One of the major challenges for hydropower operators is determining how to reduce the number of fish that are displaced from reservoirs to downstream waters through turbine intakes—a process termed entrainment [1, 2]. Entrainment can cause immediate fish mortality in a variety of ways (for example, strike, cavitation, pressure changes [3]) or delayed mortality due to injury and increased susceptibility to predation [1]. In some jurisdictions, there are regulations and guidelines that help reduce entrainment and the impacts that it can have on the abundance of fish populations. For example, resource agencies in the United States have set survival standards for salmonids migrating downstream through hydroelectric facilities in the Columbia River [4]. In Canada, the Fisheries Act prohibits any activity that causes serious harm to fish that are part of, or support, a fishery [5], and national guidelines for managing fish entrainment through turbines and other types of water intake structures are currently in development [6].

Currently, most of the efforts to quantify and reduce entrainment in hydropower facilities have focused on downstream migrating fishes, particularly diadromous species [7–9]. Detailed studies on the behavior of migrants as they enter the forebay (the area directly upstream of the dam) and approach the hydropower facility have informed the design and refinement of guidance systems to direct fish away from turbine intakes and into bypass structures [7, 10]. However, because migrants use the water flow as a cue to move past dams [11], knowledge of the movement behavior of downstream migrating fishes has very limited application for understanding and mitigating entrainment of resident fishes (that is, those that do not actively emigrate from reservoirs).

Resident fish can be accidentally entrained in hydropower facilities when using habitats near turbine intakes [11]. Indeed, many technical reports available through hydropower companies and regulatory agencies indicate variable levels of entrainment of resident fish [12–14]. Resident juvenile fish are particularly vulnerable to entrainment [11], but observed rates of entrainment appear to have little impact on populations due to the usual high abundance of juveniles [14]. Entrainment of resident adult fish has the potential for a greater impact on populations because even relatively low levels of entrainment of large, highly fecund females can reduce population growth and long-term viability, particularly in late-maturing species [15]. Important recreational and aboriginal fishery resources in many reservoirs of North America rely on such late-maturing species (for example, walleye, Sander vitreus; burbot, Lota lota; bull trout Salvelinus confluentus), making efforts to reduce entrainment of adult resident fish a crucial factor for future sustainability. Detailed knowledge of adult resident fish behavior near turbine intakes therefore can help regulators and hydropower operators to identify and implement approaches to reduce entrainment.

In this study, we investigated fine-scale behavior associated with entrainment risk of adult resident fish in a large hydropower reservoir (Kinbasket Reservoir, British Columbia, Canada, Figure 1). We focused on bull trout (Salvelinus confluentus), which is a char native to western Canada and the northwestern United States. Bull trout inhabit cold-water rivers, lakes and reservoirs and exhibit a range of life history forms (resident, fluvial, adfluvial and anadromous) [16]. The species remains active even in water temperatures below 2°C, possesses low thermal optima for growth and is highly sensitive to warm water temperature [17, 18]. As a result of climate change, overfishing and habitat loss, as well as fragmentation and degradation, a number of bull trout populations have been listed as threatened in the United States and designated as of special concern or threatened in three of five biogeographic populations in Canada [19, 20]. Reservoir populations of bull trout are further impacted by entrainment losses of adults, which occur mostly in the fall and winter and at annual rates ranging from 3.5% to 11.3% [21–23]. Seasonality in entrainment risk is most likely associated with temporal changes in physical (for example, turbine operations, water temperature) and biological (for example, prey distribution) factors affecting behavior and forebay use [11, 23].

We applied state-space models to fine-scale acoustic telemetry data to estimate true positions, depth, body temperature and behavioral states of adult bull trout. The resulting estimates were used to investigate the relationship between adult bull trout behavior in the forebay of Kinbasket Reservoir and putative factors influencing their behavior. Behavior was characterized in terms of bull trout residence time and spatial distribution in the forebay, distance to the intakes and two behavioral states based on movement patterns: transiting (fast, directed movement) and exploratory (slow, undirected movement) [24, 25]. Specifically, our objectives were to investigate (1) temporal (diel and seasonal) patterns in bull trout behavior; (2) the association between bull trout behavior and physical (that is, turbine operations, reservoir water elevation) and biological (that is, body temperature) factors; and (3) the behavior of fish preceding their entrainment (should entrainment be observed). We synthesized our results to develop an overall characterization of adult bull trout behavior in relation to entrainment risk.

A total of 85 bull trout were tagged, but only 25 individuals were detected in the forebay for a minimum of 30 minutes (see Methods). Twenty-two of these 25 individuals were detected in only one season, and the remaining three individuals were detected in two seasons. State-space model estimates were obtained for a similar number of individuals across seasons: six individuals in the summer, seven in the fall, seven in the winter and eight in the spring (see examples in Figure 2). However, the total number of positions varied markedly among seasons; they were highest in the winter (8,343, or 51.6% of the total number of 16,184 positions), followed by the fall (5,625, or 34.8%), summer (1,505, or 9.3%) and spring (711, or 4.4%). The median residence time of bull trout in the forebay was 6.3 hours (min–max = 0.6–114.9 hours) in the winter, 2.7 hours (min–max: 1.8–77.8 hours) in the fall, 1.3 hours (min–max: 0.7 - 16.9 hours) in the summer and 0.7 hours (min–max: 0.5–4.7 hours) in the spring.The estimated utilization distributions revealed a marked seasonal pattern of space use within the monitored forebay area. In the spring and summer, bull trout used areas away from the powerhouse more intensively, as indicated by the location of the 50% utilization distribution (Figure 3a and b). In the fall, their 50% utilization distribution extended to the powerhouse (Figure 3c) and was located immediately adjacent to it in the winter (Figure 3d).

Model selection indicated strong support for the relationship between mean three-dimensional distance between fish locations and intakes (D _int ) and season (Table 1). Bull trout were typically 57 to 99 m closer to the intakes in the winter than in any of the other seasons (Figure 4a and b). Visual inspection of the D _int time series for each track and the fish trajectories indicated that none of the tagged bull trout were entrained (data not shown), with the shortest distance estimated between bull trout and intakes being 23 m and occurring in the winter.

Model	AIC c	ΔAIC c	wAIC c	log(L)	K
ssn + f(tdy)	11,447.46	0.00	0.65	-5,712.62	11
ssn	11,449.19	1.73	0.27	-5,714.50	10
f(tdy) + dsg + rel	11,453.59	6.13	0.03	-5,716.70	10
dsg + rel	11,454.28	6.81	0.02	-5,718.06	9
f(tdy) + dsg	11,455.11	7.65	0.01	-5,718.48	9
dsg	11,456.62	9.16	0.01	-5,720.25	8
f(tdy) + rel	11,462.25	14.79	0.00	-5,722.05	9
f(tdy)	11,462.54	15.08	0.00	-5,723.21	8
rel	11,466.54	19.07	0.00	-5,725.21	8
No fixed effects	11,467.82	20.36	0.00	-5,726.86	7

^aAIC _c , Bias-corrected Akaike Information Criterion; ΔAIC _c , Difference in bias-corrected Akaike Information Criterion between a given model and the top-ranked model; dsg, Operational discharge; f, Smoothing function; K, Number of parameters in the models; log(L), Log-likelihood of the models; rel, Reservoir elevation; ssn, Season; tdy, Time of day; wAIC _c , Weight bias-corrected Akaike Information Criterion. All models include fish ID as a random effect. Models are ranked by increasing order of the AIC _c value.

Model selection also supported the relationship between D _int and time of day (Table 1). However, D _int varied by only 20 m over the diel cycle, with slightly reduced D _int values occurring between 13:00 and 24:00 (Figure 4c and d). The marginal and conditional R² values for the D _int models with ΔAIC _c <2 ranged from 0.22 to 0.23 and 0.31 to 0.32, respectively. None of the models with ΔAIC _c <2 included operational discharge or reservoir elevation (Table 1).

The estimated probability of being in the exploratory state (P _exp ) progressively increased from spring to winter and was less variable during the winter than in any of the other seasons (Figure 5a). Model selection, however, did not support the relationship between season and P _exp (Table 2). The top-ranked model included only body temperature as a predictor of P _exp (Table 2). Bull trout were much less likely to be in the exploratory state when their body temperature was around 6°C, with P _exp increasing rapidly when body temperature trended toward lower and higher values (Figure 5b and c). Model selection also supported the relationship between P _exp and time of day (Table 2). Bull trout were less likely to be in the exploratory state around 10:00 and slightly more likely to be in the exploratory state between 14:00 and 04:00 (Figure 5d and e).

The marginal and conditional R² values for the P _exp models with ΔAIC _c <2 ranged from only 0.04 to 0.05 and 0.15 to 0.16, respectively. None of the models with ΔAIC _c <2 included operational discharge or season (Table 2). Although the model including body temperature and operational discharge had a ΔAIC _c value of virtually 2, the effect of operational discharge was not supported, as its addition resulted in negligible improvement of the model’s log-likelihood compared to the model including only body temperature (Table 2).

Our findings revealed marked seasonal changes in adult bull trout behavior in the forebay of Kinbasket Reservoir, which helps to explain the increased entrainment rates in the fall and winter observed previously [23]. Specifically, we observed increased residence time (see also [23]) and proximity to intakes in the fall and particularly in the winter, as well as slow, undirected movement in the forebay when body temperatures were low (mostly in the winter). Although turbine operations are maximized during the fall and winter at Mica Dam [26], we did not find any evidence that operational discharge directly influenced adult bull trout behavior in the forebay. This indicates that other factors related to seasons may be associated with the seasonality observed in bull trout behavior.

The forebay of hydropower reservoirs may have high food density for adult bull trout during the late fall and winter. Indeed, kokanee (nonanadromous form of Oncorhynchus nerka), one of the main prey for overwintering bull trout [27], congregate near the dams of some hydropower reservoirs in the winter [28, 29]. In Revelstoke Reservoir (British Columbia, Canada), the density of kokanee near the dam increases particularly during periods of prolonged turbine operation in the winter, possibly due to advection [29]. Furthermore, kokanee usually occur in habitats with high light intensity during the winter [30, 31]. Relatively high light intensity may occur near the powerhouse of hydropower reservoirs in the late fall and winter due to the effect of turbine-induced flows in preventing or inhibiting formation of thick ice cover.

Our finding that P _exp increased with decreasing body temperatures provides additional indirect evidence that bull trout may forage near the powerhouse in the late fall and winter. The exploratory behavior is defined by slow movements and frequent turns, which are characteristic movement patterns of animals conducting area-restricted search and foraging [24, 32]. Furthermore, the restricted movement of bull trout near the powerhouse is consistent with a sit-and-wait foraging strategy for capturing invertebrates and fish moving with the direction of turbine-induced flows—a behavior similar to that observed in stream-dwelling salmonids (for example, [33, 34]). Such a sit-and-wait behavior was observed in adult bull trout preying on sockeye salmon smolts migrating past counting fences in the Chilko River, British Columbia, Canada (N Furey, University of British Columbia, personal communication).

The relationship between P _exp and body temperature in bull trout may also reflect the bell-shaped thermal dependency of aerobic scope for activity in fishes [35], though the exact relationship between aerobic scope and temperature has not yet been examined in bull trout. However, on the basis of the identified relationship between P _exp and body temperatures, it is possible that aerobic scope to sustain fast movements (that is, relatively low P _exp ) is highest around 6°C and decreases as body temperature trends toward 0°C or 12°C, leading to a reduction in swim speeds (that is, relatively high P _exp ). Alternatively, the increased P _exp toward 12°C may be related to a reduction in activity that would facilitate food assimilation and growth at warmer temperatures [36–38].

We also found that bull trout behavior varied slightly on a diel basis. Although diel patterns in activity should be expected to vary seasonally due to changes in the photoperiod [39], we could not evaluate interactions between time of day and season on D _int and P _exp (see Methods). However, because the majority of our data were recorded in the fall and winter, we believe that the uncovered diel patterns are more representative of bull trout activity in these seasons. The small variation (about 20 m) in D _int over the day may be partly associated with bull trout diel vertical migration, which occurs throughout most of the year, including the fall and winter [40]. Bull trout diel vertical migration in winter has been attributed to foraging for kokanee [40], which also exhibit diel vertical migration in that season [31].

Our finding that P _exp was higher over most of the night hours (corresponding to fall and winter) may indicate a reduction in bull trout activity when it is dark. However, as mentioned above, the exploratory state may also indicate foraging behavior. Interestingly, the increase in P _exp at night coincides with the time that both kokanee and bull trout are located in shallow water [40, 41]. Indeed, diel activity of fishes is linked to the activity of their prey [39], and studies conducted on stream-dwelling bull trout during periods of cold water temperature (late fall to early spring) have shown that individuals emerge from cover at night and feed in the dark ([42, 43] and N Furey, University of British Columbia, personal communication).

Although we were able to detect relationships between bull trout D _int and P _exp and time of day, season and body temperature, a large proportion of the variability in our data (as measured by conditional R ² ) could not be explained by our predictor variables and individual random effects, particularly in the P _exp model. The low ability of our models to explain the variability in the data is partly related to the stochastic component that underlies animal movements [44]. Furthermore, animal movement results from complex interactions between an individual’s internal state and environmental conditions [45], which can change at fine spatiotemporal scales. For example, turbine operations generate complex water flows over three-dimensional space in the forebay of hydropower reservoirs [46]. It is possible that bull trout moving in such an environment respond to fine spatiotemporal changes in flow properties (for example, velocity, turbulence, flow direction) that are not detected by relating behavior to total operational discharge. Indeed, the spatiotemporal variability in the characteristics of water and air flow helps to explain the trajectory of animals moving in fluids, though most work done to date has been focused on migrating animals [10, 47, 48].

We did not detect bull trout approaching or moving into the intakes in this study, though adult bull trout entrainment is known to occur through Mica Dam in the fall and winter [23]. The closest distance we detected bull trout from an intake was 23 m—a distance where water velocities are <0.2 m/s during turbine operations [49]. We do not consider these velocities challenging for adult bull trout, because even juvenile bull trout (11 to 19 cm) have mean critical swimming speeds >0.48 m/s and critical swim speed is positively correlated with body length [50]. Bull trout may have avoided approaching the flow field near the turbine intakes of Mica Dam, but we cannot exclude the possibility that our telemetry system was unable to position fish at distances <23 m from the intakes during turbine operations. Evidence for this was observed in our assessment of the telemetry system performance in positioning the receiver beacon tags (Additional file 1). During the fall and winter, the median efficiency of the telemetry system in positioning the receiver beacon tags located on the powerhouse wall was nearly 0%, with efficiency decreasing with total operational discharge. In contrast, median efficiency in the fall and winter was 16% and 73%, respectively, for the receiver beacon tag located about 275 m from the powerhouse and did not decrease with increases in operational discharge. The low efficiency in positioning the receiver beacon tags, and possibly fish, near the intakes during turbine operations may be related to reduced propagation and/or integrity of the acoustic signal in the accelerating flow field close to the intakes [51].

Our findings indicate that increased entrainment risk of adult bull trout in the fall and winter is related to a combination of maximization of turbine operations in these seasons with concomitant changes in behavioral attributes, such as increased residence and proximity of bull trout to the intakes (presumably for foraging on kokanee) and reduced movement (perhaps limiting escape responses to accelerating water flow) during periods of cold water temperatures. Therefore, it would be prudent to explore mitigation measures, such as operating deterrent devices (for example, strobe lights, sound, screens), to prevent bull trout from approaching and becoming entrained at hydropower intakes during the fall and winter. These approaches would likely benefit other resident fishes (for example, kokanee) at risk of and impacted by entrainment, but would be especially important for bull trout, given that the viability of their populations can be substantially reduced by losses of adults [16, 52]. The results of this study also show how acoustic telemetry and state-space models can be combined to understand and categorize fish behavior in reservoirs and, more generally, in other environments with fluctuating water levels.