Biology

Behavioral responses to annual temperature variation alter the dominant energy pathway, growth, and condition of a cold-water predator Matthew M. Guzzoa,1, Paul J. Blanchfielda,b, and Michael D. Renniea,c,d

aDepartment of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, Canada; bFreshwater Institute, Fisheries and Oceans Canada, Winnipeg, MB R3T 2N6, Canada; cDepartment of Biology, Lakehead University, Thunder Bay, ON P7B 5E1, Canada; and dIISD Experimental Lakes Area Inc., Winnipeg, MB R3B 0T4, Canada

Edited by Mary E. Power, University of California, Berkeley, CA, and approved July 11, 2017 (received for review February 17, 2017)

There is a pressing need to understand how ecosystems will respond to climate change. To date, no long-term empirical studies have confirmed that fish populations exhibit adaptive foraging behavior in response to temperature variation and the potential implications this has on fitness. Here, we use an unparalleled 11-y acoustic telemetry, stable isotope, and mark–recapture dataset to test if a population of lake trout (Salvelinus namaycush), a cold- water stenotherm, adjusted its use of habitat and energy sources in response to annual variations in lake temperatures during the open-water season and how these changes translated to the growth and condition of individual fish. We found that climate influenced access to littoral regions in spring (data from teleme- try), which in turn influenced energy acquisition (data from iso- topes), and growth (mark–recapture data). In more stressful years, those with shorter springs and longer summers, lake trout had reduced access to littoral habitat and assimilated less littoral en- ergy, resulting in reduced growth and condition. Annual variation in prey abundance influenced lake trout foraging tactics (i.e., the balance of the number and duration of forays) but not the overall time spent in littoral regions. Lake trout greatly reduced their use of littoral habitat and occupied deep pelagic waters during the summer. Together, our results provide clear evidence that climate-mediated behavior can influence the dominant energy pathways of top predators, with implications ranging from indi- vidual fitness to food web stability.

food web | climate change | habitat coupling | lake trout | north-temperate lake

There is growing urgency to understand how ecosystems areresponding to climate change (1, 2). Recent work, using latitudinal gradients as proxies to warming, has argued that the behavioral responses of mobile top predators to changing tem- peratures can drive fundamental shifts in aquatic food webs by altering the coupling of major energy pathways (3, 4). Although this work is intriguing, no one has yet examined long-term em- pirical data that have explicitly tested if populations of top predators can shift their foraging behavior in response to annual changes in temperature or has evaluated what implications this might have for individual fitness. Temporal studies are critically important in this context because they control for the ecosystem- specific adaptations that can confound latitudinal studies and in- stead focus on the active responses to changing conditions that are highly relevant to understanding the impacts of climate change. Mobile top predators display adaptive foraging behavior by

moving across spatially disparate habitats in response to chang- ing conditions, most notably prey densities. For example, birds feed on both terrestrial and aquatic prey, effectively coupling these ecosystems (5). Habitat coupling can also occur within ecosystems and has been well described in freshwater lakes, where predatory fish feed upon prey supported by dissimilar energy sources, such as offshore pelagic phytoplankton and nearshore littoral benthic algae (6). These adaptive foraging shifts between littoral and pelagic food

chains (i.e., littoral–pelagic coupling) in response to changes in prey densities can be a stabilizing force in aquatic food webs (7–9). As ectotherms, the body temperatures of fish closely follow

that of their ambient environment, and they must occupy species- specific temperature ranges to optimize physiological perfor- mance (10–12). Adaptive foraging behavior therefore should be particularly important in north-temperate lakes, because these sys- tems undergo annual cycles in water temperatures and stratify ther- mally in summer. During thermal stratification, surface waters often exceed the temperature preferences of cold-water fish, substantially increasing the metabolic costs associated with occupying littoral habitats (10–12). In response, cold-water predators exhibit season- ality in their foraging, feeding in the littoral zone in the spring and fall when surface waters are cool and relying on pelagic energy when surface waters are warm in summer (13, 14). Therefore, variations in both prey density and seasonality should be important factors in directing the foraging behavior of fish in north-temperate lakes. Recent studies have shown that lake-surface temperatures

have risen globally over the past 30 y (15), with north-temperate lakes also having longer open-water seasons and undergoing shifts in the phenology of seasonal water temperatures (16). These observed changes in lake temperatures suggest that future warming may alter littoral–pelagic coupling by mobile predatory

Significance

Climate warming is having wide-ranging effects on aquatic ecosystems. Fish are believed to adapt their feeding behavior as temperatures change, but empirical evidence of this be- havior in nature and its impacts on individual fitness are lack- ing. We monitored the feeding behavior and growth of a temperature-sensitive fish population in a pristine lake for 11 y. Fish adjusted their feeding behavior annually in response to differences in temperature. In cooler years, fish ate more large prey from shallow nearshore regions, resulting in higher growth and condition than in warmer years, when fish ate more small prey from deep offshore regions. This suggests that the impacts of warming on aquatic ecosystems can scale from the individual to the food web level.

Author contributions: M.M.G. and P.J.B. designed research; M.M.G., P.J.B., and M.D.R. performed research; M.M.G. analyzed data; and M.M.G., P.J.B., and M.D.R. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Freely available online through the PNAS open access option.

Data deposition: The data reported in this paper have been deposited in the open source database Zenodo at https://doi.org/10.5281/zenodo.832921. Additional data are available upon request from the IISD-Experimental Lakes Area (https://www.iisd.org/ela/science- data/our-data/data-requests/). 1To whom correspondence should be addressed. Email: mattguzzo12@gmail.com.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1702584114/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1702584114 PNAS Early Edition | 1 of 6

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fish. In fact, multilake studies of temperate food webs have shown that cold-water predatory fish alter their littoral–pelagic coupling across gradients of abiotic factors that regulate the physiological costs of foraging in the littoral zone. For example, littoral energy use by lake trout (Salvelinus namaycush), a cold- water stenotherm, has been shown to increase with latitude, because lakes at higher latitudes have littoral zones that are ei- ther thermally favorable for longer periods or cooler in summer (3). Lake trout acquisition of littoral energy also has been shown to decrease with increasing littoral zone size due to the greater ex- panse of warm water to be traversed to access nearshore prey during summer (17). In both cases, the physiological constraint imposed by temperature was suggested as the key factor in controlling littoral energy use by lake trout, and together these studies suggest that the expected warmer conditions also could alter littoral–pelagic coupling by cold-water fish populations within single lakes. Here, we sought to understand if and how annual variations in

water temperatures altered littoral–pelagic coupling by a cold- water predatory fish population and what implications these di- etary shifts had on individual fitness as inferred from growth and condition. Our study system was a small, oligotrophic north- temperate lake that did not contain pelagic prey fish. In such lakes, lake trout obtain the majority of their energy from prey fish and benthic invertebrates located in the littoral zone (18), presumably during the spring and fall, when water temperatures are cool. As the lake warms, water temperatures within the lit- toral zone exceed the thermal preference of lake trout (>15 °C), and they move offshore to deeper water within the pelagic zone and begin to rely increasingly on smaller pelagic prey, including Mysis diluviana (i.e., freshwater shrimp) and zooplankton (Fig. 1) (13, 14, 18, 19). We hypothesized that because of the direct in- fluence of temperature on fish physiology, annual changes in the phenology of littoral zone water temperatures, which are closely linked to air temperature variations (16), would influence littoral– pelagic coupling by lake trout (Fig. 1). We also expected that climate-driven year-to-year differences in access to prey-rich lit- toral regions would be manifested in the growth and condition of lake trout. To test these hypotheses, we used 11 consecutive years of acoustic telemetry and stable isotope data to quantify annual littoral habitat use and energy sources of our study population and related these findings to annual variations in water temperatures,

prey fish abundance, and the growth and condition of individual lake trout from annual mark–recapture sampling.

Results Lake Temperatures. The length of spring, when lake trout can access the littoral zone without thermal consequence (≤15 °C), averaged 43 d and varied in duration by nearly a month (31–59 d) over the study. The summer period, when lake trout are puta- tively thermally restricted from accessing the littoral zone (>15 °C), was on average 2.7 times longer than the spring and averaged 109 d with a difference of 1 mo (36 d) between the shortest (85 d) and longest (121 d) summers. Longer summers typ- ically had warmer littoral zone temperatures (Pearson correlation: n = 11, r = 0.79, P < 0.01). The length of the fall season, when lake trout spawn but can also use the littoral zone for feeding without thermal consequence, averaged 61 d (range: 51–72 d) and was on average 1.5 times longer than the spring and 1.8 times shorter than the summer. In a given year, the length of the spring and summer seasons showed a negative correlation (n = 11, r = −0.59, P = 0.06), spring and fall lengths were not significantly correlated (n = 11, r = 0.42, P = 0.20), and neither were fall and summer lengths (n = 11, r = −0.32, P = 0.34).

Habitat Use. Lake trout displayed clear seasonal shifts in habitat use and behavior that followed changes in mean littoral zone temperatures (Fig. 2). Immediately following ice-out, lake trout often spent several hours or entire days within the littoral zone (Fig. 2). As mean littoral zone water temperatures exceeded 15 °C (summer), lake trout greatly reduced their forays into the littoral zone until water temperatures cooled to 15 °C in the fall, when lake trout quickly reoccupied the littoral zone (Fig. 2). The total time spent by lake trout in the littoral zone during the spring of each year averaged 550 h and increased with spring length (log10; F1,8 = 6.75, P = 0.03, r

2 = 0.46) (Fig. 3A). In contrast, the number (F1,8 = 0.28, P = 0.61) or average duration (F1,8 = 1.13, P = 0.32) of littoral forays made in the spring was not predicted by spring length. Rather, lake trout made a greater number (F1,8 = 12.22, P < 0.01, r

2 = 0.60) of shorter (F1,8 = 5.24, P = 0.05, r2 = 0.40) forays in springs with higher prey fish den- sities (Fig. S1 A and B). The contrasting effect of number and duration of forays meant that prey fish abundance (measured as catch per unit effort, CPUE) did not alter the total time lake trout spent in the littoral zone during the spring but only how they used that time (F1,8 = 0.00, P = 0.98) (Fig. S1C). The amount of time that lake trout spent in the littoral zone

each summer averaged 43 h and was not predicted by summer length (F1,8 = 0.09, P = 0.77) (Fig. 3B) or prey fish CPUE (F1,8 = 0.01, P = 0.93). The number or average duration of littoral forays made by lake trout in the summer also was not predicted by summer length (log10; number of forays: F1,8 = 0.55, P = 0.48; average foray duration: F1,8 = 2.31, P = 0.17) or prey fish CPUE (log10; number of forays: F1,8 = 0.69, P = 0.43; average foray duration: F1,8 = 0.09, P = 0.78). The mean summer water temperature in the littoral zone also did not predict the time spent by lake trout within the littoral zone during the summer (F1,8 = 0.01, P = 0.92) Fig. S1D or the number of littoral forays (log10; F1,8 = 1.76, P = 0.22). However, lake trout made shorter forays as mean summer littoral zone water temperatures increased (F1,8 = 3.79, P = 0.08, r

2 = 0.32) (Fig. S1 E and F). The time spent within the littoral zone the during summer was not related to the length of the preceding spring (F1,8 = 0.01, P = 0.92). The amount of time that lake trout spent in the littoral zone

each fall averaged 301 h but, unlike spring, was not predicted by fall length (square-root; F1,8 = 1.13, P = 0.32) (Fig. 3C) or prey fish CPUE (square-root; F1,8 = 0.04, P = 0.85). The number or average duration of littoral forays made by lake trout in fall also was not predicted by fall length (number of forays: F1,8 = 3.14, P = 0.12; average foray duration: F1,8 = 0.02, P = 0.90) or prey

Fig. 1. Theoretical illustration of how seasonality in water temperatures during the open-water season impacts foraging behavior of lake trout in small Boreal Shield lakes. (A and B) Cold water temperatures immediately after ice-out in the spring and before ice-on in the fall allow lake trout to access the littoral zone (<6 m depth) without thermal consequence. How- ever, during summer warm littoral temperatures impose an energetic cost to lake trout accessing the littoral zone. Therefore, (B) lake trout should exhibit greater use of littoral habitat and prey (prey fish and benthic invertebrates/ aquatic insects) when springs and falls are longer, and conversely, should use more pelagic habitat and prey (Mysis and zooplankton) when summers are longer. In B, increasing arrow thickness denotes expected increased use of energy pathways based on littoral water temperatures.

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