Robert M. R. Barclay’s research while affiliated with University of Calgary and other places

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Publications (147)


Seasonal phenology of the little brown bat ( Myotis lucifugus ) at 60° N
  • Article
  • Full-text available

February 2024

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54 Reads

Jesika P. Reimer

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Robert M. R. Barclay

To investigate the impact of short summers and long summer solar periods at high latitudes on the behavior of a nocturnal, hibernating mammal, we recorded the phenology of Myotis lucifugus (little brown myotis) at 60° N in the Northwest Territories (NWT), Canada. In particular, we assessed the timing of spring emergence from, and autumn entry into, hibernation, reproduction, and seasonal mass fluctuations. We used a combination of acoustic monitoring and capture surveys at two hibernacula and two maternity roosts during 2011 and 2012. Myotis spp. were active at the hibernacula from late April to late September/early October, suggesting that the “active” season length is similar to that of populations farther south. At maternity colonies, we detected M. lucifugus activity from early May to early October, with peaks during mid‐July in both years. Lactation, fledging, and weaning all occurred later in the NWT than at more southern locations, and reproductive rates were significantly lower than rates observed farther south. The average mass of individuals fluctuated throughout the season, with an initial decline immediately following emergence from hibernation likely reflecting increased energy expenditure due to flight and decreased use of torpor, coupled with relatively low prey intake due to low prey abundance associated with cool temperatures. Females did not appear to have lower pre‐hibernation masses than those in more southern populations, suggesting that despite the cool spring and autumn temperatures, and short summer nights, bats are able to obtain enough energy for reproduction and mass accumulation for hibernation. However, the lower reproductive rates may indicate that there are limitations to life at the northern limits of the species' range.

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Female little brown bats require both building and natural roosts in a mountainous environment with short summers

December 2023

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20 Reads

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3 Citations

E. W. Micalizzi

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S. A. Forshner

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E. B. Low

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[...]

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R. M. R. Barclay

The little brown bat ( Myotis lucifugus ) is an endangered species that occurs throughout most of North America. The recovery strategy for little brown bats in Canada identifies a need to understand habitat use and protect important bat habitat across the species' Canadian range; however, bat roosting habitat requirements have not been well studied in mountainous environments within the northern part of the species' range. Our objective was to understand the use of building and natural roosts by female little brown bats in the Canadian Rocky Mountains. Over two summers, we captured little brown bats in Banff, Yoho, and Kootenay National Parks, in Alberta and British Columbia, Canada, and tracked 49 females to their day roosts. Buildings were the only roost type used by radio‐tagged bats of all reproductive stages, the dominant roost type used throughout the reproductive period, and the only structures in which we located maternity colonies. Buildings also appeared to shape the distribution of foraging female and reproductive female bats such that few were captured at long distances from towns and building clusters. Compared with bats in more southern and in non‐mountainous areas, bats in our study area had delayed juvenile weaning and volancy, began hibernation early, and had low reproductive rates. We suggest that buildings are a key habitat for female little brown bats to persist at their current levels in our study area, by providing thermal conditions that promote overwinter survival; additional reproductive delays caused by torpor use in cool natural roosts would likely reduce juvenile and adult female overwinter survival below the levels required to sustain populations. Nevertheless, building colonies were unusually small, and bats had relatively low fidelity to particular building roosts, suggesting that building roosts may not consistently meet bats' needs. Some nonreproductive and pregnant females also frequently used natural roosts, particularly after colder nights; these roosts may be important in facilitating torpor and energy conservation for these bats. Because bats are long‐lived with low reproductive output and low juvenile survival, addressing the needs of both reproductive and nonreproductive individuals is important for population persistence.


COSEWIC assessment and status report on hoary bat (Lasiurus cinereus), eastern red bat (Lasiurus borealis), and silver-haired bat (Lasionycteris noctivagans) in Canada

November 2023

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197 Reads

This report provides a review of the population trends and threats to three species of migratory bats in Canada. The report provided the basis of a conservation status assessment for these species by COSEWIC (Committee on the Status of Endangered Wildlife in Canada) in April 2023.


Frugivory and/or nectarivory has evolved repeatedly in mammalian evolution. Images are examples of frugivorous/ nectarivorous species across six orders of mammals: (top left) Rodentia, variegated squirrel (Sciurus variegatoides), image by Amanda Melin; (top middle) Carnivora, kinkajou (Potus flavos), image by Kids Saving the Rainforest; (top right) Primates, Geoffroy's spider monkey (Ateles geoffroyi), image by Amanda Melin; (lower left) Didelphimorphia, woolly opossum (Caluromus derbianus), image by Christian Ziegler, reproduced with permission; (lower middle) Chiroptera, a Seba's short-tailed bat (Carollia perspicillata), image by Roberto Leonan Morim Novaes, reproduced with permission; (lower right) Scandentia, a pen-tailed treeshrew (Ptilocercus lowii), image shared with permission by Annette Zitzmann.
Evolutionary history of ADH7 in mammals included in this study. Per cent fruit and/or nectar included in a species' diet is indicated in the first row of tip annotations. The second row indicates whether any substitutions away from the ancestral alanine are found at site 294 of ADH7 and the third row indicates whether the gene is putatively functional or pseudogenized. Red boxes with the letter psi (ψ) indicate the inferred lineage in which gene loss events occurred, based on putatively shared loss-of-function mutations. Phylogeny via TimeTree ([41]; http://timetree.org), plotted with the R package ggtree [42].
Results of the phylogenetic generalized linear models used to test if a frugivorous and/or nectarivorous diet correlates with amino acid substitutions at site 294 of the ADH class IV enzyme (encoded within exon 7 of ADH7) (a) in mammals overall and (b) in bats only, and (c) if a frugivorous and/or nectarivorous diet correlates with ADH7 gene retention. For each prediction we ran two phylogenetic generalized linear models, the MPLE and the IG10 logistic regression. The slope and p-values for each method are in blue (for the MPLE method) and yellow (for the IG10 method) on each plot. Diet and genotypes of the species included are shown in black, with size of the dot indicating sample size.
Diet and the evolution of ADH7 across seven orders of mammals

July 2023

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179 Reads

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2 Citations

Dietary variation within and across species drives the eco-evolutionary responsiveness of genes necessary to metabolize nutrients and other components. Recent evidence from humans and other mammals suggests that sugar-rich diets of floral nectar and ripe fruit have favoured mutations in, and functional preservation of, the ADH7 gene, which encodes the ADH class 4 enzyme responsible for metabolizing ethanol. Here we interrogate a large, comparative dataset of ADH7 gene sequence variation, including that underlying the amino acid residue located at the key site (294) that regulates the affinity of ADH7 for ethanol. Our analyses span 171 mammal species, including 59 newly sequenced. We report extensive variation, especially among frugivorous and nectarivorous bats, with potential for functional impact. We also report widespread variation in the retention and probable pseudogenization of ADH7. However, we find little statistical evidence of an overarching impact of dietary behaviour on putative ADH7 function or presence of derived alleles at site 294 across mammals, which suggests that the evolution of ADH7 is shaped by complex factors. Our study reports extensive new diversity in a gene of longstanding ecological interest, offers new sources of variation to be explored in functional assays in future study, and advances our understanding of the processes of molecular evolution.


Relationship between the frequency of maximum intensity for echolocation calls and the mass of aerial insectivorous bats (closed circles), other bats (open circles), and CF bats (stars). The regression line for aerial insectivorous bats is frequency = 81.3 kHz −42.0 (log body mass) (figure reprinted from Barclay and Brigham 1991 (Prey detection, dietary niche breadth, and body size in bats: why are aerial insectivorous bats so small? American Naturalist137(5): 693–703. ©1991 by the University of Chicago)).
Papers on echolocation use in interindividual communication.
Interindividual communication by bats via echolocation

November 2022

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101 Reads

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3 Citations

The majority of over 1400 species of bats produce echolocation calls of diverse designs as a means of obtaining information about their surroundings, including the presence of prey. These calls also have the potential to contain information about the caller that can be used by other bats. We review the evidence for information transfer from echolocating bats to intended or unintended conspecifics and heterospecifics. Analysis of call structure and playback experiments on over 50 species in 11 families demonstrate that information regarding the species, population, sex, age, size, and individual identity of the caller is often contained within the calls, and in some cases can be recognized and used by other individuals. Intentional or unintentional (eavesdropping) communication occurs in feeding and roosting situations, as well as between individuals in social interactions such as in mate choice and between mothers and young. We also assess limitations of the research to date and suggest avenues for future research.


Acoustic sampling locations near Whitehorse, Yukon, Canada, surveyed from May to September 2019. Recorded little brown bat (Myotis lucifugus) activity levels are indicated by color. The 900 m elevation cutoff (thick black lines) and roads (thin black lines) are also shown. Low and high activity equals 1–9 and ≥10 bat files per session, respectively.
Regression coefficients (points) and 95% confidence intervals (error bars) from the confidence set of models (ΔQAICc ≤ 6) predicting little brown bat (Myotis lucifugus) distribution near Whitehorse in Yukon, Canada. Different symbols are used for each model, which are described in Table 2. The size and direction of covariate effects are indicated by the coefficient value. Covariates with confidence intervals that do not overlap zero are considered to have a significant effect on bat distribution.
Predicted probabilities of high little brown bat (Myotis lucifugus) activity near Whitehorse, Yukon, Canada, generated using covariates from the confidence set of competing habitat models (ΔQAICc ≤ 6). Solid lines and bar graphs show the predicted covariate effect when all other variables are held constant at their mean. Confidence intervals (95%) are indicated with shading and error bars.
Foraging habitat drives the distribution of an endangered bat in an urbanizing boreal landscape

March 2021

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238 Reads

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12 Citations

The boreal forest is the largest intact forest in the world, and a refuge for species experiencing range retractions as a consequence of climate and landscape change. Yet, large tracts of the boreal forest are threatened by the cumulative impacts of climate change, natural resource extraction, agriculture, and urbanization, perhaps warranting a shift in focus from biodiversity conservation in intact wilderness to that in anthropologically modified landscapes. We investigated landscape features that influence the distribution of the endangered little brown bat (Myotis lucifugus) in an urbanizing boreal landscape at two spatial scales. We hypothesized that little brown bat activity would be influenced by proximity to available building roosts, because roosts are a potential limiting factor for boreal bats. Secondarily, we predicted that bats would use potential foraging habitat, such as waterbodies, and would avoid young, cluttered forests at the landscape scale. We conducted acoustic surveys of bat activity at 210 sites distributed across the study area in Yukon, Canada, within 1-km grid cells. We tested a priori hypotheses with a set of candidate regression models, accounting for spatial autocorrelation. Our hypothesis about the relative importance of anthropogenic roosts was not supported; little brown bats were equally active in urban areas (high building density) and rural areas (low building density), perhaps because roosts were adequately available throughout the region. Instead, habitat use was driven by the distribution of potential foraging habitat, particularly waterbodies, which are important sources of aerial insect prey. Little brown bats also avoided young (≤100-yr-old) forest at the landscape scale (including areas regenerating after fire), which may have been poor foraging or roosting habitat, and used areas with a smaller agricultural and industrial footprint. Our results suggest that waterbodies and mature forest are important little brown bat habitats that should be protected from urban encroachment. Proactive conservation of important habitat for species at risk is still possible throughout much of the boreal forest, where human densities are comparatively low and the urban footprint is currently small.


Mean daily temperature (°C) from 15 May to 6 September in Fort Smith, Northwest Territories, Canada, and Kananaskis, Alberta, Canada. Temperature data were collected from the weather station at the Fort Smith Airport (Environment and Climate Change Canada 2019a) and the BGI Institute (Environment and Climate Change Canada 2019b)
Number of fecal samples that had spiders absent (light grey) and present (black) over the summer months. Panels a and c are samples from Kananaskis, Alberta, Canada, between 1985–1988 and in 2018, whereas panels b and d are samples from Fort Smith, Northwest Territories, Canada, between 2011–2012. Panels a and b show the long-eared myotis (Myotis evotis) and the northern long-eared bat (Myotis septentrionalis), respectively, whereas panels c and d show the little brown bat (Myotis lucifugus). Sample sizes include 54 M. evotis and 58 M. lucifugus from Kananaskis and 50 M. septentrionalis and 56 M. lucifugus from Fort Smith. Data for Fort Smith 2011–2012 were adapted from Kaupas and Barclay (2018). Note: The y axes differ
The mean (±SE) percent volume consumed and the frequency of consumption of seven arthropod orders by the little brown bat (Myotis lucifugus; MYLU) and the long-eared myotis (Myotis evotis; MYEV)
Consumption of spiders by the little brown bat (Myotis lucifugus) and the long-eared myotis (Myotis evotis) in the Rocky Mountains of Alberta, Canada

December 2020

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61 Reads

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8 Citations

Intraspecific variation in diet and (or) foraging behaviour is one way in which species are able to occupy wide geographical areas with variable environments. The little brown bat (Myotis lucifugus (Le Conte, 1831)), a primarily aerial insectivorous bat, consumes spiders in low temperatures at the start and end of summer in Northwest Territories, Canada, but it consumes spiders all summer, even during high aerial insect abundance, in Alaska, USA. There are no competitors of M. lucifugus in Alaska, but there are in Northwest Territories, suggesting that aerial insect abundance and competition from gleaning bats influences when M. lucifugus consumes spiders. In the Kananaskis area of the Rocky Mountains of Alberta, Canada, we investigated spider consumption by M. lucifugus and the long-eared myotis (Myotis evotis (H. Allen, 1864)), a species more adept at gleaning, to better understand when bats consume spiders. Fecal sample analysis indicated that M. evotis consumed spiders all season long, with greater consumption when the bats were caught near water. Myotis lucifugus did not consume spiders at all. This suggests that M. lucifugus opportunistically consumes spiders when encountered, but does not encounter them in Kananaskis where it forages primarily over open water, unlike in Northwest Territories where it forages in the interior of forests and may encounter spiders more frequently.


Distributions of Eastern and Western Red Bats in Western North America

March 2020

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703 Reads

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8 Citations

Western North American Naturalist

The known distributions of eastern red bats and western red bats in western North America have changed greatly over the past 2 decades, resulting in inaccurate range maps and uncertainty regarding the presence or probable absence of these species within states and provinces. We obtained capture and specimen records from the western United States and Canada for 276 eastern red bats and for 863 western red bats. We documented the expansion of the range of eastern red bats in northwestern Canada and clarified the northern and eastern limits of western red bat distribution in the United States. We found that the eastern red bat and western red bat exhibit a mostly allopatric distribution, with western red bats mainly inhabiting warmer, drier forested ecoregions at lower latitudes than those inhabited by eastern red bats. A small zone of overlap between the species was identified only in far western Texas, although it is possible that sympatry may be more widespread due to errors on museum specimen labels and misidentification of captured red bats.


Acoustic Surveys for Bats are Improved by Taking Habitat Type into Account

December 2019

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103 Reads

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8 Citations

Wildlife Society Bulletin

Passive monitoring of bat species via acoustics is a growing field and as a result there are various software programs available that allow for species identification. However, accuracy of these programs is variable and creating a local call library is essential when trying to identify acoustically similar species. In Dinosaur Provincial Park, Alberta, Canada, 3 Myotis species are difficult to distinguish acoustically. We created an echolocation call library from known Myotis evotis, M. lucifugus, and M. ciliolabrum flying in open spaces and near clutter to test whether or not recording in the bats' local habitat type improved call library quality and identification accuracy. Bat calls recorded within open spaces (coulees) differed from those recorded near cluttered spaces (tree edges) for M. ciliolabrum and M. lucifugus. Accuracy of species identification also increased when we used models based on bat calls recorded in cluttered habitats. Using a simple model with recordings from different habitat types within a study site, we were able to improve identification accuracy and model performance. © 2019 The Wildlife Society. Passive monitoring and identification of bat species via echolocation recordings is a growing field, although accuracy of species identification varies and creating a local call library is essential for acoustically similar species. Using a simple model, with recordings from different habitat types within a study site, we were able to improve identification accuracy and model performance.



Citations (87)


... Until the advent of molecular techniques, taxonomy of Myotis bats relied on often minor morphological differences in characters to identify species. Genetic analyses have redefined some bat species classifications (e.g., Hoofer and Van Den Bussche 2003; Racey et al. 2007) and helped to clarify others (e.g., Lausen et al. 2008). In this investigation, we present population genetic evidence that long-eared Myotis groups previously thought to comprise two species (M. ...

Reference:

Population genetics reveal Myotis keenii (Keen’s myotis) and Myotis evotis (long-eared myotis) to be a single species
Beyond mtDNA: nuclear gene flow suggests taxonomic oversplitting in the little brown bat (Myotis lucifugus)

... While both species can be found in cities, big brown bats are especially common in urban areas during Nearctic summers (Neubaum et al., 2006;. For little brown bats, buildings are especially important as maternity roosts in regions without natural roosting habitat; for example, in prairies (Coleman & Barclay, 2011), or in regions with shorter summers and colder temperatures that pose energetic challenges to reproduction, such as at high elevations (e.g., Cryan et al., 2000;Johnson et al., 2019;Micalizzi et al., 2023) or higher latitudes such as Alaska (e.g., Tessler & Snively, 2014). Thus, buildings may provide suitable habitat for reproduction and allow for larger populations than would otherwise be supported (Johnson et al., 2019) and may even have allowed for range expansion into areas with otherwise unsuitable habitat (e.g., prairies and colder climates) as the number of buildings increased in North America (Kunz & Reynolds, 2003;Tessler & Snively, 2014). ...

Female little brown bats require both building and natural roosts in a mountainous environment with short summers
  • Citing Article
  • December 2023

... Fenton (1992) is arguably the first step-by-step hypothetical framework for the evolution of sanguivory in bats and acts as springboard for their lively discussion of this still open question. The use of echolocation for inter-individual communication in bats forms the focus of the contribution by Robert Barclay (C) and David Jacobs (GC) (Barclay and Jacobs 2023). This research area has blossomed into a subfield of its own, stemming largely from the seminal work of Robert's PhD thesis (Barclay 1981). ...

Interindividual communication by bats via echolocation

... In some cases, Coleoptera make up over 80% of the diet, suggesting that E. fuscus is typically a beetle specialist (Phillips 1966;Storm and Whitaker 2008;Feldhamer et al. 2009;Moosman et al. 2012;Long et al. 2013;Clare et al. 2014a;Wray et al. 2018). There are no published reports of Myotis lucifugus (Le Conte, 1831), the little brown bat, consuming periodical cicadas; however, they have also been found to consume invertebrates from many orders such as Araneae, Trombidiformes, Coleoptera, Diptera, Ephemeroptera, Hemiptera, Homoptera, Hymenoptera, Lepidoptera, Neuroptera, Plecoptera, Trichoptera, and Formicidae (Anthony and Kunz 1977;Feldhamer et al. 2009;Clare et al. 2011Clare et al. , 2014bShively et al. 2017;Wray et al. 2018;Maucieri and Barclay 2021). The largest component of the little brown bat diet varies temporally and geographically with Diptera (Antony and Kunz 1977), Ephemeroptera (Clare et al. 2011;Moosman et al. 2012), and Lepidoptera (Clare et al. 2011) being most important. ...

Consumption of spiders by the little brown bat (Myotis lucifugus) and the long-eared myotis (Myotis evotis) in the Rocky Mountains of Alberta, Canada

... Instead of class indices derived from the tree species map, the indices based on the CLC dataset ("Corine Land Cover" in the Appendix) were integrated. While the application of land cover information (e.g., Amini Tehrani et al., 2020;Bandara et al., 2022;Bellamy et al., 2020;Cable et al., 2021;Luo et al., 2020;Thomas et al., 2021;Wright et al., 2021) and/or landscape information via Fragstats or the R package landscape metrics is common in habitat modeling (e.g., Cable et al., 2021;Neubaum & Aagaard, 2022;Thomas et al., 2021), the highest resolution for forest classes typically extends no further than the categories provided by CLC, namely broadleaf, coniferous, or mixed forest (e.g., Amini Tehrani et al., 2020;Andersen et al., 2022;Bandara et al., 2022;Cable et al., 2021;Thomas et al., 2021;True et al., 2021). Therefore, the GVM approach incorporates all indices derived from the CLC dataset, amounting to 133 indices (compared to 265 for the tree species map variables with six classes for forest). ...

Foraging habitat drives the distribution of an endangered bat in an urbanizing boreal landscape

... Lasiurus frantzi (Peters, 1870) (Western Red Bat).-Known in Texas by a single specimen obtained in 1988 in the Sierra Vieja of Presidio County and a recent record from Starr County in the Lower Rio Grande Valley of southern Texas (Schmidly et al. 2022). Eastern and Western Red Bats exhibit a mostly allopatric distribution in the US, but there appears to be a zone of overlap in far western Texas and possibly in Hidalgo County in southern Texas (Solick et al. 2020). Thus, naturalists should be on the lookout for additional records of both species in these regions. ...

Distributions of Eastern and Western Red Bats in Western North America

Western North American Naturalist

... Staton and Poulton, 2012), its application in bird field studies is new. However, algorithms for automated vocalisation ID can have high false positive rates of species ID (Findlay and Barclay, 2020;Ware et al., 2023). With their increase in popularity, there is an urgent demand for further research into the capabilities and drawbacks of these novel monitoring methods when applied to real-life, farm-scale context (Gibb et al., 2019;Pérez-Granados, 2023), such as their potential use for monitoring the biodiversity benefits of planting hedgerows within AES to support future AES design and promote the uptake of hedgerow planting and management options. ...

Acoustic Surveys for Bats are Improved by Taking Habitat Type into Account
  • Citing Article
  • December 2019

Wildlife Society Bulletin

... The minimum roosting area of maternity colonies varies greatly depending on habitat contiguity, with estimates ranging from 0.3 to 88.4 ha (Henderson & Broders 2008, Gorman et al. 2022a; therefore the 200 m buffer represents an average minimum roosting area. Because home-range sizes for northern myotis are larger than the spacing between our sampled sites, results may be interpreted as relative habitat use at the local scale (Thomas et al. 2019). Covariates were estimated using the 2016 NLCD (Dewitz & USGS 2019) for Long Island and the 2016 C-CAP Land Cover Massachusetts Land Cover/Land Use Dataset (OCM 2023) for Martha's Vineyard and Nantucket. ...

Site occupancy of little brown bats (Myotis lucifugus) in response to salvage logging in the boreal forest
  • Citing Article
  • June 2019

Forest Ecology and Management

... These complexities are further evident in studies that have sampled species' responses over multiple years: inter-annual variation in response to air pollution was observed in almost half the studies in which it was tested (Table 4). For example, effects of pollution on juvenile traits of the Tree Swallow (Tachycineta bicolor) living along a pollution gradient in Canada were sensitive to precipitation, diet, sex and the order of hatching (Godwin et al., 2019). However, these responses varied across the three years in which measurements were taken, highlighting the difficulties in interpreting the results of field-based studies where multiple factors affect response parameters simultaneously and the risks to correct inference from conducting studies in one year only. ...

Tree Swallow (Tachycineta bicolor) nest success and nestling growth near oil sands mining operations in northeastern Alberta, Canada

... Snowshoe hares (Lepus americanus) and red squirrels (Tamiasciurus hudsonicus) are considered to be keystone species in the boreal and boreal-like forest due largely to their role as primary prey for a number of predators, including species of concern, such as Canada lynx (Lynx canadensis; Armstrong et al., 2011;Hodges, 2000aHodges, , 2000bIvan and Shenk, 2016;Rusch and Reeder, 1978). Throughout their range, snowshoe hare density is strongly, positively associated with horizontal, or lateral cover (Nudds, 1977) within 0-2 m of the ground which affords them both hiding cover and food (Hodges, 2000a(Hodges, , 2000bHolbrook et al., 2016;Ivan et al., 2014;Thomas et al., 2019). Consequently, snowshoe hare abundance generally peaks in early to mid-successional stands across their range (Hodges, 2000a(Hodges, , 2000bKoehler, 1990), with a potential second peak in old forests where canopy gaps maintain dense understory patches (Hodson et al., 2011). ...

Salvage logging after an insect outbreak reduces occupancy by snowshoe hare (Lepus americanus) and their primary predators

Global Ecology and Conservation