Wind Farms Have Cascading Impacts on Ecosystems Across Trophic Levels

BRIEF COMMUNICATION https://doi.org/10.1038/s41559-018-0707-z Wind farms have cascading impacts on ecosystems across trophic levels Maria Thaker 1,3*, Amod Zambre 1,2,3 and Harshal Bhosale1 Wind farms are a cleaner alternative to fossil fuels for miti- Many studies have demonstrated reduced avian density in areas gating the effects of climate change, but they also have com- with wind turbines22–26, but this in itself would not affect lower tro- plex ecological consequences. In the biodiversity hotspot of phic levels unless there is a concomitant decrease in predation pres- the Western Ghats in India, we find that wind farms reduce sure for prey. Raptors regularly prey on small terrestrial vertebrates the abundance and activity of predatory birds (for example, and are among the most important diurnal lizard predators in this Buteo, Butastur and Elanus species), which consequently landscape. We found that both the abundance of predatory birds increases the density of lizards, Sarada superba. The cas- (Z = − 13.91, P < 0.001, Cohen’s d = 0.84; Fig. 1d) and the frequency cading effects of wind turbines on lizards include changes in of predation attempts (dive attacks) by raptors on ground-dwelling behaviour, physiology and morphology that reflect a combi- prey (Z = − 4.45, P < 0.001, Cohen’s d = 0.29; Fig. 1e) were almost nation of predator release and density-dependent competi- four times lower in sites with wind turbines than those without. tion. By adding an effective trophic level to the top of food As expected from reduced predation pressure, the density of the webs, we find that wind farms have emerging impacts that most dominant terrestrial vertebrate species in this ecosystem, the are greatly underestimated. There is thus a strong need for an endemic superb fan-throated lizard Sarada superba (Fig. 1c) was ecosystem-wide view when aligning green-energy goals with significantly higher in sites with wind turbines compared with those environment protection. without (Z = 8.93, P < 0.001, Cohen’s d = 0.48; Fig. 1f). Wind energy is the fastest-growing renewable energy sector in However, predation is a strong selective force and terrestrial liz- the world, with current capacity estimates at ~500,000 MW per year ards in sites with wind turbines showed differences in physiology, (4% of global energy demand)1,2. With land requirement of as high behaviour and even morphology that were consistent with the non- as 34 hectares MW−1, close to 17 million hectares of land is currently consumptive effects of predator release14,17,18. Signatures of reduced used for wind energy generation worldwide3. Despite the benefits predation pressure in sites with wind turbines compared with of this renewable energy production, wind farms have ecological those without were detected in the lower stress-induced (t = − 2.61, costs4. Wind turbines cause high mortality in birds and bats from P = 0.05, Cohen’s d = 0.43) but not baseline (t = − 0.76, P = 0.48) lev- direct impacts5,6, impede bird migration routes7, and reduce the els of circulating corticosterone in free-ranging S. superba (Fig. 2a). density and activity of terrestrial mammals8,9. It is often assumed Physiological stress coping strategies, especially those mediated by that the greatest impacts of wind turbines are restricted to volant the steroid hormone corticosterone, are sensitive to changes in pre- species9, resulting in significant reduction in local population den- dation pressure and play a vital role in influencing energy mobi- sity (but see ref. 10). Here, we show that the effects of wind turbines lization, as well as behavioural and cognitive processes27. In some are much larger and are akin to adding an apex predator to natural terrestrial mammals, proximity to wind turbines causes an increase communities. By reducing the activity of predatory birds in the area, in glucocorticoid levels9,28, presumably because of the stress and wind turbines effectively create a predation-free environment that interference induced by mechanical noise and infrasound. In con- causes a cascade of effects on a lower trophic level. trast with these findings, the downregulation of the hypothalamus– Predator-induced trophic cascades are most apparent in eco- pituitary–adrenal axis for stress reactivity, but not homoeostatic systems where top predators are removed or added, and are often processes, in lizards from sites with wind turbines, is a good indica- driven by numerical changes in predator densities11. Changing tor of habituation to an environment with fewer intense (predation) predation pressure can affect the local density of prey through stressors15. In response to controlled simulated ‘predator attacks’ by direct consumption12,13, but predation risk can also cause non- an approaching human, lizards at sites with wind turbines showed consumptive effects by altering the behaviour, physiology and significantly lower approach distances (Z = − 5.41, P < 0.001, Cohen’s morphology of prey that survive14–18. Our study area—the lat- d = 0.12) and flight initiation distances (FIDs) compared with those eritic plateaus in the Western Ghats of India—is ecologically without (Z = − 5.86, P < 0.001, Cohen’s d = 0.52). Lizards from sites unique, with high endemism in flora and fauna19. Wind farms with wind turbines had FIDs that were five times shorter than those here have been functioning for 16–20 years20. To detect legacy from sites without, allowing researchers to approach within 3 m effects of wind farms on small vertebrates, we used a space-for- before fleeing (Fig. 2b). This reduction in the escape responsiveness time substitution21 and compared areas with and without wind of lizards in areas with wind turbines directly follows expectations turbines on the same plateau (Supplementary Fig. 1). Apart from from the low stress-induced levels of corticosterone29,30. The study the presence or absence of wind turbines, the habitats of sites plateau is used for various anthropogenic activities besides clean with (n = 3; ~0.5 km2 each) and without wind turbines (n = 3; energy production; local communities graze livestock and extract ~0.5 km2 each) were indistinguishable (Supplementary Figs. 2 non-timber resources. Despite the prevalent human activity in the and 3, and Fig. 1a,b). area, lizards showed relaxed physiological stress responses and 1Centre for Ecological Sciences, Indian Institute of Science, Bengaluru, India. 2Present address: Department of Ecology, Evolution, and Behavior, University of Minnesota, Saint Paul, MN, USA. 3These authors contributed equally: Maria Thaker, Amod Zambre. *e-mail: [email protected] NatURE ECOLOGY & EVOLUTION | www.nature.com/natecolevol BRIEF COMMUNICATION NATURE ECOLOGY & EVOLUTION a d 30 20 10 Predatory bird abundance 0 b e 5 4 3 2 1 Raptor attack frequency Raptor attack 0 c f 20 15 10 Lizard density 5 0 Wind turbines No wind turbines Fig. 1 | Numerical effect of wind turbines on predatory birds and lizard prey. a,b, Lateritic habitat on the Chalkewadi plateau (a) with (n = 3 sites) and (b) without wind turbines (n = 3 sites). c, The endemic superb fan-throated lizard S. superba, which lives on the Chalkewadi plateau. d–f, Areas with wind turbines (red box plots) had (d) a significantly lower abundance of predatory birds (birds per 3 h), (e) a significantly lower frequency of raptor attacks on ground-dwelling prey (attacks per 3 h) and (f) significantly higher densities of lizards (lizards per 100 m belt transect) compared with areas with no wind turbines (blue box plots). Box plots show the medians, quartiles, 5th and 95th percentiles, and outliers. anti-predator responses in sites with wind turbines, consistent with dewlaps, which are used during inter- and intrasexual communi- the perception of lower predation pressure. cation34. We found that males from sites with wind turbines had The numerical effects on prey density, as well as shifts in the lower chroma and brightness of the blue (chroma: t = − 3.995, physiological and behavioural responses to stressors in lizards from P = 0.01, Cohen’s d = 0.32; brightness: t = − 3.40, P = 0.02, Cohen’s sites with wind turbines, are typical effects of predator release on d = 0.23) and orange (chroma: t = − 2.23, P < 0.001, Cohen’s d = 0.30; prey in many ecosystems31. However, prey can also experience indi- brightness: t = − 5.40, P < 0.001, Cohen’s d = 0.30) patches on their rect effects of reduced predation pressure mediated through other dewlap compared with those from sites without wind turbines regulatory mechanisms. Lower predation risk allows for greater (Supplementary Fig. 4). The intensity of colours is a signal of indi- foraging opportunities by prey, which can enhance prey growth32. vidual quality in many taxa35; thus, a reduction in the chroma and However, we found the opposite pattern; free-ranging S. superba brightness of colours in males from areas with wind turbines can from sites with wind turbines had lower body condition (that is, they have consequences for sexual selection in this population. Sexual were thinner) than those at sites without (scaled body mass index; ornamentation is known to be enhanced when predation risk t = 24.5, P < 0.001, Cohen’s d = 0.22; Fig. 2c). Although we found no decreases36 and sexual selection increases37. Instead, we found that differences in habitat or substrate structure, areas with wind tur- density-dependent competition was a high cost of predator release. bines may still have lower per-capita food availability (arthropods) High lizard densities under low avian predation risk resulted in because of the higher local lizard densities33, thereby reducing the greater competition for potentially limiting resources (for example, body condition of individuals. beetles with high carotenoid content) that are needed to develop Notably, these density-dependent effects in areas with wind enhanced ornamentation.

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