Salmonids elicit an acute behavioral response to heterothermal environments

Water temperature constitutes a key physical property of riverine ecosystems. It has been described as the ‘abiotic master factor’ for fishes (Beitinger and Fitzpatrick, 1979; Brett, 1971), strongly affecting their energy balance and behavior (Volkoff and Rønnestad, 2020; Takatsu et al., 2022). In natural habitats, temperature may change on a variety of spatial and temporal scales. Thermal gradients occur at river confluences, at locations where rivers flow into lakes, and within vertically stratified lakes. As most fish species are ectotherms, their body temperature changes according to the temperature of the water they occupy (Haesemeyer, 2020). Because temperature influences the rates of most physiological processes, rapid warming or cooling can affect fish performance traits, including metabolic rates, swimming ability, and thermal tolerance (Jutfelt et al., 2024).

Because they lack physiological means to regulate body temperature, fish have two main choices when exposed to heterothermal environments (i.e. environments in which temperature varies over space and/or time): acclimate physiologically to changes in local temperature (physiological plasticity; Fry, 1967; Morgan et al., 2022) or adopt specific behaviors to regulate their body temperature (behavioral thermoregulation; Haesemeyer, 2020; Prosser and Nelson, 1981). Behavioral thermoregulation allows fish to thrive in environments where temperature fluctuates, by maximizing the time spent in areas where temperature is within their optimum performance range and by avoiding temperature extremes. While fish may generally adjust to gradual temperature changes through physiological plasticity, the risk of stress increases for more rapid temperature changes (Donaldson et al., 2008) and in this situation, behavioral thermoregulation may be of greater importance.

Fish were found to actively seek optimal temperatures in their environment through movement behavior 50 years ago (Neill et al., 1972). Recent experiments to determine the mechanisms underlying behavioral thermoregulation have identified both thermokinetic and thermotactic components (Haesemeyer et al., 2015; Haesemeyer et al., 2018). Thermokinesis refers to a change in the rate of movement of fish in response to temperature. One explanation for thermokinesis is that a change in body temperature impacts the metabolic rate, which in turn affects movement activity. In this scenario, thermal sensing is not required. For instance, zebrafish larvae (Danio rerio) increase their turn frequency, turn amplitude, and swimming speed when water temperature is increased from 18 °C to 32 °C (Le Goc et al., 2021). This thermokinetic behavior can explain how zebrafish larvae avoid warmer water, but not how they avoid colder water.

Thermotaxis, in contrast, is the directed movement along a temperature gradient, toward warmer or colder water, and requires the ability to sense a temperature gradient (Haesemeyer et al., 2015; Haesemeyer et al., 2018). Fish may achieve thermotaxis either by sensing a thermal gradient spatially along their body or temporally over a given time window as they swim. The response to a thermal gradient can then be either deterministic, through directed movement along the gradient, or biased, for example, through the increase in the turning rate when moving down the gradient, analogous to bacterial chemotaxis (Keegstra et al., 2022; Stocker and Seymour, 2012). Thermotaxis has been observed in a number of vertebrate organisms (Giacometti et al., 2021; Ye et al., 2021; Leonard, 1974). While the thermal preference of fish is a well-established field of research, very few quantitative studies of behavioral mechanisms allowing fish to seek their preferendum (i.e. thermotaxis) have been conducted in fish. Among these is work showing that larval zebrafish integrate thermal information over a 500 ms time window (Haesemeyer, 2020) and bias the magnitude and direction of their turns to favor movement toward colder regions.

Past studies have investigated the long-term (hours) behavioral response of fish to stationary thermal gradients. In contrast, very little is known about the thermoregulatory behavior in response to the exposure to sharp, rapidly occurring thermal gradients associated, for example with anthropogenic disturbances (Haesemeyer et al., 2015). Here, we report experiments to quantify the thermoregulatory behavior of a salmonid in its early life-stages in response to the rapid formation of sharp vertical temperature gradients generated using a lock-release approach. In particular, we identified a knowledge gap associated with the rapid intrusion of cold and warm water into the fish’s habituated surrounding. Thereby, we advance our understanding of thermoregulatory behavior in vertically stratified heterothermal environments. Salmonids are among the most common and well-studied families of freshwater fish in the northern hemisphere, yet little is known about their thermoregulatory behavior (McCullough et al., 2009). All salmonids spawn in the shallow gravel beds of freshwater headstreams and spend most of their juvenile stage in rivers and small creeks, where temperature regimes are often strongly affected by human activities (Antonetti et al., 2023). Due to their small body size, the early life-stages of fish gain or lose heat rapidly, making them particularly sensitive to thermal disturbances (Stevens and Sutterlin, 1976).

The natural thermal regime of rivers can be significantly altered by human activities (Vanzo et al., 2016), including the operation of storage hydropower (i.e. induced thermopeaking; Antonetti et al., 2023; Zolezzi et al., 2011), the use of water for cooling in thermal power plants (Prats et al., 2010), flow regulation at artificial barriers (Dickson et al., 2012; Olden and Naiman, 2010), urbanization (Nelson et al., 2021), and climate change (Barbarossa et al., 2021; Collas et al., 2019). If the local water temperature changes too rapidly, this might trigger an avoidance response, driving fish to abandon habitats (McCullough et al., 2009). For example, recent observations of the impact of thermopeaking show that a sudden decrease in water temperature (by 2.5 °C in 10 min) led to significantly higher downstream drift of juvenile European grayling (Thymallus thymallus) than during events with increasing water temperature (Mameri et al., 2023). However, research on this topic remains scarce (Moreira et al., 2019), and the mechanisms underlying rapid behavioral thermoregulation have remained unclear.

Human-induced thermal alterations in freshwater systems can be unnaturally rapid and strong (Zolezzi et al., 2011). For example, the water temperature downstream of hydropower facilities can decrease by up to 6 °C within minutes in spring and summer, and increase strongly (up to 4 °C) in winter (Zolezzi et al., 2011). During spring and summer, cold thermopeaking may cause significant mortality, as it coincides with the presence of early life stages of salmonids and cyprinids (Auer et al., 2023). Rapid thermal changes (multiple degrees Celsius over minutes) are likely challenging for fish, partly because their natural occurrence over evolutionary timescales might have been rare. For instance, if they are unable to relocate upon being exposed to cold water, fish can become cold-shocked, a lethargic state of slowed metabolism, reduced oxygen uptake, and muscle stiffness, resulting in reduced swimming activity and increased risk of predation (Donaldson et al., 2008).

The primary aim of our study was to quantify how brown trout parr (Salmo trutta), hereafter trout, respond to rapid (i.e. over timescales ${\mathit{\tau }}_{\text{PHYS}}$ of minutes) thermal disturbances. To mimic the rapid release of thermal effluent into a freshwater system, we developed a laboratory setup that uses the lock-release of a gravity current to rapidly expose fish acclimated to 12° (their assumed thermal preferendum) to a warmer or colder body of water. By continuously tracking individual fish, we quantified their response to incoming water of different temperatures ($T_{\text{incoming}}={4-20}^{\circ }\mathrm{C}$). We hypothesized that after rapid exposure, fish would avoid the incoming colder or warmer water across all treatments and that they would do so through a combination of thermokinesis and thermotaxis. To test this hypothesis, we developed a novel imaging approach that allowed simultaneous tracking of the thermal interface and the swimming behavior of individual fish at high spatio-temporal resolution. Our results indicate that fish use both thermokinetic and thermotactic behaviors to rapidly and effectively avoid incoming cold water, whereas they perform frequent excursions into incoming warm water, possibly as a strategy to gradually elevate their body temperature.

To test the hypothesis that strong thermal gradients trigger an avoidance response in trout, we exposed individuals (in groups of four for each replicate experiment) to heterothermal conditions in a laboratory setup. The setup consisted of a lock-exchange tank initially divided into equal halves containing water at two different temperatures (Figure 1A). To avoid behavioral bias due to visual cues, the tank was shielded with white semi-transparent material (except for the front and the water surface). The experiments were conducted in a dark room, and the tank was illuminated with a light source from behind (Figure 1—figure supplement 1). In the left side of the tank, fish were acclimated for 15 min to water at 12 °C, which was assumed to be close to their thermal preferendum (Reynolds and Casterlin, 1979a; Reynolds and Casterlin, 1979b). This water temperature was also equal to the husbandry tank at our experimental facility. The right side of the tank contained water at a different temperature (colder or warmer), dyed blue (Patent blue V sodium salt, Sigma Aldrich) to allow visualization of the thermal interface (Appendix 1—figure 1). Experiments included four cold treatments (TR1, 10 °C; TR2, 8 °C; TR3, 6 °C; TR4, 4 °C) and four warm treatments (TR6, 14 °C; TR7, 16 °C; TR8, 18 °C; TR9, 20 °C; Appendix 1—table 1). After the 15 min acclimation time, the vertical lock separating the two halves of the tank was rapidly lifted, resulting in a gravity current with warmer water intruding along the top of the tank and colder water intruding in the opposite direction along the bottom. The initial gravity current reached the end-wall of the tank after 1–2 min, creating a sharp thermal interface vertically separating the colder water in the bottom part of the tank ($T_{\text{bottom}}$) from the warmer water in the top part ($T_{\text{top}}$; Figure 1B; Appendix 1—figure 1). Owing to the oscillations triggered by the lock release, the vertical location of the thermal interface was not constant in time (Appendix 13—Videos 1 and 2), but instead oscillated around the half depth of the tank, with oscillations dissipating over time (Figure 1—figure supplement 4).

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The lateral view of the entire tank was continuously recorded for 35 min with a camera at 24 frames/s, starting 4 min after releasing the fish. Using image analysis, we obtained the two-dimensional projection of the trajectory of each fish over the entire duration of the experiment (Figure 1C), while simultaneously tracking the instantaneous location of the thermal interface (Figure 1—figure supplement 2). In this manner, we determined the water temperature experienced by each fish at each point in time. Trajectories were analyzed for the last 6 min of the acclimation period and for the 18-min treatment period, which we divided into three phases of 6 min each (treatment phases p1, p2, and p3; Figure 1D). The depth occupancy was computed from the vertical position of the fish $Y\left(t\right)$ and normalized to the range $Y_{\text{norm}}=0-1$, with 1 being the maximum depth (28 cm) of the tank. To quantitatively analyze fish movement behavior in relation to the thermal interface, each trajectory was binarized in time based on whether at a given instant a fish was in the warm or the cold water, as determined from the instantaneous vertical distance to the thermal interface, $D\left(t\right)$ (Figure 2A and B; Appendix 13—Videos 1 and 3; Methods).

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Trout parr avoid cold water by biasing their vertical turns and do not avoid warm water

Fish showed a clear thermotactic avoidance behavior of incoming cold water for $T_{\text{bottom}}\le 8^{\circ }\mathrm{C}$. During phase p3 in the three coldest treatments, TR2 ($T_{\text{bottom}}=8^{\circ }\mathrm{C}$), TR3 ($T_{\text{bottom}}=6^{\circ }\mathrm{C}$), and TR4 ($T_{\text{bottom}}=4^{\circ }\mathrm{C}$), fish predominantly occupied the upper half of the tank ($Y_{\text{norm}}=0-0.5$) and avoided the colder water in the bottom half (Figure 2C; see also Appendix 5—figure 1). From phase p1 to p3, fish spent 75–95% of the time above the thermal interface (Figure 2—figure supplement 3A). This represents a substantial change of the preferential depth occupancy compared to the acclimation phase, in which fish spent 50–90% of the time in the lower half of the tank ($Y_{\text{norm}}=0.5-1$; Appendix 5—figure 1). The response was rapid, with avoidance of the cold water being apparent already in phase p1 and persisting through to the end of the experiment (TR2 in Figure 2D; all cold-water treatments in Figure 2—figure supplement 2A-D). In contrast, incoming cold water in TR1 ($T_{\text{bottom}}={10}^{\circ }\mathrm{C}$) – that is only 2 °C colder than the acclimation temperature – did not trigger an avoidance behavior: the depth occupancy showed a bimodal distribution with peaks in both the warmer and colder water (Figure 2C).

Fish did not avoid warmer water in any of the warm-water treatments (TR6–TR9). Instead, fish transitioned to a bimodal depth occupancy, with comparable time spent above and below the interface (Figure 2F; Figure 2—figure supplement 3B). This bimodal behavior was especially pronounced in the later phases, p2 and p3 (TR7; Figure 2G; all warm-water treatments in Figure 2—figure supplement 2E-H), whereas in phase p1, the depth occupancy was similar to that exhibited during the acclimation period, with 50–70% of the time spent in the lower, colder water (Appendix 5—figure 2). Thus, over time, fish increasingly occupied warmer water across all warm-water treatments, reducing the fraction of time spent below the interface during phase p3 to 30–50% (Appendix 9—figure 4B, Appendix 8—figure 4).

Further analysis of the response to cold water treatments revealed a strong asymmetry between warm-water and cold-water excursions, defined as the periods of time during which a fish was above or below the thermal interface, respectively. This asymmetry was present in treatments with $T_{\text{bottom}}\le 8^{\circ }\mathrm{C}$: TR2 (Figure 2E), TR3, and TR4 (Appendix 8—figure 2C and D), but not TR1 (Appendix 8—figure 2A). In cold treatments TR2, TR3, and TR4, cold-water excursions were considerably shorter (91–94% shorter than 10 s) than warm-water excursions (38–49% shorter than 10 s; Appendix 8—table 7). In contrast, during all warm treatments, warm and cold excursions had similar durations (Figure 2H, Appendix 8—figure 3).

To determine the behavioral mechanism underlying cold-water avoidance, we analyzed the fine-scale features of the fish trajectories as a function of the position of the fish relative to the thermal interface. We identified upward and downward turning events within each trajectory, based on when the vertical velocity component $v_y$ changed sign (Figure 3A and B; Methods; Appendix 9—figure 1). For each turning event, we computed the corresponding vertical distance $\hat{D}$ to the thermal interface. We also quantified the median number of cold-water excursions $\tilde{N}$ of the four fish within each experimental replicate. We found that fish reduced their tendency to cross the thermal interface and rapidly redirected their swimming when in the colder water. In cold-water treatments TR2–TR4 ($T_{\text{bottom}}\le 8^{\circ }\mathrm{C}$), the median number of interface crossings was significantly lower than in TR1 ($T_{\text{bottom}}={10}^{\circ }\mathrm{C}$; ANOVA and post hoc pairwise t-tests – p < 0.01, Figure 3C). In TR2-TR4, the probability of upward turning ${\rho }_{\text{up}}$ exceeded the probability of downward turning ${\rho }_{\text{down}}$ for the entire region below the interface ($-20\text{cm}<\hat{D}<0\text{cm}$; Figure 3D and F, Appendix 9—figure 3). This difference in probabilities (${\rho }_{\text{up}}-{\rho }_{\text{down}}$) was particularly large in the region immediately above and below the interface ($-5\text{cm}<\hat{D}<5\text{cm}$; Figure 3F) and is a hallmark of a thermotactic behavior.

Figure 3

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This thermotactic avoidance behavior was absent in TR1 and all warm treatments, where the probabilities of upward and downward turning were similar (${\rho }_{\text{up}}-{\rho }_{\text{down}}\approx 0$) close to the interface ($-5\text{cm}<\hat{D}<5\text{cm}$) (Figure 3E and G). In these treatments, the probability of upward turning peaked below the thermal interface, close to the bottom of the tank ($-15\text{cm}<\hat{D}<-10\text{cm}$; Figure 3G), while the probability of downward turning peaked above the thermal interface, close to the water surface ($10\text{cm}<\hat{D}<15\text{cm}$; Figure 3E, G, Appendix 9—figure 4 for TR6–TR9).

Fish modulate the duration and depth of cold-water excursions as a function of cold-water temperature

In cold treatments, fish did not exclusively stay within the upper warmer water layer but engaged in occasional exploratory behavior of the underlying, colder water. In particular, fish did not reduce the frequency of cold-water excursions over time (Appendix 8—figure 4A). During these excursions, they crossed the interface downwards and thus experienced a sudden decrease in temperature. We found that fish modulated these cold-water excursions as a function of the temperature of the colder water. The duration $\Omega$ (s) and depth $D_{\text{max}}$ (the maximum vertical distance below the thermal interface) of cold-water excursions both decreased (Figure 4A) with decreasing temperature of the lower layer ($T_{\text{bottom}}$). This trend was statistically significant for both the median duration $\widetilde{\stackrel{~}{\Omega }}$ (Figure 4B) and the median depth ${\widetilde{\stackrel{~}{D}}}_{\text{max}}$ (Figure 4C) across treatments (Mann–Kendall test, $p<0.001$, Appendix 9—tables 1 and 2). As $T_{\text{bottom}}$ decreased from 10 °C to 4 °C (TR1 to TR4), the median excursion duration decreased by 57% (from $\stackrel{\sim }{\stackrel{\sim }{\mathrm{\Omega }}}=6\text{s}$ to $\stackrel{\sim }{\stackrel{\sim }{\mathrm{\Omega }}}=2.6\text{s}$) and the median excursion depth decreased by 57% (from ${\stackrel{\sim }{\stackrel{\sim }{D}}}_{max}=9.9\text{cm}$ to ${\stackrel{\sim }{\stackrel{\sim }{D}}}_{max}=4.3\text{cm}$, Appendix 9—table 1).

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To understand whether this exploratory behavior of the colder water changed over the 18 min duration of the experiments, we analyzed the distribution of the excursion duration $\Omega$ of warm- and cold-water excursions separately for each phase (p1, p2, and p3). For TR1 ($T_{\text{bottom}}={10}^{\circ }\mathrm{C}$, $T_{\text{top}}={12}^{\circ }\mathrm{C}$), cold and warm water excursions showed almost identical distributions of their durations, and the distributions changed little over time across the three phases (${\stackrel{\sim }{\mathrm{\Omega }}}_{\text{warm}}=6.7\text{s},7.5\text{s},7.3\text{s}$ and ${\stackrel{\sim }{\mathrm{\Omega }}}_{\text{cold}}=8.4\text{s},4.9\text{s},5.1\text{s}$, for p1, p2, and p3 respectively; Figure 4D). The same conclusions apply to all warm treatments (TR6–TR9; Figure 4—figure supplement 1E-H). In stark contrast, in cold-treatment TR3, the distributions of the durations of cold-water excursions (into $T_{\text{bottom}}=6^{\circ }\mathrm{C}$) and warm-water excursions (into $T_{\text{top}}={12}^{\circ }\mathrm{C}$) are clearly distinct already in phase p1, and this difference increases in p2 and p3 (${\stackrel{\sim }{\mathrm{\Omega }}}_{\text{warm}}=9.8\text{s},15.5\text{s},15.8\text{s}$ and ${\stackrel{\sim }{\mathrm{\Omega }}}_{\text{cold}}=3.7\text{s},2.8\text{s},2.8\text{s}$ for p1, p2, and p3, respectively; Figure 4E). In particular, short warm-water excursions ($0.1\text{s}<\mathrm{\Omega }<10\text{s}$) and long cold-water excursions ($10\text{s}<\mathrm{\Omega }<100\text{s}$) became less frequent over time. A similar pattern is observed in TR2 and TR4 (Figure 4—figure supplement 1B, D).

Fish swimming speed increases during short-term exposure to cold water

In addition to displaying a thermotactic behavior in modulating their turning events upon experiencing temperature gradients, fish further reduced cold-water exposure through a thermokinetic behavior, by increasing their swimming speed when in cold water. For $T_{\text{bottom}}\le 6^{\circ }\mathrm{C}$ (TR3 and TR4), the swimming speed normalized by the mean speed of each fish during the entire treatment phase, ${\overline{\overline{v}}}_{n,t}$ (Methods), was significantly greater (44% in TR3; 33% in TR4) when fish were located below compared to above the thermal interface (t-test, p < 0.0001 and p < 0.05, respectively, Figure 5A, Appendix 4—tables 1–4). For TR2 ($T_{\text{bottom}}=8^{\circ }\mathrm{C}$), a similar increase (22%) was observed, but was not statistically significant due to outliers (likely cold-shocked fish) in one replicate (Figure 5A). In contrast, in TR1 the swimming speed was similar during cold-water ($T_{\text{bottom}}={10}^{\circ }\mathrm{C}$) and warm-water ($T_{\text{top}}={12}^{\circ }\mathrm{C}$) excursions (Figure 5A).

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Swimming speed increased over time (from p1 to p3) across all treatments (Appendix 4—figure 2). To account for this temporal trend in the analysis of cold-water excursions, we further normalized the swimming speed by the average speed of that fish during the corresponding phase, $v_{n,p}$. To give each excursion the same weight, independently of its duration, we further averaged that quantity for each excursion, ${\overline{v}}_{n,p}$. Notably, the distribution of average swimming speeds during cold-water excursions in cold treatments with $T_{\text{bottom}}\le 8^{\circ }\mathrm{C}$ (TR2–TR4) is clearly skewed toward values larger than ${\overline{v}}_{n,p}=1$. This indicates that the swimming speed was above average during the majority of cold-water excursions (Figure 5B), indicating the presence of a thermokinetic response. In contrast, for TR1 ($T_{\text{bottom}}={10}^{\circ }\mathrm{C}$) the speed during cold-water excursions peaks at ${\overline{v}}_{n,p}=1$ (Figure 5B), similar to the warm-water excursions across all cold-water treatments (Figure 5C), indicating the absence of a thermokinetic response in these cases. This observation was further supported by more frequently detected high absolute swimming speeds (>20 cm/s) during cold-water occupation in TR2–TR4 (Appendix 10—figure 1). These findings demonstrate that fish exhibit an increase in swimming speed during excursions in cold water ($T_{\text{bottom}}\le 8^{\circ }\mathrm{C}$), indicative of a rapid and transient thermokinetic response, on a timescale of seconds, to cold-water exposure.

Using a novel experimental design, we showed that trout parr acclimated to 12 °C display within minutes a strong avoidance of incoming cold water ($T_{\text{bottom}}={8,6,4}^{\circ }\mathrm{C}$) through a combination of thermotactic and thermokinetic behavior, whereas they do not avoid incoming warm water ($T_{\text{top}}=14,16,18,{20}^{\circ }\text{C}$). Other fish species have been shown to avoid unfavorable thermal conditions, although often over timescales of hours to days (Berman and Quinn, 1991; Magnuson et al., 1979; Sutton et al., 2007). For example, vertical relocation over timescales of hours has been observed for marine sablefish, Anoplopoma fimbria, acclimated to 12 °C and exposed to 2–8 °C (Sogard and Olla, 1998).

Our observations revealed that the avoidance of cold water was mediated by two distinct behavioral responses: fish biased their vertical turns, which enabled them to redirect their swimming out of the colder water, and increased their swimming speed, which allowed them to reduce the time spent in the colder water. Cold-water excursions were shorter in duration and shallower as the temperature of the cold water decreased. Larval zebrafish have been found to exhibit thermotactic behavior similar in some respects to that of trout in our experiments, biasing both turn magnitude and turn direction to swim toward warmer water (Gillooly et al., 2001). However, in contrast to our observation of increased swimming speeds in colder water, swimming activity of larval zebrafish decreased in cold water (Le Goc et al., 2021). Furthermore, to guide their movement, zebrafish have recently been found to integrate temperature information over a time window of 0.4 s preceding the next swimming bout (Haesemeyer et al., 2015). The duration of cold-water excursions of trout in our experiments was of a similar order of magnitude ($0.1\text{s}<\mathrm{\Omega }<10\text{s}$), suggesting that thermal sensing in trout may occur over similar timescales to zebrafish.

Surprisingly, no superficial cold receptor has yet been identified in trout skin (Ashley et al., 2007) or in fish more broadly (Haesemeyer, 2020), and recent studies suggest that fish may instead respond to temporal changes of their internal body temperature (Pépino et al., 2015). To investigate how body temperature might trigger behavioral responses, we used a heat transfer model for fish (Stevens and Sutterlin, 1976) to estimate the decrease in internal body temperature $T_{\text{body}}$ over the duration of cold-water excursions (see Methods). We found that the median body temperature $T_{\text{body}}$ during cold-water excursions decreased by only 0.2 °C in TR1 up to 0.5 °C in TR4 (Appendix 12—figure 1). This suggests that the avoidance response could have been triggered by a small decrease in internal body temperature, in the order of 0.2–0.5 °C. Further, this analysis indicates that by reducing the duration of cold-water excursions, fish maintained body temperatures within the range 11.5–12 °C, ultimately preventing body cooling and the need to acclimate physiologically to the colder temperature.

Our results suggest that the observed thermoregulation behavior in warm-water treatments is a strategy to gradually increase body temperature. When the temperature of the incoming water was higher than 12 °C (TR6–TR9), fish exhibited a bimodal distribution of depth occupancy that was distinctly different from the acclimation phase and the cold-water treatments. This bimodal distribution was not due to variability in the temperature preference among individual fish, but rather to individual fish periodically moving between warmer and colder regions (Figure 2—figure supplement 3B). Interestingly, fish gradually increased the occupancy of warmer water over time (Figure 2—figure supplement 1B). In contrast to the cold treatments, no avoidance response was observed at the thermal interface in warm treatments. We propose that this periodic relocation between warmer and colder regions is a behavioral strategy to slowly elevate body temperature while avoiding rapid and drastic body warming to 14–20 °C (TR6–TR9). It has indeed been shown theoretically that frequent transitions between cold- and warm-water regions that are each, per se, thermally suboptimal, could allow fish to maintain body temperatures between the available extremes while avoiding excessive heating or cooling (Pépino et al., 2015). Our observations resemble this mode of behavioral thermoregulation, in which fish progressively favor warmer regions within a heterothermal environment. However, additional experimental evidence is required to determine the mechanisms underlying this behavior.

We conclude from the behavior of fish when warmer water was available that their acute thermal preferendum exceeded 12 °C, departing from the acclimation temperature we had chosen based on the thermal preferendum for trout reported in literature (Reynolds and Casterlin, 1979b). Indeed, the thermal biology for any fish species is more complex than a single, static thermal preferendum. Many internal and external factors, such as hypoxia, satiation, time of day, and life stage (Haesemeyer, 2020), can influence the temperature preference of fish. For example, the level of satiation can have an impact because when fish are well fed, their growth rate increases with body temperature as metabolic performance increases (Gillooly et al., 2001). This modifies the preferred temperature, as observed in Bear Lake sculpin (Cottus extensus) that ascend into warmer water after feeding to stimulate digestion and thereby achieve a threefold higher growth rate (Wurtsbaugh and Neverman, 1988). In contrast, field studies with adult fish have observed movement from warm to cold water in summer (Chiaramonte et al., 2016; Goniea et al., 2006), allowing fish to lower their metabolic rate, likely in an effort to conserve energy (Brett, 1971; McLaren, 1963). We propose that the behavior of trout parr upon exposure to warmer water in our experiments served to achieve a higher body temperature to ultimately increase growth rate, which is critical for this life stage (Elliott and Hurley, 1995; Forseth et al., 2009). Indeed, growth experiments on brown trout populations have shown that optimal growth temperatures can range between 15 and 19 °C, depending on the stream of origin (Forseth et al., 2009).

The behavioral thermoregulation exhibited by trout in our experiments also included a strong thermokinesis response. Fish rapidly increased swimming speed while in colder water, on a timescale of seconds during individual cold-water excursions (in cold treatments TR2 -TR4). This contrasts with the established paradigm for thermokinesis in fish. For a variety of species including trout (Kieffer and Tufts, 1998), swimming speed was found to decrease with decreasing water temperature. This is thought to be a physiological effect, as a lower temperature results in a lower metabolic rate and locomotory capacity due to decreased contractile rates in the red and white swimming muscles and the heart (Vornanen, 1994). This type of thermokinetic response cannot serve to avoid cold water.

Our results instead suggest that trout parr employ a very different form of thermokinesis. Our analysis showed that increasing swimming speed during cold-water excursions allowed fish to shorten the exposure to cold water. This conclusion is supported by our model predictions that body temperature during cold-water excursions remained above 11.5 °C. Anecdotal observations from our experiments suggest that prolonged exposure to cold water (in the order of minutes) can nonetheless reduce swimming speed. Two individual fish in TR2 ($T_{\text{bottom}}=8^{\circ }\mathrm{C}$) appear to have become trapped within the cold water (Figure 2—figure supplement 1A) and displayed reduced swimming speeds, in line with previously described deactivation upon cold-water exposure (Steiner and Olla, 1985; Taugbøl et al., 2019).

Taken together, these observations suggest that the thermokinetic response to cold water is timescale dependent. If the exposure to cold water is short (seconds), fish accelerate to escape the cold. If exposure is longer (minutes), however, fish slow down, likely due to a reduction in metabolic rate. Importantly, this timescale dependence implies that long-term (hours) measurements of behavior at constant water temperatures cannot be used to model fish movement response to thermal gradients occurring over shorter timescales. Our findings may help explain why recent modeling of fish behavior in heterothermal environments could not reproduce the observed avoidance of cold water in stationary thermal gradients (Le Goc et al., 2021).

Despite the avoidance response to cold water, fish engaged in repeated cold-water excursions, potentially reflecting a behavioral strategy to map the thermal environment. This pattern may also reflect an inherent tendency to occupy the lower part of the tank, as observed during homogeneous temperature of 12 °C during the acclimation phase. However, over time, the frequency of longer cold-excursions (>10 s) diminished, reflecting a modulation of this exploratory behavior. While most studies have associated thermoregulation with sustained relocation from colder to warmer water or vice versa (Amat-Trigo et al., 2023), it has been suggested that short excursions into water of a different temperature might be a thermoregulatory behavior that allows fish to exploit resources in suboptimal thermal regions within a heterothermal environment (Pépino et al., 2015). For example, by keeping excursions into cold water short, hammerhead sharks can access deep-sea foraging habitats without critically cooling their body temperature (Royer et al., 2023).

Our findings show that fish were able to perform upward turns while still located above the thermal interface and that is, before actually sampling the cold water below the interface. In fact, our simulation of the vertical extent of the thermal gradient revealed that a substantial fraction of upward turns occurred before fish encountered the gradient itself—that is, prior to any sensory detection of the temperature change (Appendix 9—figure 5). This finding may be evidence of associative learning, whereby fish used information on the presence of colder water at depth obtained at prior times. While the current data do not provide conclusive evidence in this regard, they prompt the possibility that, rather than responding solely to immediate thermal cues, fish use spatial memory or associative learning to anticipate the location of colder water based on prior experience. Indeed, fish are able to perform associative learning based on non-visual cues de A Moura and Luchiari, 2016; create mental maps of their surroundings Holbrook and Burt de Perera, 2011; and retain memory for hours (de P Cognato et al., 2012), days (Tarrant, 1966), and months (Triki and Bshary, 2019; Zion et al., 2012).

Determining the mechanisms underlying fish behavior in heterothermal environments is challenging because thermokinesis and thermotaxis may co-exist and play out across different spatio-temporal scales. In rivers and lakes, heterothermic environments form naturally and persist over a variety of spatial and temporal scales (Torgersen et al., 1999). Anthropogenic warm- and cold-water releases expose fish to rapid (minutes) thermal changes, known as thermopeaking (Antonetti et al., 2023), which can affect river sections hundreds of kilometers downstream (Toffolon et al., 2010). Here, we mimicked such rapid thermal changes for environmentally relevant thermal contrasts of 2–8 °C using a lock-release setup. We have demonstrated that trout use a combination of thermotaxis (modulation of turning behavior) and thermokinesis (modulation of swimming speed) to avoid cold water, while occasionally still exploring it through brief cold-water excursions. In contrast, we found that for incoming warm water, fish explore both warm- and cold-water regions and do not display any thermotactic avoidance.

While limited to laboratory conditions, these observations provide a framework for interpreting the thermal behavior of fish in nature. For example, a recent study observed a significant increase in downstream displacement for early life stages of a cypriniform fish in response to cold-water thermopeaking (Mameri et al., 2023). The authors hypothesized that this response was caused by reduced swimming capacity and cold shock. Our findings suggest that the observed downstream displacement could alternatively have been caused by an avoidance response at the interface with cold water. However, a generalization of our observations to horizontally oriented thermal gradients remains elusive. Our results are inherently tied to the vertical stratification created in our experiments. As warm water was always positioned above and cold water below, we could not control for the effect of vertical position (i.e. we could not do cold over warm layer experiments). This limits our ability to directly compare our findings to those obtained from horizontally oriented thermal gradients. On the other hand, the case we addressed is of direct environmental relevance, as natural waters often experience vertical thermal stratification.

By capturing the multifaceted response of fish to thermal change, our results may help to predict the larger-scale distribution of species and their response to unnatural disturbances, and thus inform environmental conservation policies. Our study also highlights the importance of deepening our understanding of the fundamental behavioral mechanisms of fish to alterations in their environment, particularly anthropogenic ones. Ultimately, the large-scale distribution of an organism results from the combined effects of responses to countless stimuli on the individual scale. Our experimental setup provides a platform to investigate these stimuli through a reductionist approach, and a blueprint for how to investigate responses to other stimuli such as chemicals or salinity for diverse aquatic organisms.

The Python scripts used for the analyses are available through a public GitHub repository https://github.com/naroberto/Thermal_paper/, copy archived at Naudascher, 2026. The generated videos for fish-tracking can be accessed in an open access archive (https://doi.org/10.3929/ethz-b-000660506).

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Author details

1. Robert Naudascher

   Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland

   Contribution

   Conceptualization, Data curation, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   rnaudascher@yahoo.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0009-0001-6169-1701

2. Stefano Brizzolara

   1. Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland
   2. Swiss Federal Institute of Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland

   Contribution

   Conceptualization, Data curation, Investigation, Methodology, Writing – review and editing, Experimentation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4616-5033

3. Jonasz Slomka

   Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland

   Contribution

   Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7097-5810

4. Robert M Boes

   Laboratory of Hydraulics, Hydrology and Glaciology (VAW), Swiss Federal Institute of Technology Zurich, Zurich, Switzerland

   Contribution

   Resources, Supervision, Funding acquisition, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

5. Markus Holzner

   1. Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland
   2. Swiss Federal Institute of Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland

   Contribution

   Supervision, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

6. Luiz GM Silva

   Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland

   Contribution

   Conceptualization, Resources, Supervision, Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2329-5601

7. Roman Stocker

   Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH Zurich, Zurich, Switzerland

   Contribution

   Resources, Supervision, Funding acquisition, Investigation, Writing – review and editing

   For correspondence

   romanstocker@ethz.ch

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3199-0508

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