Lord of the Diptera (and Moths and a Spider): Molecular Diet Analyses and Foraging Ecology of Indiana Bats in Illinois

Effective management of endangered or threatened wildlife requires an understanding of how foraging habitats are used by those populations. Molecular diet analysis of fecal samples offers a cost-effective and non-invasive method to investigate how diets of wild populations vary with respect to spatial and temporal factors. For the federally endangered Indiana bat (Myotis sodalis), documenting its preferred food sources can provide critical information to promote effective conservation of this federally endangered species. Using cytochrome oxidase I amplicon sequence data from Indiana bat guano samples collected at two roosting areas in Cypress Creek National Wildlife Refuge, we found that dipteran taxa (i.e., flies) associated with riparian habitats were the most frequently detected taxon and represented the majority of the sequence diversity among the arthropods sampled. A select few arthropods from other taxa—especially spiders—are also likely important to Indiana bat diets in this refuge. A supervised learning analysis of diet components suggest only a small fraction of the frequently detected taxa are important contributors to spatial and temporal variation. Overall, these data depict the Indiana bat as a generalist consumer whose diet includes some prey items associated with particular seasonal or spatial components, along with other taxa repeatedly consumed throughout the entire foraging season. These molecular diet analyses suggest that protecting foraging resources specifically associated with the riparian habitat of Cypress Creek National Wildlife Refuge is essential to promote effective Indiana bat conservation.

Habitat suitability and connectivity modeling reveal priority areas for Indiana bat (Myotis sodalis) conservation in a complex habitat mosaic

Context Conservation for the Indiana bat (Myotis sodalis), a federally endangered species in the United States of America, is typically focused on local maternity sites; however, the species is a regional migrant, interacting with the environment at multiple spatial scales. Hierarchical levels of management may be necessary, but we have limited knowledge of landscape-level ecology, distribution, and connectivity of suitable areas in complex landscapes. Objectives We sought to (1) identify factors influencing M. sodalis maternity colony distribution in a mosaic landscape, (2) map suitable maternity habitat, and (3) quantify connectivity importance of patches to direct conservation action. Methods Using 3 decades of occurrence data, we tested a priori, hypothesis-driven habitat suitability models. We mapped suitable areas and quantified connectivity importance of habitat patches with probabilistic habitat availability metrics. Results Factors improving landscape-scale suitability included limited agriculture, more forest cover, forest edge, proximity to medium-sized water bodies, lower elevations, and limited urban development. Areas closer to hibernacula and rivers were suitable. Binary maps showed that 30% of the study area was suitable for M. sodalis and 29% was important for connectivity. Most suitable patches were important for intra-patch connectivity and far fewer contributed to inter-patch connectivity. Conclusions While simple models may be effective for small, homogenous landscapes, complex models are needed to explain habitat suitability in large, mixed landscapes. Suitability modeling identified factors that made sites attractive as maternity areas. Connectivity analysis improved our understanding of important areas for bats and prioritized areas to target for restoration.

Nine years of Indiana bat (Myotis sodalis) spring migration behavior

The endangered Indiana bat (Myotis sodalis) congregates in large hibernation groups in winter and travels after spring emergence to form summer maternity colonies, but information on migration behavior in this species remains limited to mostly band recovery observations. We tracked female Indiana bats in spring migration toward summer grounds using aerial radiotelemetry. Adult female Indiana bats were radiotagged in spring from 2009 through 2017, with 15 individuals successfully tracked to summer grounds and an additional 11 bats located in summer grounds via aerial telemetry after migration was complete. This resulted in the location of 17 previously unknown summer grounds for female Indiana bats, including adding Georgia, Alabama, and Mississippi to the summer maternity range. Two of the colonies identified in this study were south of the previously known southernmost colony in Tennessee, expanding the summer maternity range for the species by 178 km. Time-stamped location fixes along the migration path provided information about nightly and overall distances traveled, duration of travel, migration speed, and weather-related influences on bat behavior. Bats traveled 164.6 ± 26.2 km (± SE) on average from hibernacula to summer grounds and were migrating for an average of 7.3 ± 1.4 calendar nights. Bats alternated between foraging and traveling throughout each night of their migration route. Nightly migration rate was 9.9 ± 0.8 km/h and bats were active on the landscape for an average of 6.1 ± 0.4 h/night. Lower nighttime temperatures and lower barometric pressure correlated with use of layover areas during a migration night. Understanding bat behavior during migration can provide pertinent information for land managers to consider in efforts to conserve potential migration corridors, foraging areas, and roosting habitats of species in decline.

Effectiveness of Acoustic Lures for Increasing Indiana Bat Captures in Mist-Nets

As bat (Chiroptera) populations continue to decline in the eastern United States due to threats such as white-nose syndrome and interactions with wind facilities, capturing already rare species such as the federally endangered Indiana bat Myotis sodalis to assess health and demographics has become increasingly difficult. Mist-nets are a standard method for capturing and studying bats, but bats have the ability to escape from or avoid mist-nets. Past research has shown that the use of acoustic lures may increase mist-net capture success. Using prerecorded Indiana bat social calls, we tested the effectiveness of acoustic lures on capture rates across 24 nights at 37 sites in summers 2013 and 2014 in north-central Kentucky. Each site consisted of two nets (treatment and control) placed >35 m apart: we placed an acoustic lure set 1 m in front of the treatment net, whereas the control net received no lure. At the species level, we recorded significantly more captures in treatment nets (n = 262) than in control nets [n = 128; t(36) = 5.08, P < 0.001]. However, although we found a trend toward higher Indiana bat captures, the only species' with significant positive responses were evening bats Nycticeius humeralis [t(15) = 6.25, P < 0.001] and eastern red bats Lasiurus borealis [t(36) = 3.60, P < 0.001]. Further study is required to determine whether modifications to lure settings or call types result in increased Indiana bat captures.

Airport Expansion and Endangered Bats: Development and Mitigation Actions Near the Indianapolis International Airport

Economic prosperity and globalization are major drivers for development of international airports, but aviation-oriented businesses and residential developments are a by-product of airport business models. Among the multitude of planning and development considerations is the habitat needs of endangered wildlife species. Foraging data were analyzed from 57 bats during three time periods (1998–1999: pre-mitigation; 2005–2006: during mitigation, and 2014–2016: post-mitigation) of a long-term study of Indiana bats ( Myotis sodalis) near the Indianapolis International Airport. At this site, both developed land cover and forested land cover increased between 1998 and 2016 (34.1% and 3.3%, respectively). Mitigation actions included converting 323 ha of residential lots back to forest, and creation of a 56 ha wetland and an 85 ha multi-use park. Bat use of landscape cover types was related to changes in land cover during each period and competing hypotheses were compared to explain changes in bat foraging space use. With the addition of a major highway interchange where the colony foraged, bats increased foraging ranges, presumable in search of new habitat. In all periods, bats selected for forested habitat; as trees in replanted forest and designated parks aged, bats reduced their foraging ranges. Restoring hardwood forest and setting aside parklands were effective proactive mitigation measures for the colony of Indiana bats near the Indianapolis International Airport, and similar actions should benefit other wildlife where human development and habitat needs intersect.

Genetic Mark–Recapture Improves Estimates of Maternity Colony Size for Indiana Bats

Genetic mark–recapture methods are increasingly being used to estimate demographic parameters in species where traditional techniques are problematic or imprecise. The federally endangered Indiana bat Myotis sodalis has declined dramatically and threats such as white-nose syndrome continue to afflict this species. To date, important demographic information for Indiana bats has been difficult to estimate precisely using traditional techniques such as emergence counts. Successful management and protection of Indiana bats requires better methods to estimate population sizes and survival rates throughout the year, particularly during summer when these bats reproduce and are widely dispersed away from their winter hibernacula. In addition, the familial makeup of maternity colonies is unknown, yet important for understanding local and regional population dynamics. We had four objectives in this study. For the first two objectives we investigated the potential use of DNA from fecal samples (fecal DNA) collected at roosts to obtain genetically based mark–recapture estimates of 1) colony size and 2) survival rates, for an Indiana bat maternity colony in Indianapolis, Indiana. The third objective was to compare our genetically based colony-size estimates with emergence counts conducted at the same roost tree to evaluate the genetic mark–recapture method. Our fourth objective was to use fecal DNA to estimate levels of relatedness among individuals sampled at the roost. In the summer of 2008, we collected fecal pellets and conducted emergence counts at a prominent roost tree during three time periods each lasting 7 or 8 d. We genotyped fecal DNA using five highly polymorphic microsatellite loci to identify individuals and used a robust-design mark–recapture approach to estimate survival rates as well as colony size at the roost tree. Emergence count estimates at the roost tree ranged from 100 to 215, whereas genetic mark–recapture estimates were higher, ranging from 122 to 266 and more precise. Apparent survival was 0.994 (SE = 0.04) between sampling periods suggesting that few bats died or permanently emigrated during the course of the study. Relatedness estimates, r, between all pairs of individuals averaged 0.055 ranging from 0 to 0.779, indicating that most individuals were not closely related. We demonstrate here the promise of using fecal DNA to estimate demographic information for Indiana bats and potentially other bat species.

Experts correctly describe demography associated with historical decline of the endangered Indiana bat, but not recent period of stationarity

Demographic characteristics of bats are often insufficiently described for modeling populations. In data poor situations, experts are often relied upon for characterizing ecological systems. In concert with the development of a matrix model describing Indiana bat (Myotis sodalis) demography, we elicited estimates for parameterizing this model from 12 experts. We conducted this elicitation in two stages, requesting expert values for 12 demographic rates. These rates were adult and juvenile seasonal (winter, summer, fall) survival rates, pup survival in fall, and propensity and success at breeding. Experts were most in agreement about adult fall survival (3% Coefficient of Variation) and least in agreement about propensity of juveniles to breed (37% CV). The experts showed greater concordance for adult ( mean CV, adult = 6.2%) than for juvenile parameters ( mean CV, juvenile = 16.4%), and slightly more agreement for survival (mean CV, survival = 9.8%) compared to reproductive rates ( mean CV, reproduction = 15.1%). However, survival and reproduction were negatively and positively biased, respectively, relative to a stationary dynamic. Despite the species exhibiting near stationary dynamics for two decades prior to the onset of a potential extinction-causing agent, white-nose syndrome, expert estimates indicated a population decline of -11% per year (95% CI = -2%, -20%); quasi-extinction was predicted within a century ( mean = 61 years to QE, range = 32, 97) by 10 of the 12 experts. Were we to use these expert estimates in our modeling efforts, we would have errantly trained our models to a rapidly declining demography asymptomatic of recent demographic behavior. While experts are sometimes the only source of information, a clear understanding of the temporal and spatial context of the information being elicited is necessary to guard against wayward predictions.

Experts correctly describe demography associated with historical decline of the endangered Indiana bat, but not recent period of stationarity

Demographic characteristics of bats are often insufficiently described for modeling populations. In data poor situations, experts are often relied upon for characterizing ecological systems. In concert with the development of a matrix model describing Indiana bat (Myotis sodalis) demography, we elicited estimates for parameterizing this model from 12 experts. We conducted this elicitation in two stages, requesting expert values for 12 demographic rates. These rates were adult and juvenile seasonal (winter, summer, fall) survival rates, pup survival in fall, and propensity and success at breeding. Experts were most in agreement about adult fall survival (3% Coefficient of Variation) and least in agreement about propensity of juveniles to breed (37% CV). The experts showed greater concordance for adult ( mean CV, adult = 6.2%) than for juvenile parameters ( mean CV, juvenile = 16.4%), and slightly more agreement for survival (mean CV, survival = 9.8%) compared to reproductive rates ( mean CV, reproduction = 15.1%). However, survival and reproduction were negatively and positively biased, respectively, relative to a stationary dynamic. Despite the species exhibiting near stationary dynamics for two decades prior to the onset of a potential extinction-causing agent, white-nose syndrome, expert estimates indicated a population decline of -11% per year (95% CI = -2%, -20%); quasi-extinction was predicted within a century ( mean = 61 years to QE, range = 32, 97) by 10 of the 12 experts. Were we to use these expert estimates in our modeling efforts, we would have errantly trained our models to a rapidly declining demography asymptomatic of recent demographic behavior. While experts are sometimes the only source of information, a clear understanding of the temporal and spatial context of the information being elicited is necessary to guard against wayward predictions.

Effects of wind energy generation and white-nose syndrome on the viability of the Indiana bat

Wind energy generation holds the potential to adversely affect wildlife populations. Species-wide effects are difficult to study and few, if any, studies examine effects of wind energy generation on any species across its entire range. One species that may be affected by wind energy generation is the endangered Indiana bat (Myotis sodalis), which is found in the eastern and midwestern United States. In addition to mortality from wind energy generation, the species also faces range-wide threats from the emerging infectious fungal disease, white-nose syndrome (WNS). White-nose syndrome, caused byPseudogymnoascus destructans, disturbs hibernating bats leading to high levels of mortality. We used a spatially explicit full-annual-cycle model to investigate how wind turbine mortality and WNS may singly and then together affect population dynamics of this species. In the simulation, wind turbine mortality impacted the metapopulation dynamics of the species by causing extirpation of some of the smaller winter colonies. In general, effects of wind turbines were localized and focused on specific spatial subpopulations. Conversely, WNS had a depressive effect on the species across its range. Wind turbine mortality interacted with WNS and together these stressors had a larger impact than would be expected from either alone, principally because these stressors together act to reduce species abundance across the spectrum of population sizes. Our findings illustrate the importance of not only prioritizing the protection of large winter colonies as is currently done, but also of protecting metapopulation dynamics and migratory connectivity.