Thomas H. Kunz

An emerging disease causes regional population collapse of a common North American bat species.

Threats to and from Bats Bats appear to be able to host an assortment of alarming pathogens, which, if they do not extirpate the bats, have implications for human health (see the Perspective by Daszak). For example, exposure to bats is the main source of human rabies in the Americas. But rabies is not generally transmitted among people; humans are a dead end for the virus. Streicker et al. (p. 676, see the cover) show that rabies virus lineages tend to be specific for bat lineages. It seems that although rabies viruses have the potential for rapid evolution, this property alone is not enough to overcome genetic barriers, which inhibit the onward transmission of rabies virus into a new species. White-nose syndrome, an exotic fungal infection of bats, has, over the past 3 years, spread from upstate New York to West Virginia, killing on average 70% of the animals in a hibernating colony. The infection makes bats restless over winter when they should be dormant, which makes them exhaust their fat reserves, resulting in the death of over a million bats. Frick et al. (p. 679) have analyzed population data collected on bats in the northeastern United States for the past 30 years and show that, mainly owing to white-nose syndrome, the once abundant little brown bat is heading for regional extinction in the next 16 years or so. This scale of loss of an insectivorous mammal is expected to have repercussions for ecosystem integrity and for the economic costs of agricultural pest control. Like the passenger pigeon, millions of little brown bats face the possibility of rapid extinction, this time from disease. White-nose syndrome (WNS) is an emerging disease affecting hibernating bats in eastern North America that causes mass mortality and precipitous population declines in winter hibernacula. First discovered in 2006 in New York State, WNS is spreading rapidly across eastern North America and currently affects seven species. Mortality associated with WNS is causing a regional population collapse and is predicted to lead to regional extinction of the little brown myotis (Myotis lucifugus), previously one of the most common bat species in North America. Novel diseases can have serious impacts on naïve wildlife populations, which in turn can have substantial impacts on ecosystem integrity.

Roosting Ecology of Bats

Bats spend over half their lives subjected to the selective pressures of their roost environment; thus it is not surprising that the conditions and events associated with roosting have played a prominent role in their ecology and evolution. Roosts provide sites for mating, hibernation, and rearing young; they promote social interactions and the digestion of food; and they offer protection from adverse weather and predators. Conditions that balance natality and mortality and enhance survivorship are intimately linked to roost characteristics and are paramount to the success of a species. The roosting ecology of bats can be viewed as a complex interaction of physiological, behavioral, and morphological adaptations and demographic response. The roosting habits of bats may be influenced by roost abundance and availability, risks of predation, the distribution and abundance of food resources, social organization, and an energy economy imposed by body size and the physical environment. For many bats the availability and physical capacity of roosts can set limits on the number and dispersion of roosting bats, and this in turn can influence the type of social organization and foraging strategy employed. For example, some bats as refuging animals (see Hamilton and Watt, 1970) may benefit from improved metabolic economy and information transfer but may be subjected to the added costs associated with increased commuting time, competition for food, and risks of predation.

Ecological impacts of wind energy development on bats: questions, research needs, and hypotheses

At a time of growing concern over the rising costs and long-term environmental impacts of the use of fossil fuels and nuclear energy, wind energy has become an increasingly important sector of the electrical power industry, largely because it has been promoted as being emission-free and is supported by government subsidies and tax credits. However, large numbers of bats are killed at utility-scale wind energy facilities, especially along forested ridgetops in the eastern United States. These fatalities raise important concerns about cumulative impacts of proposed wind energy development on bat populations. This paper summarizes evidence of bat fatalities at wind energy facilities in the US, makes projections of cumulative fatalities of bats in the Mid-Atlantic Highlands, identifies research needs, and proposes hypotheses to better inform researchers, developers, decision makers, and other stakeholders, and to help minimize adverse effects of wind energy development.

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

Feeding Strategies of the Little Brown Bat, Myotis Lucifugus, in Southern New Hampshire

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.

Energetics of Pregnancy and Lactation in Freeranging Little Brown Bats (Myotis lucifugus)

Feeding strategies of the little brown bat, Myotis lucifugus, were investigated in southern New Hampshire USA from early May through late 1974. Nightly food consumption was estimated by comparing mean prefeeding body weights with postfeeding weights taken as individuals returned to the roost from their first feeding period (at 2200 to 2400h) and from a subsequent foraging period (at 0330 to 0500 h). Pregnant bats consumed an average of 2.5g of insects (2.72kJ/g prefeeding body weight) nightly. lactating females ate 3.7 g (4.23 kJ/g), and juveniles ingested 1.8 g (2.47 kJ/g). Increased food consumption in lactating bats accommodated reproductive energy demands and was facilitated by rising food availability. Increasing levels of independent food consumption in juveniles accompanied weaning. Fecal analysis revealed that diets of individual bats were diverse. All available insects 3 to 10 mm in body length were accepted as food items. Nematoceral Diptera were by far the most common insects taken in light—trap samples, and constituted a major portion of the diet throughout the summer. Coleoptera, Trichoptera, Lepidopter, Ephemeroptera, and Neuroptera were also consumed in appreciably numbers. Comparison of dietary composition with prey availability indicates that pregnant bats consumed 3—10 mm prey in approximate proportions encountered during June, when insect availability was low and unpredictable. However, lactating, postlactating, and nonproductive ♂ ♂ exhibited more selective feeding in July, when insects were more abundant. This increase in selectivity reflected exploitation of beetles and mayflies, which were uncommon in trap samples. In August, juveniles approximated random feeding patterns, as they learned to forage. We suggest that increased resource availability allowed selective feeding in adult bats during July, as predicted by presy selection models. However, reduced discriminatory abilities may prevent similar levels of prey selection in juveniles.

Bat Guano Virome: Predominance of Dietary Viruses from Insects and Plants plus Novel Mammalian Viruses

We combined field measurements of metabolic rate, made with doubly labeled water, with data from our previous studies to examine reproductive energetics in 24 female little brown bats (Myotis lucifugus). Including estimates of tissue or milk production, M. lucifugus required an average of 33.7 kJ d⁻¹ of assimilated energy in pregnancy compared to 41.3 kJ d⁻¹ during lactation. Predicted insect consumption was 5.5 g d⁻¹ for a 9-gpregnant female and 6.7g d⁻¹ for a 79-g lactating female. About 2% of total energy assimilated during pregnancy was stored as new tissue, whereas lactating females exported 32% as milk. Estimated assimilated energy demand on the first day of lactation was 33.8 kJ d⁻¹ and increased to 60.3 kJ d⁻¹ at peak lactation. By subtracting laboratory measurements of roosting costs from observed metabolized energy expenditure, we calculated that foraging flight by 9-g pregnant M. lucifugus required 4.46 kJ h⁻¹; this was 13% less than allometric predictions. Foraging fight accounted for the largest proportion of the daily metabolized energy budget during pregnancy (61%) and lactation (66%). The large amount of energy devoted to foraging by this aerial-feeding bat may partially explain the low proportion of energy it allocates to tissue production and milk export.

Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms

ABSTRACT Bats are hosts to a variety of viruses capable of zoonotic transmissions. Because of increased contact between bats, humans, and other animal species, the possibility exists for further cross-species transmissions and ensuing disease outbreaks. We describe here full and partial viral genomes identified using metagenomics in the guano of bats from California and Texas. A total of 34% and 58% of 390,000 sequence reads from bat guano in California and Texas, respectively, were related to eukaryotic viruses, and the largest proportion of those infect insects, reflecting the diet of these insectivorous bats, including members of the viral families Dicistroviridae, Iflaviridae, Tetraviridae, and Nodaviridae and the subfamily Densovirinae. The second largest proportion of virus-related sequences infects plants and fungi, likely reflecting the diet of ingested insects, including members of the viral families Luteoviridae, Secoviridae, Tymoviridae, and Partitiviridae and the genus Sobemovirus. Bat guano viruses related to those infecting mammals comprised the third largest group, including members of the viral families Parvoviridae, Circoviridae, Picornaviridae, Adenoviridae, Poxviridae, Astroviridae, and Coronaviridae. No close relative of known human viral pathogens was identified in these bat populations. Phylogenetic analysis was used to clarify the relationship to known viral taxa of novel sequences detected in bat guano samples, showing that some guano viral sequences fall outside existing taxonomic groups. This initial characterization of the bat guano virome, the first metagenomic analysis of viruses in wild mammals using second-generation sequencing, therefore showed the presence of previously unidentified viral species, genera, and possibly families. Viral metagenomics is a useful tool for genetically characterizing viruses present in animals with the known capability of direct or indirect viral zoonosis to humans.

Global Conservation Significance of Ecuador's Yasuní National Park

An inverse correlation between free radical production by isolated mitochondria and longevity in homeotherms has been reported, but previous comparative studies ignored possible confounding effects of body mass and phylogeny. We investigated this correlation by comparing rates of hydrogen peroxide (H2O2) production by heart mitochondria isolated from groups or pairs of species selected to have very different maximum lifespans but similar body masses (small mammals, medium‐sized mammals, birds). During succinate oxidation, H2O2 production rates were generally lower in the longer‐lived species; the differences arose at complex I of the electron transport chain during reverse electron transport. Additional data were obtained from large species and the final dataset comprised mouse, rat, white‐footed mouse, naked mole‐rat, Damara mole‐rat, guinea pig, baboon, little brown bat, Brazilian free‐tailed bat, ox, pigeon and quail. In this dataset, maximum lifespan was negatively correlated with H2O2 production at complex I during reverse electron transport. Analysis of residual maximum lifespan and residual H2O2 production revealed that this correlation was even more significant after correction for effects of body mass. To remove effects of phylogeny, independent phylogenetic contrasts were obtained from the residuals. These revealed an inverse association between maximum lifespan and H2O2 production that was significant by sign test, but fell short of significance by regression analysis. These findings indicate that enhanced longevity may be causally associated with low free radical production by mitochondria across species over two classes of vertebrate homeotherms.

Assessing Impacts of Wind-Energy Development on Nocturnally Active Birds and Bats: A Guidance Document

Background The threats facing Ecuadors Yasuní National Park are emblematic of those confronting the greater western Amazon, one of the worlds last high-biodiversity wilderness areas. Notably, the countrys second largest untapped oil reserves—called “ITT”—lie beneath an intact, remote section of the park. The conservation significance of Yasuní may weigh heavily in upcoming state-level and international decisions, including whether to develop the oil or invest in alternatives. Methodology/Principal Findings We conducted the first comprehensive synthesis of biodiversity data for Yasuní. Mapping amphibian, bird, mammal, and plant distributions, we found eastern Ecuador and northern Peru to be the only regions in South America where species richness centers for all four taxonomic groups overlap. This quadruple richness center has only one viable strict protected area (IUCN levels I–IV): Yasuní. The park covers just 14% of the quadruple richness centers area, whereas active or proposed oil concessions cover 79%. Using field inventory data, we compared Yasunís local (alpha) and landscape (gamma) diversity to other sites, in the western Amazon and globally. These analyses further suggest that Yasuní is among the most biodiverse places on Earth, with apparent world richness records for amphibians, reptiles, bats, and trees. Yasuní also protects a considerable number of threatened species and regional endemics. Conclusions/Significance Yasuní has outstanding global conservation significance due to its extraordinary biodiversity and potential to sustain this biodiversity in the long term because of its 1) large size and wilderness character, 2) intact large-vertebrate assemblage, 3) IUCN level-II protection status in a region lacking other strict protected areas, and 4) likelihood of maintaining wet, rainforest conditions while anticipated climate change-induced drought intensifies in the eastern Amazon. However, further oil development in Yasuní jeopardizes its conservation values. These findings form the scientific basis for policy recommendations, including stopping any new oil activities and road construction in Yasuní and creating areas off-limits to large-scale development in adjacent northern Peru.