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BEHAVIORAL RESPONSES TO THE ENVIRONMENT | Temperature Preference: Behavioral Responses to Temperature in Fishes
Temperature Preference: Behavioral Responses to Temperature in Fishes LI Crawshaw and JE Podrabsky, Portland State University, Portland, OR, USA ª 2011 Elsevier Inc. All rights reserved.
Introduction Species Preferences
Glossary Behavioral thermoregulation Regulation of body temperature by utilizing behavioral movements to control body temperature. It is potentially utilized by all fish. Final thermal preferendum The temperature preference obtained when a species remains in a temperature gradient long enough that a stable preferred temperature is observed. Physiological (or autonomic) thermoregulation Utilization of autonomic responses to control body temperature; utilized in rare cases by fish.
Introduction Temperature can be considered a master factor for fish as it affects all physiological processes and ecological systems. Thermal extremes can prove detrimental or even lethal (see also Temperature: Measures of Thermal Tolerance). Within the range of temperatures that a fish normally encounters, temperature directly speeds up and slows down biochemical reactions (see also Temperature: Effects of Temperature: An Introduction), thus impacting all aspects of a fish’s behavior and physiology. While all motile animals have evolved behaviors that deal with the thermal variation present in their environ ment, fish and other vertebrates possess a particularly sophisticated system to maintain body temperature within narrow limits. The properties of this regulatory system are very similar to those found in other verte brates, although in fish such responses are largely limited to behavioral adjustments and, with only a few exceptions (see also Pelagic Fishes: Endothermy in Tunas, Billfishes, and Sharks), body temperature quickly equili brates to within a few tenths of a � C ambient water temperature. When a range of temperatures is available, fish are able to maintain body temperature at or near the preferred level by positioning themselves in water of that temperature, that is, behavioral temperature regulation. However, despite the power and sophistication of the nervous elements involved with behavioral temperature regulation, a particular species of fish at a given time is
758
Environmental Observations Further Reading
Temperature preference The temperature that a particular species selects, under a particular set of conditions, in a situation where a range of temperatures are available. Thermal acclimation The responses of a fish to maintain in a particular thermal regimen in the laboratory under a specified set of conditions. Thermal acclimatization Organismal adjustments to temperature that occur in nature, and are thus affected by other factors such as season and day length.
not always found at their preferred temperature. During some seasons, the preferred temperature is simply not part of the prevailing environment, while at other times predator avoidance, food acquisition, territorial defense, mating requirements, and gradients of light, oxygen, or salinity may displace a fish from its normally preferred temperature. Nevertheless, temperature is a predominant factor in determining habitat selection by fish, and is a major influ ence on their daily and seasonal movements (see also The Pituitary: Development of the Hypothalamus-PituitaryInterrenal Axis) as well as in their overall distribution and their physiological and biochemical capabilities (see also Design and Physiology of the Heart: Physiology of Cardiac Pumping and Temperature: Membranes and Temperature: Homeoviscous Adaptation). Examples of these effects can be seen in the behavior of the chimaera (Hydrolagus colliei) and the Atlantic mackerel (Scomber scombrus). In its southerly extremes, the chimaera is a deep-water fish, usually being found at depths that exceed 90 m. However, in the cold North Pacific, the chimaera is typically found in shallow water. In both the southern and northern environments, this species is found at the same temperature. Thus, the temperature preference of this spe cies may explain its depth distribution. In contrast to the chimaera, the Atlantic mackerel is a rapidly moving fish and can quickly shift its location in order to maintain a particular body temperature. For the Atlantic mackerel, a 1 � C increase in ocean temperature causes the fish to swim north about 110 km to maintain its preferred temperature.
Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses
Species Preferences
759
fish, and is one of many responses that serve to maintain a species within its recognized habitat.
The preferred temperature can vary under different states, and for each species, the conditions under which the pre ferred temperature is determined should be specified. Thermal preference can be most clearly demonstrated in laboratory temperature gradient or choice devices, which provide fish with the ability to choose specific temperatures from a broad range of available temperatures. If nonthermal influences are minimized, and unstressed fish are placed in a thermal gradient, results similar to those shown in Figure 1 are typically obtained. In Table 1, the temperature prefer ences of various species of fish are shown. The thermal preference is seen to relate to the general habitat of the
Small Alterations in the Preferred Temperature In addition to examples of the preferred temperature for various species, Table 1 also illustrates some of the con ditions where the preferred temperature may be altered within a species. These shifts in preferred temperature are typically on the order of 2 or 3 � C, and are often made by a given species in order to better utilize available tempera tures under different conditions. Such effects include time of day (see also Sensory Systems, Perception, and Learning: Circadian Rhythms in Fish), season, sex, repro ductive stage, presence of a bacterial infection (fever), nutritional status, and geographical location of a subspecies. The degree and presence of such shifts in preferred tem perature are specific to each fish species.
0.20
Frequency
0.15
Major Alterations in the Preferred Temperature 0.10
In certain cases, there can be major alterations in the pre ferred temperature within a species. One case involves developmental state. Typically, younger animals prefer warmer temperatures, which can be considerably higher than the adult preferences. Thus, young salmonids often select temperatures in the upper teens, whereas larger adults typically exhibit temperature preferences in the lower teens. Larger individuals may also exhibit a lower tolerance to high temperatures than juveniles. These differ ences likely reflect both environmental and physiological differences between the developmental stages. Smaller fish can avoid predation more effectively in shallow, covered areas and are also more likely to find appropriate nourish ment in these areas. Higher temperatures, up to a point, can
0.05 0.00 16 18 20 22 24 26 28 30 32 34 36 38 40 Temperature (°C) Figure 1 Fish prefer a narrow range of temperatures when presented with a continuous gradient of temperature options. This figure represents the frequency of temperatures selected by seven female Austrofundulus limnaeus over a period of 24 h in a linear thermal gradient ranging from 12 to 42 � C. The data are calculated from 10 321 one-min averages calculated from data collected every 6 s. Fish were acclimated to a cycling temperature regime ranging from 20–37 � C daily with a photoperiod of 14L:10D for several weeks prior to determination of temperature preference.
Table 1 The laboratory temperature preference of a variety of fish species
Common name
Species
Laboratory temperature preference (� C)
Conditions
Desert pupfish
Cyprinodon macularius
38–40
Summer
Common killifish
Fundulus heteroclitus
28–30 24–26
Northern population Southern population
Common goldfish
Carassius auratus
28–30 24–25
Small Adult
Large mouth bass
Micropterus salmoides
27–29
Adult
Rainbow trout
Oncorhynchus mykiss
21–22 17–18 13–17
Fed fingerlings Starved fingerlings Adults
Coho salmon
Oncorhynchus kisutch
11–12
Adult
Polar cod
Boreogadus saida
2–3 4–5
Early morning Afternoon – early evening
From Richards FP, Reynolds WW, and McCauley RW (1977) Temperature preference studies in environmental impact assessments: An overview with procedural recommendations. Journal of the Fisheries Research Board of Canada 34: 728–761.
760 Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses
is decreased further, to 10 torr (1.3 kPa), the preferred temperature drops by about 10 � C. While this low tem perature is stressful, it enables the fish to survive by increasing the affinity of hemoglobin for oxygen (see also Transport and Exchange of Respiratory Gases in the Blood: Hemoglobin), augmenting gill extraction efficiency, and by reducing the metabolic demands for maintaining minimal function.
Accuracy and Constancy of the Preferred Temperature Given the general ability of fishes to adapt to a broad range of temperatures (just below 0 � C to just above 40 � C), the stability of their preferred temperature, as seen in Figure 1, is somewhat enigmatic. A closer look at several factors may elucidate the reason for such per sistent maintenance of a particular temperature. First, as mentioned earlier, adjustments to a new tem perature take both time and energy. When a fish moves to water of a different temperature, all aspects of its physio logical and behavioral capabilities are somewhat compromised. The rapidity with which a change in ambi ent water temperature affects overall body temperature is often underestimated. Typically, body temperature is measured at a deep site and the temperature at that site is found to change relatively slowly, even if a fish quickly moves to water of a radically different temperature. The net thermal effect on a fish is better estimated by evaluat ing the change in mean body temperature, which can be done by placing a fish in a calorimeter containing water of a different temperature. The results of such a maneuver for a 0.56 kg carp (Cyprinus carpio) are seen in Figure 2. While 50% of the change in mean body temperature occurs within 1 min, 50% of the change in brain and deep dorsal muscle temperature requires 4 and 5 min, respectively. The magnitude and rapidity of heat transfer T mean body T brain T dorsal muscle Heat loss rate
25 24 23 22 21 20 19 18 17 16 15
800 700 600 500 400 300 200 100
−1 Heat loss rate, watts (J s )
Temperature (°C)
also support faster growth. Larger fish, on the other hand, are more vulnerable to predation in shallow, warm areas. A second case involves adjustment to extreme tem peratures. While fish can adjust body processes to operate effectively over a range of different environmental temperatures (see also Temperature: Membranes and Temperature: Homeoviscous Adaptation), this process takes time and varies for different species, with indivi duals from areas of high thermal variability showing greater capabilities for such thermal acclimatization. With acclimatization to extreme temperatures, metabolic and other physiological processes are greatly altered, and the normally preferred temperature can become harmful or lethal. Not surprisingly, thermal acclimatization alters the preferred temperature, and to a greater degree for temperatures farther from the normally preferred tem perature. Thus, the brown bullhead (Ictalurus nebulosus), which normally prefer water temperatures of about 30 � C, prefer a temperature of 16 � C after being maintained in the laboratory at 7 � C for several weeks. When left undis turbed in a temperature gradient, the preferred temperature gradually increases, and returns to 30 � C in about 1 day. The thermal preference that fish finally stabilize at after a long period in a thermal gradient is termed the ‘final thermal preferendum’. A third case involves survival under physiological stress. Many species of fish have the ability to survive severe hypoxia (see also Hypoxia: The Expanding Hypoxic Environment) by selecting very cold tempera tures. While broad variations in levels of dissolved oxygen in the water normally do not affect the temperature pre ference, when oxygen levels fall to near-lethal levels, thermal preference decreases drastically. Adult goldfish, for example, normally prefer 25 � C. If the oxygen partial pressure is lowered from a normal saturated value of 160 torr (21.3 kPa) to 31 torr (4.1 kPa), there is little change in the preferred temperature. However, if the oxygen level
0 0
2
4
6
8 10 12 14 16 18 20 Time (min)
Figure 2 Changes in temperature and heat loss rates in a 0.56-kg carp transferred from 25 � C into a calorimeter at 15 � C. About half of the heat loss occurs within the first minute after transfer. Temperatures asymptote above 15 � C due to an increase in calorimeter temperature. Adapted with permission from Figure 2 in Crawshaw LI (1976) Effect of rapid temperature change on mean body temperature and gill ventilation in carp. American Journal of Physiology 231: 837–841.
Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses
are emphasized by the heat loss rate illustrated in Figure 2. Note that the metabolic heat produced by the carp in this situation would be less than 1 W. For such a carp, when equilibrium is finally reached, about half of the heat exchange occurs at the body surface and about half is due to conductance across the gill surface. The thermal exchange times exhibited for this 0.56-kg carp would be faster for smaller fish and slower for larger fish due to the differences in surface-area-to volume ratios (see also Temperature: Effects of Temperature: An Introduction). Another reason for the persistent selection of a parti cular temperature relates to the overall optimization of organismal function. While most fish can make adjust ments to function well over a range of temperatures, there is a much narrower temperature range that, after thermal acclimatization, provides an optimal behavioral and phy siological set of responses for functioning in the fish’s particular habitat. Such responses include optimization of growth (see also Energy Utilization in Growth: Growth: Environmental Effects), metabolic scope, cardiac scope, power output of aerobic muscles, and overall per formance. In the cases investigated, the preferred temperature fell within the narrow range of temperatures for overall optimal function. Characteristics of the Thermoregulatory System The regulatory system which is utilized by fish to main tain a particular body temperature is anatomically and functionally similar in Chondrichthyes and Osteichthyes, and is closely related to the system utilized by other (a) Chondrichthyes
vertebrates (see Figure 3 and Brain and Nervous System: Autonomic Nervous System of Fishes). To func tion correctly, a thermoregulatory system must sense the controlled variable, make a comparison with an ideal value, and determine an appropriate behavioral response. In fish and other vertebrates, temperature sensing occurs both peripherally and centrally. Sensitivity occurs over the entire fish surface, and is likely subserved by highly responsive, rate-sensitive, free nerve endings. In condi tioning experiments, fish have proved capable of responding to a surface temperature change of less than 0.05 � C. While, in most conditions, fish would probably not respond to such small temperature differences, they clearly have a capability for detecting extremely small thermal variation. This capability is undoubtedly useful for specific situations that could involve locating critical thermal refuges or guiding large-scale migrations. An important area for central thermal sensing and processing occurs in the anterior brainstem regions in vertebrates, as shown in Figure 3. In fish, an area of particular impor tance is the nucleus preopticus periventricularis. Lesions within the anterior brainstem area destroy thermoregula tory behavior in fish, and heating and cooling this area (including adjacent tissue) leads to the selection of cooler and warmer water, respectively.
Environmental Observations Field observations that relate fish location (and some times actual body temperature) to local water temperature are particularly valuable. Such data clarify
(c) Osteichthyes
ON
(e) Mammalia
ON
ON (b) Osteichthyes
761
(d) Osteichthyes
OC
(f) Mammalia
OC AC ON
AC NPP
PO
OC
Figure 3 Similar anatomical locations are responsible for body temperature regulation in various groups of vertebrates. Ventral brain surfaces are represented in (a), (b), and (e). Shaded areas represent surfaces that overlie interior regions of the brain that are critical for thermoregulatory control and integration. (c) A side view of the brain with a line depicting the plane of the cross section depicted in (d). A cross section of the shaded region of (e) is depicted in (f). Major thermoregulatory effects are induced by the application of bioactive compounds to the shaded areas of the cross sections in (d) and (f). AC, anterior commissure; OC, optic chiasma; ON, optic nerve; NPP, nucleus preopticus periventricularis; PO, preoptic nucleus. Adapted from Fig. 1 in Crawshaw LI and O’Connor CS (1997) Behavioral compensation for long-term thermal change. In: Wood CM and McDonald DG (eds.) Society for Experimental Biology Seminar Series 61: Global Warming: Implications for Freshwater and Marine Fish, pp. 351–376. Cambridge: Cambridge University Press.
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the operation of temperature selection in a natural environment, illustrate its use in the maintenance of an optimal body temperature, and show how fish avoid deleterious environmental temperatures in a local envir onment and during migrations. The value and limitations of temperature selection for fish attempting to survive during an era of global climate change will also be touched upon.
(a) Moose River
24 24
Avoidance of Dangerous Temperatures While the lethal limit for brook trout (Salvelinus fontina lis) is just below 25 � C, they prefer to remain in temperatures below 17 � C. In spite of this, during the summer period of low flow and warm water, brook trout are often found in habitats where mainstream tempera tures exceed lethal limits. Figure 4 illustrates an example of how brook trout are able to survive such dangerously warm conditions. In this instance, the trout congregated near the confluence of the main river and a much cooler tributary. Although their ther mal preference is considerably lower than the area of the river they occupied, they likely avoided moving into even cooler areas nearer the tributary due to the dangers of predation involved with occupying very shallow water. The location of these fish indicates a compromise between the preferred temperature and a combination of water depth plus river surface characteristics. Over the course of the summer, the brook trout maintained a body temperature of about 3 � C lower than that of the main river temperature. In addition to utilizing confluences with cooler streams, fish in overly warm rivers have also been observed to make use of cold groundwater dis charges and thermally stratified deep pools to avoid thermally induced injury or death. Similar examples exist for migrating Pacific salmon (Oncorhynchus sp.) that, during their migration through large rivers, can take advantage of cooler water from tributaries and sometimes lakes. However, in this case, this preference behavior can only act as a temporary respite because the river migration must be completed in relatively short order (see also Fish Migrations: Pacific Salmon Migration: Completing the Cycle). Fish utilize similar strategies in reservoirs and lakes. Figure 5 depicts the body temperature of striped bass (Morone saxatilis) that were introduced into a reservoir in the southeastern USA. This area has warmer tem peratures than those present in the normal habitat of this species. The larger adults prefer to remain at temperatures below 22 � C, but this becomes very diffi cult during the months of summer. The cooler, lower depths become progressively deoxygenated, while the surface waters become untenably warm. Nevertheless, as seen in Figure 5, the large adults were usually able to maintain body temperatures and (presumably)
22 20 18 17.9
Bottom temperature (°C)
Combs creek
(b) Moose River
100 100 80 60 40
Depth (cm) Combs creek N 0
5
15 m
Figure 4 Aggregation of brook trout (shaded areas) depicted in relationship to surface water temperature (a) and depth (b) in the Moose River at the confluence with the cooler Combs Creek. Adapted from Fig. 5 in Baird OE and Krueger CC (2003) Behavioral thermoregulation of brook and rainbow trout: Comparison of summer habitat use in an Adirondack river, New York. Transactions of the American Fisheries Society 132: 1194–1206.
dissolved oxygen within acceptable levels by utilizing discrete areas near cold groundwater discharge or cool tributary entrances.
Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses 32 30 28
Temperature (°C)
26 24 22 20 18 16 14 12 10 Selected temperature Surface temperature Bottom temperature
8 6 4 A
M J
J
A
S
O N
D
J
F
M
Month Figure 5 Temperatures selected by free-living striped bass (open circles) in Lake Seminole for a 1-year period starting in March/April of 1984. Surface and bottom water temperatures are plotted to indicate that the fish utilize a unique subset of their thermal habitat for large portions of the year. Redrawn from Fig. 3 in van den Avyle MJ and Evans JW (1990) Temperature selection by striped bass in a Gulf of Mexico coastal river system. North American Journal of Fisheries Management 10: 58–66.
Global Climate Change, Environmental Degradation, and Temperature Preference Although the above strategies will, to some extent, ameliorate gradual increases in ambient water tempera ture due to climate change (see also Temperature: Effects of Climate Change) and other anthropomorphic effects (see also Behavioral Responses to the Environment: Anthropogenic Influences on Fish Behavior), disadvantages also accrue. In scenarios where preferred temperatures become limiting in a fish’s natural environment, the usable habitat may also become restricted due to behavioral limitations. For example, fish may be forced to occupy small tributaries with cooler temperatures and be excluded from using or migrating through large mainstem rivers where tem peratures can reach lethal heights or at least be many degrees above the fish’s preferred temperature. As large numbers of fish are forced to aggregate into small areas, crowding can increase stress, parasitism, disease, as well as decrease food availability and perhaps the oxygen contained in the water. For species which are linked to a particular geographic area, environmental warming brings added hazards. Migratory salmonids are a prime example, since nonthermal (largely olfactory) factors provide the primary cues that tie them to their natal streams. Adult salmon require relatively low body temperatures during
763
migration to maintain energetic stores necessary for the arduous events required for swimming upstream and spawning. In many cases, migrants have already become dependent upon judicious behavioral thermoregulatory strategies in order to survive. Chum salmon (Oncorhynchus keta), migrating along the coast in Japan, encounter high surface temperatures in early fall as they search for their spawning grounds. When the surface waters are warm, they achieve a compromise by mainly remaining in cool, deep water, but with occa sional movements to the surface, presumably to obtain directional cues. Later in the year when the surface water is cooler, these migrating salmon spend most of the time in shallow water. There are also examples of sockeye salmon (Oncorhynchus nerka) being unable to complete their spawning migration because the river water tem perature was simply too hot for them to swim. Upstream migrating Chinook salmon (Oncorhynchus tshawytscha) also routinely encounter temperatures well above the optimal level. The importance of both beha vioral thermoregulation and thermal refuges was highlighted by studies measuring deep body tempera ture as the salmon moved up the Columbia River. For all measurements obtained, body temperature was below the mean river temperature. The average mea surement was 2.5 � C below mid-river temperature. This difference between the river temperature and fish body temperature extended down to river temperatures as low as 9 � C. This indicates that, during upstream migration, the preferred temperature of these large fish is likely below 9 � C. Problems for juvenile salmon migrating into the ocean can also accrue due to ocean warming. As increased numbers of large and fast predatory fish migrate north ward to attain their preferred temperature, the young salmon face the dual challenge of unduly warm tempera tures and novel highly effective predators that they did not historically encounter.
See also: Brain and Nervous System: Autonomic Nervous System of Fishes. Design and Physiology of the Heart: Physiology of Cardiac Pumping. Energy Utilization in Growth: Growth: Environmental Effects. Fish Migrations: Pacific Salmon Migration: Completing the Cycle. Hypoxia: The Expanding Hypoxic Environment. Pelagic Fishes: Endothermy in Tunas, Billfishes, and Sharks. Sensory Systems, Perception, and Learning: Circadian Rhythms in Fish. Temperature: Effects of Temperature: An Introduction; Measures of Thermal Tolerance; Membranes and Temperature: Homeoviscous Adaptation. The Pituitary: Development of the Hypothalamus-Pituitary-Interrenal Axis. Transport and Exchange of Respiratory Gases in the Blood: Hemoglobin.
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Further Reading Berman CH and Quinn TP (1991) Behavioral thermoregulation and homing by spring chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Yakima River. Journal of Fish Biology 39: 301–312. Bicego KC, Barros RCH, and Branco LGS (2007) Physiology of temperature regulation: Comparative aspects. Comparative Biochemistry and Physiology, Part A 147: 616–639. Coutant CC (1987) Thermal preference: When does an asset become a liability? Environmental Biology of Fishes 18: 161–172. Crawshaw LI (1975) Attainment of the final thermal preferendum in brown bullheads acclimated to different temperatures. Comparative Biochemistry and Physiology 52A: 171–173. Crawshaw LI (1976) Effect of rapid temperature change on mean body temperature and gill ventilation in carp. American Journal of Physiology 231: 837–841. Crawshaw LI and O’Connor CS (1996) Behavioral compensation for long-term thermal change. In: Wood CM and McDonald DG (eds.) Society for Experimental Biology Seminar Series 61: Global Warming: Implications for Freshwater and Marine Fish. pp. 351–376. Cambridge, UK: Cambridge University Press. Crawshaw LI, Wollmuth LP, O’Connor CS, Rausch RN, and Simpson L (1990) Body temperature regulation in vertebrates: Comparative aspects and neuronal elements. In: Schonbaum E and Lomax P (eds.) Thermoregulation: Physiology and Biochemistry, pp. 209–220. New York, NY: Pergamon Press, Inc. Farrell AP (2009) Environment, antecedents and climate change: Lessons from the study of temperature physiology and river migration of salmonids. Journal of Experimental Biology 212: 3771–3780. Farrell AP, Hinch SG, Cooke SJ, et al. (2008) Pacific salmon in hot water: Applying aerobic scope models and biotelemetry to predict the success of spawning migrations. Physiological and Biochemical Zoology 81: 697–708. Hazel JR (1993) Thermal biology. In: Evans DH (ed.) The Physiology of Fishes, ch. 14, pp. 427–467. Boca Raton, FL: CRC Press. High B, Peery CA, and Bennett DH (2006) temporary staging of Columbia River summer steelhead in coolwater areas and its effect
on migration routes. Transactions of the American Fisheries Society 135: 519–528. Hinch SG, Cooke SJ, Healey MC, and Farrell AP (2006) Behavioral physiology of fish migrations: Salmon as a model approach. In: Sloman KA, Wilson RW, and Balshine S (eds.) Behaviour and Physiology of Fish. Fish Physiology 24. San Diego, CA: Elsevier Academic Press. Imsland AK, Foss A, Folkvord A, Stefansson SO, and Jonassen TM (2005) The interrelation between temperature regimes and fish size in juvenile Atlantic cod (Gadus morhua): Effects on growth and feed conversion efficiency. Fish Physiology and Biochemistry 31: 347–361. Jobling M (1996) Temperature and growth: modulation of growth rate via temperature change. In: Wood CM and McDonald DG (eds). Society for Experimental Biology Seminar Series 61: Global Warming: Implications for Freshwater and Marine Fish pp. 351–376. Cambridge, UK: Cambridge University Press. Norris KS (1963) The functions of temperature in the ecology of the percoid fish Girella nigricans (Ayres). Ecological Monographs 33: 23–62. Podrabsky JE, Clelen D, and Crawshaw LI (2008) Temperature preference and reproductive fitness of the annual killifish Austrofundulus limnaeus exposed to constant and fluctuating temperatures. Journal of Comparative Physiology A 194: 385–393. Rausch RN, Crawshaw LI, and Wallace HL (2000) Effects of hypoxia, anoxia, and endogenous ethanol on thermoregulation in goldfish, Carassius auratus. American Journal of Physiology. Regulatory, Integrative, and Comparative Physiology 278: R545–R555. Richards FP, Reynolds WW, and McCauley RW (1977) Temperature preference studies in environmental impact assessments: An overview with procedural recommendations. Journal of the Fisheries Research Board of Canada 34: 728–761. Schurmann H and Christiansen JS (1994) Behavioral thermoregulation and swimming activity of two arctic teleosts (subfamily Gadinae) – the polar cod (Boreogadus saida) and the navaga (Eleginus navaga). Journal of Thermal Biology 19: 207–212. Tanaka H, Takagi Y, and Naito Y (2000) Behavioral thermoregulation of chum salmon during homing migration in coastal waters. Journal of Experimental Biology 203: 1825–1833.
Introduction Species Preferences
Glossary Behavioral thermoregulation Regulation of body temperature by utilizing behavioral movements to control body temperature. It is potentially utilized by all fish. Final thermal preferendum The temperature preference obtained when a species remains in a temperature gradient long enough that a stable preferred temperature is observed. Physiological (or autonomic) thermoregulation Utilization of autonomic responses to control body temperature; utilized in rare cases by fish.
Introduction Temperature can be considered a master factor for fish as it affects all physiological processes and ecological systems. Thermal extremes can prove detrimental or even lethal (see also Temperature: Measures of Thermal Tolerance). Within the range of temperatures that a fish normally encounters, temperature directly speeds up and slows down biochemical reactions (see also Temperature: Effects of Temperature: An Introduction), thus impacting all aspects of a fish’s behavior and physiology. While all motile animals have evolved behaviors that deal with the thermal variation present in their environ ment, fish and other vertebrates possess a particularly sophisticated system to maintain body temperature within narrow limits. The properties of this regulatory system are very similar to those found in other verte brates, although in fish such responses are largely limited to behavioral adjustments and, with only a few exceptions (see also Pelagic Fishes: Endothermy in Tunas, Billfishes, and Sharks), body temperature quickly equili brates to within a few tenths of a � C ambient water temperature. When a range of temperatures is available, fish are able to maintain body temperature at or near the preferred level by positioning themselves in water of that temperature, that is, behavioral temperature regulation. However, despite the power and sophistication of the nervous elements involved with behavioral temperature regulation, a particular species of fish at a given time is
758
Environmental Observations Further Reading
Temperature preference The temperature that a particular species selects, under a particular set of conditions, in a situation where a range of temperatures are available. Thermal acclimation The responses of a fish to maintain in a particular thermal regimen in the laboratory under a specified set of conditions. Thermal acclimatization Organismal adjustments to temperature that occur in nature, and are thus affected by other factors such as season and day length.
not always found at their preferred temperature. During some seasons, the preferred temperature is simply not part of the prevailing environment, while at other times predator avoidance, food acquisition, territorial defense, mating requirements, and gradients of light, oxygen, or salinity may displace a fish from its normally preferred temperature. Nevertheless, temperature is a predominant factor in determining habitat selection by fish, and is a major influ ence on their daily and seasonal movements (see also The Pituitary: Development of the Hypothalamus-PituitaryInterrenal Axis) as well as in their overall distribution and their physiological and biochemical capabilities (see also Design and Physiology of the Heart: Physiology of Cardiac Pumping and Temperature: Membranes and Temperature: Homeoviscous Adaptation). Examples of these effects can be seen in the behavior of the chimaera (Hydrolagus colliei) and the Atlantic mackerel (Scomber scombrus). In its southerly extremes, the chimaera is a deep-water fish, usually being found at depths that exceed 90 m. However, in the cold North Pacific, the chimaera is typically found in shallow water. In both the southern and northern environments, this species is found at the same temperature. Thus, the temperature preference of this spe cies may explain its depth distribution. In contrast to the chimaera, the Atlantic mackerel is a rapidly moving fish and can quickly shift its location in order to maintain a particular body temperature. For the Atlantic mackerel, a 1 � C increase in ocean temperature causes the fish to swim north about 110 km to maintain its preferred temperature.
Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses
Species Preferences
759
fish, and is one of many responses that serve to maintain a species within its recognized habitat.
The preferred temperature can vary under different states, and for each species, the conditions under which the pre ferred temperature is determined should be specified. Thermal preference can be most clearly demonstrated in laboratory temperature gradient or choice devices, which provide fish with the ability to choose specific temperatures from a broad range of available temperatures. If nonthermal influences are minimized, and unstressed fish are placed in a thermal gradient, results similar to those shown in Figure 1 are typically obtained. In Table 1, the temperature prefer ences of various species of fish are shown. The thermal preference is seen to relate to the general habitat of the
Small Alterations in the Preferred Temperature In addition to examples of the preferred temperature for various species, Table 1 also illustrates some of the con ditions where the preferred temperature may be altered within a species. These shifts in preferred temperature are typically on the order of 2 or 3 � C, and are often made by a given species in order to better utilize available tempera tures under different conditions. Such effects include time of day (see also Sensory Systems, Perception, and Learning: Circadian Rhythms in Fish), season, sex, repro ductive stage, presence of a bacterial infection (fever), nutritional status, and geographical location of a subspecies. The degree and presence of such shifts in preferred tem perature are specific to each fish species.
0.20
Frequency
0.15
Major Alterations in the Preferred Temperature 0.10
In certain cases, there can be major alterations in the pre ferred temperature within a species. One case involves developmental state. Typically, younger animals prefer warmer temperatures, which can be considerably higher than the adult preferences. Thus, young salmonids often select temperatures in the upper teens, whereas larger adults typically exhibit temperature preferences in the lower teens. Larger individuals may also exhibit a lower tolerance to high temperatures than juveniles. These differ ences likely reflect both environmental and physiological differences between the developmental stages. Smaller fish can avoid predation more effectively in shallow, covered areas and are also more likely to find appropriate nourish ment in these areas. Higher temperatures, up to a point, can
0.05 0.00 16 18 20 22 24 26 28 30 32 34 36 38 40 Temperature (°C) Figure 1 Fish prefer a narrow range of temperatures when presented with a continuous gradient of temperature options. This figure represents the frequency of temperatures selected by seven female Austrofundulus limnaeus over a period of 24 h in a linear thermal gradient ranging from 12 to 42 � C. The data are calculated from 10 321 one-min averages calculated from data collected every 6 s. Fish were acclimated to a cycling temperature regime ranging from 20–37 � C daily with a photoperiod of 14L:10D for several weeks prior to determination of temperature preference.
Table 1 The laboratory temperature preference of a variety of fish species
Common name
Species
Laboratory temperature preference (� C)
Conditions
Desert pupfish
Cyprinodon macularius
38–40
Summer
Common killifish
Fundulus heteroclitus
28–30 24–26
Northern population Southern population
Common goldfish
Carassius auratus
28–30 24–25
Small Adult
Large mouth bass
Micropterus salmoides
27–29
Adult
Rainbow trout
Oncorhynchus mykiss
21–22 17–18 13–17
Fed fingerlings Starved fingerlings Adults
Coho salmon
Oncorhynchus kisutch
11–12
Adult
Polar cod
Boreogadus saida
2–3 4–5
Early morning Afternoon – early evening
From Richards FP, Reynolds WW, and McCauley RW (1977) Temperature preference studies in environmental impact assessments: An overview with procedural recommendations. Journal of the Fisheries Research Board of Canada 34: 728–761.
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is decreased further, to 10 torr (1.3 kPa), the preferred temperature drops by about 10 � C. While this low tem perature is stressful, it enables the fish to survive by increasing the affinity of hemoglobin for oxygen (see also Transport and Exchange of Respiratory Gases in the Blood: Hemoglobin), augmenting gill extraction efficiency, and by reducing the metabolic demands for maintaining minimal function.
Accuracy and Constancy of the Preferred Temperature Given the general ability of fishes to adapt to a broad range of temperatures (just below 0 � C to just above 40 � C), the stability of their preferred temperature, as seen in Figure 1, is somewhat enigmatic. A closer look at several factors may elucidate the reason for such per sistent maintenance of a particular temperature. First, as mentioned earlier, adjustments to a new tem perature take both time and energy. When a fish moves to water of a different temperature, all aspects of its physio logical and behavioral capabilities are somewhat compromised. The rapidity with which a change in ambi ent water temperature affects overall body temperature is often underestimated. Typically, body temperature is measured at a deep site and the temperature at that site is found to change relatively slowly, even if a fish quickly moves to water of a radically different temperature. The net thermal effect on a fish is better estimated by evaluat ing the change in mean body temperature, which can be done by placing a fish in a calorimeter containing water of a different temperature. The results of such a maneuver for a 0.56 kg carp (Cyprinus carpio) are seen in Figure 2. While 50% of the change in mean body temperature occurs within 1 min, 50% of the change in brain and deep dorsal muscle temperature requires 4 and 5 min, respectively. The magnitude and rapidity of heat transfer T mean body T brain T dorsal muscle Heat loss rate
25 24 23 22 21 20 19 18 17 16 15
800 700 600 500 400 300 200 100
−1 Heat loss rate, watts (J s )
Temperature (°C)
also support faster growth. Larger fish, on the other hand, are more vulnerable to predation in shallow, warm areas. A second case involves adjustment to extreme tem peratures. While fish can adjust body processes to operate effectively over a range of different environmental temperatures (see also Temperature: Membranes and Temperature: Homeoviscous Adaptation), this process takes time and varies for different species, with indivi duals from areas of high thermal variability showing greater capabilities for such thermal acclimatization. With acclimatization to extreme temperatures, metabolic and other physiological processes are greatly altered, and the normally preferred temperature can become harmful or lethal. Not surprisingly, thermal acclimatization alters the preferred temperature, and to a greater degree for temperatures farther from the normally preferred tem perature. Thus, the brown bullhead (Ictalurus nebulosus), which normally prefer water temperatures of about 30 � C, prefer a temperature of 16 � C after being maintained in the laboratory at 7 � C for several weeks. When left undis turbed in a temperature gradient, the preferred temperature gradually increases, and returns to 30 � C in about 1 day. The thermal preference that fish finally stabilize at after a long period in a thermal gradient is termed the ‘final thermal preferendum’. A third case involves survival under physiological stress. Many species of fish have the ability to survive severe hypoxia (see also Hypoxia: The Expanding Hypoxic Environment) by selecting very cold tempera tures. While broad variations in levels of dissolved oxygen in the water normally do not affect the temperature pre ference, when oxygen levels fall to near-lethal levels, thermal preference decreases drastically. Adult goldfish, for example, normally prefer 25 � C. If the oxygen partial pressure is lowered from a normal saturated value of 160 torr (21.3 kPa) to 31 torr (4.1 kPa), there is little change in the preferred temperature. However, if the oxygen level
0 0
2
4
6
8 10 12 14 16 18 20 Time (min)
Figure 2 Changes in temperature and heat loss rates in a 0.56-kg carp transferred from 25 � C into a calorimeter at 15 � C. About half of the heat loss occurs within the first minute after transfer. Temperatures asymptote above 15 � C due to an increase in calorimeter temperature. Adapted with permission from Figure 2 in Crawshaw LI (1976) Effect of rapid temperature change on mean body temperature and gill ventilation in carp. American Journal of Physiology 231: 837–841.
Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses
are emphasized by the heat loss rate illustrated in Figure 2. Note that the metabolic heat produced by the carp in this situation would be less than 1 W. For such a carp, when equilibrium is finally reached, about half of the heat exchange occurs at the body surface and about half is due to conductance across the gill surface. The thermal exchange times exhibited for this 0.56-kg carp would be faster for smaller fish and slower for larger fish due to the differences in surface-area-to volume ratios (see also Temperature: Effects of Temperature: An Introduction). Another reason for the persistent selection of a parti cular temperature relates to the overall optimization of organismal function. While most fish can make adjust ments to function well over a range of temperatures, there is a much narrower temperature range that, after thermal acclimatization, provides an optimal behavioral and phy siological set of responses for functioning in the fish’s particular habitat. Such responses include optimization of growth (see also Energy Utilization in Growth: Growth: Environmental Effects), metabolic scope, cardiac scope, power output of aerobic muscles, and overall per formance. In the cases investigated, the preferred temperature fell within the narrow range of temperatures for overall optimal function. Characteristics of the Thermoregulatory System The regulatory system which is utilized by fish to main tain a particular body temperature is anatomically and functionally similar in Chondrichthyes and Osteichthyes, and is closely related to the system utilized by other (a) Chondrichthyes
vertebrates (see Figure 3 and Brain and Nervous System: Autonomic Nervous System of Fishes). To func tion correctly, a thermoregulatory system must sense the controlled variable, make a comparison with an ideal value, and determine an appropriate behavioral response. In fish and other vertebrates, temperature sensing occurs both peripherally and centrally. Sensitivity occurs over the entire fish surface, and is likely subserved by highly responsive, rate-sensitive, free nerve endings. In condi tioning experiments, fish have proved capable of responding to a surface temperature change of less than 0.05 � C. While, in most conditions, fish would probably not respond to such small temperature differences, they clearly have a capability for detecting extremely small thermal variation. This capability is undoubtedly useful for specific situations that could involve locating critical thermal refuges or guiding large-scale migrations. An important area for central thermal sensing and processing occurs in the anterior brainstem regions in vertebrates, as shown in Figure 3. In fish, an area of particular impor tance is the nucleus preopticus periventricularis. Lesions within the anterior brainstem area destroy thermoregula tory behavior in fish, and heating and cooling this area (including adjacent tissue) leads to the selection of cooler and warmer water, respectively.
Environmental Observations Field observations that relate fish location (and some times actual body temperature) to local water temperature are particularly valuable. Such data clarify
(c) Osteichthyes
ON
(e) Mammalia
ON
ON (b) Osteichthyes
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(d) Osteichthyes
OC
(f) Mammalia
OC AC ON
AC NPP
PO
OC
Figure 3 Similar anatomical locations are responsible for body temperature regulation in various groups of vertebrates. Ventral brain surfaces are represented in (a), (b), and (e). Shaded areas represent surfaces that overlie interior regions of the brain that are critical for thermoregulatory control and integration. (c) A side view of the brain with a line depicting the plane of the cross section depicted in (d). A cross section of the shaded region of (e) is depicted in (f). Major thermoregulatory effects are induced by the application of bioactive compounds to the shaded areas of the cross sections in (d) and (f). AC, anterior commissure; OC, optic chiasma; ON, optic nerve; NPP, nucleus preopticus periventricularis; PO, preoptic nucleus. Adapted from Fig. 1 in Crawshaw LI and O’Connor CS (1997) Behavioral compensation for long-term thermal change. In: Wood CM and McDonald DG (eds.) Society for Experimental Biology Seminar Series 61: Global Warming: Implications for Freshwater and Marine Fish, pp. 351–376. Cambridge: Cambridge University Press.
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Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses
the operation of temperature selection in a natural environment, illustrate its use in the maintenance of an optimal body temperature, and show how fish avoid deleterious environmental temperatures in a local envir onment and during migrations. The value and limitations of temperature selection for fish attempting to survive during an era of global climate change will also be touched upon.
(a) Moose River
24 24
Avoidance of Dangerous Temperatures While the lethal limit for brook trout (Salvelinus fontina lis) is just below 25 � C, they prefer to remain in temperatures below 17 � C. In spite of this, during the summer period of low flow and warm water, brook trout are often found in habitats where mainstream tempera tures exceed lethal limits. Figure 4 illustrates an example of how brook trout are able to survive such dangerously warm conditions. In this instance, the trout congregated near the confluence of the main river and a much cooler tributary. Although their ther mal preference is considerably lower than the area of the river they occupied, they likely avoided moving into even cooler areas nearer the tributary due to the dangers of predation involved with occupying very shallow water. The location of these fish indicates a compromise between the preferred temperature and a combination of water depth plus river surface characteristics. Over the course of the summer, the brook trout maintained a body temperature of about 3 � C lower than that of the main river temperature. In addition to utilizing confluences with cooler streams, fish in overly warm rivers have also been observed to make use of cold groundwater dis charges and thermally stratified deep pools to avoid thermally induced injury or death. Similar examples exist for migrating Pacific salmon (Oncorhynchus sp.) that, during their migration through large rivers, can take advantage of cooler water from tributaries and sometimes lakes. However, in this case, this preference behavior can only act as a temporary respite because the river migration must be completed in relatively short order (see also Fish Migrations: Pacific Salmon Migration: Completing the Cycle). Fish utilize similar strategies in reservoirs and lakes. Figure 5 depicts the body temperature of striped bass (Morone saxatilis) that were introduced into a reservoir in the southeastern USA. This area has warmer tem peratures than those present in the normal habitat of this species. The larger adults prefer to remain at temperatures below 22 � C, but this becomes very diffi cult during the months of summer. The cooler, lower depths become progressively deoxygenated, while the surface waters become untenably warm. Nevertheless, as seen in Figure 5, the large adults were usually able to maintain body temperatures and (presumably)
22 20 18 17.9
Bottom temperature (°C)
Combs creek
(b) Moose River
100 100 80 60 40
Depth (cm) Combs creek N 0
5
15 m
Figure 4 Aggregation of brook trout (shaded areas) depicted in relationship to surface water temperature (a) and depth (b) in the Moose River at the confluence with the cooler Combs Creek. Adapted from Fig. 5 in Baird OE and Krueger CC (2003) Behavioral thermoregulation of brook and rainbow trout: Comparison of summer habitat use in an Adirondack river, New York. Transactions of the American Fisheries Society 132: 1194–1206.
dissolved oxygen within acceptable levels by utilizing discrete areas near cold groundwater discharge or cool tributary entrances.
Behavioral Responses to the Environment | Temperature Preference: Behavioral Responses 32 30 28
Temperature (°C)
26 24 22 20 18 16 14 12 10 Selected temperature Surface temperature Bottom temperature
8 6 4 A
M J
J
A
S
O N
D
J
F
M
Month Figure 5 Temperatures selected by free-living striped bass (open circles) in Lake Seminole for a 1-year period starting in March/April of 1984. Surface and bottom water temperatures are plotted to indicate that the fish utilize a unique subset of their thermal habitat for large portions of the year. Redrawn from Fig. 3 in van den Avyle MJ and Evans JW (1990) Temperature selection by striped bass in a Gulf of Mexico coastal river system. North American Journal of Fisheries Management 10: 58–66.
Global Climate Change, Environmental Degradation, and Temperature Preference Although the above strategies will, to some extent, ameliorate gradual increases in ambient water tempera ture due to climate change (see also Temperature: Effects of Climate Change) and other anthropomorphic effects (see also Behavioral Responses to the Environment: Anthropogenic Influences on Fish Behavior), disadvantages also accrue. In scenarios where preferred temperatures become limiting in a fish’s natural environment, the usable habitat may also become restricted due to behavioral limitations. For example, fish may be forced to occupy small tributaries with cooler temperatures and be excluded from using or migrating through large mainstem rivers where tem peratures can reach lethal heights or at least be many degrees above the fish’s preferred temperature. As large numbers of fish are forced to aggregate into small areas, crowding can increase stress, parasitism, disease, as well as decrease food availability and perhaps the oxygen contained in the water. For species which are linked to a particular geographic area, environmental warming brings added hazards. Migratory salmonids are a prime example, since nonthermal (largely olfactory) factors provide the primary cues that tie them to their natal streams. Adult salmon require relatively low body temperatures during
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migration to maintain energetic stores necessary for the arduous events required for swimming upstream and spawning. In many cases, migrants have already become dependent upon judicious behavioral thermoregulatory strategies in order to survive. Chum salmon (Oncorhynchus keta), migrating along the coast in Japan, encounter high surface temperatures in early fall as they search for their spawning grounds. When the surface waters are warm, they achieve a compromise by mainly remaining in cool, deep water, but with occa sional movements to the surface, presumably to obtain directional cues. Later in the year when the surface water is cooler, these migrating salmon spend most of the time in shallow water. There are also examples of sockeye salmon (Oncorhynchus nerka) being unable to complete their spawning migration because the river water tem perature was simply too hot for them to swim. Upstream migrating Chinook salmon (Oncorhynchus tshawytscha) also routinely encounter temperatures well above the optimal level. The importance of both beha vioral thermoregulation and thermal refuges was highlighted by studies measuring deep body tempera ture as the salmon moved up the Columbia River. For all measurements obtained, body temperature was below the mean river temperature. The average mea surement was 2.5 � C below mid-river temperature. This difference between the river temperature and fish body temperature extended down to river temperatures as low as 9 � C. This indicates that, during upstream migration, the preferred temperature of these large fish is likely below 9 � C. Problems for juvenile salmon migrating into the ocean can also accrue due to ocean warming. As increased numbers of large and fast predatory fish migrate north ward to attain their preferred temperature, the young salmon face the dual challenge of unduly warm tempera tures and novel highly effective predators that they did not historically encounter.
See also: Brain and Nervous System: Autonomic Nervous System of Fishes. Design and Physiology of the Heart: Physiology of Cardiac Pumping. Energy Utilization in Growth: Growth: Environmental Effects. Fish Migrations: Pacific Salmon Migration: Completing the Cycle. Hypoxia: The Expanding Hypoxic Environment. Pelagic Fishes: Endothermy in Tunas, Billfishes, and Sharks. Sensory Systems, Perception, and Learning: Circadian Rhythms in Fish. Temperature: Effects of Temperature: An Introduction; Measures of Thermal Tolerance; Membranes and Temperature: Homeoviscous Adaptation. The Pituitary: Development of the Hypothalamus-Pituitary-Interrenal Axis. Transport and Exchange of Respiratory Gases in the Blood: Hemoglobin.
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Further Reading Berman CH and Quinn TP (1991) Behavioral thermoregulation and homing by spring chinook salmon, Oncorhynchus tshawytscha (Walbaum), in the Yakima River. Journal of Fish Biology 39: 301–312. Bicego KC, Barros RCH, and Branco LGS (2007) Physiology of temperature regulation: Comparative aspects. Comparative Biochemistry and Physiology, Part A 147: 616–639. Coutant CC (1987) Thermal preference: When does an asset become a liability? Environmental Biology of Fishes 18: 161–172. Crawshaw LI (1975) Attainment of the final thermal preferendum in brown bullheads acclimated to different temperatures. Comparative Biochemistry and Physiology 52A: 171–173. Crawshaw LI (1976) Effect of rapid temperature change on mean body temperature and gill ventilation in carp. American Journal of Physiology 231: 837–841. Crawshaw LI and O’Connor CS (1996) Behavioral compensation for long-term thermal change. In: Wood CM and McDonald DG (eds.) Society for Experimental Biology Seminar Series 61: Global Warming: Implications for Freshwater and Marine Fish. pp. 351–376. Cambridge, UK: Cambridge University Press. Crawshaw LI, Wollmuth LP, O’Connor CS, Rausch RN, and Simpson L (1990) Body temperature regulation in vertebrates: Comparative aspects and neuronal elements. In: Schonbaum E and Lomax P (eds.) Thermoregulation: Physiology and Biochemistry, pp. 209–220. New York, NY: Pergamon Press, Inc. Farrell AP (2009) Environment, antecedents and climate change: Lessons from the study of temperature physiology and river migration of salmonids. Journal of Experimental Biology 212: 3771–3780. Farrell AP, Hinch SG, Cooke SJ, et al. (2008) Pacific salmon in hot water: Applying aerobic scope models and biotelemetry to predict the success of spawning migrations. Physiological and Biochemical Zoology 81: 697–708. Hazel JR (1993) Thermal biology. In: Evans DH (ed.) The Physiology of Fishes, ch. 14, pp. 427–467. Boca Raton, FL: CRC Press. High B, Peery CA, and Bennett DH (2006) temporary staging of Columbia River summer steelhead in coolwater areas and its effect
on migration routes. Transactions of the American Fisheries Society 135: 519–528. Hinch SG, Cooke SJ, Healey MC, and Farrell AP (2006) Behavioral physiology of fish migrations: Salmon as a model approach. In: Sloman KA, Wilson RW, and Balshine S (eds.) Behaviour and Physiology of Fish. Fish Physiology 24. San Diego, CA: Elsevier Academic Press. Imsland AK, Foss A, Folkvord A, Stefansson SO, and Jonassen TM (2005) The interrelation between temperature regimes and fish size in juvenile Atlantic cod (Gadus morhua): Effects on growth and feed conversion efficiency. Fish Physiology and Biochemistry 31: 347–361. Jobling M (1996) Temperature and growth: modulation of growth rate via temperature change. In: Wood CM and McDonald DG (eds). Society for Experimental Biology Seminar Series 61: Global Warming: Implications for Freshwater and Marine Fish pp. 351–376. Cambridge, UK: Cambridge University Press. Norris KS (1963) The functions of temperature in the ecology of the percoid fish Girella nigricans (Ayres). Ecological Monographs 33: 23–62. Podrabsky JE, Clelen D, and Crawshaw LI (2008) Temperature preference and reproductive fitness of the annual killifish Austrofundulus limnaeus exposed to constant and fluctuating temperatures. Journal of Comparative Physiology A 194: 385–393. Rausch RN, Crawshaw LI, and Wallace HL (2000) Effects of hypoxia, anoxia, and endogenous ethanol on thermoregulation in goldfish, Carassius auratus. American Journal of Physiology. Regulatory, Integrative, and Comparative Physiology 278: R545–R555. Richards FP, Reynolds WW, and McCauley RW (1977) Temperature preference studies in environmental impact assessments: An overview with procedural recommendations. Journal of the Fisheries Research Board of Canada 34: 728–761. Schurmann H and Christiansen JS (1994) Behavioral thermoregulation and swimming activity of two arctic teleosts (subfamily Gadinae) – the polar cod (Boreogadus saida) and the navaga (Eleginus navaga). Journal of Thermal Biology 19: 207–212. Tanaka H, Takagi Y, and Naito Y (2000) Behavioral thermoregulation of chum salmon during homing migration in coastal waters. Journal of Experimental Biology 203: 1825–1833.