Fundulus heteroclitus (Fangue et al., 2006) have a and CT ). Indeed, maximum and minimum temperatures; CT low aerobic scope and a broader thermal niche (eurythermal) max min the aerobic scope concept is now being used broadly to examine compared with salmonids. the impacts of the aquatic warming trends and other environmental Scaling up of laboratory-derived aerobic scope data to ecology climate changes on marine ectotherms (Pörtner, 2001; Pörtner, and biogeography will not necessarily be a simple task because 2002; Mark et al., 2002; Pörtner and Knust, 2007; Pörtner and other environmental factors reduce aerobic scope and narrow an THE JOURNAL OF EXPERIMENTAL BIOLOGY Toleration –1 –1 –1 –1 Aerobic scope (ml O kg min ) V (ml O kg min ) 2 O2 2 Animal abundance Ultimate upper incipient lethal temperature Salmon in hot water 3773 9.0 found to lose nearly 50% of their aerobic scope with only a 2°C Gates increase above the average summer temperature (Nilsson et al., sockeye 7.5 2009), and an increase of 3°C compromised growth of spiny- Weaver damselfish (Acanthochromis polyacanthus) (Munday et al., 2008). sockeye 6.0 However, the collapse of aerobic scope at warm temperatures was Chehallis Rainbow coho less evident (Fig.2A) for the bullhead (Ameiurus nebulasa) and trout 4.5 brown trout (Salmo trutta), suggesting that other factors may set thermal tolerance. Lake trout 3.0 Brook Brown bullhead trout The rise and fall of aerobic scope in salmonids 1.5 As temperature increases, exponentially more oxygen must be Brown trout Goldfish delivered to tissues, which is the task of the cardiorespiratory fails to increase beyond T , the system. Since maximum V O opt 010 20 30 40 2 (i.e. the downward trend of a decline in aerobic scope beyond T opt Fry curve) therefore reflects the inability of the maximum 0.08 cardiorespiratory capability to keep pace with these increasing corresponds with a failure Brook trout tissue oxygen demands. By contrast, T crit 0.06 of the resting cardiorespiratory capability to keep pace with increasing tissue oxygen demands. The resultant mismatch between oxygen supply and oxygen demand forces animals to progressively 0.04 switch to anaerobic metabolism to survive (Pörtner, 2001; Bull trout Frederich and Pörtner, 2000), perhaps causing an acceleration of 0.02 cardiorespiratory collapse (Farrell et al., 2008) and the rightward Allopatry skew often seen in Fry curves. At present, cardiorespiratory information pertaining to the collapse of aerobic scope during warming is most abundant for 0 5 10 15 20 25 30 salmonids. The data are examined below within the context of the Acclimation temperature (°C) cardiorespiratory oxygen cascade in order to explore why active does not increase beyond T and why minimum V collapses Fig.2. The influence of temperature on aerobic scope and growth rate. V O opt O 2 2 (A)Fry curves for a range of salmonids and other species (Fry, 1947; Fry, . at T crit 1948; Fry and Hart, 1948; Lee et al., 2003). (B)Growth rates of brook trout and bull trout grown either separately (solid lines with the accompanying Active V and the cardiorespiratory oxygen cascade dashed lines showing the 95% confidence limits) or together (long dashed The cardiorespiratory oxygen cascade conceptualizes the lines grouped by allopatry) (McMahon et al., 2007). movement of oxygen down its partial pressure gradient from a corresponds to the respiratory medium to tissues. Hence, V oxygen flux per unit time through this cascade and oxygen animal’s functional thermal niche (Fry, 1947; Fry, 1971; Brett, diffusion rates are proportional to the relevant oxygen partial 1971; Pörtner and Farrell, 2008; Munday et al., 2009). For example, pressure (P ) gradients. For fish, oxygen diffuses from water aquatic hypoxia, independent of temperature, can reduce aerobic across gill secondary lamellae and binds to haemoglobin (Hb) in scope (Graham, 1949; Gibson and Fry, 1954; Fry, 1971; Brett, red blood cells, which are transported by the circulatory system to 1971) to the extent that feeding and growth are halted, and tissues where oxygen diffuses across the capillary wall and into the development and reproduction are delayed (see Richards et al., cell to be used in mitochondrial respiration (Fig. 3). 2009). Therefore, both hypoxia and hypercapnia are likely to A countercurrent arrangement of blood and water flow at the constrain the breadth and height of a Fry curve (Pörtner and Farrell, secondary lamellae ensures that the arterial blood leaving the gills (Pa ) close to ambient water, and its Hb is almost fully 2008). Furthermore, the aerobic scope for a developing fish may has a P O O 2 2 ) is near not reach its full potential until the cardiorespiratory system is fully saturated, i.e. the oxygen content of arterial blood (Ca developed. Therefore, a family of Fry curves may exist for different maximal. Convection of oxygen to tissues by the arterial system is and cardiac output. Thus, life stages. Behaviour adds further complexity. For example, inter- quantified as the product of Ca for growth (Fig.2B), as seen specific competition can shift the T increasing cardiac output is the only means to internally transport opt in brook trout (Salvelinus fontinalis) when growth was suppressed more oxygen to the tissues, unless stored red blood cells are while competing with bull trout (Salvelinus confluentus), but not released from the spleen to increase Hb concentration [Hb] and (see Gallaugher and Farrell, 1998). Once in tissue vice versa (McMahon et al., 2007). hence Ca An important index that can be derived from a Fry curve is the capillaries, factors such as the architecture of the capillaries, the and T . thermal window, the temperature difference between T presence of myoglobin and lipid droplets in the cytoplasm and the opt crit This thermal window is an index of a species’ resilience to actual location of mitochondria within the cell significantly temperature change. In salmonids, the thermal window for the influence the rate of diffusion of oxygen from the red blood cell to collapse of aerobic scope with warming is just 6–7°C (Fry, 1947; the mitochondria. Farrell et al., 2008), which is a relatively small safety margin in the In a resting fish, increasing tissue oxygen delivery with context of global warming scenarios. Tropical species apparently increasing temperature could simply recruit mechanisms that are have narrow thermal windows too (Hoegh-Guldberg et al., 2007; normally used during exercise. When salmonids exercise at a . For example, Tewksbury et al., 2008) and live close to their T constant temperature, there are increases in gill ventilation (to crit cardinalfishes (Ostorhinchus doederleini and O. cyanosoma) were deliver more water), cardiac output (to transport more oxygen to THE JOURNAL OF EXPERIMENTAL BIOLOGY –1 –1 –1 Aerobic scope (ml O kg min ) Growth (g day ) 2 3774 A. P. Farrell (Clark et al., 2008a). In fact, Pa actually increased in resting Pa 2 (Steinhausen et al., 2008). sockeye salmon warm to T crit data during warming is more complex because Interpreting Ca Increase of potential pH and temperature effects on the Hb–oxygen affinity gill Gills Tissues curve, and because warming has variable effects on blood [Hb] ventilation Increase O (Taylor et al., 1997; Farrell, 1997; Sandblom and Axelsson, 2007). extraction was maintained in resting sockeye salmon warmed Even so, Ca by tissues O as well as in exercising sockeye salmon warmed above T 2 to T crit opt (Steinhausen et al., 2008). By contrast, Ca decreased at T in O crit Increase 2 cardiac output resting rainbow trout (O. mykiss) (Heath and Hughes, 1973) and in resting Chinook salmon (Clark et al., 2008a). The modest decrease Fig. 3. A schematic diagram representing the oxygen cascade for a fish , in the absence of an effect on Pa , in resting Chinook in Ca O O 2 2 during rest (shaded lines and arrows) and swimming (dark lines and salmon probably reflects a decrease in Hb–oxygen affinity rather arrows). The oxygen partial pressure is an arbitrary scale (see text for than a limitation on oxygen diffusion at the gills. details). A limitation in the circulatory system? If a circulatory limitation exists for exercising salmonids during the tissues) and tissue oxygen extraction from blood (Stevens et al., is warming, increases in cardiac output should cease once T opt 1967; Kiceniuk and Jones, 1977). Increased tissue oxygen reached. Indeed, maximum cardiac output in exercising sockeye as extraction can contribute almost as much to the increased V salmon (Brett, 1971; Steinhausen et al., 2008) and rainbow trout cardiac output because resting fish remove only about one third of (Taylor et al., 1996) reached a maximum value at a temperature ) and , as did V . Thus, ultimately as warming the arterial oxygen and so venous oxygen content (Cv well below T O crit O 2 2 (Pv ) can decrease considerably during exercise the potential to increase maximum cardiac output venous blood P approaches T O O opt 2 2 (Fig.3). While all of these exercise-induced cardiorespiratory (as revealed by exercising fish) fails to keep up with the required changes are possible during warming, as shown below, not all of increase in cardiac output in a resting fish (Fig. 4). As a result, them occur when resting fish are warmed up to T because scope for cardiac output does not increase above T crit opt (Fig. 5), swimming effort either declines or stops. When an exercising fish is warmed, it is more a matter of how is even more much the warming increases the rate and force of muscle For resting salmonids, the cardiac limitation at T crit contraction to enhance maximum cardiorespiratory capacity. In obvious. Cardiac arrhythmias and bradycardia often develop at T crit (Heath and Hughes, 1973; Clark et al., 2008a), although their addition, oxygen diffuses at a faster rate, potentially allowing a . Furthermore, the temperature sensitivity of the lower Pv physiological basis has not been studied. Thus, experimental Hb–oxygen binding curve (e.g. Clark et al., 2008a) is such that a evidence points unequivocally towards a cardiac limitation both at of fully saturated in exercising salmonids and at T in resting salmonids. Further rightward shift with warming increases the Pa T O opt crit arterial blood. This also promotes a faster unloading of oxygen at insight into the mechanistic basis of the cardiac response to could decrease during warming without a the tissues. In fact, Cv warming and its limitations comes from an analysis of heart rate (this direct temperature effect is in addition to a decrease in Pv (the rate function) and cardiac stroke volume (the capacity similar benefit from the Root- or Bohr-shifts as tissues release more function). carbon dioxide and H during exercise). The importance of increased heart rate during acute warming is Some fairly simple theoretical predictions can be made using this extremely clear. Warming increases cardiac output solely by conceptual framework, against which existing cardiorespiratory increasing heart rate. This is true for both resting and exercising data on warming in fishes can be compared. The analysis is further salmonids (Sandblom and Axelsson, 2007; Clark et al., 2008a; simplified by asking where the potential limitation might exist Steinhausen et al., 2008), presumably through a direct temperature (gills, circulatory system or tissues), and by focusing on underlying effect on the cardiac pacemaker rate (Randall, 1970). However, for resting fish and at T for exercising mechanisms (at near T because fish have a maximum heart rate (Farrell, 1991) and heart crit opt fish). rate is already elevated by the exercise, the maximum heart rate must be reached at a temperature well below that for resting fish Changes in cardiorespiratory variables with acute warming in (Steinhausen et al., 2008). In fact, the scope for heart rate plummets association with T in exercising salmonids and T in to zero near T (Fig.5). Fred Fry made from its maximum at T opt crit opt crit resting salmonids a similar observation for heart rate in Salvelinus fontinalis alevins A limitation at the gills? (Fig. 6A) (Fry, 1947) and commented that this might reflect the T opt Oxygen is poorly soluble in water. Compounding this, its solubility for the activity of an organ (i.e. the heart)! We now know that Fry’s for the maximum in water decreases ~2% per degree centigrade. Therefore, gill assertion was correct because the T opt ventilation must compensate for the decreased oxygen availability performance of isolated rainbow trout hearts is well below T crit (Fig.6B). and the lower Hb–oxygen affinity, as well as increased tissue oxygen demand as temperature increases. Therefore, a decrease in In contrast to heart rate, cardiac stroke volume appears to be Pa during warming would indicate a clear problem associated thermally insensitive to warming. This is true for resting and with gill oxygen delivery and transfer. However, the data for exercising salmonids (Sandblom and Axelsson, 2007; Clark et al., salmonids are inconsistent on this matter. 2008a; Steinhausen et al., 2008), but it is an especially surprising When exercising adult sockeye salmon (Oncorhynchus nerka) result for resting fish. In fact, it seems paradoxical, given that , Pa was were warmed to a temperature well above T cardiac stroke volume can triple during swimming at constant opt O maintained (Steinhausen et al., 2008). Similar results were found temperature (Stevens et al., 1967; Brett, 1971; Kiceniuk and Jones, in resting Chinook salmon (O. tshawytscha) warmed up to T 1977; Farrell and Jones, 1992; Thorarensen et al., 1996; Gallaugher crit THE JOURNAL OF EXPERIMENTAL BIOLOGY Tissue O extraction –1 (ml O ml blood ) Tissue O extraction –1 (ml O ml blood ) Salmon in hot water 3775 80 50 O2 Heart rate 0.05 15 17 19 21 23 0.10 Temperature (°C) 0.15 16 Fig.5. Changes in scope for oxygen uptake (V ), cardiac output (V ) and O b heart rate (f ) in swimming sockeye salmon during acute warming. Note that although all fish continued swimming in temperatures up to and including 19°C, some fish stopped swimming at higher temperatures and B so the data are only for those that continued to swim (Steinhausen et al., 2008). 40 filling pressure also increased (Sandblom and Axelsson, 2007). , venous However, with further warming to 16°C, which is near T opt blood pressure was unchanged and cardiac stroke volume decreased when heart rate increased further. Although a complete systolic emptying of the ventricle may be a disadvantage with 0 regard to the capacity to increase cardiac stroke volume during warming, it may be more important in ensuring a completely ‘fresh’ 0.05 supply of oxygen enters the lumen of the heart with each heart beat 0.10 20 given oxygen diffusion to the myocardium is driven by a low Pv 0.15 (see Farrell, 2002). The increase in cardiac stroke volume when salmonids swim at a constant temperature is supported by an increase in venous blood pressure (Kiceniuk and Jones, 1977) and by contraction of Fig.4. Cardiac output and tissue oxygen extraction (Ca –Cv ) for 12°C- O O 2 2 locomotory muscles aiding venous return (Farrell et al., 1988). acclimated sockeye salmon either (A) at rest, or (B) swimming continuously at about 70% of maximum swimming speed, while the temperature was There are several potential reasons why warming does not increase –1 acutely increased at 2°Ch and held at the temperature for 1h while cardiac stroke volume any further. There could be physical upper cardiorespiratory measurements were made. All resting fish completed the limits to venous return and end-diastolic volume. Also, increasing temperature challenge and recovered, but above 19°C swimming fish heart rate during warming reduces cardiac filling time and creates began to stop swimming and so progressively fewer are represented at a negative frequency effect on cardiac contraction, both of which higher temperatures. The x–y surface at each temperature represents could constrain cardiac stroke volume (Farrell, 2007). In addition, oxygen uptake (i.e. the product of cardiac output and tissue oxygen extraction), which clearly increases with temperature in resting but not at a time when the heart is working maximally, its extracellular swimming fish above their optimum temperature of around 15°C. Changes environment (the venous blood) becomes acidemic and in cardiac output with temperature are a result of increased heart rate (see (Steinhausen et al., 2008). hyperkalemic, and has a low Pv text) (Steinhausen et al., 2008). Although the negative inotropic effects of these extracellular changes were prevented by adrenergic stimulation of the heart (Driedzic and Gesser, 1994; Nielsen and Gesser, 2001; Hanson et et al., 2001), that this additional capacity for increasing cardiac al., 2006), this adrenergic protection was greatly reduced at 18°C stroke volume is not exploited by resting fish when they are compared with 10°C in rainbow trout (Hanson and Farrell, 2007). (Fig.4). So why is this? warmed to T crit A limitation at the tissues? The difficulty may revolve around the fact that cardiac end- The rate and degree of oxygen diffusion from capillaries to tissues systolic volume is essentially zero in salmonids (Franklin and gradient. These Davie, 1992). This means that, unless venous return and end- is influenced by several factors besides the P diastolic volume are increased first, an increase in cardiac include tissue capillary density, the intracellular mitochondrial contractility cannot increase cardiac stroke volume appreciably location, regional blood flow and red blood cell capillary contact (Sandblom and Axelsson, 2007). Furthermore, there are indications time. Taylor et al. (Taylor et al., 1997) suggested that regional that during warming inadequate venous return may limit cardiac oxygen delivery by convective transport in exercising rainbow trout stroke volume in the first instance. In resting rainbow trout warmed is determined mainly by changes in cardiac output as temperature from 10 to 13°C, cardiac stroke volume was maintained when heart changes, i.e. active peripheral redistribution of blood flow is rate increased because venous blood pressure and mean circulatory modest. Even so, red muscle blood flow during aerobic swimming THE JOURNAL OF EXPERIMENTAL BIOLOGY Temperature (°C) Temperature (°C) –5 –1 –1 Scope for: V (µmol 10 min kg ) –1 –1 –1 V (ml min kg ) Heart rate (min ) –1 –1 Cardiac output (ml min kg ) –1 –1 Cardiac output (ml min kg ) 3776 A. P. Farrell 120 was acidemia and Cv decreased (Clark et al., 2008a). When again remained exercising sockeye salmon were warmed, Pv Sockeye 2 temperature insensitive, albeit it at a lower level compared with resting fish (Steinhausen et al., 2008). This consistent temperature points to a diffusion limitation for oxygen insensitivity of Pv unloading (see Farrell, 2002; Farrell and Clutterham, 2003). Why to the level seen in resting fish warming does not decrease Pv with swimming at a constant temperature is unclear. just prior to T may In resting salmonids, the decrease in Cv O crit Brook trout reflect a desperate situation created by inadequate tissue perfusion. The ability of fish to recover from warming may be informative in this regard. For example, when sockeye salmon and Chinook were –1 and kept at a constant incrementally warmed at 2–4°Ch 0 5 10 15 20 temperature for 1h between temperature steps, the fish recovered Temperature (°C) well at the control temperature and within 1–2h, especially if the heat stress was terminated before cardiac arrhythmias developed (Steinhausen et al., 2008; Clark et al., 2008a). In these experiments, 10 and Chinook salmon decreased sockeye salmon maintained Cv only in association with acidemia at 24°C. By contrast, when Cv ‘opportunistic’ blood samples were taken from resting rainbow 7/7 14/14 –1 ), all but one fish died trout during continuous warming (1.5°Ch 11/13 9/15 and venous blood became depleted of oxygen (Heath and Hughes, 1973). 14/14 What emerges from the above is that the heart becomes a weak link for the cardiorespiratory oxygen cascade when exercising . Although a direct temperature salmonids are warmed above T opt effect on the cardiac pacemaker rate appears to be the predominant 0 5 10 15 20 25 mechanism for improving tissue oxygen transport, a crucial Acclimation temperature (°C) limitation is reached when this rate function reaches its maximum. Fig.6. (A)A comparison of heart rates measured in brook trout alevins (Fry, for exercising fish and at T for This apparently occurs at T opt crit 1947) and adult sockeye salmon (Steinhausen et al., 2008) to illustrate the resting fish. What follows during warming is a sequela of events: convergence of heart rate in resting (lower lines) and active (upper lines) a decrease in scope for heart rate preceding that for cardiac output, fish such that there is no scope for heart rate at T . (B)A composite of the crit which precedes that for aerobic scope (Fig.5). It is also evident that maximum cardiac performance for isolated perfused rainbow trout hearts during warming the contributions of several capacity functions acclimated to different temperature to illustrate that there is a peak performance around 15°C for the heart. Beyond this temperature, an ([Hb], tissue oxygen extraction and cardiac stroke volume) are only increasing number of preparations would fail as indicated by the ratio of small and variable. Why this excess capacity is not exploited when successful/attempted preparations besides each data point (Farrell et al., resting fish are warmed is particularly perplexing and warrants 1988; Keen and Farrell, 1994; Farrell et al., 1996). further study. Beyond salmon was lower at 18°C than at 11°C (Taylor et al., 1997). In addition, The details provided above for salmonids apparently apply more the basal oxygen requirement of white (fast glycolytic) muscle in broadly to other fishes. For example, warming of three species fish increases during warming because it accounts for >50% of showed that like rainbow trout: (1) cardiac output increases body mass and receives 28–50% of routine cardiac output in resting predominantly through increased heart rate, (2) routine heart rate that is species specific, and rainbow trout (Randall and Daxboeck, 1982; Bushnell et al., 1992). shows a plateau or collapse before T crit Indeed, the finding that blood flow to white muscle increased from (3) cardiac stroke volume is temperature insensitive (Fig.7) 40% to 75% of cardiac output at 6°C versus 18°C in resting rainbow (Sandblom and Axelsson, 2007 and references therein). In addition, trout (Barron et al., 1987) clearly reflects a significant elevation of the temperature dependence of Hb–oxygen affinity and the variable . White white muscle oxygen demand relative to whole animal V effects of warming on [Hb] are well known among fishes (Cech et muscle also has a low capillary density (Egginton, 2000), which al., 1976; Gallaugher and Farrell, 1998; Gollock et al., 2006), and increases the likelihood of a diffusion limitation developing for a direct temperature effect on the spontaneous pacemaker rate is oxygen diffusion. recognised for plaice (Pleuronectes platessa) (Harper et al., 1995). Further insight into potential limitations on tissue oxygen Furthermore, in resting Atlantic cod (Gadus morhua), although , heart rate removal during warming is evident from measurements of Cv heart rate and cardiac output both collapsed before CT O max and Pv . For example, Pv and Cv could not decrease if there (at 18°C versus at reached a plateau before cardiac output and V O O O O 2 2 2 2 was a diffusion limitation. In fact, a decrease in Cv is a very 20°C) (Gollock et al., 2006). important mechanism for increasing tissue oxygen extraction The effects of acute warming have been thoroughly studied in during swimming at constant temperature (Fig.4). However, for winter flounder (Pseudopleuronectes americanus) seasonally resting sockeye salmon, warming actually increased Pv and acclimated between 5°C and 18°C (Cech et al., 1975; Cech et al., Cv and tissue oxygen extraction (Fig.4) remained unchanged 1976). After a 5°C warming at each acclimation temperature, an O , was temperature (67–83% per 5°C increment) was always (Steinhausen et al., 2008). Similarly, Pv increase in V O O 2 2 insensitive in resting Chinook salmon, except at 25°C when there accompanied by a nearly equivalent increase heart rate (54–77% THE JOURNAL OF EXPERIMENTAL BIOLOGY Maximum myocardinal –1 –1 Heart rate (min ) power output (mW g ) Tissue O extraction –1 (ml O ml blood ) Tissue O extraction –1 (ml O ml blood ) Salmon in hot water 3777 75 80 Trout Wolfish Cod Flounder 0.01 0.02 0.03 0.75 0.01 0.02 0.50 10 0.03 0.25 0 5 10 15 20 25 30 Fig.8. Cardiac output (V ) and tissue oxygen extraction (Ca –Cv ) for b O O 2 2 Temperature (°C) winter flounder either (A) seasonally acclimated to a temperature, or (B) acutely warmed by 5°C increments from the acclimation temperature. The Fig.7. Changes in cardiorespiratory variables in resting fishes during acute x-y surface at each temperature represents oxygen uptake (the product of warming: a comparison of wolffish, winter flounder and Atlantic cod with V and Ca ), which clearly increases with temperature and either reaches b O rainbow trout. (Data kindly supplied by Dr Kurt Gamperl: wolffish – N. a plateau between acclimation temperatures of 15 and 18°C, or collapses Joaquim and A. K. Gamperl, unpublished; trout – A. K. Gamperl, with an acute increase to 23°C. The greatest contributor to increases in unpublished; Atlantic cod – L. H. Petersen and A. K. Gamperl, unpublished; V is almost always V , which is a result of increased heart rate (see text) O b flounder – P. C. Mendonca and A. K. Gamperl, unpublished.) (Cech et al., 1975; Cech et al., 1976). per 5°C increment). However, with warming from 18°C to a near- environmental factors on aerobic scope to be properly explored. lethal temperature, cardiac output and cardiac stroke volume Accompanying such fieldwork is the need to better understand the , Pa , collapsed even though heart rate increased (Fig. 8). Ca control of heart rate at high temperature and to determine if the O O 2 2 and Pv were all maintained, except for 5°C- and 18°C- Cv heart is operating at its maximum pacemaker rate. O O 2 2 acclimated fish when tissue oxygen extraction increased (Fig.8). Temperature and the river migration of sockeye salmon Heart rate may be a limiting factor during warming in decapod Beyond direct temperature reactions (i.e. acute effects occurring in crustaceans as well. Heart rate is reported to reach a plateau near in various crab species: the spider crab [Maja squinado T minutes to hours considered above), two other time scales can be crit (Frederich and Pörtner, 2000)], the rock crab [Cancer irroratus applied to temperature effects. Thermal adaptation spans (Frederich et al., 2009)] and the kelp crab [Taliepus dentatus generations and occurs at the population level through natural (Storch et al., 2009)]. Cardiac stroke volume was also temperature selection acting on individual variability. The study of heritable insensitive in the kelp crab. Therefore, the upper limit for heart rate factors related to thermal tolerance is in its infancy. Thermal may emerge as a valuable, yet simple predictor of T in active acclimation (or thermal compensation), however, occurs when an opt in resting animals. If this is the case, biotelemetry animals and T individual undertakes physiological and biochemical adjustments crit of heart rate could easily extend this work to field situations (Clark over days to weeks [or perhaps months for Antarctic fishes at near et al., 2008b; Clark et al., 2009), allowing the full interplay of freezing temperatures (Franklin et al., 2007)]. Here, a new THE JOURNAL OF EXPERIMENTAL BIOLOGY Temperature (°C) Temperature (°C) –1 –1 –1 –1 Stroke volume (ml kg ) Heart rate (min ) Cardiac output (ml min kg ) Cardiac output Cardiac output –1 –1 –1 –1 (ml min kg ) (ml min kg ) 3778 A. P. Farrell phenotype emerges from an existing genome as an animal to river temperature above T . In fact, migration success was only opt (at 18–21°C), but acclimates to a new thermal environment. Given the potential for 0–11% when river temperature was near T crit thermal acclimation and adaptation, the obvious question becomes: increased to 77% when the river seasonally cooled to 14°C and near (Farrell et al., 2008). This result suggests that a warm river Do the acute responses to temperature in fishes have any ecological their T opt or evolutionary relevance? In the specific case of adult sockeye temperature limited aerobic scope, and impaired upriver migration salmon that return to the Fraser River, BC, Canada to spawn, the and lifetime fecundity. These warm river temperatures experienced answer is categorically yes. During this return migration, sockeye by Weaver Creek sockeye salmon in 2004, which turned out to be salmon can experience large and rapid temperature changes when record highs, contributed to a catastrophic 70% loss of the they make daily vertical ocean movements prior to river entry and migrating population! exploit deeper, cool water in lakes (Fig. 9). Thermal acclimation Adult sockeye salmon return migrations also provide a Warm acclimation alters thermal tolerance (Fry et al., 1942), fascinating insight into something that is normally difficult to and T . The linkage , T and maximum aerobic scope (Fry and Hart, witness, an ecological significance for T increasing T opt crit opt crit between aerobic scope and lifetime fecundity is obvious for 1948). Warm acclimation, in addition to permitting a higher sockeye salmon because their entire lifetime fitness hinges on a maximum heart rate, also decreases routine heart rate at the level single, precise spawning date that is preceded by an energetic of the pacemaker. This acclimatory change then provides upstream migration lasting up to several weeks. Therefore, to compensation for the limitation that maximum heart rate imposes spawn, they are committed to an upriver migration that periodically on aerobic scope by restoring the scope for heart rate either fully may require their full aerobic scope, with only a sensory imprint (Harper et al., 1995) or partially (Farrell, 1997). However, the for navigation, while developing gonads, without feeding and benefits of temperature acclimation for specialists like salmon are without prior experience of the temperature conditions en route small compared with temperature generalist. For example, CT max for salmon increases by only 2°C over a 15°C acclimation (Hinch et al., 2006). Consequently, if a warm river temperature of 10°C for goldfish reduces aerobic scope, sockeye salmon do not have an option of temperature range versus an increase in CT max postponing reproduction as other fishes might do. In fact, with just over a 30°C acclimation range (Brett, 1956). In fact, routine and 4–6 weeks to live after entering the river, even a slower migration maximum heart rate in 22°C-acclimated sockeye salmon –1 –1 and 106beatsmin , respectively (Brett, 1971)] are could reduce lifetime fecundity. [86beatsmin Using Weaver Creek sockeye salmon as an example and barely different for a 14°C-acclimated fish acutely warmed to 22°C –1 –1 and 106beatsmin (Steinhausen et al., 2008)]. considering only aerobic swimming, upstream migration should be [90beatsmin for aerobic scope) but impossible at favoured at 14.3°C (their T Other documented responses to warm acclimation, such as the opt ) (Lee et al., 2003). As predicted, when adult 20.4°C (their T decrease in cardiac mass (Gamperl and Farrell, 2004) and decrease crit Weaver Creek sockeye salmon were intercepted in 2004, implanted in capillary density the red (slow aerobic) muscle of rainbow trout with biotelemetry devices and released back to the river to follow (Taylor et al., 1996; Egginton, 2000), even seem counterproductive. their subsequent progress, migration success was inversely related Conversely, compensatory decreases in gill epithelial thickness, as seen for other species (Taylor et al., 1997), would be beneficial. Antecedents and concluding remarks Adams River sockeye thermal experience 2006 20 Like a salmon down on the Fraser, swimmin’ with their Shuswap battered fins, Lake Searchin’ for their childhood home, A patch of gravel they knew as their own. Excerpt from ‘The Ballad of Old Tom Jones’ by Barney Bentall The genomic information passed down by antecedents determines an individual’s potential for survival, growth and reproduction. The 11 antecedents of present day Fraser River salmon have passed on their environmental experiences through natural selection for over Lower ~10,000 years since their post-glacial invasion. However, we have Fraser River only ~60 years of reliable archival records of the river temperatures Georgia Strait experienced during recent salmon migrations (Farrell et al., 2008). Nevertheless, remarkably the historic mean and median river migration temperature for Weaver Creek sockeye salmon is 14.5°C 21-Aug 31-Aug 10-Sep 20-Sep 30-Sep 10-Oct 20-Oct is 14.3°C). This observation, combined with the fact that (their T opt and T is only 7.3°C and that the thermal window between T opt crit Fig.9. Hourly temperature recordings from an I-button temperature logger , suggests that thermal acclimation provides little benefit to CT max that was recovered from an Adams River sockeye salmon after is potentially a product of natural selection. If this is the their T implantation in the peritoneal cavity in the Georgia Strait (ocean conditions) opt and a 40-day migration through the Fraser River watershed to its spawning case, one has to question whether or not natural selection among area near the Shuswap Lake, BC, Canada. The highlighted areas sockeye salmon can accommodate the rapid warming trend already represent periods where the fish behaviourally sought out water that was evident for the Fraser River (peak summer temperature has cooler than either the mainstem river or at the surface of lakes. The increased 1.8°C in the past 60 years). general downward trend over time represents seasonal cooling of the If the salmonid genome is too inflexible to adapt to a new T opt watershed, and daily oscillations in temperature can be resolved in the perhaps the genetic determinants of the spawning date are more shallow spawning streams towards the end of the trace. (Data kindly supplied by David Patterson.) flexible. Dangerously high temperatures could then be avoided by THE JOURNAL OF EXPERIMENTAL BIOLOGY Internal hourly temperature (°C) Salmon in hot water 3779 migrating when the river is seasonally cooler (see Keefer et al., Brander, K. M., Blom, G., Borges, M. F., Erzini, K., Hendersen, G., MacKenzie, B. R., Mendes, H., Ribeiro, J., Santos, A. M. P. and Toresen, R. (2003). Changes in 2008), but this may result in a fish encountering other unfavourable fish distribution in the eastern North Atlantic: are we seeing a coherent response to conditions such as faster river flows earlier in the year and an changing temperature. ICES Mar. Sci. Symp. 219, 262-270. Brett, J. R. (1956). Some principles in the thermal requirements of fishes. Q. Rev. inevitable run-on-effect on the timing of larval emergence. Biol. 31, 75-87. Alternatively, warm water could be avoided behaviourally if Brett, J. R. (1971). Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon opportunities exist. Behavioural temperature preferences are (Oncorhynchus nerka). Amer. Zool. 11, 99-113. certainly shown by adult salmon during migration, which include Bushnell, P. G., Jones, D. R. and Farrell, A. P. (1992). The arterial system. In Fish Physiology Vol. 12A (ed. W. S. Hoar, D. J. Randall and A. P. Farrell), pp. 89-139. seeking water cooler than their T (Fig.9) to lower V and opt O San Diego: Academic Press. perhaps slow energy depletion, suggest they likely know which Cech, J. J., Jr, Bridges, D. W. and Levigne, J. R. (1975). Cardiovascular responses of the winter flounder, Pseudopleuronectes americanus, to near-lethal temperatures. temperature conditions are best for them. However, opportunities In Respiration of Marine Organisms (ed. J. J. Cech, Jr, D. W. Bridges and D. B. to seek cool refuges are very limited in the Fraser River (Donaldson Horton) pp. 155-162. Proc. Marine Section, First Maine Biomedical Science Symp., Mar. 14-16, 1975. Augusta. The Research Inst. Gulf of Maine (TRIGOM) Publ.: et al., 2009). Without such behavioural responses, the warmer than South Portland. normal river temperatures may force Pacific salmon near the Cech, J. J., Jr, Bridges, D. W., Rowell, D. M. and Balzer, P. J. (1976). Cardiovascular responses of winter flounder, Pseudopleuronectes americanus southern limit of their geographic distribution to follow the fate of (Walbaum), to acute temperature increase. Can. J. Zool. 25, 1383-1388. other species, a heart-breaking (Wang and Overgaard, 2006) Chown, S. L., Jumbam, K. R., Sørensen, J. G. and Terblanche, J. S. (2009). Phenotypic variance, plasticity and heritability estimates of critical thermal limits northward shift in their distribution. The response of tropical coral depend on methodological context. Funct. Ecol. 23, 133-140. reef fish species to climate change could be equally dramatic. Clark, T. D., Sandblom, E., Cox, G. K., Hinch, S. G. and Farrell, A. P. (2008a). In closing, the best, albeit limited data set for a single animal Circulatory limits to oxygen supply during an acute temperature increase in the Chinook salmon (Oncorhynchus tshawytscha) Amer. J. Physiol. 295, R1631-R1639. group appears to provide a mechanistic understanding for the Fry Clark, T. D., Taylor, B. D., Seymour, R. S., Ellis, D., Buchanan, J., Fitzgibbon, Q. curve. Heart rate, which is the main driver for the increase in V P. and Frappell, P. B. (2008b). Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna. Proc. R. Soc. B 275, 2841- during warming, reaches its maximum rate at T and becomes a opt weak link for the cardiorespiratory oxygen cascade. Shelford Clark, T. D., Hinch, S. G., Taylor, B. D., Frappell, P. B. and Farrell, A. P. (2009). Sex differences in circulatory oxygen transport parameters of sockeye salmon (Shelford, 1931) recognized that ‘Animals are better short-period (Oncorhynchus nerka) on the spawning ground. J. Comp. Physiol. B, 179, 663-671. indicators (of environmental change) than plants’ because animals Donaldson, M. R., Cooke, S. J., Patterson, D. A., Hinch, S. G., Robichaud, D., Hanson, K. C., Olsson, I., Crossin, G. T., English, K. K. and Farrell, A. P. (2009). can potentially move away from unfavourable environments. Limited behavioural thermoregulation by upriver-migrating sockeye salmon However, this behavioural response requires an aerobic scope, (Oncorhynchus nerka) in the lower Fraser River, British Columbia. Can. J. Zool. 87, 480-490. which is both controlled and limited by temperature. Future study Driedzic, W. R. and Gesser, H. (1994). Energy metabolism and contractility in on aerobic scope will continue to inform us of an animal’s ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature. Physiol. Rev. 74, 221-258. fundamental thermal niche. By contrast, a continued focus on Dulvy, N. K., Rogers, S. I., Jennings, S., Stelzenmuller, V., Dye, S. R. and temperature tolerances for resting animals will only inform us of Skjoldal, H. R. (2008). Climate change and deepening of the North Sea fish thermal niche for existence and perhaps create needless worry assemblage: a biotic indicator of warming seas. J. Appl. Ecol. 45, 1029-1039. Egginton, S. (2000). The influence of environmental temperature on microvascular about the precise techniques for such measurements (Chown et al., development in fish. Zoology 102, 164-172. 2009). Fangue, N. A., Hofmeister, M. and Schulte, P. M. (2006). Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J. Exp. Biol. 209, 2859-2872. The Natural Sciences and Engineering Research Council, Canada funds my Farrell, A. P. (1991). From hagfish to tuna: a perspective on cardiac function in fish. research. I am grateful for the expert assistance with artwork provided by Linda Physiol. Zool. 64, 1137-1164. Hanson, Steve Tang and Dustin Farrell, and for the improvements to the Farrell, A. P. (1997). Effects of temperature on cardiovascular performance. In Global manuscript provided by Dr Tim Clark, Dr Gina Galli and Ms Erika Eliason. Original Warming Implications for Freshwater and Marine Fish (ed. C. M. Wood and D. G. material is cited where appropriate because I deeply appreciate my scientific McDonald), pp. 135-158. Cambridge: Cambridge University Press. antecedents, who laid the conceptual groundwork, developed techniques and Farrell, A. P. (2002). Cardiorespiratory performance in salmonids during exercise at provided the stimulating intellectual environment that ultimately benefited my high temperature: insights into cardiovascular design limitations in fishes. Comp. Biochem. Physiol. 132, 797-810. research and scientific thinking. Dr David Randall is singled out in this regard. Farrell, A. P. (2007). Tribute to P. L. Lutz: a message from the heart – why hypoxic Parts of this article were presented for the Fry Medal Award Lecture at the bradycardia in fishes? J. Exp. 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Published: Dec 1, 2009

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