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

Seasonal Dynamics of Lipid Metabolism and Energy Storage in the Brazilian Free-Tailed Bat

As small, flying, mammalian endotherms, insectivorous bats are adapted to operate at high levels of energy expenditure. In response to seasonally variable challenges, we predicted that bats should balance energy budgets by flexibly adjusting aspects of their physiology or behavior in ways that elevate metabolic capacity. We examined variation in energy storage and pathways for oxidative metabolism in Brazilian free-tailed bats (Tadarida brasiliensis) related to estimated costs associated with reproduction and migration. We collected pectoral muscle and liver from female T. brasiliensis at six time points during the summer and fall and measured changes in the activity of four enzymes involved with lipid metabolism. Body mass varied substantially with life-cycle stage, suggesting that rapid accumulation and use of fat stores occurs in response to current and anticipated energy demands. Catabolic enzyme activity (carnitine palmitoyltransferase [CPT], 3-hydroxyacyl-CoA dehydrogenase [HOAD], and citrate synthase [CS]) in the muscle was increased during lactation compared with early pregnancy but exhibited no change before fall migration. While there was no temporal change in lipid biosynthetic capacity in the liver, fatty acid synthase activity was negatively correlated with body mass. Variation in body mass and enzyme activity in T. brasiliensis during the summer suggests that stored energy is mobilized and lipid oxidative capacity is increased during periods of increased demand and that lipid biosynthetic capacity is increased with depletion of fat stores. These results suggest that bats are able to flexibly adjust metabolic capacity based on energy requirement to maintain energy balance despite high levels of expenditure

Considerations of Varied Thermoregulatory Expressions in Migration Theory

This is the peer reviewed version of the following article: Considerations of Varied Thermoregulatory Expressions in Migration Theory, which has been published in final form at https://doi.org/10.1111/oik.08178. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions.Optimal migration theory has been used for 3 decades to generate predictions of stopover behavior and understand migration ecology. Yet, to date, there have been no attempts to understand the impacts of thermoregulation on migration theory predictions of stopover behavior. Though most migrants are homeothermic, a diverse group of migrants from bats to hummingbirds and warblers make use of some degree of heterothermy. We consider how thermoregulation influences stopover fuel deposition rates, and thus alters optimal migration theory predictions of stopover behavior using a hypothetical migratory bat as a model organism. We update the analytical models of optimal migration theory by considering scenarios of fixed metabolic rate (the current assumption of optimal migration theory) and 3 different mass-specific metabolic rates including homeothermy, shallow torpor heterothermy, and deep torpor heterothermy. Our results predict that heterotherms will make shorter stopovers, have a decreased departure fuel load, and reduce the overall time and energy costs associated with stopovers relative to homeotherms, highlighting that thermoregulation can drastically influence stopover behavior and ultimately play a critical role in population level patterns of migration.Texas Tech University Department of Biological Sciences

Island biogeography theory and the urban landscape: stopover site selection by the silver-haired bat (Lasionycteris noctivagans)

Many migratory bats require forested sites for roosting and foraging along their migration path, but increased urbanization and intensive agricultural practices may reduce the availability of stopover sites. Urban forests may provide important stopover habitat, maintaining landscape connectivity in regions where the majority of natural habitat has been cleared for development. Island biogeography theory can be applied to urbanized temperate forest biomes where small urban forests represent islands separated from the larger “mainland” forest. We used acoustic monitoring during the fall migration period to investigate the use of urban forest habitat by the migratory species Lasionycteris noctivagans Le Conte, 1831. We predicted that recorded activity would have a positive relationship with forest patch area and shape and a negative relationship with isolation from other forest patches, as suggested by island biogeography theory. We observed greater activity at larger forest patches, and although relationships for shape and isolation were not statistically supported the observed patterns were consistent with predictions. Our results demonstrate the need for more in-depth research on the habitat requirements for both migratory and resident bat species and the impact that ongoing urbanization has on local bat populations.Natural Sciences and Engineering Research Council of Canada, RGPIN-2021-02639

Personality Variation in Little Brown Bats

Animal personality or temperament refers to individual differences in behaviour that are repeatable over time and across contexts. Personality has been linked to life-history traits, energetic traits and fitness, with implications for the evolution of behaviour. Personality has been quantified for a range of taxa (e.g., fish, songbirds, small mammals) but, so far, there has been little work on personality in bats, despite their diversity and potential as a model taxon for comparative studies. We used a novel environment test to quantify personality in little brown bats (Myotis lucifugus) and assess the short-term repeatability of a range of behaviours. We tested the hypothesis that development influences values of personality traits and predicted that trait values associated with activity would increase between newly volant, pre-weaning young-of-the-year (YOY) and more mature, self-sufficient YOY. We identified personality dimensions that were consistent with past studies of other taxa and found that these traits were repeatable over a 24-hour period. Consistent with our prediction, older YOY captured at a fall swarming site prior to hibernation had higher activity scores than younger YOY bats captured at a maternity colony, suggesting that personality traits vary as development progresses in YOY bats. Thus, we found evidence of short-term consistency of personality within individuals but with the potential for temporal flexibility of traits, depending on age."Funding was provided by a Natural Sciences and Engineering Research Council (NSERC) Canada Graduate Scholarship to AKM and post-doctoral fellowship to LPM as well as grants to CKRW from NSERC, the Canada Foundation for Innovation, the Manitoba Research and Innovation Fund and Manitoba Hydro Forest Enhancement Program."https://journals.plos.org/plosone/article?id=10.1371/journal.pone.008023

Lack of Foraging Site Fidelity Between Years by Common Nighthawks (Chordeiles minor)

Birds in the family Caprimulgidae generally exhibit high nest site fidelity, but it is not known if fidelity extends to foraging sites, especially for Common Nighthawks (Chordeiles minor), which are otherwise one of the most studied species. Common Nighthawks are ecologically distinct from other caprimulgids, being one of the few true aerial hawking species and among the longest distance migrants in the group. We predicted these birds would exhibit fidelity between years to a foraging site in British Columbia, Canada, where they forage in large numbers on a nightly basis and the same individuals return nightly. We banded individuals and, for a subset of birds, attached transmitters programmed to activate upon return to the foraging area the next year. We estimate we marked approximately 10% of the birds foraging at the site, but did not recapture a single marked bird despite capturing potentially 50% of birds foraging at that site over the two subsequent years. Furthermore, we did not detect any of the subset of birds with radiotransmitters, indicating they did not return to the foraging site in the year following initial capture. Our data suggest low fidelity between years to a foraging site, in contrast with the published records for nesting by this species and with the general expectations for the group.National Geographic Society || Natural Sciences and Engineering Research Council of Canada || Texas Tech University || Southern Illinois Universit

Light enough to travel: migratory bats have smaller brains, but not larger hippocampi, than sedentary species

Migratory bird species have smaller brains than non-migratory species. The behavioural flexibility/migratory precursor hypothesis suggests that sedentary birds have larger brains to allow the behavioural flexibility required in a seasonally variable habitat. The energy trade-off hypothesis proposes that brains are heavy, energetically expensive and therefore, incompatible with migration. Here, we compared relative brain, neocortex and hippocampus volume between migratory and sedentary bats at the species-level and using phylogenetically independent contrasts. We found that migratory bats had relatively smaller brains and neocortices than sedentary species. Our results support the energy trade-off hypothesis because bats do not exhibit the same degree of flexibility in diet selection as sedentary birds. Our results also suggest that bat brain size differences are subtler than those found in birds, perhaps owing to bats' shorter migration distances. Conversely, we found no difference in relative hippocampus volume between migratory and sedentary species, underscoring our limited understanding of the role of the hippocampus in bats

Long-distance Movement over a Period of Days by a Female Myotis lucifugus in Newfoundland, Canada

Myotis lucifugus (Little Brown Myotis) is a regionally migrating bat, widely distributed throughout North America. Through long-term monitoring systems deployed in 2 locations in Newfoundland, Canada, we recorded the movement of an adult female of at least 375 km over a period of 4 nights. Although not the longest travel distance recorded for this species, this observation emphasizes the capabilities of Little Brown Myotis for long-distance flights, the potential connectivity among distant maternity groups, and the value of long-term monitoring programs. To fully understand the movement patterns of Little Brown Myotis, advancements in technology and greater research effort are needed.Natural Sciences and Engineering Research Council of Canada || Newfoundland and Labrador Wildlife Division || Saint Mary’s University || University of Waterlo

Glycerophospholipid Profiles of Bats with White-Nose Syndrome

Pseudogymnoascus destructans is an ascomycetous fungus responsible for the disease dubbed white-nose syndrome (WNS) and massive mortalities of cave-dwelling bats. The fungus infects bat epidermal tissue, causing damage to integumentary cells and pilosebaceous units. Differences in epidermal lipid composition caused by P. destructans infection could have drastic consequences for a variety of physiological functions, including innate immune efficiency and water retention. While bat surface lipid and stratum corneum lipid composition have been described, the differences in epidermal lipid content between healthy tissue and P. destructans–infected tissue have not been documented. In this study, we analyzed the effect of wing damage from P. destructans infection on the epidermal polar lipid composition (glycerophospholipids [GPs] and sphingomyelin) of little brown bats (Myotis lucifugus). We hypothesized that infection would lead to lower levels of total lipid or higher oxidized lipid product proportions. Polar lipids from three damaged and three healthy wing samples were profiled by electrospray ionization tandem mass spectrometry. We found lower total broad lipid levels in damaged tissue, specifically etherlinked phospholipids, lysophospholipids, phosphatidylcholine, and phosphatidylethanolamine. Thirteen individual GP species from four broad GP classes were present in higher amounts in healthy tissue. Six unsaturated GP species were absent in damaged tissue. Our results confirm that P. destructans infection leads to altered lipid profiles. Clinical signs of WNS may include lower lipid levels and lower proportions of unsaturated lipids due to cellular and glandular damage."This project was funded by an Arkansas State Wildlife Grant, the National Speleological Society, the Graduate Program of Environmental Science at Arkansas State University (ASU), the US Fish and Wildlife Service, a Government of Canada Postdoctoral Fellowship (PDRF), the Natural Sciences and Engineering Research Council (NSERC; Canada), the German Academic Exchange Service (DAAD), and the Center for North American Bat Research and Conservation at Indiana State University. Instrument acquisition and method development at KLRC was supported by NSF grants MCB 0455318, MCB 0920663, and DBI 0521587; Kansas Networks of Biomedical Research Excellence (INBRE; National Institutes of Health grant P20 RR16475 from the INBRE program of the National Center for Research Resources); National Science Foundation Experimental Program to Stimulate Competitive Research grant EPS-0236913; Kansas Technology Enterprise Corporation; and Kansas State University."https://www.journals.uchicago.edu/doi/10.1086/68193

Similar hibernation physiology in bats across broad geographic ranges

This is a post-peer-review, pre-copyedit version of an article published in Journal of Comparative Physiology B. The final authenticated version is available online at: http://dx.doi.org/10.1007/s00360-021-01400-xSpecies with broad geographic ranges may experience varied environmental conditions throughout their range leading to local adaptation. Variation among populations reflects potential adaptability or plasticity, with implications for populations impacted by disease, climate change, and other anthropogenic influences. However, behavior may counteract divergent selection among populations. We studied intraspecific variation in hibernation physiology of Myotis lucifugus (little brown myotis) and Corynorhinus townsendii (Townsend's big-eared bat), two species of bats with large geographic ranges. We studied M. lucifugus at three hibernacula which spanned a latitudinal gradient of 1500 km, and C. townsendii from 6 hibernacula spread across 1200 km latitude and 1200 km longitude. We found no difference in torpid metabolic rate among populations of either species, nor was there a difference in the effect of ambient temperature among sites. Evaporative water loss was similar among populations of both species, with the exception of one C. townsendii pairwise site difference and one M. lucifugus site that differed from the others. We suggest the general lack of geographic variation is a consequence of behavioral microhabitat selection. As volant animals, bats can travel relatively long distances in search of preferred microclimates for hibernation. Despite dramatic macroclimate differences among populations, hibernating bats are able to find preferred microclimate conditions within their range, resulting in similar selection pressures among populations spread across wide geographic ranges.Department of Defense Strategic Environmental Research and Development Program || United States Fish and Wildlife Service, Grant F17AP00593 || Texas Tech University || Alberta Conservation Association