Justin G. Boyles

Economic Importance of Bats in Agriculture

Insectivorous bat populations, adversely impacted by white-nose syndrome and wind turbines, may be worth billions of dollars to North American agriculture. White-nose syndrome (WNS) and the increased development of wind-power facilities are threatening populations of insectivorous bats in North America. Bats are voracious predators of nocturnal insects, including many crop and forest pests. We present here analyses suggesting that loss of bats in North America could lead to agricultural losses estimated at more than

Experimental infection of bats with Geomyces destructans causes white-nose syndrome

3.7 billion/year. Urgent efforts are needed to educate the public and policy-makers about the ecological and economic importance of insectivorous bats and to provide practical conservation solutions.

Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology

White-nose syndrome (WNS) has caused recent catastrophic declines among multiple species of bats in eastern North America. The disease’s name derives from a visually apparent white growth of the newly discovered fungus Geomyces destructans on the skin (including the muzzle) of hibernating bats. Colonization of skin by this fungus is associated with characteristic cutaneous lesions that are the only consistent pathological finding related to WNS. However, the role of G. destructans in WNS remains controversial because evidence to implicate the fungus as the primary cause of this disease is lacking. The debate is fuelled, in part, by the assumption that fungal infections in mammals are most commonly associated with immune system dysfunction. Additionally, the recent discovery that G. destructans commonly colonizes the skin of bats of Europe, where no unusual bat mortality events have been reported, has generated further speculation that the fungus is an opportunistic pathogen and that other unidentified factors are the primary cause of WNS. Here we demonstrate that exposure of healthy little brown bats (Myotis lucifugus) to pure cultures of G. destructans causes WNS. Live G. destructans was subsequently cultured from diseased bats, successfully fulfilling established criteria for the determination of G. destructans as a primary pathogen. We also confirmed that WNS can be transmitted from infected bats to healthy bats through direct contact. Our results provide the first direct evidence that G. destructans is the causal agent of WNS and that the recent emergence of WNS in North America may represent translocation of the fungus to a region with a naive population of animals. Demonstration of causality is an instrumental step in elucidating the pathogenesis and epidemiology of WNS and in guiding management actions to preserve bat populations against the novel threat posed by this devastating infectious disease.

Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome

White-nose syndrome (WNS) is causing unprecedented declines in several species of North American bats. The characteristic lesions of WNS are caused by the fungus Geomyces destructans, which erodes and replaces the living skin of bats while they hibernate. It is unknown how this infection kills the bats. We review here the unique physiological importance of wings to hibernating bats in relation to the damage caused by G. destructans and propose that mortality is caused by catastrophic disruption of wing-dependent physiological functions. Mechanisms of disease associated with G. destructans seem specific to hibernating bats and are most analogous to disease caused by chytrid fungus in amphibians.

Adaptive Thermoregulation in Endotherms May Alter Responses to Climate Change

White-nose syndrome (WNS) is an emergent disease estimated to have killed over five million North American bats. Caused by the psychrophilic fungus Geomyces destructans, WNS specifically affects bats during hibernation. We describe temperature-dependent growth performance and morphology for six independent isolates of G. destructans from North America and Europe. Thermal performance curves for all isolates displayed an intermediate peak with rapid decline in performance above the peak. Optimal temperatures for growth were between 12.5 and 15.8°C, and the upper critical temperature for growth was between 19.0 and 19.8°C. Growth rates varied across isolates, irrespective of geographic origin, and above 12°C all isolates displayed atypical morphology that may have implications for proliferation of the fungus. This study demonstrates that small variations in temperature, consistent with those inherent of bat hibernacula, affect growth performance and physiology of G. destructans, which may influence temperature-dependent progression and severity of WNS in wild bats.

A New Comparative Metric for Estimating Heterothermy in Endotherms

Climate change is one of the major issues facing natural populations and thus a focus of recent research has been to predict the responses of organisms to these changes. Models are becoming more complex and now commonly include physiological traits of the organisms of interest. However, endothermic species have received less attention than have ectotherms in these mechanistic models. Further, it is not clear whether responses of endotherms to climate change are modified by variation in thermoregulatory characteristics associated with phenotypic plasticity and/or adaptation to past selective pressures. Here, we review the empirical data on thermal adaptation and acclimatization in endotherms and discuss how those factors may be important in models of responses to climate change. We begin with a discussion of why thermoregulation and thermal sensitivity at high body temperatures should be co-adapted. Importantly, we show that there is, in fact, considerable variation in the ability of endotherms to tolerate high body temperatures and/or high environmental temperatures, but a better understanding of this variation will likely be critical for predicting responses to future climatic scenarios. Next, we discuss why variation in thermoregulatory characteristics should be considered when modeling the effects of climate change on heterothermic endotherms. Finally, we review some biophysical and biochemical factors that will limit adaptation and acclimation in endotherms. We consider both long-term, directional climate change and short-term (but increasingly common) anomalies in climate such as extreme heat waves and we suggest areas of important future research relating to both our basic understanding of endothermic thermoregulation and the responses of endotherms to climate change.

Bats initiate vital agroecological interactions in corn

A major focus in the study of endothermic thermoregulation has been the description of thermoregulatory patterns used by various species and/or populations. Compared with ectotherms, relatively few attempts have been made to study the thermoregulation of endotherms in an adaptive framework. We believe that one of the main factors limiting this area of research has been the lack of an appropriate metric to directly compare body temperature (Tb) variation across all endothermic species. Thus, we present a simple comparative metric, the heterothermy index (HI), to quantify the expression of heterothermy by endotherms during a given time frame. Key advantages of HI are that (1) it represents a new analytical technique that has different strengths than the metrics commonly used to describe variation in Tb, (2) it allows for evaluation of nonenergetic costs and benefits that affect the expression of heterothermy, and (3) it has the potential to unify research on homeotherms and heterotherms through quantitative comparative analyses that examine the entire continuum of thermoregulatory patterns. In short, we suggest that our metric provides a means to overcome one of the hurdles presently slowing the advancement of research on endothermic thermoregulation beyond the simple description of thermoregulatory patterns.

Torpor in Dark Times: Patterns of Heterothermy Are Associated with the Lunar Cycle in a Nocturnal Bird:

Significance Bats are thought to provide valuable services to agriculture by suppressing crop pests, but their ecological role in agricultural systems remains unclear. We implemented a unique field experiment to assess the ecological and economic effect of bats in corn agriculture and found that bats initiated strong and surprising ecological interactions in corn fields. Bats not only suppressed crop pest numbers and crop damage but also indirectly suppressed the presence of pest-associated fungus and a toxic compound produced by the fungus. As nocturnal flying insectivores, bats occupy unique ecological roles and provide valuable services to society, and it is therefore essential that we conserve this often-maligned group. In agroecosystems worldwide, bats are voracious predators of crop pests and may provide services to farmers worth billions of U.S. dollars. However, such valuations make untested assumptions about the ecological effect of bats in agroecosystems. Specifically, estimates of the value of pest suppression services assume bats consume sufficient numbers of crop pests to affect impact pest reproduction and subsequent damage to crops. Corn is an essential crop for farmers, and is grown on more than 150 million hectares worldwide. Using large exclosures in corn fields, we show that bats exert sufficient pressure on crop pests to suppress larval densities and damage in this cosmopolitan crop. In addition, we show that bats suppress pest-associated fungal growth and mycotoxin in corn. We estimate the suppression of herbivory by insectivorous bats is worth more than 1 billion USD globally on this crop alone, and bats may further benefit farmers by indirectly suppressing pest-associated fungal growth and toxic compounds on corn. Bats face a variety of threats globally, but their relevance as predators of insects in ubiquitous corn-dominated landscapes underlines the economic and ecological importance of conserving biodiversity.

Stacking the odds: light pollution may shift the balance in an ancient predator–prey arms race

Many studies have shown that endotherms become more heterothermic when the costs of thermoregulation are high and/or when limited energy availability constrains thermoregulatory capacity. However, the roles of many ecological variables, including constraints on foraging opportunities and/or success, remain largely unknown. To test the prediction that thermoregulatory patterns should be related to foraging opportunities in a heterothermic endotherm, we examined the relationship between the lunar cycle and heterothermy in Freckled Nightjars (Caprimulgus tristigma), which are visually orienting, nocturnal insectivores that are dependent on ambient light to forage. This model system provides an opportunity to assess whether variation in foraging opportunities influences the expression of heterothermy. The nightjars were active and foraged for insects when moonlight was available but became inactive and heterothermic in the absence of moonlight. Lunar illumination was a much stronger predictor of the magnitude of heterothermic responses than was air temperature (Ta). Our data suggest that heterothermy was strongly related to variation in foraging opportunities associated with the lunar cycle, even though food abundance appeared to remain relatively high throughout the study period. Patterns of thermoregulation in this population of Freckled Nightjars provide novel insights into the environmental and ecological determinants of heterothermy, with the lunar cycle, and not Ta, being the strongest predictor of torpor use.

White-nose syndrome in bats: illuminating the darkness.

Bat Conservation International and the South African National Research Foundation n(grant number 74604).