The Effects of Sex, Energy, and Environmental Conditions on the Movement Ecology of Migratory Bats

Lack of knowledge about the behaviour of migratory species during the migratory period is a major barrier to conservation efforts. In this thesis I focus primarily on differences between the sexes of the bat Lasionycteris noctivagans, during spring migration. Females are pregnant during spring migration and this overlap between migration and reproduction may affect the time and energy management of females as compared to males. In Chapter 2 I examine spring migration phenology of bats at a stopover site. Females arrived earlier than males, likely to give their pups a long growing season. Fat stores appeared to reflect a strategy to provision for upcoming lactation demands. In Chapter 3 I explore stopover behaviour and I show that despite the use of torpor to minimize roosting energy expenditure, cold weather extends stopover duration. There was no sex difference in the length of time spent at stopover. By regressing the time of night bats were captured against their fat and lean mass I demonstrate that bats have greater fat and lean masses closer to dawn, and therefore are likely using stopover periods to refuel. In Chapter 4 I compare sex and seasonal differences in daytime torpor use at stopover. I found that in spring bats used torpor for fewer hours than in autumn, even after accounting for the effect of ambient temperature. Further, females used torpor for fewer hours than males. I propose that these seasonal differences are due to lower prey abundance and predictability in spring; sex differences may be attributable to a higher foraging intensity by females compared to males. Finally, in Chapter 5 I use a radio-telemetry array in southwestern Ontario, Canada to track the spring and autumn long distance migratory movements of L. noctivagans, Lasiurus borealis, and Lasiurus cinereus. No migration corridors were identified in either season. Estimated migration speeds indicate that multiday stopovers are also used in the autumn. These studies combined show that sex affects the spring migration time and energy management of bats. Bat migration research is still in its formative stages and my studies provide new information on bat migration in North America

Stable isotope investigation of the migratory behavior of silverhaired bats (Lasionycteris noctivagans) in eastern North America

We investigated the migratory movements of silver-haired bats (Lasionycteris noctivagans) across the eastern extent of the species’ range. We conducted stable hydrogen isotope analysis of fur samples (δ2Hfur) from museum specimens collected across latitudes and at all times of the year. We first used these data to estimate the timing of fur replacement and to develop a model associating δ2Hfur with that of local precipitation (δ2Hprecip) at the location where fur replacement occurred. We then used this model to 1) identify individuals that had migrated across latitudes, and 2) investigate the presence of continental-scale patterns in the estimated distance traveled. Bats were at their location of fur replacement between 20 June and 26 August, and there was a strong linear relationship between δ2Hfur and δ2Hprecip in bats collected during this time. There was substantial variation in the migratory movements of this species. Twenty-four of 38 females and 14 of 30 males showed isotopic evidence of leaving the area where fur replacement occurred (i.e., migrating across latitudes), whereas the remaining bats were either sedentary or moved at a small spatial scale. Males appeared to migrate consistently, regardless of latitude of origin, whereas there was a partial leapfrog pattern in migratory movements of females. To our knowledge, this is the first evidence of leapfrog migration in bat

Stable isotope analyses of bat fur: Applications for investigating North American bat migration

Many aspects of North American bat migration are not well documented. Stable isotope analyses of animal tissues can elucidate migratory origin, but this technique has not been widely applied to bats. This dissertation i) uses fur stable isotope analyses to investigate North American bat migration and ii) highlights some of the strengths and weaknesses of this analytical technique when applied to bat systems. I conducted stable hydrogen, carbon, and nitrogen isotope analyses on fur from five bat species. I documented δDfur heterogeneity in summer resident populations of Myotis lucifugus, Lasiurus borealis, Lasiurus cinereus, and Lasionycteris noctivagans. Stable hydrogen isotope composition varied systematically within and among individuals, age groups, species, sites, and over time. Bats from proximate colonies were discriminated using multi- isotope analyses and stable isotope correlations existed in some species. I investigated the origins of fall migrant L. noctivagans and L. borealis in Ontario. Stable isotope evidence did not indicate that migrant L. noctivagans originated from a wide range of latitudes, or that latitudinal origin varied with time or migrant “wave”. Lasiurus borealis results were highly variable and further work is required before ecological conclusions can be drawn from stable isotope results from this species. I investigated the annual migratory movements of tri-colored bats (Perimyotis subflavus), a presumed regional migrant. Stable hydrogen isotope results indicated that some bats engaged in southern migration, a behavior not previously described for this species. More males than females migrated south and southern migrants were at the latitudinal extremes of the species’ range

Distributional Limits of Bats in Alaska

Bats in temperate regions are relatively well studied, yet little research has focused on the northern limit of their distribution. We document the northwestern extent of bats in North America using museum holdings, literature records, and field research in Alaska. Six bat species are confirmed from Alaska: Myotis lucifugus, M. keenii, M. californicus, M. volans, Lasionycteris noctivagans, and Eptesicus fuscus. M. lucifugus occurs throughout much of Alaska south of the Arctic Circle, whereas four other species occur only in Southeast Alaska. Climate, roost availability, extent of forested habitat, geographic barriers, length of night, and prey abundance appear to influence the distribution of bats in Alaska, although the relative contribution of these factors is unknown.Si, dans les régions tempérées, les chauves-souris ont fait l'objet d'études relativement approfondies, on a par contre mené peu de recherches sur la limite septentrionale de leur répartition. Cet article décrit l'extension nord-ouest de l'aire des chauves-souris en Amérique du Nord en faisant appel à des pièces muséologiques, des documents comportant des relevés, et des recherches sur le terrain en Alaska. On confirme que six espèces de chauves-souris se retrouvent en Alaska: Myotis lucifugus, M. keenii, M. californicus, M. volans, Lasionycteris noctivagans et Eptesicus fuscus. M. lucifugus est répandue presque partout en Alaska au sud du cercle polaire, tandis que quatre autres espèces ne se retrouvent que dans le sud-est de l'Alaska. Il semble que le climat, la disponibilité des sites de reproduction, l'étendue de l'habitat forestier, les barrières géographiques, la longueur de la nuit et l'abondance des proies influencent la distribution des chauves-souris en Alaska, bien qu'on ne connaisse pas la contribution relative de ces facteurs

Determining nightly bat activity with, and sampling effectiveness of, modified NABat driving transects in urban areas

Time of peak bat activity during the night differs among bat species. Foraging strategies may differ among species due to prey availability, habitat availability, and/or interactions between species. Habitat availability is altered in urban areas, which may affect insect prey availability and interspecies interactions. Monitoring changes in bat diversity and behavior associated with habitat conversion is important, but some traditional bat monitoring methods may not be appropriate for all study sites. Acoustic monitoring techniques, including mobile monitoring using driving transects, may be good alternatives to study nightly activity in urban bat populations. Acoustic monitoring is an important component of many monitoring programs including the North American Bat Monitoring Program (NABat). Driving transects that are approximately 25 to 48 kilometers long within 100 km2 grid cells are used by NABat, but choosing appropriate transect routes can be difficult in urban areas. Shorter transects could be used to alleviate sampling issues, but a modified protocol may be less effective at sampling some bat species. My objectives were to use mobile acoustic monitoring to determine when bat species are active in a single night in urban and non-urban sites, if nightly bat activity patterns in urban sites differ from nightly bat activity patterns in non-urban sites, and whether sampling using a modified mobile acoustic monitoring protocol with reduced transect lengths is effective compared to the standardized NABat protocol. I recorded bat echolocation calls using Anabat acoustic detectors while driving transects through the night at five sites (three “urban” and two “non-urban”) located in the Piedmont region of north-central North Carolina from May through August 2016. Transects were driven three times per night in each site starting 45 minutes, 180 minutes, and 300 minutes after sunset using a modified NABat protocol with 6 “short” transects (about 3.2 km long each). An additional “long” transect (about 25 km long, using NABat protocol) was sampled in 4 sites (two of the urban sites and both non-urban sites) starting 45 minutes after sunset. Recorded echolocation call sequences were analyzed manually using AnalookW and automatically using Bat Call Identification and Echoclass software. Total bat activity and Lasiurus borealis activity was decreased later in the night in urban sites. There were also fewer Eptesicus fuscus, Lasionycteris noctivagans, and Nycticeius humeralis calls on the latest time period. There were more E. fuscus, L. noctivagans, and Tadarida brasiliensis calls and fewer L. borealis, N. humeralis, and Perimyotis subflavus calls in urban sites than non-urban sites. Fewer short transects were needed to match the detection probability on long transects for E. fuscus, L. borealis, and P. subflavus, while more short transects were needed for L. noctivagans, N. humeralis, and T. brasiliensis. These results suggest that bats in urban areas partition time differently, which is important to consider as urbanization impacts bat populations. They also suggest that short transects can be used effectively for NABat sampling in urban areas

Determining species-specific nightly bat activity in sites with varying urban intensity

Time of peak bat activity during the night differs among bat species due to temperature, prey availability, habitat availability, and/or interactions between species. Habitat availability is altered in urban areas, which may affect insect prey availability and interspecies interactions. Our objectives were to use mobile acoustic monitoring to determine when bat species were active in a single night in urban and nonurban sites and if nightly bat activity patterns differed in urban versus nonurban sites. Bat echolocation call sequences were recorded using Anabat acoustic detectors while driving transects through the night at five sites (three “urban” and two “nonurban”) located in the Piedmont region of north-central North Carolina from May through August 2016. Transects were driven three times per night starting 45 min, 180 min, and 300 min after sunset. Recorded echolocation call sequences were analyzed manually using AnalookW and automatically using Bat Call Identification and Echoclass software. Total bat activity was not different between urban and nonurban sites. However, total bat activity was lower later in the night in urban sites, but stayed the same in nonurban sites. Species specifically, there were more Eptesicus fuscus, Lasionycteris noctivagans, and Tadarida brasiliensis call sequences and fewer Lasiurus borealis, Nycticeius humeralis, and Perimyotis subflavus call sequences in urban sites than nonurban sites. There were also fewer E. fuscus, L. noctivagans, and N. humeralis call sequences later in the night in both urban and nonurban sites. Only Lasiurus borealis activity in urban sites later in the night reduced and L. borealis activity in nonurban sites remained at the same. These results suggest that bats in urban areas partition time differently, which is important to consider for urban conservation efforts and planning

Migratory and winter activity of bats in Yellowstone National Park

A substantial body of work exists describing timing of migration and hibernation among bats in eastern North America, but less is known about these events among bats inhabiting the Rocky Mountain region. Yellowstone National Park is a geothermally influenced landscape comprised of diverse habitats, creating the opportunity for unique behaviors to develop among local bat populations. We identified the timing of migration for the local bat community and determined if bats overwinter in Yellowstone. To accomplish this, we radiotracked 7 little brown myotis (Myotis lucifugus), 5 western long-eared myotis (M. evotis), 4 big brown bats (Eptesicus fuscus), 4 silver-haired bats (Lasionycteris noctivagans), and 1 western small-footed myotis (M. ciliolabrum) from August to September 2010 and September to October 2011. We also used acoustic detectors to record bat activity from November through April 2011–2014 and sampled abundance of nocturnal insects using black-light traps from 2011 to 2012. Although availability of insects declined rapidly during August and afterward, several bat species remained active throughout autumn and winter. Bat activity was recorded during all months, even during periods of extreme cold. Radiotagged big brown bats, little brown myotis, and western small-footed myotis remained active in the study area throughout October, after the 1st snowfall of the season. While data for activity patterns in late autumn and winter prevented an estimation of the onset of hibernation, spring emergence occurred in April despite persistence of winter conditions. These data provide insights into the migration and hibernation strategies of bat populations in the Rocky Mountains and highlight gaps in our understanding of seasonal changes in these species

Separating the effects of water quality and urbanization on temperate insectivorous bats at the landscape scale

[2017-2018 UNCG University Libraries Open Access Publishing Fund Grant Winner.] Many local scale studies have shown that bats respond to water quality degradation or urbanization in a species-specific manner. However, few have separated the effects of urbanization versus water quality degradation on bats, in single city or single watershed case studies. Across North Carolina, USA, we used the standardized North American Bat Monitoring Program mobile transect protocol to survey bat activity in 2015 and 2016 at 41 sites. We collected statewide water quality and urban land cover data to disentangle the effects of urbanization and water quality degradation on bats at the landscape scale. We found that statewide, water quality degradation and urbanization were not correlated. We found that bats responded to water quality degradation and urbanization independently at the landscape scale. Eptesicus fuscus and Lasiurus cinereus negatively responded to water quality degradation. Lasiurus borealis and Perimyotis subflavuspositively responded to water quality degradation. Lasionycteris noctivagans did not respond to water quality degradation but was more active in more urbanized areas. Tadarida brasiliensis positively responded to urbanization and was less active in areas with degraded water quality. We show that bat–water quality relationships found at the local scale are evident at a landscape scale. We confirm that bats are useful bioindicators for both urbanization and water quality degradation. We suggest that water quality can be used to predict the presence of bat species of conservation concern, such as P. subflavus, in areas where it has not been studied locally

Physiological Ecology of Bat Migration

Migration is perhaps the most poorly understood aspect of bat biology and the underlying physiological basis is virtually unstudied. Although distantly related, bats and birds are both endothermic flying vertebrates and bird migration physiology has been studied for decades. Therefore, I used migratory birds as a model system to make predictions regarding the physiological ecology of bat migration. First, I compared brain size of migratory and sedentary bat species. Migratory species have smaller brains which suggests the costs of carrying and maintaining a large brain are incompatible with the demands of migration. Next, I studied silver-haired bats (Lasionycteris noctivagans) during migratory stopover. Bats arrived at the site with fat stores comparable to migratory birds, rarely foraged, and had short stopover durations. I proposed that bats use daily torpor to minimize energy expenditure during non-flight periods, thus sparing fuel stores for migratory flight. Finally, I compared body composition and flight muscle physiology in migrating and non-migrating hoary bats (Lasiurus cinereus). Changes in digestive and exercise organ sizes, the composition of adipose stores, and increased catabolic enzyme activities all reflected the increased energetic demands of migration. Sex-specific changes in muscle membrane fatty acid composition and the expression of fatty acid transport proteins suggest pregnant females are subject to different pressures than males. The energetic demands of bat migration lead to many physiological changes as observed in migratory birds. However, several factors specific to bats (especially heterothermy and the timing of reproduction) result in bat migration as a distinct phenomenon compared to birds