Barotrauma is a significant cause of bat fatalities at wind turbines

Magazine R695 analogous to forward and backward collected hoary (Lasiurus cinereus) mutation at the individual level; and Correspondences and silver-haired bats (Lasionycteris the intensity of selection for other noctivagans) killed at a wind energy traits such as oogamy that may cause facility in south-western Alberta, uniparental inheritance secondarily. Barotrauma is a Canada, and examined them for None of these parameters is known for any organism. significant cause of external and internal injuries. Of 188 bats killed at turbines the In fact, all of these factors must bat fatalities at wind previous night, 87 had no external be considered in order to achieve a injury that would have been fatal, complete explanation for the relative turbines for example broken wings or frequencies of uniparental and lacerations (Table 1). Of 75 fresh biparental inheritance of organelle Erin F. Baerwald, Genevieve H. bats we necropsied in the field, 32 genes. Moreover, the explanation must D’Amours, Brandon J. Klug and had obvious external injuries, but 69 be sought in a phylogenetic context Robert M.R. Barclay had haemorrhaging in the thoracic in which the ancestral state of the and/or abdominal cavities (Table 1). organisms can be reconstructed. It Bird fatalities at some wind energy Twenty-six (34%) individuals had may be more fruitful to analyze the facilities around the world have internal haemorrhaging and external evolution of mechanisms of uniparental been documented for decades, injuries, whereas 43 (57%) had inheritance (organelle exclusion from but the issue of bat fatalities at internal haemorrhaging but no the zygote, selective silencing, and so such facilities — primarily involving external injuries. Only six (8%) bats on) as opposed to patterns. Given the migratory species during autumn had an external injury but no internal complexity of the task, it will almost migration — has been raised haemorrhaging. certainly be necessary to treat one relatively recently [1,2]. Given that Among 18 carcasses examined limited group of organisms at a time, echolocating bats detect moving with a dissecting microscope, and combine them into successively objects better than stationary ones ten had traumatic injuries. Eleven larger trees to achieve more general [3], their relatively high fatality bats had a haemothorax, seven of explanations, or more likely, to show rate is perplexing, and numerous which could not be explained by a that the evolutionary consequences explanations have been proposed traumatic event. Ten bats had small of uniparental inheritance vary from [1]. The decompression hypothesis bullae — air-filled bubbles caused one group to another, just as the proposes that bats are killed by rupture of alveolar walls — visible mechanisms vary. by barotrauma caused by rapid on the lung surface (Figure 1A). All It should be clear from this Primer air- pressure reduction near moving 17 bats examined histologically had that uniparental inheritance is a turbine blades [1,4,5]. Barotrauma lesions in the lungs consistent with quantitative trait with many different involves tissue damage to barotrauma (Table 1), with pulmonary underlying mechanisms; moreover it air- containing structures caused by haemorrhage, congestion, edema, is potentially subject to any or all of rapid or excessive pressure change; lung collapse and bullae being the evolutionary forces of mutation, pulmonary barotrauma is lung present in various proportions random genetic drift, and selection damage due to expansion of air in (Figure 1). In 15 (88%), the main within and between species. Unraveling the lungs that is not accommodated lesion was pulmonary haemorrhage, the evolutionary history, causes, and by exhalation. We report here the which in most cases was most consequences of the trait will almost first evidence that barotrauma severe around the bronchi and large certainly be much more difficult than is the cause of death in a high vessels. we thought, and should provide many proportion of bats found at wind Although the pressure reduction years of good scientific fun. energy facilities. We found that 90% required to cause the type of of bat fatalities involved internal internal injuries we observed in bats Further reading haemorrhaging consistent with is unknown, pressure differences Birky, C.W. Jr. (2001). The inheritance of genes in mitochondria and chloroplasts: Laws, barotrauma, and that direct contact as small as 4.4 kPa are lethal to mechanisms, and models. Proc. Nat. Acad. with turbine blades only accounted Norway rats (Rattus norvegicus) [6]. Sci. USA 35, 125–148. Lynch, M., and Blanchard, J.L. (1998). Deleterious for about half of the fatalities. Air The greatest pressure differential at mutation accumulation in organelle genomes. pressure change at turbine blades wind turbines occurs in the blade- Genetica 102, 103, 29–39. is an undetectable hazard and helps tip vortices which, as with airplane Piganeau, G., Gardner, M., and Eyre-Walker, A. (2004). A broad survey of recombination in explain high bat fatality rates. We wings, are shed downwind from the animal mitochondria. Mol. Biol. Evol. 21, suggest that one reason why there tips of the moving blades [7]. The 2319–2335. Piganeau, G., and Eyre-Walker, A. (2004). A are fewer bird than bat fatalities is pressure drop in the vortex increases reanalysis of the indirect evidence for that the unique respiratory anatomy with tip speed, which in modern recombination in human mitochondrial DNA. of birds is less susceptible to turbines turning at top speed varies Heredity 92, 282–288. Xu, J. (2005). The inheritance of organelle genes barotrauma than that of mammals. from 55 to 80 m/s. This results and genomes: patterns and mechanisms. As with any airfoil, moving in pressure drops in the range of Genome 48, 951–958. wind- turbine blades create zones 5–10 kPa (P. Moriarty, personal of low pressure as the air flows communication), levels sufficient to Department of Ecology and Evolutionary over them. Animals entering cause serious damage to various Biology, Biological Sciences West, The University of Arizona, Tucson, Arizona 85745, these low pressure areas may mammals [6]. USA. suffer barotrauma. To test the Barotrauma helps explain the E-mail: [email protected] decompression hypothesis, we high fatality rates of bats at some Current Biology Vol 18 No 16 R696 Table 1. Injuries observed in bats killed at wind turbines in south-western Alberta, Canada. Supplemental Data Supplemental data are available at http:// L. cinereus L. noctivagans Other species Total www.current-biology.com/cgi/content/ No external injury 38% (103) 55% (77) 75% (8) 46% (188) full/18/16/R695/DC1 Internal haemorrhage 90% (48) 96% (26) 100% (1) 92% (75) Pulmonary lesions 100% (6) 100% (8) 100% (3) 100% (17) Acknowledgments We thank J. Carpenter, K. Jonasson, and Internal haemorrhage was detected by visual examination of dissected carcasses, while pulmonary lesions were detected using stained histological sections. Numbers in parentheses are sample sizes. B. McKnight for assistance in the field, and J. West, P. Moriarty, and R. Thresher for discussions regarding the aerodynamics of turbines and the adaptations of bat wind energy facilities. Even if These flight adaptations suggest lungs. Logistical support was provided echolocation allows bats to detect that bats are particularly susceptible by J. Edworthy, T. Kwas, M. Hopkins, and and avoid turbine blades, they to barotrauma. Although birds have B. Brown. B. Fenton, M. Brigham, C. Willis, may be incapacitated or killed by even thinner blood-gas barriers, M. Holder and three anonymous reviewers internal injuries caused by rapid they have compact, rigid lungs provided comments that improved the pressure reductions they can not with unidirectional ventilation and a manuscript. Funding was provided by detect. cross-current blood-gas relationship, grants from the Natural Sciences and Birds are also killed at wind as opposed to mammals which Engineering Research Council of Canada, turbines, but at most wind energy have large pliable lungs with the the University of Calgary, TransAlta Wind, facilities fewer birds than bats blood- gas relationship in a uniform Enmax, Suncor, Alberta Wind Energy are killed [8], and barotrauma has pool in the pulmonary alveoli [9,10]. Corp., Shell Canada, Bat Conservation not been suggested as a cause In addition, the pulmonary capillaries International, the North American Bat of bird fatalities. This may be of birds are exceptionally strong Conservation Partnership, and the Alberta explained partly by differences compared to those of mammals, and Conservation Association. in the respiratory anatomy and do not change as much in diameter susceptibility to barotrauma of when exposed to extreme pressure References 1. 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Biol. 111, 43–61. 10. West, J.B., Watson, R.R., and Fu, Z. (2007). Major differences in the pulmonary circulation Figure 1. Pulmonary barotrauma in bats killed at wind turbines. between birds and mammals. Respir. Physiol. (A) Formalin-fixed L. noctivagans lung with multifocal hemorrhages and a ruptured bulla with Neurobiol. 157, 382–390. hemorrhagic border (arrow). Histological sections of bat lungs stained with hematoxylin and eosin (100X). (B) Normal lung of an L. noctivagans. (C) Lung of Eptesicus fuscus found dead at Department of Biological Sciences, a wind turbine with no traumatic injury. There is extensive pulmonary hemorrhage (H), conges- University of Calgary, Calgary, tion, and bullae (b). (D) Lung of L. cinereus found dead at a wind turbine with a fracture of the AB Canada T2N 1N4. distal ulna and radius. 90% of the alveoli and airways are filled with edema. Bar = 100 µm. E-mail: [email protected]