General behavior

Rainbow trout restrict station holding to smaller areas as flow speed increases (Fig. 2), perhaps to avoid more costly exploratory or turning behaviors (Enders and Herrmann, 2003) or to simplify sensory processing in an unfamiliar environment (Liao, 2006). Kármán gaiting fish are the exception and show a decrease in site fidelity, most probably because of the difficulty in holding station in increased turbulence at the highest flow speed.

We conducted experiments in a relatively large respirometer to avoid wall effects, but as a result could not control the percentage of time that a fish would occupy a cylinder region. This introduces the possibility that is inflated at low flow because fish show less fidelity to a given region. For example, at 1.8 L s^–1 fish spend 83% of the time bow waking (and therefore the rest of the time performing other behaviors), whereas at 5.0 L s^–1 fish spend 99% of the time bow waking (Fig. 2). However, measurements of behaviors other than the intended behavior compose a small percentage of the total activity budget and would not be responsible for the similarity of at 1.8 L s^–1 (Fig. 3A). It is more probable that similarity at low flow is due to stability costs given that trimming forces (i.e. the passive production of lift and drag due to flow interactions with the body and fins) play a smaller role at low flow velocity (Webb, 2002).

Energetics hierarchy around a cylinder

To summarize our findings, we introduce the concept of an ‘energetics hierarchy’. We define an energetics hierarchy as an arrangement of oxygen consumption values in which either certain behaviors are more energetically costly than others at the same prescribed flow speed, or in which certain flow speeds are more energetically costly than others for a particular behavior.

The behavioral repertoire of a rainbow trout allows it to adapt to its hydrodynamic environment as flow velocity increases. Otherwise, trout would always swim in the bow wake to the exclusion of other behaviors, because it requires, on average, the least amount of oxygen across speeds (Fig. 4). When is examined for each speed and behavior, values do not simply increase with flow velocity. This is an unexpected result given studies that document the general increase in oxygen consumption with swimming speed (Fig. 5A) (Beamish, 1978; Brett, 1964; Claireaux et al., 2006; Enders, 2003). For behaviors around cylinders, more complex patterns emerge with speed, with minimum for entraining and swimming in the bow wake occurring at two separate flow velocities (Fig. 5C,D). Therefore, our data allow us to reject our first hypothesis and conclude that station-holding behaviors can become less energetically demanding as flow speed increases. Our results expand the growing pool of knowledge on the interactions between fish and turbulence, by demonstrating that can decrease in the presence of periodic or otherwise predictable flows. Indeed, our results are consistent with a similar study in which entraining and Kármán gaiting rainbow trout showed decreased oxygen consumption relative to free stream swimming (Cook and Coughlin, 2010). However, our measurements of were substantially lower than those of Cook and Coughlin (Cook and Coughlin, 2010). One possible explanation for this discrepancy may lie in the variation in interpreting each behavior. Although kinematics have been quantified in detail (Liao et al., 2003a), behaviors are commonly identified on the basis of the position of a fish relative to the cylinder, because different regions around a cylinder have unique hydrodynamic conditions that produce characteristic swimming kinematics. However, kinematics (and therefore oxygen consumption) can change substantially given differences in cylinder shape (i.e. round cylinder vs D-cylinder) or even slight differences in station holding position relative to the cylinder. For example, in fig. 2 of Cook and Coughlin, kinematics for entraining trout show substantially larger lateral displacements (attributed to vortex interactions) compared with the trout in fig. 5A of Liao (Cook and Coughlin, 2010; Liao, 2006). Periodic body oscillations have not been previously observed for entraining fishes (Liao, 2006; Przybilla et al., 2010; Webb, 1998) and would probably increase the oxygen demand. In addition, Cook and Coughlin show Kármán gaiting trout holding position within the suction region, which is approximately two cylinder diameters immediately downstream of the cylinder (Zdravkovich, 1997; Cook and Coughlin, 2010). In our experience, fish located in the suction region actively recruit their pectoral fins to stabilize themselves and avoid contacting the cylinder. The differences in kinematics and fish position probably account for the higher values in Cook and Coughlin's study (Cook and Coughlin, 2010). Nevertheless, taken together these studies clearly discourage using U_crit to evaluate swimming performance in situations where fish commonly encounter turbulent flows.

• Download figure
• Open in new tab
• Download powerpoint

Fig. 5.

(A) Oxygen consumption increases with flow speed when all behaviors are pooled. When the contribution of each behavior to this trend is individually examined, diverse patterns emerge. (B) Fish swimming in the free stream (FS) consume more oxygen as flow speed increases. (C,D) during entraining (EN) and bow waking (BW) varies non-linearly as flow speed increases. Entraining requires the least amount of oxygen at 3.5 L s^–1, whereas bow waking requires the least amount of oxygen at 5.0 L s^–1. (E–G) The same data re-plotted reveal the least energetically costly behavior at each speed. (E) At 1.8 L s^–1, entraining (EN) requires the least oxygen consumption of all behaviors, followed closely by bow waking (BW) and then free stream swimming (FS). (F) At 3.5 L s^–1, bow waking uses 64% of the oxygen required to swim in the free stream. Entraining is the most energetically favorable behavior, using less than a half (38%) of the oxygen requirement of free stream swimming. At the highest flow of 5.0 L s^–1 (G), bow waking fish consume less than a third (29%) of the oxygen required by fish swimming in the free stream. All behaviors are significantly different from each other at P<0.05, with the exception of bow waking and entraining at 1.8 L s^–1 and entraining and bow waking at 3.5 L s^–1 and 5.0 L s^–1, respectively. Data are averaged from three trials for each speed × behavior treatment (N=3 individuals). Values are means ± s.e.m.

The interplay between lift-based propulsion and stability costs is probably what determines the complex patterns of oxygen consumption for station-holding behaviors across speeds. Once speed-dependent vortical flows become sufficiently developed, fish can exploit them with great energetic savings. For example, entraining and bow waking fish only exhibit intermediate values at the lowest flow, suggesting that stability costs may be higher at low flow. As velocity increases, fluid interactions with body and fin posture can generate trimming forces to increase thrust passively and lower stability costs (Webb, 2002; Webb, 2004). In addition, lower values for entraining and bow waking arise from the transition from branchial pumping to ram ventilation, which has been shown to decrease oxygen consumption by 10% in rainbow trout (Steffensen, 1985).

Instances when increases with speed suggest that turbulence contributes to the cost of station holding at low and high flows. This interpretation is supported by the fact that during entraining is most costly at low and high flow, and experiences a minimum at 3.5 L s^–1 (Fig. 5C). At 1.8 L s^–1 the flow is insufficient to fully develop the suction region downstream of the cylinder (Liao, 2004; Zdravkovich, 1997). We suspect that the costs associated with stabilizing movements make it suboptimal for trout to entrain under these circumstances. Fins serve as important control surfaces (Drucker and Lauder, 2003; Liao, 2006; Arnold et al., 1991), and trout use them frequently to maintain stability at low flow (Webb, 1998). We hypothesize that 3.5 L s^–1 is the optimum speed to release entraining fish from stabilization costs associated with low flow, while not requiring larger, more costly corrective movements of the fins and body to negotiate turbulence at 5.0 L s^–1. We speculate that optimum flow with regards to stability is also seen for bow waking fish, which consume more oxygen as flow speed increases up to a point after which the drops (Fig. 5D). We feel certain that future studies subjecting rainbow trout to a wider flow velocity range would identify increased during bow waking as turbulence increases with speed. Thus, along with body length playing a key role in exploiting vortices (Liao et al., 2003a), the selective abilities of fin posture and activity to stabilize the body probably dictate the patterns of across speed.

• Download figure
• Open in new tab
• Download powerpoint

Fig. 6.

Statistical comparison of between Kármán gaiting (KG) and other behaviors at 3.5 L s^–1. Kármán gaiting requires significantly less oxygen than swimming in the free stream (FS; 47%) and bow waking (BW; 73%), but requires more oxygen than entraining (EN; 116%). Kármán gaiting fish use less oxygen (79%) compared with fish swimming in the free stream at 1.8 L s^–1 (asterisk). This supports the original hypothesis that Kármán gaiting fish save energy by exploiting vortices in addition to receiving the benefit of the velocity deficit behind a cylinder (Liao et al., 2003a). Note that the average for FS at 1.8 L s^–1 was not included in the original ANOVA analysis (see text). Values are means ± s.e.m.

Average flow velocity experienced by the head of the fish is not a predictor of oxygen consumption. The pattern across the three prescribed flow speeds (Fig. 5B–D) did not mirror the increasing pattern of absolute flow velocity for each region (Fig. 7). For example, of all behaviors associated with non-oscillatory flow, the absolute flow velocity was lowest for fish swimming in the free stream at 3.5 L s^–1, but showed the highest of all behaviors. Kármán gaiting fish experienced by far the lowest flow velocities of all behaviors at 3.5 L s^–1, and yet still consumed more oxygen than entraining fish (Fig. 6). Therefore, our results suggest that for behaviors associated with stable flows (i.e. entraining and bow waking) around cylinders, velocity gradients dominate the mechanism for holding station and establish a lower than would be expected based on average flow velocity. Low average velocity may contribute to low for Kármán gaiting, but exploiting periodic shedding of vortices provides a distinct additional benefit. It is interesting that even with this benefit Kármán gaiting fish still consume more oxygen than entraining fish. This is possibly the reason for the observation that fish will opt to entrain behind a cylinder over Kármán gait under certain situations (Liao, 2006; Przybilla et al., 2010; Webb, 1998).

• Download figure
• Open in new tab
• Download powerpoint

Fig. 7.

Bar graph showing the average flow velocity at the head of the fish for each of the four behaviors at each of the three prescribed speeds. The average velocity at the tail was also measured for bow waking fish (BWTail). Note that the only reliable measurement for Kármán gaiting occurred at 3.5 L s^–1 (see text), but results from all three prescribed speeds are included.

Do trout always prioritize saving energy?

Why do fish not choose the most energetically favorable behavior at each flow speed? Fish motivated by saving energy should entrain at low and middle speeds, but then switch to bow waking at the highest flow speed. Yet we did not always observe this behavioral pattern. One explanation is that the greater risk of instability (and thus more energy expended from forfeiting and recovering position) during a behavior may be just as important in selecting a position near a cylinder as is the actual cost of the behavior. For example, fish may bow wake at 3.5 L s^–1 even though it requires more oxygen than entraining because the risk of forfeiting position from flow instabilities is less than the control costs associated with recovering position after being displaced from entraining (Liao, 2006). This lower-risk, lower-payoff strategy is consistent with our observations of rainbow trout choosing bow waking and Kármán gaiting over entraining at an intermediate flow speed. Another possibility is that the cost of station holding is outweighed by the benefits of maintaining an optimal state of sensory awareness. Bow waking offers the least-obstructed visual field of all behaviors near cylinders as well as the simplest hydrodynamic environment for the lateral line, and thus would seem to enable the most rapid response to avoiding predators or capturing prey. Still, fish that Kármán gait at 5.0 L s^–1 will explore the bow wake (which is less energetically demanding) but return to Kármán gaiting (Fig. 2), indicating that other important factors have not been described that influence the decision to hold station in specific cylinder regions. By documenting an energetics hierarchy across behavior and flow speed, we provide a baseline to be able to evaluate the importance of these factors in the future.

Kinematics correlates to oxygen consumption

Trout swimming in different hydrodynamic regions around a cylinder can show kinematic similarities to one another. Bow waking kinematics at low to middle speeds resemble free stream swimming (Liao et al., 2003a). This reflects the observation that average flow velocity experienced by the head is the same as that for fish swimming in the free stream flow. Periodic tail beating is present, but tail beat amplitudes are greatly reduced given that the tail is located in the stagnation point just upstream of the cylinder and experiences little to no flow (i.e. the flow can be less than 50% of that at the head; Fig. 7). At 5.0 L s^–1 the stagnation region develops to enable bow waking fish to stop regular tail beat motions and adopt a straight body posture with few corrective movements from the pectoral fins. A rainbow trout positioned in the bow wake experiences a high-pressure region by the tail that allows it to balance in front of the cylinder. Another interpretation is that a suction force is drawing the head upstream, in so much as the steep upstream–downstream velocity gradient within the distance of one body length establishes differential pressure across the body. We think this mechanism allows trout to drastically reduce their energetic requirements for holding station in fast flows, as seen in cetaceans riding in the bow wake of ships (Bose and Lien, 1990; Fejer, 1960; Scholander, 1959). A previous paper suggested, based on kinematics, that rainbow trout swimming in the bow wake may use less energy than swimming in the free stream or Kármán gaiting (Liao et al., 2003a). This idea is now directly supported by our experimental measurements; metabolic costs of bow waking are lowest at 5.0 L s^–1 when the velocity difference between the head and the tail are the greatest. Therefore, even though the flow velocity experienced by the head may be similar between fish swimming in the bow wake and free stream, bow waking is much less costly to perform. In this regard, traditional point source measurements of flow velocity in the field (Fausch and White, 1981; Heggenes, 1988) can fail to reveal hydrodynamic habitats that have important energetic consequences to station-holding trout.

Entraining fish exploit a steep velocity gradient established by the formation of a suction region immediately downstream of the cylinder (Zdravkovich, 1997). By tilting the body relative to the axis of free stream flow (Liao, 2006), trout use their body as an airfoil to hold station. This mechanism was recently elucidated by modeling the hydrodynamic forces that are exerted on a rainbow trout during entraining (Przybilla et al., 2010). These investigations revealed that for trout to hold station, an outward (i.e. away from the cylinder) lift force is counteracted by an inward suction force, drawing the body towards the cylinder. When these forces become imbalanced, corrective motions of the pectoral and caudal fins are initiated. We found that the cost of these corrective movements increased dramatically at the highest flow speed, and, like Przybilla et al., attribute this cost to an increase in turbulence (Przybilla et al., 2010). During the course of our experiments we found that bow waking behavior at 5.0 L s^–1 is very similar to entraining at 3.5 L s^–1 in that they both involve a remarkable absence of body undulation. Not surprisingly, the for these two treatments is almost identical (Fig. 5F,G). This observation suggests that it is possible that relative swimming costs may be more accurately predicted from kinematics than from average flow velocity under certain circumstances (Fig.7). The importance of developing a non-invasive method for measuring the energetics of swimming in natural populations (Farrell et al., 2003) makes this a potentially useful tool for estimating swimming costs in the field.

Behavior reveals an energetics minimum

The observation that rainbow trout will Kármán gait continuously for several hours at 3.5 L s^–1 (but not at 1.8 L s^–1 or 5.0 L s^–1) in itself may indicate that the minimum cost for this behavior occurs at intermediate flow speeds. Rainbow trout do not Kármán gait at 1.8 L s^–1 because the vortex street has not developed sufficiently (Liao, 2004) (Fig. 2). At higher Reynolds numbers, flow instabilities are magnified, where merging and pairing between initial shear layer vortices give rise to secondary structures that contribute to irregular vortex shedding frequencies and amplitudes (Blevins, 1990; Williamson, 1996). We hypothesize that rainbow trout cannot sustain Kármán gaiting at 5.0 L s^–1 because the turbulent vortex street exceeds the stabilization abilities of the fish, as evidenced by their ability to Kármán gait at 3.5 L s^–1 but their frequent impingement on the downstream baffle at 5.0 L s^–1. We fully expect that if fish were forced to Kármán gait continuously for several hours at 1.8 L s^–1 and 5.0 L s^–1 then values would be higher than those observed at 3.5 L s^–1.

Do rainbow trout benefit from vortices in addition to a velocity deficit behind a cylinder?

Of all the cylinder station-holding behaviors we know the most about the Kármán gait, from previous work (Liao et al., 2003a; Liao et al., 2003b). Kármán gaiting consists of sensing and moving with the lateral component of the sinusoidal flow established by vortices shed downstream from a cylinder (Liao, 2006). Although Kármán gaiting has a large passive component (Beal et al., 2006), rainbow trout do activate anterior red axial muscle (Liao, 2004). Detailed kinematic measurements suggest that fish use their body to establish thrust by interacting with oncoming vortices in addition to experiencing the benefits of being positioned in a reduced velocity zone (Liao et al., 2003a; Streitlien and Triantafyllou, 1996). Although electromyograms reveal fewer regions of red muscle activity compared with free stream swimming at a comparable reduced velocity, we cannot directly evaluate the magnitude of muscle activity between the two behaviors because of differences in resistance across electrodes (Loeb and Gans, 1986). A more consistent measurement of activity is needed to better understand the cost of Kármán gaiting. Although the oscillating body of a Kármán gaiting trout might be expected to require more corrective body and fin motions than when holding station in stable flows (i.e. bow waking and entraining), our results suggest that this cost is offset by the benefits of vortex exploitation (Fig. 6). The cost of Kármán gaiting at 3.5 L s^–1 should be similar to free stream swimming at a flow equal to the cylinder's velocity defect (i.e. 1.8 L s^–1), but it is in fact lower. Our data provide the first direct evidence that Kármán gaiting rainbow trout save energy beyond that of simply swimming in the velocity deficit behind a cylinder, confirming that trout are able to recapture energy from cylinder vortices. Based on previous work, this indicates that it is more costly to activate red muscle in the posterior half of the body during free stream swimming than it is to activate anterior red muscle activity during Kármán gaiting (Liao, 2004). This is significant because although exploiting self-generated vortices has been championed as a mechanism to increase efficiency of locomotion in a diversity of animals (Dickinson et al., 1999; Drucker and Lauder, 2005; Triantafyllou et al., 2000) these data illustrate how exploiting environmentally generated vortices can lead to potentially larger savings in the cost of locomotion.

Ecological implications

The mechanisms of how fish relate to structures in flow have important ecological implications. For example, body length is the most important factor in determining the optimal cylinder diameter that enables Kármán gaiting (Liao et al., 2003a), implying that fish in nature best exploit habitats that scale to their body size. Matching vortex orientation to the axis of undulation is crucial to enable station holding (Tritico and Cotel, 2010; Webb, 1998), suggesting that fish can only use flows created from structures of certain shapes and orientations in the water column. This study expands our understanding by looking at the energetics of station holding in multiple regions around a cylinder. A key finding is that even within a single size class and flow velocity, rainbow trout have substantially different oxygen demands depending on which locations they choose to hold station around a cylinder. Similarly, different behaviors can have similar costs when surveyed across different flow velocities. For example, entraining at 3.5 L s^–1 requires the same amount of oxygen as bow waking at 5.0 L s^–1. Bow waking at 3.5 L s^–1 is very similar to free stream at 1.8 L s^–1. What this means in a river with temporal and spatial velocity gradients is that fish can maintain constant energy expenditure by choosing different hydrodynamic microhabitats. Likewise, a Kármán gaiting fish located in turbulent flows off a main stream channel may actually be using less energy than a fish swimming in slower free stream flow near the bank. Therefore, without more detailed measurements of fish position, kinematics and local hydraulics, we cannot assume fish holding station in faster flow are exerting more energy than fish in slower flow. The interactions between flow speed and behavior exposes a complexity previously undocumented when considering the effects of turbulence on fish distributions and swimming costs in the natural environment.