Behavior of bats at wind turbines

Discussion

Our video observations indicate that many bats passing close (<50 m) to wind turbines with stationary or slow-moving blades during late summer and autumn are attracted to and actively approach them using minimally turbulent air currents, vision, and to some degree echolocation for orientation. In contrast, radar observations indicate that nocturnally migrating vertebrates, presumed to be mostly birds, likely far outnumbered bats in the airspace, yet their near absence from video observations suggests that birds did not interact with turbines in the same way as bats, possibly avoiding them. Furthermore, acoustic detectors pointing upward from the tops of the turbine nacelles regularly detected the calls of bats not observed by video cameras, indicating that some bats passed high in the airspace above the turbines without closely approaching. It remains to be determined what proportion of passing bats approach turbines and whether they might respond to the presence of turbines over greater distances than those we observed with video cameras.

Bats likely can sense and respond to air currents. We saw no preference in the directions from which they approached turbines when the wind was not blowing or was blowing very gently, but bats consistently approached from leeward at wind speeds >1 m/s. The downwind direction of activity only when air was moving suggests that bats know which way the wind blows and approach tall structures in a patterned way that is independent of cardinal direction. As do many animals that move through air (15), bats orient by sensing and responding to flows through which they fly. Bats sometimes commute and forage on the leeward sides of windbreaks, such as tree rows and cliffs, with the postulated benefits of leeward activity including lower risk of predation, favorable conditions for energy-efficient flight, and greater availability of insect prey, particularly during high winds (16, 17). Being able to follow flows can provide substantial selective advantages to animals, particularly when other sensory cues are limited and when important resources can be predictably found within flows (15). It was once believed that bats made their way through darkness with the help of highly sensitive touch receptors in their wings and ears (18), but this concept of landscape orientation received little subsequent attention after the discovery of echolocation (19). Highly evolved hair-cell receptors on the skin surfaces of bat wings recently have been studied in detail; hair receptors in bat wings are now known to play an important role in flight control by sensing minute changes in airflow across the wing surfaces (20). Whether wing receptors help bats to sense subtle patterns of airflow at larger spatial scales is unclear, but Brazilian free-tailed bats (Tadarida brasiliensis) show evidence of orienting through wind currents and exploiting migrating insects concentrated in airflows in the absence of other visual or acoustic cues at high altitudes [up to 3,000 m above ground level (21, 22)]. In light of previous general observations of bat activity in the lee of windbreaks and our observations of consistent leeward bat activity at turbines, we suspect that bats are well adapted for sensing and orienting by airflows at landscape scales and that going with the flow, or against in the case of bats at turbines, may be an underappreciated sensory modality that evolved in these night-flying mammals.

Our thermal video cameras detected bats at turbines more often during periods of night with bright moon illumination and less often during periods with lower levels of moonlight, suggesting that vision plays a role in bats perceiving and approaching wind turbines. Bats rely on vision for long-distance orientation (23⇓–25), are known or suspected to orient through landscapes using light cues, such as stars and postsunset glow (26, 27), and use visual cues to help them find roosts in trees (28). The effects of moonlight on bat activity and fatality at turbines are not well understood, but a study in Alberta, Canada, reported higher fatality rates of silver-haired bats (Lasionycteris noctivagans) at wind turbines on nights when the moon was fully illuminated (29). There is no evidence that tree bat activity in the absence of, or distant from, turbines varies with lunar cycles or illumination (30). Acoustic data gathered on the turbines we monitored, which included many calls from bats passing higher in the airspace than our cameras could image, did not show a trend toward proportionally more activity under moonlit conditions (SI Results), further indicating general activity levels are not influenced by moonlight. The patterns we observed on video could be attributable to the visual conspicuousness of the wind turbines waxing and waning with the moon, affecting the probability of passing bats seeing and moving closer to them to investigate.

Despite our observations that suggest bats orient toward wind turbines using flow and visual cues, the reasons why they do so remain unknown. Although we could not determine why bats behaved the way they did around turbines, we suspect that such behaviors evolved in association with trees. At a fundamental level, tree bats may not be able to discriminate wind turbines from trees (3). Both trees and turbines have tall and cylindrical “trunks” (monopoles), visually conspicuous “crowns” (nacelles), and radially extending “limbs” (blades). Bats are rarely reported interacting or colliding with other tall structures (7), as might be expected if the behaviors we observed were a general response to structural stimuli. However, a recent study revealed higher activity of tree bats during late summer and autumn at tall communication towers compared with surrounding habitats (31). Bats may not have the cognitive ability to differentiate wind turbines or other tree-like structures from real trees either at a distance or at close range, particularly if visual cues, such as similar silhouettes against the night sky, are accompanied, reinforced, or overwhelmed by other perceptual cues, such as similar downwind airflow patterns. For example, the predatory beetle (Rhizophagus grandis) responds to disturbance of airflow around a simulated tree more than the tree’s visual silhouette (32).We do not know if the patterns of behavior we observed apply to cave-roosting species of bats that die at wind turbines [e.g., genera Myotis and Tadarida (6)], but even cave-roosting bats may occasionally visit trees for the reasons discussed below.

Key findings of our study were that wind speed and blade rotation speed influenced the way that bats approached turbines. Bats approached turbines less frequently when their blades were spinning fast and the prevalence of leeward approaches to the nacelle increased with wind speed at turbines with slow-moving or stationary blades. A plausible explanation for these patterns (see SI Discussion for others) is that airflow profiles around tall trees and turbines with stationary blades may be very similar to each other (e.g., oscillating swirling patterns, called a Kármán vortex street), whereas the spinning blades of turbines cause chaotic downwind turbulence (33) that is unlikely to resemble any natural airflow patterns that bats might associate with trees. If tree bats find and orient toward trees by sensing and moving into upstream airflows, turbines may resemble trees only when the blades are moving slowly or are stationary. In other words, airflow paths that bats potentially follow may not be present downwind of turbines with fast-spinning blades. Nighttime flight behaviors of bats around tall trees during late summer and autumn have not been reported, but finding and observing such behaviors if they exist might help explain why tree bats are susceptible to wind turbines.

Compounding the potential for bats to mistake wind turbines for trees is the possibility that they expect important resources when they arrive at the “trees.” Such possible expectations may not apply to concurrently migrating birds, which radar detected in apparently high abundance in the surrounding airspace yet were infrequently observed on video near turbines. Bats may exploit streams of air flowing downwind from trees, turbines, and perhaps other tree-like structures [e.g., communication towers (31)] at night while searching for roosts, conspecifics, and possibly feeding on nocturnal insects that could accumulate in such flows. Many of the hypothesized causes of tree bat susceptibility to turbines involve attraction (8). Our observations are consistent with the possibility that bats are attracted at close distances (<50 m) to turbines with stationary or slow-moving blades, but the potential source of attraction remains unknown. We did not see evidence of close-scale attraction based solely on physical phenomena, such as heat, electromagnetic fields, or sounds generated by specific parts of the turbines, because focal behaviors were dispersed across many different parts of the turbine structure, often involving motionless blades and inert monopoles. A prior study also reported bats focusing attention on monopoles, nacelles, and blades of wind turbines, but no part stood out as attracting disproportionately more bats than others (13). The variety of turbine parts toward which bats focus their attention suggests a general close-range attraction, but the strong leeward component to these varied focal behaviors may offer clues as to what bats might be trying to find.

Resource-based hypotheses of attraction include bats seeking shelter, social opportunities, or food at turbines (3, 8, 9, 13), all of which may occur more often on the leeward sides of tall, tree-like structures. The simplest explanation for bats closely approaching turbines may be that they are seeking places to roost in what they perceive as trees while migrating. We regularly observed hoary bats and eastern red bats (Lasiurus borealis) flying in under the bottom of the leeward nacelle and making close approaches to the recessed exhaust port (Movie S4). Although we did not see clear evidence of bats consistently trying to land on turbines, we frequently observed bats approaching the monopoles very closely, as previously reported (4, 13, 34). The high proportions of close approaches focused on nacelles and monopoles (Table S1) are consistent with bats trying to find places to land. After not finding suitable places to alight upon (e.g., close investigations reveal turbine surfaces too smooth), bats may simply move on.

Bats might also closely approach turbines while looking for social opportunities. Similarities in the social behaviors of tree bats in North America and Europe led to speculation that bats might use the tallest trees in landscapes as flocking or gathering places (35). Tree bats tend to begin mating during the time when most mortality is documented at turbines (36), and bats seeking mates at trees may be drawn toward turbines (37) and other tall structures (31). We observed pairs of bats in 3% of our observations, and in about half of those cases they appeared to be following or chasing each other. In one case we observed two hoary bats in the lee and recorded social calls (Movie S10), but did not see evidence of larger social aggregations that were hypothesized for this species (37). Many species of tree bats in Europe exhibit mating flight displays centered on trees during late summer and autumn, but such flight behaviors have not been reported for any temperate North American bats (37). We speculate that some of the sustained leeward focal behaviors that we observed at turbines in our study, such as repeated looping returns and dives (Movie S2), might be associated with mating displays that could occur at trees. The “upstream orientation” we frequently observed is common in other types of flying and swimming organisms during foraging and mate-searching movements (15).

Bats may be drawn in by insects whose distribution is concentrated around wind turbines. Empirical data demonstrating the consistent presence and aggregation of insects at turbines during the night are lacking, but insects are known to foul turbine blades (38), be attracted to certain turbine paint colors (39), and migrate in large numbers during periods of bat fatality at turbines (40). In addition, bats have been observed foraging near turbines (4, 34) or found dead beneath them with full stomachs (41, 42), highlighting the plausibility of the feeding hypothesis. Although we regularly observed insects in the video imagery, we did not observe the frequent presence of insects with bat detections or record any unambiguous feeding calls of bats at turbines (SI Results), nor did we regularly observe what we would consider typical foraging behaviors of bats during our study. However, this observed lack of insects and typical foraging patterns does not preclude the possibility that bats expected to find insects at the turbines they approached.

There are several general patterns of insect behavior and distribution that give us reason to suspect the leeward behaviors we observed at turbines might be associated with bats expecting insects at the structures as they approached, irrespective of the actual presence of insects. Insects often accumulate on the leeward sides of artificial and natural structures, and behind windbreaks insects tend to increase in number and density with wind speed (43, 44). Many diurnal and crepuscular insects swarm above prominent high points in landscapes during calm conditions and such aggregations often blow leeward in windy conditions (45, 46). Certain nocturnal insects, such as gypsy (Lymantria dispar) and spruce-budworm (Choristoneura spp.) moths, lay eggs in and disperse from the tops of tall trees during late summer and autumn (47, 48). Bats sometimes feed on insects dispersing from trees. For example, Lloyd et al. (49) reported bats feeding on emerging spruce-budworm moths, and Lewis (50) reported eastern red bats feeding on moths in the airflows leeward of human-made structures: “When a moderate, steady wind is blowing over a moth-infested [corn] crib I have seen bats strung out in a narrow belt to a distance of 200 yards or more, catching moths that were carried by the wind.” Given the likelihood of insects accumulating at night above and in the lee of tall trees in natural environments, the leeward focus of bat behaviors at tree-like structures may not be coincidental.

Resource-based attraction hypotheses involving shelter, social opportunities, and food all seem plausible in the light of our results, but gathering direct evidence of such resource use by bats may not be possible at wind turbines or other anthropogenic structures. The roosts, conspecifics, and insect prey that bats might expect at turbines or other tree-like artificial structures would not necessarily have to occur there to draw them in and put them at risk. Bats may be acting upon the expectation of resources rather than the actual presence of resources. Fatalities of bats at turbines may be the consequence of behaviors that evolved to provide selective advantages when elicited by tall trees, but are now maladaptive when elicited by wind turbines. Paradoxically, direct evidence of the causes of tree bat susceptibility to wind turbines may not be observable at wind turbines, but instead at the trees and their associated resources where potentially causal behaviors evolved.

Our observations have practical implications. Although our scope of inference is limited to certain tree bats (L. borealis, L. cinereus, and L. noctivagans), areas of turbines from the rotor-swept zone around the nacelle to near the ground (different behaviors may occur higher in the airspace), and are based on observations from just three turbines in midwestern North America, efforts to monitor bat activity near turbines (e.g., acoustic detectors and video cameras), or deter bats from turbines [e.g., devices producing startling sounds (51)] may benefit by aiming instruments from the back of the nacelle into the leeward airspace, an area where we consistently observed higher bat activity regardless of changing wind directions. Strategies for minimizing fatalities of bats at turbines currently focus on preventing blades from spinning during low wind periods (4, 11, 12). Our observations that tree bats show a tendency to closely investigate inert turbines and sometimes linger for minutes to perhaps hours (in the cases of clustered observations) highlight the plausibility of a scenario in which bats are drawn toward turbines in low winds, but sometimes remain long enough to be put at risk when wind picks up and blades reach higher speeds. Therefore, the frequency of intermittent, blade-spinning wind gusts within such low-wind periods might be an important predictor of fatality risk; fatalities may occur more often when turbine blades are transitioning from potentially attractive (stationary or slow) to lethal (fast) speeds. Efforts to minimize bat fatalities at wind facilities might benefit by averaging wind-speed curtailment thresholds over longer periods of time (e.g., >10 min) to prevent gusts from intermittently pushing blades to lethal speed during low-wind periods. Finally, fatalities may be reducible by altering the appearance of turbines. Fewer fatalities of eastern red bats were found under turbines with flashing red aviation lights at a large wind facility in Texas (52), hinting at the possibility that supplemental lighting of turbines might make some bats less likely to mistake them for trees.