Little brown myotis, northern myotis and tri-coloured bat: COSEWIC assessment and status report 2013

Document Information

Committee on the Status of Endangered Wildlife in Canada (COSEWIC) status reports are working documents used in assigning the status of wildlife species suspected of being at risk. This report may be cited as follows:

COSEWIC. 2013. COSEWIC assessment and status report on the Little Brown Myotis Myotis lucifugus, Northern Myotis Myotis septentrionalis and Tri-colored Bat Perimyotis subflavus in Canada. Committee on the Status of Endangered Wildlife in Canada. Ottawa. xxiv + 93 pp. (Species at Risk Public Registry website).

Previous report(s):
COSEWIC. February 2012. Technical summary and supporting information for an emergency assessment of the Little Brown Myotis Myotis lucifugus in Canada. Committee on the Status of Endangered Wildlife in Canada. Ottawa. 29 pp.

COSEWIC. February 2012. Technical summary and supporting information for an emergency assessment of the Northern Myotis Myotis septentrionalis in Canada. Committee on the Status of Endangered Wildlife in Canada. Ottawa. 24 pp.

COSEWIC. February 2012. Technical summary and supporting information for an emergency assessment of the Tri-colored Bat Perimyotis subflavus in Canada. Committee on the Status of Endangered Wildlife in Canada. Ottawa. 25 pp.

For additional copies contact:

COSEWIC Secretariat
c/o Canadian Wildlife Service
Environment Canada
Ottawa, ON
K1A 0H3

Tel.: 819-953-3215
Fax: 819-994-3684
COSEWIC E-mail
COSEWIC web site

Également disponible en français sous le titre Ếvaluation et Rapport de situation du COSEPAC sur la Petite chauve-souris brune (Myotis lucifugus), Chauve-souris nordique (Myotis septentrionalis) et Pipistrelle de l’Est (Perimyotis subflavus) au Canada.

Cover illustration/photo:
Little Brown Myotis, Northern Myotis and Tri-colored Bat -- Photograph of Myotis bats, several of which have the white muzzle typical of White-nose Syndrome. Photo taken March 17, 2011, Berryton Cave, New Brunswick. (photo used with permission: K. Vanderwolf, NB Museum).

©Her Majesty the Queen in Right of Canada, 2014.

Catalogue No. CW69-14/688-2014E-PDF
ISBN 978-1-100-23569-1

COSEWIC Assessment Summary

COSEWIC Executive Summary

Little Brown Myotis
Myotis lucifugus

Northern Myotis
Myotis septentrionalis

Tri-colored Bat
Perimyotis subflavus

Wildlife Species Description and Significance

All three bat species are small (average 7.4 g), brown-pelaged, insectivorous species of the Family Vespertilionidae. Little Brown Myotis (Myotis lucifugus) likely is the most common bat species in Canada and the most familiar of the three species to the public because they often use buildings as day-roosts and forage in areas where they are visible (e.g., over lakes, aound streetlights, etc.). Northern Myotis (M. septentrionalis) are common in forests and Tri-colored Bat (Perimyotis subflavus) is found in variety of habitats, but is rarer than the other two. Public concern over zoonotic diseases (i.e., rabies, histoplasmosis), noise, and hygiene has resulted in periodic extermination of maternity colonies and/or elimination of their roosts. Bats are predators of insects, some of which are considered pests in the agriculture and forestry sectors, and provide an important ecological service in this regard.

Distribution

In Canada, Myotis lucifugus and M. septentrionalis occur from Newfoundland to British Columbia, and northward to near the treeline in Labrador, Northwest Territories (NT) and the Yukon. Perimyotis subflavus occurs in Nova Scotia (NS), New Brunswick (NB), Quebec, and Ontario. All three species occur in much of the eastern half of the United States (US), and M. lucifugus extends to the US west coast, including Alaska.

Habitat

All three species overwinter in cold and humid hibernacula (caves/mines). Their specific physiological requirements limit the number of suitable sites for overwintering. In the east, large numbers (i.e., >3000 bats) of several species typically overwinter in relatively few hibernacula. In the west, there are fewer known hibernacula, and numbers appear lower per site. Females establish summer maternity colonies, often in buildings (mainly Myotis lucifugus), or large-diameter trees. Foraging occurs over water (mainly M. lucifugus, P. subflavus), along waterways, forest edges, and in gaps in the forest (mainly M. septentrionalis). Large open fields or clearcuts generally are avoided. In autumn, bats return to hibernacula, which may be hundreds of kilometres from their summering areas, swarm near the entrance, mate, and then enter that hibernaculum, or travel to different hibernacula to overwinter.

Biology

Breeding is promiscuous. Females produce one pup (potentially two in Perimyotis subflavus) after one year of age. Maximum recorded longevity is 15 years (P. subflavus) to >30 years (Myotis lucifugus). Survivorship is low in year one, then highly variable (e.g., 0.6-0.9) afterwards. Generation time is estimated as 5-10 years for M. lucifugus and M. septentrionalis, and 5-7 years for P. subflavus. Finite population growth rate is slow, with a range of 0.98-1.2.

Population Sizes and Trends

Population sizes are unknown but were likely over a million for each of the Myotis species prior to the 2010 arrival in Canada of White-nose Syndrome (WNS), a disease caused by a cold-loving fungus Pseudogymnoascus destructans (Pd), likely originating in Europe. M. lucifugus and M. septentrionalis were considered to be common in much of their range in eastern Canada and northeastern US, and are still common in Canada outside the range of WNS. Perimyotis subflavus was considered rare to uncommon in parts of Canada. Approximately 95% of the hibernating Myotis bats that have been counted occur in the range from Nova Scotia to Manitoba, with relatively few bats having been recorded west of Manitoba. However, the number in the north and west is considered an underestimate and the proportion of the populations of the two Myotis that has been affected by WNS since its arrival in Canada is unknown. During 2006-2012, an estimated 5.7-6.7 million bats in eastern North America died due to WNS. M. lucifugus is predicted to be functionally extirpated (i.e., <1% of former population) by 2026 in northeastern US. The same prediction likely applies to M. septentrionalis because of similar life history traits. P. subflavus populations have declined in the US by approximately 75%.

WNS has been recorded in Ontario, Quebec, NB, NS, and Prince Edward Island (PEI). Most population trend data are derived from counts in some of the few, known hibernacula. Data on Myotis lucifugus and M. septentrionalis often are combined but percent change is assumed to be equal between species.Declines recorded at hibernacula having pre- and post-WNS data have been catastrophic: 93% (Ontario); 99% (NB), 93% (NS) for Myotis combined, and 98% for M. lucifugus and 99.8% for M. septentrionalis in Quebec. The total decline in Myotis bats known to be present in NS, NB, Ontario, and Quebec hibernacula from the time of WNS arrival to most recent data for the same sites is 94% (86,952 to 5,225). Relatively few Perimyotis subflavus occur in Canada and it is difficult to determine trends; declines of 94% and 75% were recorded in caves in Quebec and NB, respectively. Trend data on bats in summer are limited but are similar to winter data, suggesting winter hibernacula data likely are an accurate reflection of declines in the population. Extent of occurrence has not declined, and may not in the future if very low numbers persist across the species’ ranges. Major population declines have not been reported outside WNS range.

WNS was first recorded in Canada in spring 2010, and has spread in all directions from the epicentre in northern New York at a rate of 200-250 km/yr. There is uncertainty about the rate of spread to the western range of the two Myotis species. The amount of east-west bat movements, and the wintering ecology and hibernacula conditions that may affect the ecology of the disease in western and northern Canada, are largely unknown. However, predictions that WNS will spread throughout the range of both species rest upon: 1) no evidence of containment to date; 2) evidence that abiotic conditions in western hibernacula are conducive to Pd growth; and 3) evidence that hibernacula with lower bat densities are still susceptible to WNS. Model predictions and present rate of spread suggest that WNS will reach the western edge of M. lucifugus range in 12-18 yrs, and western edge of M. septentrionalis in 12-15 yrs, or within three generations, which is 15-30 yrs. There are also concerns WNS may move more quickly to western Canada if transmitted via human clothing from infected caves. The Canadian range of P. subflavus already is contained within WNS range.

Rescue effect is not likely because mortality is high in adjacent areas of the US and any future immigrants likely will be vulnerable to Pd. A few sites near the epicentre have possibly stabilized at approximately 1,000 bats for several years (albeit following >90% decline), but it is unknown if these numbers indicate survival, or movement between hibernacula. There is the hope that some individuals have genetically based resistance to WNS and they will survive and reproduce resistant offspring. However, the slow population growth rate of all three species means populations would take many generations to recover.

Threats and Limiting Factors

Other threats besides WNS include colony eradication, chemical contamination, change in forest structure, and wind turbines. Although cases of colony eradication have been documented (mainly chemical or physical destruction of maternity colonies of Myotis lucifugus in buildings), the overall number of colonies exterminated, or impacts on the larger-scale population is unknown. The extent of disturbance by people on hibernating bats and the impacts of chemical contamination on bats, or insecticide on prey availability, are unknown. To date, the impact of wind turbines is highly variable among sites, but generally they have been less of a mortality factor on the three species than on other bat species that conduct long-distance migration. There is potential concern for M. lucifugus in some regions of Canada where higher mortality has been recorded.

Protection, Status, and Ranks

Regulations protecting bats vary across their range; removal of maternity colonies is permitted but some hibernacula are closed to the public. Ontario listed M. lucifugus and M. septentrionalis as Endangered, due to WNS, in autumn 2012. Both NB and NS listed all three species as Endangered in summer 2013.

NatureServe ranks for Perimyotis subflavus are Global; G3 (vulnerable), National; N2N3, and S1 (critically imperilled) to S3 at the sub-national level. Myotis lucifugus (G3; N3) and M. septentrionalis (G1G3; N2N3) are ranked sub-nationally as apparently secure-secure (S4-S5) over much of their range, although jurisdictions within the area affected by WNS changed status to vulnerable or endangered in the last year, or are conducting a review because of WNS.

Technical Summary (Little Brown Myotis)

Technical Summary (Northern Myotis)

Technical Summary (Tri-colored Bat)

Preface

In October 2011, the Province of Nova Scotia requested an emergency assessment on three species of bat, Little Brown Myotis (Myotis lucifugus), Northern Myotis (M. septentrionalis), and Tri-colored Bat (Perimyotis subflavus). The request was due to: concerns regarding the mortality levels from White-nose Syndrome (WNS) on various bat species in the northeastern United States since 2006; the apparent rate of spread of the disease; and its confirmation in NS, NB, Quebec, and Ontario. WNS is caused by a fungus, Pseudogymnoascus destructans (previously called Geomyces destructans, and hereafter referred to as Pd). In November 2011, the Chair of COSEWIC decided to proceed, and G. Forbes, the co-chair of the Terrestrial Mammals Subcommittee prepared a summary document with supporting evidence of the emergency condition. An Emergency Assessment Subcommittee met in February 2012 and made a recommendation to assign endangered status on an emergency basis to each species, which the Chair of COSEWIC communicated to the Minister of the Environment.

The rationale for the recommendation was: 1) catastrophic population declines have occurred in all three species in northeastern United States and similar impacts have occurred in Canada, with inference that future impacts to Canada will be same as had occurred in the United States; 2) a population model for Myotis lucifugus (considered applicable also to M. septentrionalis and P. subflavus), predicts functional extirpation (decrease to <1% of population) by 2026 for the northeastern region; and 3) predicted rate of spread was fast enough to impact >50% of the Canadian population within three generations. The criteria for designation for all three species were A3bce, A4bce, E.

As per COSEWIC policy, the three species were referred to the Terrestrial Mammals Subcommittee for immediate status report preparation and deliberation through the full COSEWIC process. The Species at Risk Act mandates the preparation of a full status report and a reassessment of the species within one year of an emergency listing decision by the Minister. At the time of COSEWIC’s November 2013 assessment no such decision had been made. All three species are addressed here in a single status report because WNS was considered to be the dominant threat and it is common to all, and the biology of the species is sufficiently similar.

COSEWIC History

The Committee on the Status of Endangered Wildlife in Canada (COSEWIC) was created in 1977 as a result of a recommendation at the Federal-Provincial Wildlife Conference held in 1976. It arose from the need for a single, official, scientifically sound, national listing of wildlife species at risk. In 1978, COSEWIC designated its first species and produced its first list of Canadian species at risk. Species designated at meetings of the full committee are added to the list. On June 5, 2003, the Species at Risk Act (SARA) was proclaimed. SARA establishes COSEWIC as an advisory body ensuring that species will continue to be assessed under a rigorous and independent scientific process.

COSEWIC Mandate

The Committee on the Status of Endangered Wildlife in Canada (COSEWIC) assesses the national status of wild species, subspecies, varieties, or other designatable units that are considered to be at risk in Canada. Designations are made on native species for the following taxonomic groups: mammals, birds, reptiles, amphibians, fishes, arthropods, molluscs, vascular plants, mosses, and lichens.

COSEWIC Membership

COSEWIC comprises members from each provincial and territorial government wildlife agency, four federal entities (Canadian Wildlife Service, Parks Canada Agency, Department of Fisheries and Oceans, and the Federal Biodiversity Information Partnership, chaired by the Canadian Museum of Nature), three non-government science members and the co-chairs of the species specialist subcommittees and the Aboriginal Traditional Knowledge subcommittee. The Committee meets to consider status reports on candidate species.

Definitions (2013)

The Canadian Wildlife Service, Environment Canada, provides full administrative and financial support to the COSEWIC Secretariat.

Wildlife Species Description and Significance

Name and Classification

Class:

Mammalia

Order:

Chiroptera

Family:

Vespertilionidae

Scientific name:

Myotis lucifugus (LeConte 1831)

Scientific name:

Myotis septentrionalis (Trouessart 1897)

Scientific name:

Perimyotis subflavus (Cuvier 1832)

Common Names:

For M. lucifugus: Little Brown Myotis or Little Brown Bat (English) and Petite chauve-souris brune (French). For M. septentrionalis: Northern Myotis, Northern Long-eared Myotis or Northern Long-eared Bat (English) and Chauve-souris nordique (French). For P. subflavus: Tri-colored Bat or Eastern Pipistrelle (English) and Pipistrelle de l’Est (French).

Myotis lucifugus has been recognized as a species for over a century. M. septentrionalis was formerly considered a subspecies of M. keenii (van Zyll de Jong 1979) but the two species have numerous morphological differences and their ranges do not overlap; M. septentrionalis is now recognized as a species (Wilson and Reeder 2005). Perimyotis subflavus was previously called Pipistrellus subflavus (Eastern Pipistrelle) but the genus and common name were changed based on taxonomic work that indicated that this taxon differed significantly from European pipistrelles, in both morphology and genotype (Hoofer et al. 2006).

Morphological Description

All three bat species (Figure 1) are small-bodied bats typical of the Vespertilionidae, the plain-nosed bats. External characteristics, with measurements from Canadian specimens (van Zyll de Jong 1985), are used here to describe the three species below:

Figure 1: Images of the three bat species; clockwise, from top left; Myotis lucifugus (dead bat with visual signs of WNS on muzzle ears and wings; Berryton Cave, NB); M. septentrionalis (with visual signs of WNS on forearm; Lake Charlotte, NS); Perimyotis subflavus (Hayes Cave, NS). Note the elongated ears and pointed tragus typical of M. septentrionalis. (Photo credits: M. lucifugus: K. Vanderwolf; M. septentrionalis and P. subflavus: H. Broders.)

Myotis lucifugus:

A small to medium-sized (Avg. mass 7.9 g; range 5.5-11.0 g; wingspan 22-27 cm) brown-pelaged bat. The tragus is short and blunt (Fenton and Barclay 1980; van Zyll de Jong 1985).

Myotis septentrionalis:

This species is very similar in colour and size (Avg. mass 7.4 g; range 4.3-10.8 g; wingspan 23-26 cm) to M. lucifugus but distinguished by their long, slender, and pointed tragus, and ears that extend beyond the nose when pressed forward (van Zyll de Jong 1985; Caceres and Barclay 2000).

Perimyotis subflavus:

A small bat (Avg. mass 6.9 g; range 6-7.9 g; wingspan 20-26 cm) identifiable, as adults, by distinctive tri-coloured hairs.

Population Structure and Variability

There is weak population genetic structure within Myotis lucifugus (Dixon 2011)and M. septentrionalis (Arnold 2007). The lack of strong structure likely is due to their vagility (i.e., seasonal movements of several hundred km; see Migration section) and swarming behaviour in autumn, during which bats from a large area mix and mate (Fenton 1969). Any existing structure may result from females returning each year to the same maternity colonies where they were born (i.e., natal philopatry). Analyses of microsatellite loci of female M. septentrionalis indicate local-scale population structuring, which suggests that dispersal is greater in males (Arnold 2007). Philopatry is not well understood because some females move between maternity colonies within and between years (Watt and Fenton 2008; Dixon 2011).

Perimyotis subflavus females also show philopatry to maternity colonies each year (Griffin 1934; Veilleux and Veilleux 2004) and presumably have similar population genetic structure as M. lucifugus. There are no published data on genetic structuring in P. subflavus.

Designatable Units

Myotis lucifugus:

The taxonomy of Myotis lucifugus in western Canada and the United States (US) is under debate. Four of six subspecies recognized by van Zyll de Jong (1985) are found in Canada. Myotis l. lucifugus is found from Newfoundland (NL) to British Columbia (BC) and eastern Yukon, while M. l. alascensis is found in BC and western Yukon (Lausen et al. 2008; T. Dewey and B. Slough, unpub. data). M. l. carissima is in the Okanagan region of BC, and M. l. pernox in the Rocky Mountains. The subspecies designations are based on size (mainly forearm length) and pelage colour. More recent analyses based on genetics have led to a debate ranging from whether M. lucifugus in western Canada are actually separate species or not even subspecies. Preliminary population genetic studies on M. lucifugus on either side of the Rocky Mountain Continental Divide suggested evidence of genetic structuring (Russel et al. 2012) supporting some morphological differentiation (i.e., significant forearm differences east vs west of Rocky Mountains; C. Lausen unpub. data). Analyses using mtDNA suggested that the four western subspecies may be separate species (Carstens and Dewey 2010; Dewey 2006). The subspecies in BC and Alaska (M. l. alascencis) has been suggested as a separate species (ADFG 2013). However, Lausen et al. (2008) concluded that the validity of using mtDNA to determine subspecies of this group is problematic and, based on nuclear DNA analyses, determined that even the subspecific status for one (M. l. carissima) is invalid. Also, Lausen et al. (2008) question the validity of other subspecies because haplotypes of one subspecies (M. l. lucifugus) were found within the ranges of the other subspecies (Carstens and Dewey 2010; Dewey 2006). In addition, differences in pelage were not consistent to either putative subspecies.

In conclusion, differences in morphology and genotype somewhat exist in western M. lucifugus range, but it is unlikely that designatable units (DUs) can be applied for any species across their range because uniqueness and significance has not been established. The same situation applies in eastern Canada; genetic analyses of bats in Newfoundland and Labrador (NL) are underway, but not complete (B. Rodrigues, pers. comm.) and it is unknown if M. lucifugus (and M. septentrionalis) on NF are isolated and distinct. The distribution of M. lucifugus in Canada is continuous (with the possible exception of NF) and, in lieu of clarity on taxonomy in western Canada and NF, and a confirmation of uniqueness and significance, the report recognizes a single designatable unit.

Myotis septentrionalis:

Systematic research on M. septentrionalis is limited. No Canadian subspecies are recognized (van Zyll de Jong 1985). There are no apparent barriers to the movement of subpopulations in Canada. M. septentrionalis in Canada are considered to comprise a single designatable unit.

Perimyotis subflavus:

The Canadian population is assigned to P. s. subflavus (van Zyll de Jong 1985). There is a possibility that P. subflavus in NS are isolated from the rest of the population (Broders et al. 2003) and warrant subspecies status because of morphometric differences (Hunyh 2010, H. Broders, unpub. data) including larger average size (Poissant and Broders 2008). However, genetic analyses did not identify uniqueness (Hunyh 2010), although more work is required. Also, isolation has not been confirmed. A single designatable unit is proposed for use in this report.

Special Significance

The public have both negative and positive attitudes towards bats. Negative attitudes relate to their secretive, nocturnal habits, and their association with diseases such as rabies and histoplasmosis. Bats are viewed positively because they consume insects, many of which are considered pests in the forestry, agriculture, and health sectors. Individual Myotis lucifugus each consume 4-8 g of insects per night (Anthony and Kunz 1977; Kurta et al. 1989) and a decline of one million bats equates to a potential reduction in consumption of 660-1,320 metric tons annually (Boyles et al. 2011). The most recent estimate of a minimum decline of 5.7 million bats from White-nose Syndrome (WNS) (see Population Sizes and Trends and Threats) equates to reduction in consumption of 3,762-7,523 metric tons annually. A reduction in bats has been shown to result in increased populations of some insect species (Wilson and Barclay 2006; Kalka et al. 2008; Williams-Guillen et al. 2008). Given the small scale of inquiry of these studies, the relationship between bat and insect populations at a regional level is difficult to establish because the compensatory or additive response by insects to bat predation is unknown. If bat predation is the limiting factor in the insect population then removal of bats could increase insect populations.

The economic value of bats has been estimated based on the cost to farmers if they had to control insects not removed by bats. Based on work in Texas on the consumption of various agricultural pests by Mexican Free-tailed Bat (Tadarida brasiliensis), the cost to farmers would approximate US$22.9 billion per year if all insect-eating bats were removed (Cleveland et al. 2006; Boyles et al. 2011). It is not known how well these data on Tadarida in Texas apply to smaller Myotis species in the northeast. The impact to the forestry industry is not known but numerous Lepidopteran pests are consumed by bats (e.g., spruce budworm, Choristoneura spp.) (Wilson and Barclay 2006) and decreases in wood production may occur with reduced levels of bat depredation. The impact to society and environment of increased pesticide use (e.g., water quality, health, conflict) would be an additional cost. The value of bats in suppressing mosquito-borne diseases (e.g., West Nile virus) is unknown.

Distribution

Global Range

Myotis lucifugus:

This species is distributed over much of North America, including the Sierra Nevada range of Mexico, and into Alaska (Figure 2). They are rare to absent in much of Texas and Florida, and north of the treeline in Canada and Alaska (van Zyll de Jong 1985).

Figure 2: Approximate distribution of Myotis lucifugus and White-nose Syndrome, as of August 2013. See text for details on bat distribution; some records in NT and Nunavut (indicated with ‘?’) are probable but unconfirmed, or may be extralimital. WNS map contains locations of confirmed Pseudogymnoascus destructans and clinical WNS characteristics (see Figure 5; National Wildlife Health Center 2013). (Map created by J. Wu, COSEWIC Secretariat.)

Myotis septentrionalis:

The range covers much of North America, although it is smaller than that of M. lucifugus and located more eastward, particularly in the US where the species is absent in the mid-western US (Figure 3). M. septentrionalis can be found in a few sites in the southeastern US (i.e., Alabama, North Carolina) but is generally rare south of the Appalachian mountain range (van Zyll de Jong 1985). The species appears more common in northern parts of its range.

Figure 3. Approximate distribution of Myotis septentrionalis and White-nose Syndrome, as of August 2013. See text for details on bat distribution. WNS map contains locations of confirmed Pseudogymnoascus destructans and clinical WNS characteristics (see Figure 5; National Wildlife Health Center 2013). (Map created by J. Wu, COSEWIC Secretariat.)

Perimyotis subflavus:

P. subflavus is an eastern North American species that ranges from the Maritimes to the Great Lakes, and south to the eastern coast of Central America (van Zyll de Jong 1985; Figure 4). The species appears to be expanding its range westward into the US prairies, possibly by using new dams and mines for hibernacula (Geluso et al. 2004).

Figure 4. Approximate distribution of Perimyotis subflavus and White-nose syndrome, as of August 2013. See text for details on bat distribution. WNS map contains locations of confirmed Pseudogymnoascus destructans and clinical WNS characteristics (see Figure 5; National Wildlife Health Center 2013). Question marks indicate areas where status of P. subflavus is uncertain. (Map created by J. Wu, COSEWIC Secretariat.)

Figure 5. Location of confirmed and suspected cases of White-nose syndrome in North America, as of September 2013. Suspected cases are positive tests for Pseudogymnoascus destructans (Pd), confirmed cases are where mortality events have occurred. First record was in Albany, New York in February 2006 (coincides with circle on map key). A suspected case in Oklahoma is 2400km from epicentre. Pd was recorded in northeastern Minnesota near the Canadian border, in 2012. (Source: National Wildlife Health Center 2013.)

Canadian Range

Myotis lucifugus:

Approximately 50% of this species’ global range is in Canada, and it occurs in every province and territory, with occasional records in southwestern Nunavut (Figure 2). It occurs throughout much of NF and south-central Labrador, and across Canada below tree-line to the Pacific Ocean, including Haida Gwaii and Vancouver Island (van Zyll de Jong 1985; Grindal et al. 2011; Burles et al. 2014). Its distribution at the northern range boundary is less defined because of less survey effort, the large expanse of land, and lack of knowledge of hibernacula location. M. lucifugus is found across the southern third of the NT and south of 64° in the Yukon (Slough and Jung 2007) but it is unknown whether they hibernate in the Yukon. Scattered records exist further north than the range shown in Figure 2, but it is unknown if these are extralimital records or residents (J. Wilson, pers. comm.). The most northerly hibernaculum known is in NT, between 60-61° latitude, and there is one suspected but not confirmed site near 65° (J. Wilson, pers. comm.).

Myotis septentrionalis:

Approximately 40% of this species’ global range is in Canada. The species has been recorded from parts of Newfoundland westward and south of the treeline to the Yukon and northern BC (van Zyll de Jong 1985; Brown et al. 2007; Henderson et al. 2009; Park and Broders 2012; Broders et al. 2013; Reimer and Kaupas 2013) (Figure 3). It is absent from the Canadian prairies (Lausen 2009) but can be found on the western slopes of the Selkirk Mountains from Trout Lake, BC, northwards, and in the coastal mountains of northern BC (Caceres 1998; Lausen and Hill 2010). Breeding is confirmed in Yukon (Lausen et al. 2008) and NT (J. Reimer, unpub. data). M. septentrionalis appear to be common in the oil sands region (Grindal et al. 2011) and exist in southern parts of NT, west to the Liard River watershed of northern BC and southeastern Yukon. Overwintering has not been recorded in the Yukon (Jung et al. 2006; Slough and Jung 2007) but is likely in NT (J. Wilson, pers. comm.); M. septentrionalis have been captured mid-September flying into the single known hibernacula for M. lucifugus in southeastern NT (Lausen 2011).

Perimyotis subflavus:

Approximately 15% of this species’ global range is in Canada. The range of P. subflavus in Canada is the smallest of the three species, with the species having been recorded only in southern parts of NS, NB, Quebec, and central Ontario, southward (van Zyll de Jong 1985; Fraser et al. 2012; Figure 4). Broders et al. (2003) suggested that the population in southeastern NS may be isolated. Breeding occurs in NS (H. Broders, pers. comm. 2012; Broders et al. 2003) but is uncertain for NB (Broders et al. 2001).

The extent of occurrence (EO) for the three species was not calculated because the range covers much of Canada for the Myotis spp., and from NS to the southern half of Ontario for Perimyotis subflavus; the EO for each species is well over 20,000 km², exceeding the relevant threshold for COSEWIC critieria. Index of area of occurrence (IAO) also was not calculated because the EO and IAO would essentially be the same area; these bat species forage widely over many habitats. It would have been informative to construct an IAO on just hibernacula because hibernacula likely are the most important spatial feature for survival; however, most hibernacula have not been mapped.

Search Effort

The distribution of bats in Canada was delineated from observational surveys using mist-netting and ultrasonic detectors that can detect echolocation calls. The search effort in more remote areas is limited but the general distribution and relative abundance of the species has been established across their range. Intensive fieldwork and research programs (i.e., capture and echolocation surveys at multiple sites, banding, radio-tagging over multiple years) has been ongoing in parts of Quebec, Ontario, MB, and BC for over 40 years, and nearly as long in parts of the Prairies. Similar field research began in the 1990s in NB, NS, and the Yukon, and after 2000 in NL, PEI, and NT.

Monitoring of bat populations was localized before the arrival of WNS, mainly because species like Myotis lucifugus were considered ubiquitous and the other two species were not conservation priorities. Most summer surveys were conducted over small areas and for short periods of time and focused mainly on relative abundance and habitat use. Systematic surveys are lacking for most of the range.

The number and location of most hibernacula are unknown because hibernacula are difficult to locate. Caves and abandoned mines have the most potential as hibernacula but often are unsafe to enter to conduct winter hibernacula counts. Researchers may be able to establish use by documenting activity at the entrance during the fall swarming season and spring emergence, but equipment and staff required to monitor bats acoustically or trap and identify bats is not widely available. Caves and mines known to contain large numbers of bats occur in the Maritimes, southern Quebec, and Ontario, but more are being discovered (M. Elderkin, pers. comm.; Fenton 1970a; Mainguy et al. 2011; D. McAlpine and H. Broders, pers. comm. 2012; C. Willis, pers. comm.). No natural hibernacula are known in PEI (Henderson et al. 2009) and a single large (i.e., 1,000 bats) and several small (i.e., <20 bats) are known in Newfoundland (S. Moores, pers. comm. 2012).Information on hibernacula in the northern parts of their range (e.g., Labrador and northern Quebec, westward) is very limited. New surveys have begun in various mines in Kirkland Lake, North Bay, and Algoma District of northcentral Ontario (P. Davis, pers. comm.). A number of sites between Wawa, Ontario and Winnipeg, Manitoba are known (Dubois and Monson 2007) but few hibernacula are recorded in much of the western range of M. lucifugus and M. septentrionalis. In Alberta, four hibernacula are known (Schowalter 1980; Lausen and Barclay 2006, Hobson, pers. comm.). A single winter hibernaculum for M. lucifugus recently was discovered in southern NT (Lausen 2011) and no winter hibernacula have been recorded in the Yukon, to date (Jung et al. 2006).

In most jurisdictions, only a subset of the known hibernacula are surveyed. In Newfoundland, hibernacula have been monitored since 2009, with consistent methods at two hibernacula since 2011. The main known hibernacula in NS have been internally surveyed for the last several years (H. Broders, pers. comm.), and in NB all known hibernacula (n= 10) were internally surveyed in 2009/10 (before arrival of WNS) and annually since WNS arrived (D. McAlpine, pers. comm.). In Quebec, the entrances of three caves were externally monitored from 2002-2008 using automated ‘beam-break’ laser systems. Abundance counts were made inside an additional five hibernacula after WNS was detected in nearby New York. The monitoring of hibernacula increased to over 12 sites in 2009/10 but was discontinued for security issues and data exist for only 4-5 sites, at present. In southcentral Ontario, eight hibernacula were internally surveyed and five maternity colonies are being monitored (L. Hale, pers. comm.). An additional 51 sites from eastern Ontario to Wawa have been monitored with acoustic (n = 51) and capture (n = 13) surveys since the arrival of WNS (J. Bowman, pers. comm.). A total of 11-13 sites have been monitored in Manitoba since 1988 (Dubois and Monson 1987), and sites in northwestern Ontario were surveyed for presence of WNS during winter 2011/12 (Martinez et al. 2012). Cadomin Cave, the largest hibernaculum known in Alberta, has been surveyed periodically since the 1970s (Olson et al. 2011). In Ontario, the Craigmont site has been monitored for varying periods since 1946 (Keen and Hitchcock 1980).

Identification to species is generally reliable using captured individuals, at least east of the Canadian Rockies (see Abundance). In the last 20 years, ultrasonic detectors have been widely used to determine bat distribution and abundance. Myotis species are difficult to separate to species level using ultrasonic detectors (Brigham et al. 2002) and extra analyses are often required (e.g., Lausen and Barclay 2006; Broders et al. 2004). The greater richness of Myotis species (i.e., seven species in BC versus two species in the Maritimes; van Zyll de Jong 1985) potentially limits the effective use of bat detectors, particularly in western Canada.

Surveillance for the presence of Pseudogymnoascus destructans (Pd) (see Threats) began in southeastern Canada in 2009. In NS, public reporting of sightings and carcasses is coordinated using a dedicated government web page (M. Elderkin, pers. comm.). Agencies in Manitoba westward have recently prepared protocols for testing suspected cases of WNS. An inter-agency survey is coordinated by the Canadian Cooperative Wildlife Health Centre. From November 2012 - May 2013, 178 suspected WNS bats from five provinces (Ontario to NS) were submitted (CCWHC 2013). Similar efforts are underway in the US; 1,500 specimens of 24 bat species from 41 states and seven provinces had been tested as of summer 2012 by the US National Wildlife Health Center (Ballmann 2012).

Habitat

Habitat Requirements

Habitat for bats is composed of: 1) hibernacula for overwinter survival and 2) summering areas with suitable foraging areas within commuting range to structures used for roosting or maternity colonies. The habitat requirements of temperate-region bats vary by season.

Maternity sites (trees, rock crevices, buildings, bat houses) and hibernacula (cave, mine, or building used for hibernation) are the main limiting habitat features for the three species within their range (Barclay and Brigham 1996;Norquay et al. 2013). Hibernation allows non-migratory, insect-eating bats to persist in a region when ambient temperature declines and insects are not available in winter. The physiological needs of the species (see Physiology) results in only specific sections of a site being useful as hibernacula. Although the recorded range for each species varies (Myotis lucifugus: -4 to 13°C, M. septentrionalis: 0.6 to 14°C, Perimyotis subflavus: 0 to 17.8°C, Webb et al. 1996), the sections used as hibernacula typically have a temperature range of 2-10°C (Fenton 1970a; Anderson and Robert 1971; McNab 1974; Vanderwolf et al. 2012). Small-bodied bats also use hibernacula with high humidity (>80%) levels. However, sites with running water can experience wide fluctuations in temperature and often are avoided. Numerous structural features influence temperature and humidity, such as number of openings, cave size, and length and angle of tunnels (Davis 1970; Raesly and Gates 1987). Not all sites with appropriate micro-habitat features are hibernacula; macro-habitat features, such as quality and quantity of autumn foraging habitat, may influence selection of a particular site (Raesly and Gates 1987).

None of the three species typically overwinters in buildings. Among the three species, Myotis septentrionalis may hibernate in cooler sections of a cave, compared to M. lucifugus (Barbour and Davis 1969). Perimyotis subflavus is considered to have the most rigid overwintering habitat requirements; they often roost in the deepest part of caves where temperature is the least variable, have the strongest correlation with humidity levels, and use warmer walls than other species (Fujita and Kunz 1984; Raesly and Gates 1987; Briggler and Prather 2003).

In spring, females of each species leave winter hibernacula and give birth and raise pups in maternity colonies. For Myotis lucifugus, the maternity colonies often exist in warm sites that facilitate pup growth rates, such as attics of buildings and under bridges, in rock crevices, or in cavities of canopy trees in forests (Fenton and Barclay 1980; Coleman and Barclay 2011).

Myotis septentrionalis rarely use human-made structures for roosting and are more strongly associated with the density and characteristics (e.g., height, diameter, age, decay class) of trees (Caceres and Barclay 2000; Jung et al. 2004; Broders and Forbes 2004; Henderson and Broders 2008; Henderson et al. 2008). Maternity colonies in NF, NS, and NB usually were in larger trees, ranging from 25 - 44 cm diameter at breast height (Broders and Forbes 2004; Garroway and Broders 2008; Park and Broders 2012). The location of a maternity colony is important because it may contain hundreds of females with young and be the only maternity site in a large area (Broders and Forbes 2004).

Males roost during daytime in a wide variety of structures, including buildings and bridges (mainly M. lucifugus), rock crevices, behind flaking bark, and within tree cavities, often at many different sites during the summer (Fenton and Barclay 1980; Caceres and Barclay 2000). Myotis species generally roost in tall, large-diameter snags that are in the early to middle stages of decay and located in open areas within mature-overmature forest (Jung et al. 2004).

Less is known about summer roosts of P. subflavus. In the US, females returned to same area (0.4 ha) each summer and used the same 4-6 trees per year, suggesting value in familiar (and possibly limited) structures (Veilleux and Veilleux 2004). Roosts can also be in dead clusters of leaves on trees (Veilleux et al. 2003). In NS, all 30 radio-tagged bats had day and maternity roosts in large clumps of arboreal lichens (Usnea spp.) that grow on coniferous or deciduous tree species; as many as 18 P. subflavus were found in a cluster (Poissant et al. 2010). In more modified landscapes, many maternity colonies are located in barns or similar human-made structures (Fujita and Kunz 1984).

Bat abundance in summer may be a function of available roost sites and prey, but information is lacking (Fenton 1997). For example, the minimum density of roost trees required to support bats in a stand has not been established. Insect availability in different forest types is difficult to quantify and it is unknown how much of the relative abundance of bats is due to differences in prey or roost availability, foraging conditions (i.e., wind, clutter), or predator avoidance. The interaction among these variables complicates the issue further. Small openings in the canopy, created either by gap dynamics or forest harvest, are used by foraging bats (Grindal and Brigham 1999; Jung et al. 1999; Patriquin and Barclay 2003). However, large-scale removal of canopy creates windy conditions, different prey abundance, and possibly an increased risk of predation (papers in Barclay and Brigham 1996; Grindal and Brigham 1999). Small Myotis bats generally avoid large areas of cleared land, such as farm fields (Henderson and Broders 2008), clearcuts (Hogberg et al. 2002), and large post-fire landscapes (Randall et al. 2011). Instead, they forage over still water (mainly M. lucifugus, Perimyotis subflavus), rivers (all three species), and in forest gaps, edges, or along trails (all three species, particularly M. septentrionalis) (Crampton and Barclay 1996; Jung et al. 1999; Holloway and Barclay 2000; Broders et al. 2003). Centres of clearcuts (>30 m from forest edge) in northern Alberta were used 2-2.5 times less than the edges of forest islands in clearcuts, or forest edges by M. lucifugus (Hogberg et al. 2002), and avoided completely by M. septentrionalis (Patriquin 2001). Natural roosts are located in forest and bats commute between roost and forage areas, often along waterways, forest edges, and above the canopy.

Both Myotis species have been captured in a wide range of deciduous and coniferous forest stands (i.e., Kunz 1973; Caire et al. 1979; Crampton and Barclay 1996; Henderson and Broders 2008). In a comparison of Trembling Aspen (Populus tremuloides), Aspen-Spruce (Picea glauca), and Jack Pine (Pinus banksiana) stands of the same age, only 2% of M. lucifugus/M. septentrionalis echolocation calls were recorded in Jack Pine stands, possibly because the less complex forest may have had lower prey abundance (Kalcounis et al. 1999). For Perimyotis subflavus, the effect of forest type likely is even less important because the species mainly forages over watercourses and streamside vegetation (Davis and Mumford 1962) and roosts in a range of tree species (i.e., Quercus, Pinus, Picea) found in adjacent forest (Perry and Thill 2007; Poissant et al. 2010).

Numerous bat species are more abundant in the oldest forest stands (e.g., ‘old growth’) and stand age appears to be more important than type of forest (Barclay and Brigham 1996). Myotis lucifugus and M. septentrionalis were more abundant in old versus young Aspen mixedwood forest of central Alberta (Crampton and Barclay 1996) and were detected 2.7-5.3 times more in old-growth White Pine (Pinus strobus) stands than in younger and harvested White Pine and boreal mixedwood stands in central Ontario (Jung et al. 1999). The use of old forest likely is related to increased snag availability for roosting (Crampton and Barclay 1996; Krusic et al. 1996) and ease of foraging under closed canopy (Jung et al. 1999). M. septentrionalis select sites with higher density of snags and large diameter trees (Sasse and Pekins 1996; Broders et al. 2005). Evidence of a reliance on older forest also has been shown for Perimyotis subflavus (Perry and Thill 2007; Farrow and Broders 2011).

Myotis lucifugus may be less vulnerable than the other species to clearing of forest land in southern parts of their range, possibly because M. lucifugus often have maternity roosts in buildings, and forage over water. In contrast, M. septentrionalis numbers were positively associated with increasing amount of forest cover in PEI (Henderson et al. 2008) and NF (Park and Broders 2012) and Perimyotis subflavus in NS were negatively associated with amount of non-forested land (e.g., agricultural, clearcut sites) (Farrow and Broders 2011).

Habitat Trends

Hibernacula are permanent structures that may be used for many years because they have specific, unchanging micro-climates suitable for over-wintering bats. The quality of the habitat generally has declined wherever WNS has established; after two years’ exposure to WNS, most hibernacula are fully infected and declines of over 90% have been typical (see Fluctuations and Trends section). Spores of Pd likely persist (see Transmission and Risk of Infectionsection) and infected sites act as population sinks and are functionally no longer available. Closure of abandoned mines may represent lost overwinter habitat, but is unquantified.

Summer habitat for the three species is characterized as foraging and roost locations, with the emphasis on roosts, and particularly maternity colonies. Myotis lucifugus maternity colonies often are in buildings (Henderson et al. 2008), although this may be biased by easier detection because sites are reported by the public. For M. septentrionalis and Perimyotis subflavus, the extent of habitat loss for summer roosts cannot be quantified because of the variable intensity of forest harvest and practices across the species’ large range. Also, the structures most associated with maternity colonies are difficult to identify, and have not been inventoried. The age of forest can be used as a coarse indicator of trends in the amount of roosting habitat. Intensively managed stands (i.e., even-aged plantations with short rotation periods) over large areas could be a decrease in habitat because they typically create a forest with fewer large-diameter trees and snags that could house roost and maternity colonies (Hayes and Loeb 2007). Selective harvesting (as compared to clearcuts) can maintain large-diameter snags and is the common harvesting method in most sub-boreal forest types, but clearcut harvesting is the dominant harvest type in most of the boreal forest in Canada. In 2010, for example, 88% of 690,000 ha were cut with one or two-stage (clearcut) harvest, and most of this was in the boreal forest (National Forestry Database 2012). Large openings, such as clearcuts, are avoided for foraging (see Habitat Requirements section) but how much of an area has to be open before bats respond in abundance, or fitness, is unknown.

Historical conversion of forest to agricultural or urban conditions is prevalent in much of the Canadian range of Perimyotis subflavus, and the southern regions of the Canadian range of Myotis lucifugus and M. septentrionalis, particularly in Ontario and Quebec, and parts of AB and BC. Parts of some regions, such as in eastern Ontario, have reverted from agriculture to forest cover (Lancaster et al. 2008), which likely increased the amount of bat summer habitat. In summary, the overall amount of habitat for the three species is unknown.

Biology

General

The following information on general biology and reproduction of the three species is derived from species accounts by Fenton and Barclay (1980), Fujita and Kunz (1984), and Caceres and Barclay (2000), unless otherwise referenced. All three species consume a wide range of insects and spiders. Spiders are gleaned from webs, while insects are captured in flight. Prey items range from 4-10 mm and are dominated by Diptera (mainly chironomids [particularly for Myotis lucifugus]), Coleoptera (carabids), Homoptera (cicadillids), Hymenoptera (formicids), Trichoptera, and Lepidoptera.

Life Cycle and Reproduction

All three species are promiscuous, with mating occurring during late summer/autumn swarming periods, and during winter. Females store sperm and ovulate in spring with a single pup (potentially two pups for Perimyotis subflavus) born after a 44-60 day gestation period, usually in late June or early July. Females form maternity colonies to birth and raise the pups. Pups are weaned at approximately 26 days (Burnett and Kunz 1982). Sexual maturity generally occurs after the first year and breeding occurs for life.

The demographic population structure is poorly known for all three species, particularly in Canada where parameters such as reproduction and survivorship likely vary from those used in studies conducted in the US. Reproductive rates for Myotis lucifugus vary and generally decline with increasing latitude (Barclay et al. 2004). Higher rates are reported in eastern areas (e.g., >96 % in eastern US, Cagle and Cockram 1943; Humphrey and Cope 1976), and lower rates in northwestern areas (e.g., 42-57% in BC, Firman et al. 1995, Holroyd et al. 1993, C. Lausen, unpub. data). The lowest and most variable rates seem to be from the northern edge of the range; maternity colonies in Yukon are reported to vary between sites and years, with reproductive rates of 33-74% (Talerico 2008).

Survivorship is an important component of generation length and population trend criteria used in a COSEWIC assessment. Unfortunately, there is uncertainty with the application of most specific survival data because of problems in design and analyses. Average survival rate of Myotis lucifugus from band recoveries in Indiana was 1.55 years for males and 1.2-2.2 for females, but these rates were considered underestimates (Humphrey and Cope 1976). Mean annual survival of M. lucifugus in Ontario was 0.82 for males (monitored for 16 yrs) and 0.71 for females (monitored for 10 yrs) (Keen and Hitchcock 1980) but the conclusions are limited because the number of juveniles in the sample is unknown. In Indiana, average life expectancy after year one for M. lucifugus was 3.8 years for males, and 6.5 years for females (Humphrey and Cope 1976).

Movement by bats during winter is such a significant problem for survivorship estimates that it is now recommended that closed-population methods should be avoided, and missing animals cannot be assumed to be dead (O’Shea et al. 2004; O’Donnell 2009). Instead, robust design survivorship techniques that partially account for temporary emigration should be used. To date, however, there is only a single study (Frick et al. 2010b), and only on Myotis lucifugus, that has a long-enough time period to begin to minimize variability in recapture probabilities and survival estimates (O’Donnell 2009). In this study, Frick et al. (2010b) reported on M. lucifugus that were monitored for 16 years in a summer maternity colony in New Hampshire. Survivorship of adult females was highly variable and ranged from 0.63-0.90, depending on amount of cumulative precipitation over the summer. Juvenile female survivorship was lower, ranging from 0.23-0.46. Survivorship was higher for juveniles born later in a summer versus early summer. Survivorship is lowest in the first year of hibernation because juveniles often lack sufficient fat reserves needed for hibernation (Fenton and Barclay 1980).

Although rigorous, the Frick et al. (2010b) study still does not fully address the survivorship issue. The survivorship of juveniles likely is still an underestimate because the proportion of one-year-old females returning was variable (23-53% probability) and a robust design accounts for temporary emigration, but not permanent emigration. Recapture rates from 2,891 (1295 juvenile:1596 adult) female bats were low (0.10-0.35). Also, survivorship for males is unknown; males often do not return to maternity colonies after weaning.

A similar problem exists for data on Perimyotis subflavus. Using returns on banded P. subflavus, Davis (1966) concluded survivorship was low in first and second winters (0.41-0.51 adult female; 0.46-0.68 adult male), high in the third year (0.74 adult female; 0.98 adult male), then declined again. Baker (1978) refuted those results, noting that much of the movement out of caves occurs in year one and two, whereas residency is high in year four, and movement again increases, a behaviour that would explain Davis’s estimates. Baker suggested that survivorship estimates are poor without accounting for intra-cave movement. The Davis results have also been questioned by O’Shea et al. (2004) because of faulty correction factors used on recapture data.

Generation Time

Two methods (median age of breeding/longevity, and mean age of cohort breeding; IUCN 2011) are used to estimate a range of generation time because neither method is satisfactory by itself. The mean age of cohort breeding is the preferred method (IUCN 2011) but existing data on estimating annual survivorship is limited and biased (see Life Cycle and Reproduction section). For the median age method, Myotis lucifugus and M. septentrionalis start breeding after one year old, continue breeding annually, and have been recorded to live over 30 (Fenton and Barclay 1980), and 19 years (Hall et al. 1957), respectively. M. septentrionalis likely live to be the same maximum age (≈30 yrs) as the similar M. lucifugus and the two species are considered together here. Using the median age of longevity method, generation length is 14 years (median of 15, minus one year to account for the sub-adult period).

However, the median age method may overestimate generation length if few bats reach maximum lifespan, and this seems to be the case. For example, a long-term study in Manitoba indicated that the proportion of Myotis lucifugus >3 years is low and few bats are >20 years old (C. Willis, unpub. data) and in Yukon, 26% of bats banded as adults were recaptured after nine years, and 9% were recaptured after 10-14 years (B. Slough and T. Jung, unpub. data). Therefore, it was deemed important to also determine generation length from the mean age that a cohort breeds. Data from several studies were used; the Frick et al. (2010b) study is the most rigorous but only has data on females at summer maternity colonies. A Canadian study (Keen and Hitchcock 1980) is biased but has data from both sexes in hibernacula. Using the Generation Length calculator (IUCN 2011) with both data sets leads to an estimate ranging from 4-10 years (Frick et al. 2010b) and 3-17 years (Avg. 4 yrs) (Keen and Hitchcock 1980) for females. For males, applying the average survival rate (Keen and Hitchcock 1980) over 30 years suggests a generation length of six years (range 4-10 yrs). A combination of results from both studies would suggest that the generation time for both species is approximately five years.

In summary, because the median age of breeding/longevity potentially overestimates generation time, while mean age of cohort potentially underestimates it, the most plausible estimate for generation time for M. lucifugus and M. septentrionalis is a range of 5-10 years, based on both methods.

Perimyotis subflavus:

Mean breeding age is unknown but wild P. subflavus start breeding after their first year, continue breeding annually, and have been recorded to live over 15 years (Walley and Jarvis 1971). This suggests the median age of breeding is seven years for P. subflavus (median age of maximum longevity is eight minus one year to account for the sub-adult period). Although the survival data analysis for the species (Davis 1966) is biased (see Life Cycle and Reproduction section), the data are the best available; using these data in the Generation Length calculator (IUCN 2011) leads to an estimate of five years (using both sexes combined and with either one or two offspring annually after year one, for 14 years). This suggests a range of 5-7 years as a plausble estimate for generation time for P. subflavus.

Physiology

The physiology of non-migratory, temperate bats is well-studied, mainly because of interest in the ability of such species to process fat reserves into energy and rapidly enter and exit torpor, while balancing energy intake and expenditure as a small-bodied, flying mammal possessing a large surface area (Studier and Howell 1969; Fenton and Barclay 1980; Willis 2006). Only the physiological aspects related to a status assessment are presented in this report.

Bats survive the winter using stored fat reserves accumulated during summer/autumn (Jonasson and Willis 2011). They then minimize use of these reserves by decreasing body temperature to within a few degrees of the ambient temperature in the hibernaculum, with a corresponding 96-98% reduction in metabolic rate (Henshaw and Folk 1966). The decreased metabolism is facilitated by overwintering in a cold environment. The optimal ambient temperature for maintaining the lowest metabolic rate is 2°C for Myotis lucifugus (and presumably similar for M. septentrionalis and Perimyotis subflavus) (Hock 1951). However, functioning at such a low temperature creates an extra energetic cost to arouse and access water, a higher energetic cost to maintain core temperature when temperature fluctuates, and increases predation risk (Boyles and McKechnie 2010). As a result, it is more efficient to hibernate at a temperature a few degrees above the minimal level; most small bat species typically hibernate where the temperature is 2-10°C (Anderson and Robert 1971).

At 5°C, Myotis lucifugus arouse from torpor every 13 days, on average (Brack and Twente 1985; Twente et al. 1985), approximately 15 times a winter (Thomas et al. 1990). Bats will arouse from torpor to access water, to groom, and to mate (Avery 1985; Whitaker and Rissler 1993; Thomas 1995). Each arousal event requires approximately five minutes to one hour (C. Willis, pers. comm.), and three hours to re-enter hibernation, consuming up to 109 mg fat per event and 29% of their total body mass over a winter (Thomas et al. 1990; Jonasson and Willis 2011, 2012). A bat in flight consumes greater amounts of fat. This energy budget is relevant to bat conservation because bats at the northern edge of their range in Canada spend longer periods in hibernation (Fenton and Barclay 1980; Fujita and Kunz 1984) and likely are more vulnerable to disturbance than those in warmer climates.

Water balance also is important for hibernating bats (Thomas and Geiser 1997). Humidity levels need to exceed 99% to compensate for the evaporative water loss of a hibernating bat (Thomas and Cloutier 1992). Moisture loss is a particular problem because the non-furred wing and tail membranes represent a high proportion of body surface area (Thomas and Cloutier 1992). The humidity levels of hibernacula always exceed 65% relative humidity, and usually exceed 90% (Fenton 1970a; Raesly and Gates 1987; Kurta and Teramino 1994).

Adaptability

Insectivorous bat species survive the lack of insects in winter by migrating south, or overwintering in hibernacula. The northern limit of an overwintering species appears related to winter temperature (Humphries et al. 2006; Boyles and Brack 2009), ability to cluster as a group and thereby maintain body temperature (Boyles et al. 2008), and physiological thermal neutral zones, as determined by local adaptations (Dunbar and Brigham 2010). Myotis bats typically hibernate with their own species but in clusters of two to thousands of bats, either touching, or within a few centimetres of each other (Tuttle 2003). Perimyotis subflavus typically roost singly (Barbour and Davis 1969). Hibernation likely lasts from late September/October to late April/early June in much of the Canadian range of the three species (Fenton and Barclay 1980; Fujita and Kunz 1984; Caceres and Barclay 2000). Emergence from hibernacula may be earlier along the Pacific coast than other regions (T. Jung, pers. comm.).

Interspecific Interactions

In eastern Canada, the three species often overwinter in the same hibernacula, but not in mixed-species clusters. In summer, foraging areas overlap, particularly for Myotis lucifugus and Perimyotis subflavus, both of which commonly forage over water. Numerous other species of bats (e.g., Lasiurus cinereus, L. borealis, Eptesicus fuscus) forage in the same areas with the three species in much of the Canadian range (van Zyll de Jong 1985) but there is limited evidence of competition or interaction between any species during foraging. Davis and Mumford (1962) suggested, however, that M. lucifugus and P. subflavus may avoid each other while foraging because P. subflavus were generally absent where M. lucifugus foraged.

Predators of the three bat species are varied but not considered significant; no predator specializes on bats in Canada. Incidental observations of predation have been recorded for owls, rodents, domestic cats, snakes, and frogs (Fenton and Barclay 1980; Fujita and Kunz 1984; Caceres and Barclay 2000).

Several species of endo-, and ecto-parasites are common to all three species of bats, including various cestodes and trematodes, batbugs (Cimex spp.), fleas (Myodopsylla spp.), and mites (Euschoengastia, Macronyssus, Spinturnax) (Fenton and Barclay 1980; Fujita and Kunz 1984; Sasse and Pekins 2000; Poissant and Broders 2008; Czenze and Broders 2011). Differences in parasite abundance exist between males and females (Czenze and Broders 2011) and between maternity colonies (T. Jung, pers. comm.), but it is unknown if susceptibility to WNS is associated with parasite abundance or diversity.

North American rabies is caused by a virus (family Rhabdoviridae, Genus Lyssavirus) typically transmitted by saliva among mammals. The following summary is derived from the review by Messenger et al. (2003). The impact of rabies on bats is not clear because recorded die-offs may not be entirely due to rabies, and there is evidence of a degree of immunity in bats (i.e., 2% of Myotis lucifugus showed antibodies to the virus, but no lesions in the brain). However, immunity is difficult to confirm because extended incubation periods of >1 year are known and ‘immune’ bats may not yet have been clinically affected. Prevalence is difficult to establish because of sampling bias but it appears a proportion of bats are rabid at any one time (i.e., <4% in a sample of apparently healthy Eptesicus fuscus, and <1% in M. lucifugus [Girard et al. 1965]). There is evidence of Red Fox (Vulpes vulpes) being infected by bat rabies strains in association with living in caves or dens, and presumably feeding on, or interacting with bats (Daoust et al. 1996; Messenger et al. 2003).

Dispersal and Migration

Dispersal

Little is known about dispersal behaviour of the three species. Most data are on seasonal movements between summer and winter range, rather than permanent dispersal from natal range. Newborns are difficult to mark and most studies rely on recaptures of banded juveniles, which are generally very low. Based on existing data, most females do not appear to disperse far; female Perimyotis subflavus (Veilleux and Veilleux 2004) and Myotis lucifugus (Frick et al. 2010b) often return to the maternity colony where they were born and weaned. Natal philopatry also occurs in female M. septentrionalis (Arnold 2007). Males typically do not return to natal sites and their dispersal movements are less understood.

Space Use

Peak foraging activity typically is in the first few hours after dusk, and often again before sunrise (Fenton 1970b; Kunz 1973; Broders et al. 2003). Myotis lucifugus in southeastern Ontario roosted at night only if ambient temperature declined below 5°C (Barclay 1982). All three bat species forage within small (i.e., <2 km²) areas. In Indiana, the summer roosting area of P. subflavus ranged from 0.1-2.3 ha, with a range of 21-926 m between roost trees (Veilleux and Veilleux 2004). In Michigan, 11 radio-tagged M. septentrionalis moved an average of 333 m ± 88 S.D. (range: 6-2,000 m) to new roost sites every two days over a 9-day tracking period (Foster and Kurta 1999). Average distance from capture to roost site for 18 radio-tagged M. septentrionalis in NF was 1,136 m (range: 71-2,375m) (Park and Broders 2012) and 1,100 m on PEI, with a minimum foraging area of 6.1 ha (Henderson and Broders 2008). In the Yukon, radio-tagged female M. lucifugus moved at least 6.3 km nightly between their roost and foraging grounds (Randall et al. in press). Average home range of nine female M. septentrionalis was 65 ha (Owen et al. 2003). Lactating M. lucifugus in Quebec reduced their home range area from an average 30.1 ha (± 15 S.D.) to 17.6 ha (± 9.1 S.D.) and foraging distance from 2.6 km (± 0.6 S.D.) to 1.7 km (± 0.6 S.D.) between pregnancy and lactation stages, likely to facilitate feeding of young at the roost (Henry et al. 2002).

Most of the known hibernating bats of a region are found in only a few hibernacula. For example, four hibernacula in Minnesota contain 99% of their known overwintering population (Nordquist 2000), eight hibernacula contain 75% of Virginia’s bats (Dalton 1987) and many of the bats in several New England states are believed to hibernate ‘in a few sites’ along the Vermont and New York state border (Davis and Hitchcock 1965). In NB, one hibernaculum contained 86% of the known hibernating Myotis and the remaining nine sites had <300 each (Vanderwolf et al. 2012). In NS, Hayes Cave had 17,000 bats, compared to <3,500 in all others (H. Broders, pers. comm.). Similar situations exist for Manitoba (i.e., 9,000 M. lucifugus in one cave; Dubois and Monson 2007; C. Willis, pers. comm.) and Alberta (Schowalter 1980; Lausen and Barclay 2006). However, so few hibernacula have been discovered across much of the range that it is difficult to determine average density per hibernaculum (C. Willis and H. Broders, pers. comm.).

Migration

All three bat species are considered short-distance regional migrants with a small proportion moving hundreds of kilometres between summer and wintering areas (Barbour and Davis 1969; Fenton and Barclay 1980; Fujita and Kunz 1984; Caceres and Barclay 2000). Distances of 35-554 km were recorded in Manitoba for banded Myotis lucifugus moving between winter hibernacula and summer maternity sites (Dubois and Monson 2007; Norquay et al. 2013) and M. lucifugus were recaptured as far as 250 km from summer maternity colonies in Ontario (Fenton 1970a).

Most bats seem to return to the same site annually; 94% of recaptures of 10,432 banded Myotis lucifugus from Manitoba over a 21-year period were only recaptured at a single hibernaculum or summer colony (Norquay et al. 2013). A small percentage (0.8%) were recaptured in a new summer or winter location from where they were initially captured. Although relocations were rare, the distances moved by bats from one hibernaculum to another (n=54) were considerable; 13 (25%) of these bats moved >500 km (range: 6-569 km) (Norquay et al. 2013). It appears movement between hibernacula occurs annually by a small percentage of bats (Griffin 1940, 1945; Fenton 2012). In Ontario, Fenton (1970a) recaptured four M. lucifugus, 45-125 km from a previous capture site, of which two animals moved to different caves in the same winter. Bats have been recorded swarming at one site but hibernating in another (Humphrey and Cope 1976, Norquay et al. 2013). A single banded M. lucifugus captured in northern Ontario was recaptured while swarming at Renfrew Mine in southwestern Ontario in September 1967, and again at the original northern site one month later, 800 km away (Fenton 1969).

Migration by M. septentrionalis is less known but they likely have similar movements to M. lucifugus. M. septentrionalis typically returned to specific caves in homing experiments, including one bat that returned from 52 km in three hours after being captive for three days (Griffin 1945). Another M. septentrionalis was recaptured 13 km from its release point, four years later (Davis 1966).

The longest distance moved by Perimyotis subflavus, based on recapture of banded individuals, was 53 km (Griffin 1940) but there is some indirect evidence individuals may move up at least several hundred kilometres further. Fraser et al. (2012) found a sample of 24 of 73 males moved southward from their northern range, based on changes in stable isotope signatures. The movement was directional (i.e., north-south, as compared to typical migration that radiates out from hibernacula; Fenton and Barclay 1980) and, because P. subflavus hibernate singly, the southward movement may be related to their need to keep warm. The maximum distance was from central Ontario to southwestern Ontario (approx. 780 km).

Population Sizes and Trends

Sampling Effort and Methods

Bats are surveyed by acoustic survey or capture with visits into hibernacula to count bats, external visits to the mouth of the hibernacula, and wider area surveys in forests, farmland and urban areas. WNS would not be detected using acoustic surveys and capture data may detect WNS if bats were swabbed and/or if there was evidence of wing damage (see Cause and Impact on Batssection). Determining the direct impact of WNS on a population is best assessed by entering the hibernacula but few hibernacula are actually entered because of safety reasons. There has been an increasing reliance on acoustic work for detecting relative abundance and population trends, but this work mainly began after the arrival of WNS and is of limited use in comparing pre- and post-WNS trends.

Hibernacula surveys involve counts by one or more observers conducted between October and April. Confidence limits generally do not exist on population estimates. The ability to estimate bat numbers varies because some hibernacula (i.e., mines) have low-lying, relatively smooth surfaces where accurate counts may be possible, while others (i.e., limestone solution caves) have narrow passageways that are too high or narrow to count bats. In some jurisdictions (i.e., Ontario, NB, NS) Myotis species are combined into a single estimate because it is too difficult to identify some species beyond several metres.

Data that combine species into ‘Myotis’ are not a significant problem for a COSEWIC assessment because some criteria are based on percent change, rather than actual population numbers. Virtually all bats in central-eastern hibernacula in Canada are either Myotis lucifugus or M. septentrionalis (see Abundance section) and both species respond equally to WNS (see Fluctuations and Trends section). Therefore, recorded percentage declines can be assumed to apply to each species.

Summer surveys are conducted with live-capture mist nets or harp traps set along trails, near waterways, nursery colonies (i.e., Slough and Jung 2008), or at hibernacula entrances. Acoustic surveys have been commonly used since the early 1990s and involve hand-held or automated recording of distinctive echolocation signals with specialized ‘bat detectors’. M. septentrionalis make quieter echolocation calls, and likely are under-sampled (Fenton and Bell 1991). Determining abundance estimates is difficult because the same bat may be counted repeatedly; duplication can be avoided if bat detection occurs from a vehicle that is travelling faster than a flying bat (Roche et al. 2011). This method has been employed in the northeastern US since 2009 (C. Herzog, pers. comm.) and in parts of Ontario since 2010 (J. Bowman, pers. com.). Data collected using this technique do not exist before the impact of WNS, except for Quebec, which has conducted acoustic surveys on roads in several regions since 2000 (Jutras et al. 2011).

Most information on subpopulations is derived from local studies that capture and wing-band animals for later recapture. Projects with data exceeding 10 years are few but have been undertaken in Ontario (Hitchcock 1965; Fenton 1970a), Manitoba (C. Willis, pers. comm.), and Yukon (Slough and Jung 2008). Banding with pit-tags has begun in Manitoba and NS, but these are for shorter time series (H. Broders and C. Willis, pers. comm.).

Some jurisdictions have estimated the number of bats but mark-recapture methods typically were not used and the estimates are coarse. Winter data are constrained by the number of hibernacula visited, detectability of bats in different hibernacula, and unknown number of total hibernacula. Often, more bats appear to be present in summer than are recorded in winter. Due to the limited search effort, it is believed that the discrepancy is due to unidentified hibernacula, rather than most bats migrating out of Canada. There is seasonal movement in Myotis bats (see Migration, Wind Turbines sections) but movements would be considered regional, with some proportion of Ontario and Quebec bats hibernating in upper NY and Vermont, and though not reported, possibly bats in the Maritimes hibernating in upper New England.

Abundance

This report separates the population data into two periods; a pre-WNS period and a post-WNS period. The pre-WNS data are presented in the Abundance section. The post-WNS data are presented in the Fluctuations and Trends section.

The population sizes of the three bat species in Canada are unknown pre- or post-WNS. Relative abundance patterns across the range of each species are unknown, and the question remains as to whether they are as abundant in northern and western parts of their range as they appear to be in northeastern North America. Kunz and Reichard (2010) suggested that most of the pre-WNS population of Myotis lucifugus resided in the northeastern US. In Canada, 95% of the hibernating Myotis bats (combined M. lucifugus and M. septentrionalis) that have been counted occur in the range from NS to Manitoba, with relatively few bats having been recorded west of Manitoba (see below).

However, the number of Myotis spp. in the north and west that have been counted relative to the east may not be a true reflection of regional relative abundances. Hence, the proportion of the population in western Canada is unknown.

At present, WNS has affected approximately 30% of the Canadian range of M. lucifugus, 40% of M. septentrionalis, and close to 100% of P. subflavus. Estimates of overall decline already experienced by the Canadian populations of the two Myotis species are not possible without knowledge of either the proportion of the Canadian populations that has already been affected by WNS, or the proportion residing in the area of Canada where WNS has not yet appeared.

Myotis lucifugus:

The population size is unknown but available data suggest that M. lucifugus is the most common bat in much of Canada; they are frequently the most recorded in surveys and buildings during summer and are observed over many ponds, rivers, and lakes across their range (Fenton and Barclay 1980). The pre-WNS estimate for NS was 300,000 in summer (based on numbers at lakes and extrapolated to total number of lakes) and 30,000 at known hibernacula in winter (Scott and Hebda 2004). In Quebec, M. lucifugus are considered common (echolocation surveys in Quebec do not separate Myotis calls into species and more exact numbers are unavailable; Jutras et al. 2011). Data on abundance in the prairie region of Saskatchewan are unavailable but M. lucifugus is considered common in similar, adjacent habitat of North Dakota (Jones et al. 1983). In Alberta, the species is considered common in the Prairie region near Calgary (Coleman and Barclay 2011). The typical abundance in 196 maternity colonies was 50-300 bats (range 15 - 1100) (Schowalter et al. 1979). The species is relatively common in summer in parts of BC (Nagorsen and Brigham 1993) but rarer in other parts; M. lucifugus comprised 9% (39 individuals) of a sample of 11 species in the Okanagan valley region (Fenton et al. 1980). Over three years of survey in southern BC, M. lucifugus (based on genetics, morphology, acoustics) comprised 20% of the 805 captures of 14 species (C. Lausen, D. Nagorsen, D. Burles, unpub. data). Mis-identification may be an issue in BC; differentiating M. lucifugus from M. yumanensis is difficult (Luszcz et al. 2003; Weller et al. 2007) and identification on morphology alone had an error rate up to 34% (C. Lausen, unpub. data). Historical data on M. lucifugus needs genetic confirmation because M. yumanensis appears to be common in the datasets, which raises the possibility of misidentification errors (C. Lausen, pers. comm.). Abundance levels in the northern end of their range are harder to estimate but M. lucifugus is considered relatively common. For example, based on mark-recapture population estimates, some maternity colonies in the Yukon have >800 bats (Jung 2013).

Overwintering data for Myotis lucifugus are patchy, with extensive data existing for some sites in southern Ontario and Quebec, but limited elsewhere, particularly in NL, NT, and PEI where mainly single sites have been surveyed (Brown et al. 2007, S. Moores, pers. comm., Lausen 2011). The PEI site contained 648 (83%) M. lucifugus (Brown et al. 2007). In NS and NB, Myotis sp. are combined during surveys but M. lucifugus appear much more common; in an NB sample of bats killed by WNS, 91.6% were M. lucifugus, which would extrapolate to 6,466 M. lucifugus in the 10 hibernacula at the onset of WNS (D. McAlpine, pers. comm.). In Quebec, the total abundance estimate from five caves was 13,108 M. lucifugus in 2007/08 (Mainguy et al. 2011). In Ontario, two mines each contained approximately 10,000 overwintering bats annually (Fenton 1970a). In Manitoba and northwestern Ontario, 11 hibernacula contained >10,000 M. lucifugus, most of which were in one cave in Manitoba (Nagorsen 1980; Dubois and Monson 2007; C. Willis, pers. comm.). The four known hibernacula in Alberta contain approximately 1,980 M. lucifugus (D. Hobson, pers. comm.) and only a few bats have been recorded in mines in central BC (Nagorsen and Brigham 1993).A total of 3,000 M. lucifugus were recorded overwintering in a single site in southern NT (Lausen 2011).The Canadian population size of M. lucifugus is unknown but foraging individuals appear to be present on most waterbodies within its large range; the population likely exceeded one million bats before the arrival of WNS.

Myotis septentrionalis:

The population size of Myotis septentrionalis is unknown but they are less common than M. lucifugus and have a more restricted distribution on the landscape, likely due to their reliance on forested areas. Captures at swarming sites during autumn in NS over the last 10 years yielded 1,678 M. septentrionalis versus 4,249 M. lucifugus (H. Broders, pers. comm.). Schowalter (1980) recorded 10 M. septentrionalis, compared to 899 M. lucifugus, swarming at two hibernacula in Alberta. In contrast, Grindall et al. (2011) captured 260 M. septentrionalis, compared to 193 M. lucifugus, in mist nets in the oil sands region of northeastern Alberta. The species appears to be relatively common in southern NT (J. Wilson, pers. comm.) and uncommon at the edge of their western and northern range (T. Jung, unpub. data); 15 (15.1% of a total 98 bats of seven species) were captured from 332 net-nights over two summers in the Columbia River valley of BC (Caceres 1998).On Newfoundland, similar numbers of M. lucifugus (n=22) and M. septentrionalis (n=29) were captured in 280 trap nights during summer 2008 (Park and Broders 2012). Similar evenness was found in PEI (Henderson et al. 2009) and less so in NS (127 M. lucifugus versus 37 M. septentrionalis), but the main trap site was at a bridge that may have favoured M. lucifugus (Poissant et al. 2010).

Relatively few (i.e., <100) Myotis septentrionalis are recorded in individual hibernacula (Barbour and Davis 1969; Caire et al. 1979; Amelon and Burhans 2006). The disparity between summer and winter abundance exists across the species’ range, likely because M. septentrionalis may be harder to detect than M. lucifugus in hibernacula. Although M. septentrionalis are known to roost in clusters, they often roost by themselves, and use small openings to hide in (Whitaker and Rissler 1993). Abundance data for M. septentrionalis in winter do not exist for NL. In PEI, M. septentrionalis comprised 132 bats (17%) in the only known hibernaculum (Brown et al. 2007). In NS, Myotis species are not separated to species during hibernation counts but 1,678 M. septentrionalis were captured at the entrances to 17 hibernacula (H. Broders, pers. comm.). In NB, the two Myotis species are combined as Myotis sp., but M. septentrionalis comprised8.4% of a collection of carcasses killed by WNS (D. McAlpine, pers. comm. 2012). In Quebec, Lafleche Cave had 17 M. septentrionalis and five M. lucifugus (Hitchcock 1940), and 58 M. septentrionalis were banded between 1939 and 1958, compared with 124 M. lucifugus (Hitchcock 1965).A total of 2,592 M. septentrionalis (19% of total Myotis) were recorded in five caves in 2008/09 (Mainguy et al. 2011). In Ontario, Hitchcock (1965) was confident he could capture most bats in five caves of the Ottawa-Belleville region, and identified 17 (18%), 58 (21%), six (0.5%), 183 (14%) and 96 (3.3%) as M. septentrionalis. A total of 117 M. septentrionalis (2% of total Myotis) and 5,712 M. lucifugus were recorded at Renfrew Mine (Fenton 1969). The pre-WNS Canadian population likely was >1 million animals.

Perimyotis subflavus:

The population size is unknown but the species is relatively rare in the Maritimes and Quebec, and rare or uncommon in parts of Ontario. It also is rare in adjacent US states of Vermont (Darling and Smith 2011) and Maine (Zimmerman and Glanz 2000). In NB, very low numbers (i.e., 49 echolocation calls out of 160,000; <0.2%) of P. subflavus were recorded during summer (Broders et al. 2001). In NS, 12% of >30,000 echolocation calls, and 6% of captured bats during summer, were P. subflavus (Broders et al. 2003). Based on work from three graduate projects, H. Broders (pers. comm.) estimates 1,000-2,000 adult female P. subflavus existed in NS, pre-WNS. In Quebec, P. subflavus accounted for 30 (0.2%) of 10,268 total bat echolocation calls recorded between 2000 and 2009 on several (i.e., 3-15), 20-km-long summertime acoustic survey routes (Jutras et al. 2011). On Montréal Island, P. subflavus was the least recorded (4.3%) in echolocation passes among four bat species at 24 survey sites (Fabianek et al. 2011). The abundance of P. subflavus in Ontario appears patchy; records exist for central Ontario (i.e., Algonquin Park), and they are considered relatively common in the Kingston area of southeastern Ontario (MacDonald et al. 1994; B. Fenton, pers. comm.). However, P. subflavus was found only twice before 1940 (Hitchcock 1940) and was not recorded in summer at 198 survey sites in southwestern Ontario and the Bruce Peninsula during 133 hours of echolocation monitoring (Furlonger et al. 1987).

In most of the Canadian range, the numbers of Perimyotis subflavus recorded in hibernacula are similar to those recorded in summer, suggesting that the winter data are an adequate reflection of the Canadian population, and declines measured in hibernacula are valid. Of approximately 7,000 bats recorded in six NB hibernacula in 2010/11, only 20 (<0.2%) were P. subflavus (Vanderwolf et al. 2012). A similarly small number (47) were recorded at entrances to NS hibernaculum (H. Broders, pers. comm.). In Quebec, four (1.4%) of 281 total bats banded in Laflèche cave (Saint-Pierre de Wakefield) were P. subflavus (Hitchcock 1965). P. subflavus were recorded in two of five caves in 2007/08 and 2008/09 and accounted for 17 (0.1%) and 19 (0.1%) of all bats, respectively (Mainguy et al. 2011). In Ontario, a small proportion (i.e., 0.2, 1, 4.5%) of all bat species in caves of various sizes were P. subflavus (Hitchcock 1949, 1965).

Fluctuations and Trends

Prior to WNS (see Threats section), regional populations were believed to be relatively stable (Frick et al. 2010a; b), but populations at a local scale varied because individual bat colonies are susceptible to localized and rare events. For example, flash flooding in a Kentucky hibernaculum caused >5,000 deaths (DeBlase et al. 1965). An estimated 1,000 bats (Myotis sp. and Hoary Bats) died at a lake near Edmonton, AB due to exposure to a toxic alkaloid produced by blue-green algae (Pybus et al. 1986). Although these events cause significant mortality, they typically have been limited to single hibernacula or maternity colonies, and the larger population in the region is not substantially affected.

Population trend information is limited, and most information exists only for the area affected by WNS. Of 42 US subpopulations of Myotis lucifugus monitored over 10-30 years until the onset of WNS, 64% did not show a population trend, 31% increased, and 5% declined (Ellison et al. 2003). In Vermont, data on 23 hibernacula that have been monitored for variable periods (e.g., 10-60 years) indicate that the M. lucifugus population was generally stable or increasing, pre-WNS. Subpopulations at some hibernacula had intra-annual variation of +/- <20%, and several times declined by approximately 50% for periods of 2-3 years over a 60-year period (Trombulak et al. 2001). For M. septentrionalis, 25% of 12 pre-WNS subpopulations in the US were increasing, and 75% showed no trend (Ellison et al. 2003). The same trend of stable or increasing was recorded in the US for Perimyotis subflavus in 44 subpopulations.

Frick et al. (2010a) concluded that before WNS, 19 of 22 (86%) of hibernacula in the northeastern US had stable or increasing populations during the last 30 years. Data on regional subpopulation trends in Canada are unavailable; several studies occurred in southern Ontario (i.e., Hitchcock 1965; Fenton 1970a; Keen and Hitchcock 1980) but these data are >30 years old.

Population declines of some cave-dwelling bat species in the eastern US have been documented since the 1950s (Mohr 1952; Pierson 1998) and several species, most notably the Indiana Bat (Myotis sodalis), are listed as endangered in the US.

An unprecedented decline began in 2006 with the arrival of WNS (see Threats section); an estimated one million bats (multiple species) died in the northeastern US within three years of the arrival of WNS (Kunz and Tuttle 2009), and 5.7 to 6.7 million bats have been estimated to have died within six years (U.S. Fish and Wildlife Service news release; January 17, 2012). The following trend information is presented for the northeastern US because WNS has occurred there for longer and the impacts have been well surveyed; impacts there foreshadowed events that have since occurred in the Maritimes, and are likely to occur in other parts of Canada. The total decline in Myotis bats known to be present in NS, NB, Ontario, and Quebec hibernacula at time of WNS arrival, to most recent data for the site, is 94% (86,952 to 5,225; see below). Recent events in Canada are presented after the US data. See Appendix 1 for a discussion on data issues.

Myotis lucifugus - US Data

A minimum of 115 hibernacula were infected with WNS four years after WNS was initially detected in North America; annual decreases in bats within hibernacula averaged 73% (range 30-99%) (Frick et al. 2010a). Most of these bats were Myotis lucifugus. Average decline in 54 hibernacula in six northeastern US states after two years’ exposure to WNS was 91% for M. lucifugus (Table 1; Turner et al. 2011). Twelve of 54 sites declined to zero bats. As of 2011, WNS had been recorded in 190 hibernacula in 16 states and four provinces. A survey of state biologists in spring 2012 led to the conclusion that virtually all known significant hibernacula in the northeastern US were infected with WNS (Herzog and Reynolds 2012).

Note: For Vermont, species identification facilitated by all sites having low ceilings (S. Darling pers. comm.).

Myotis lucifugus is predicted to be functionally extirpated (i.e., 1% of pre-WNS population) in the northeastern US by 2026 (Frick et al. 2010a). The population analysis used population growth rates from 22 hibernacula in the northeastern US over 30 years, calibrated with specific growth rates from a detailed study population (Frick et al. 2010b), and compared declines in infected versus uninfected sites. Simulations on a stochastic population model started with 6.5 million bats and predicted population levels at various rates of infection in hibernacula, while assuming a growth rate of 1.08. Using average declines recorded in the first three years of infection (of 85, 62 and 45% in years 1-3, respectively) and fixing future decline rates at 45%, the subpopulation had a 99% probability of extinction by 2026. If future declines are 10% per year, the probability of extinction is 90% within 65 years. Population declines rates would need to be <5% to significantly decrease the probability of extinction in 100 years.

When available, summer data indicate declines similar to those reported during winter. Dramatic declines of >70% are consistent across the region, regardless of location and method of detection (Table 2). Dzal et al. (2011) recorded a 78% decline in summer activity of Myotis lucifugus within 100 km of the original WNS site, two years after exposure. A 72% decrease in activity (mainly M. lucifugus; Brooks 2009) was recorded in central Massachusetts after WNS (Brooks 2011). In northwestern NY, M. lucifugus activity declined significantly in a comparison before and after WNS, with a decrease from 14 to 2 mean echolocation passes/hour in late summer (Ford et al. 2011). Monitoring results from surveys of summer maternity colonies of M. lucifugus in Massachusetts indicated declines of >70% over the last three years (Gillman et al. 2011; unpub. data) and correspond to average decline for bats based on winter data (Frick et al. 2010a). In West Virginia, annual capture rates of M. lucifugus after one year of WNS declined by 80%, compared with a 12-year, pre-WNS period (Francl et al. 2012).

Myotis lucifugus - Canadian Data

Declines in regions where WNS has established in Canada have been similar to those in the US. In eastern Ontario, eight hibernacula were inspected internally from 2009-2011 and each became infected, with an average total decline of 74% after one year, and 92% for three sites >2 years. The total decline from time of infection to most recent data has been 93% (Table 3). The number of Myotis lucifugus is unknown but they are considered the most abundant species, based on incidental identification during these surveys, plus past work (e.g., Fenton (1969) captured 5,770 M. lucifugus, 91% of all bats at some of these hibernacula). Data from capture and acoustic surveys in Ontario are not yet available (J. Bowman, pers. comm.).

Notes
1) Population counts are conducted October-November. Survey data do not separate Myotis lucifugus or M. septentrionalis.
2) Values in bold italics indicate survey when WNS was first detected, as determined by visual or diagnostic methods.
3) * Croft and MacDonald sites were gated in 2012 after initial survey; only 50% of Croft was surveyed in 2010.
4) Regional total is best available data on total of maximum bat number recorded when WNS was detected that year in the region or at a site (46,049) and most recent number for the same sites (3,422). Data from Croft and MacDonald sites are incomplete and not included.

In Quebec, of four hibernacula with data before winter 2009/10 (WNS was first recorded in winter 2009/10), declines have been 98-100%; overall decline from all six sites with data before and soon after first incidence of WNS to last available survey is 98% (Table 4; Mainguy et al. 2011). In autumn 2011, Mine-aux-Pipistrelles, in southern Quebec near the US border and the closest site to the origin of WNS, decreased from >5,000 to eight bats (min. 99% decline), concurrent with hundreds of dead bats observed on the ground. Signs of WNS and “many dead bats” were recorded at another site (Emerald Mine) in February 2010. Most (99%) of the bats in the hibernacula were M. lucifugus.

Notes
1) Abundance based on visual counts. ‘Late’ = March to April; ‘Early’ = November to February.
2) Value in bold italics = the survey when WNS was first detected at that site; Halifax and Copper sites likely had WNS in 2009/10. Most sites not surveyed in 2010/11 due to budget constraints.
3) % Change = difference between first detection at site, or year of detection in Quebec (2009/10), and most recent abundance estimate.
4) Only partial survey conducted at Quebec Copper in 2012 due to flooding, but areas surveyed should have contained bats, as in previous years.
5) Total only includes data from sites that were surveyed across years.
6) Additional sites have been surveyed (e.g., St. Robert Metal, Copperstream Frontenac) but are omitted because data do not extend past 2009/10 arrival date of WNS.
* Regional change is best available data on total of maximum bat number recorded when WNS was detected that year in the region or at a site (9,092 bats; 2009/10 – 2010/11), compared with most recent count (151 bats in 2012/13).

In NB, 10 sites were monitored for WNS in 2010-2013. The first record of WNS was in March 2011 when 83% of 6,084 bats in Berryton Cave died or disappeared in one month (McAlpine et al. 2011). The following winter, 350 bats were counted in December 2011, and zero bats in April 2013, two years later (Table 5). Bats typically remain in hibernacula until mid-May and so the reductions indicate decline, rather than bats leaving for the summer (D. McAlpine, pers. comm.). Myotis are combined as ‘Myotis spp.’ in the data but M. lucifugus are known to be present; 607 (66%) of 919 captures in August 2010 during swarming at Berryton and Whites Caves, and nine (20%) of 45 captures at Howes Cave in 2011, were M. lucifugus (H. Broders, pers. comm.). Also, a sample of 357 dead bats from the 2011 event in Berryton Cave contained 91% M. lucifugus (D. McAlpine, pers. comm.). During 2010-12, diagnostic testing and post-mortems confirmed WNS in 27 of 31 M. lucifugus collected from hibernacula and the landscape (S. McBurney, pers. comm.). By March 2013, WNS was recorded in all 10 known hibernacula, with declines of 33-100%; a total of 79 Myotis remain in the known NB hibernacula, as of April 2013. The average decline for NB from the first record of WNS to March 2013 was 99%.

Notes
1) Abundance based on average counts from 2-3 surveyors; ‘Late’ = March to April, ‘Early = November to February.
2) Values in bold italics = survey when WNS was first detected by visual methods.
3) % Change is difference between first detection of WNS and most recent count; repeat visits facilitated detection of decline that winter.
4) * Increase believed due to previously hidden bats moving to entrance, where most were found dead or infected with WNS.
5) Total only includes data from sites that are available across years. Percent change is total from 1st year of WNS being recorded (2011), to late 2013.
^ Regional change is best available data on total of maximum bat number recorded when WNS was detected that year in the region or at a site (7,473 bats; 2010/11 – 2011/12), compared with most recent count (79 bats in 2012/13).

Until 2012/13,most data on WNS in NS were from reports of winter-flying bats and submissions of >550 carcasses; 35 of 45 Myotis lucifugus tested from 2010-2012 were positive for WNS (S. McBurney, pers. comm.).The following data are from H. Broders (Saint Mary’s University): WNS was first observed on bats in hibernacula in spring 2012 and all five sites were infected. Declines were evident in some caves (i.e., 23, 25%) but one increased (27%), and overall there was a modest decline of 5% (Table 6). As predicted based on trends elsewhere, the second winter was catastrophic; in 2012/13, counts of Myotis (M. lucifugus and M. septentrionalis combined) decreased by 20,177 bats; declines of 89-99% were recorded in each cave, with an average decline for NS of 93%. The late winter count was conducted during the second week of April and it was expected that 2-6 weeks of hibernation remained. Therefore, whole winter mortality likely exceeded 93%. A high proportion was likely M. lucifugus; 71% of 5,974 bats captured at the entrances of the five hibernacula were M. lucifugus.

Notes
1) Abundance based on average of 2-3 independently derived, systematic counts by St. Mary’s University staff.
2) Data on two additional sites not included because surveys have not been conducted after WNS detection.
3) Values in bold italics = survey when WNS was first detected.
4) * Site was surveyed three times (by unknown methods) with counts of 2,973 (1996/97), 2,079 (2000/01), and 2,761 (2003/04).
5) Total based on sites with data across years; Lake Charlotte data not included in 2011/12 total.
^ Regional change is best available data on total of maximum bat number recorded when WNS was detected that year in the region or at a site (22,729 bats; 2011/12), compared with most recent count (1,571 bats in 2012/13).

Fewer data are available for summer. In Ontario, numbers of bats using four of five maternity colony sites declined (range: 4-89%) and one site increased (12%) but overall percent difference in total maximum number per colony at time of WNS arrival to most recent data is -71% (Table 7). In Quebec, best available data from four maternity colonies indicate average decline of 96% (Table 8). Summer data from maternity colonies for population size or trends are not available for the Maritimes, except for recent declines noted in summer 2012 at four maternity colonies in NS where ‘hundreds of bats are down to a few’, including a decline from 45 to 11 female pit-tagged Myotis lucifugus at one site (H. Broders, pers. comm.). There are anecdotal reports of ‘only a few bats’ being seen in parts of NB, but no quantitative data exist. In Quebec, acoustic data on roads suggest provincial abundance of Myotis sp. (M. lucifugus, M. septentrionalis, M. leibii, combined) had not significantly changed from 2000 to 2011. However, the lowest average abundance of Myotis was in 2011 and there were significant decreases in the Quebec, Lanaudière, Outaouais, and Abitibi regions of southwestern Quebec, where WNS has been recorded (N. Desrosiers, M. Delorme, A. Simard, and I. Gauthier, pers. comm. 2013).

Notes
Total % Change is difference between total maximum count per colony in 2010 (n=1105 bats) and total most recent count per colony (n=316 bats).

Note:
1) Values for Domaine Joly in 2009 and 2011 are estimates.
2) % Change is difference from highest to lowest count.
3) Total % Change is difference between total maximum count per colony in 2009 or later (n=2144) and most recent count per colony (n=88). Using only data since arrival of WNS, average decline based on three sites is -95%.

Myotis septentrionalis - US Data

The population trends of Myotis septentrionalis in the northeastern US mirror the results for M. lucifugus. Data from winter indicate that population declines in 32 hibernacula (infected for two years or more) in the northeastern US have been >98% for M. septentrionalis (Table 9; Turner et al. 2011). Bats were extirpated in 23 of 32 hibernacula (72%). Data from summer corroborate declines recorded in winter. All studies, conducted with a range of methods, indicate a decline of 30 to 100% (Table 10). A significant decline in bat activity was recorded by Ford et al. (2011) in northwestern New York, with declines from 0.7 to 0.4 mean echolocation passes/hour (43% decline). Preliminary results from 200 transects conducted during summer in 24 states indicates significant declines in summer abundance in WNS range (i.e., near extirpation of M. septentrionalis in New York with most transects no longer detecting this species; Britzke et al. 2011 unpub. data). Acoustic data are corroborated by capture data; the species was commonly captured pre-WNS but now is rarely caught in New York (C. Herzog, pers. comm.) with probability of capture declining from 0.3 to 0.015. In West Virginia, mist net surveys at the same 46 trap sites and with same trap effort documented significant decline from average 14.7 captures pre-WNS period (2005-2008) to 7.3 in 2011 (Johnson and Sanders 2012; C. Johnson, pers. comm.). A state-wide assessment of 5,469 M. septentrionalis captured in West Virginia found a 77% decline in capture rates between pre- (1998-2007), and post-WNS (2010) periods (Francl et al. 2012). In Vermont, trapping results at fall swarm events, and acoustic surveys at fixed sites, indicate dramatic declines (S. Darling, pers. comm.).

Note: For Vermont, species identification facilitated by all sites having low ceilings (S. Darling pers. comm.).

Myotis septentrionalis - Canadian Data

The average total decline of Myotis from Ontario hibernacula being monitored was 93% since detection of WNS (Table 3). Myotis are not separated to species in Ontario data but each of the eight hibernacula being monitored contained M. septentrionalis (L. Hale, pers. comm.). Based on results elsewhere, it is assumed that M. septentrionalis declined at similar rates as M. lucifugus. M. septentrionalis comprised 3.2% of 6,361 bats captured at 10 hibernacula in the same region from 1966-1968 (Fenton 1969) and their continued presence is likely. In Quebec, at the four sites with data after the arrival of WNS, M. septentrionalis abundance declined from 1,609 to 2 bats, a 99.8% decline (Table 11).

Note:
1) Abundance based on visual counts. ‘Late’ = March to April; ‘Early’ = November to February.
2) Value in bold italics = the survey when WNS was first detected at that site; Halifax and Copper sites likely had WNS in 2009/10. Most sites not surveyed in 2010/11 due to budget constraints.
3) % Change is difference between first detection or year of detection in Quebec (2009/10), and most recent abundance estimate.
4) Partial survey conducted at Quebec Copper in 2012 due to flooding but areas surveyed should have contained bats, as in previous years.
5) Total only includes data from sites that were surveyed across years.
6) Additional sites have been surveyed (e.g. St. Robert Metal, Copperstream Frontenac) but are omitted because data do not extend past arrival of WNS (2009/10).
*^ Regional change is best available data on total of maximum bat number recorded when WNS was detected that year in the region or at a site (1,609 bats; 2009/10), compared with most recent count (2 bats; 2011/12).

The declines recorded for Myotis in NB (99%; Table 5) and NS (93%; Table 6) (see Myotis lucifugus – Canadian Data section) likely applies to M. septentrionalis, based on the following: M. septentrionalis are likely, or known, to be present in the hibernacula; 312 (34%) of 919 captures in August 2010 during swarming at Berryton and White caves, and 36 (80%) of 45 captures at Howes Cave in 2011, were M. septentrionalis (H. Broders, pers. comm.). Also, 30 (8.4%) M. septentrionalis were identified from a sample of 357 dead bats collected at Berryton Cave from a 2011 mass mortality event of 83% of 6,084 bats (McAlpine et al. 2011; D. McAlpine, pers. comm.). All three Myotis septentrionalis submitted for WNS testing in 2011/12 tested positive (S. McBurney, pers. comm.). In NS, M. septentrionalis comprised 28% of 5,974 captures over 11 years at the entrance to the hibernaculum (H. Broders unpub. data). Four carcasses found on the landscape and submitted for testing in 2011-2012 tested positive for WNS (S. McBurney, pers. comm.).

There are no summer data on population size or trends from maternity colonies of M. septentrionalis for Canada.

Frick et al. (2010a) predicts Myotis lucifugus to be functionally extirpated by 2026 (see Myotis lucifugus – US Data section). The extension of Frick et al. (2010a) to M. septentrionalis appears warranted because of the very similar life history characterstics of the two species (see Morphological Description, Habitat, General Biology sections) and because both have experienced similar dramatic declines in populations in the northeastern US and Maritimes. Also, Langwig et al. (2012) results suggest M. septentrionalis populations in the northeastern US are likely to be functionally extirpated (see Transmission and Risk of Infection section).

Perimyotis subflavus - US Data

Population declines in infected areas (much of the northeastern US) have been similarly dramatic. Average population decline of Perimyotis subflavus in hibernacula for the northeastern US was 76%, as of 2011 (Table 12; Turner et al. 2011).Thirteen of 36 hibernacula declined to zero bats.One site (Coon Cave, Virginia), unusual for containing so many P. subflavus, declined from 920 bats before WNS, to 112 in 2011 (R. Reynolds, pers. comm.).

Summer declines in abundance of Perimyotis subflavus are evident where data are available for sites with post-WNS data (Table 13). For example, in NY, in a state-wide, acoustic-based monitoring effort, detection of P. subflavus in summer was 0.7 detections/30 km of road in 2009 and declined to 0.4/30 km in 2011. This decline is an underestimate because monitoring was not initiated until severe bat declines from WNS had already taken place (C. Herzog, pers. comm., unpub. data). Also in NY, Dzal et al. (2011) found P. subflavus bat activity declined from 3.7% of bat passes among seven species, to 1.5%, a 59% decline. Captures of P. subflavus from mist netting in NY were rare before WNS (38 total from 737 net nights [0.052] in 2003-2007) and are essentially absent after WNS (3 total from 1,856 net nights [0.002] in 2008-2011) (C. Herzog, unpub. data). Ford et al. (2011) noted a decline in late summer versus early summer in bat activity in pre- and post-WNS in northwestern NY, but not when all summer data were combined. In West Virginia, 386 P. subflavus were captured pre- WNS (2008) and 101 were captured post-WNS (2010), using the same methodology and capture sites (C. Stihler, pers. comm., unpub. data). Capture rates in West Virginia after WNS (data collected in 2010) were 77% lower than capture rates during a pre-WNS period (1997-2008) (Francl et al. 2012). In Pennsylvania, capture rates were 0.005 during summer pre-WNS (55-70 P. subflavus with a trap effort of approx. 10-14,000 1 m2 mesh units set for one hour) and declined to 0.0004 post-WNS in 2010 (13 bats from approx. 31,000 1 m2 mesh unit) (C. Butchkoski, pers. comm.; Butchkoski 2011). In Virginia, captures at six autumn swarm sites declined from early-WNS levels of 15 P. subflavus captures per site to approximately two bats per site in 2011 (R. Reynolds, pers. comm., unpub. data). These data are limited and confined to small areas, but all demonstrate the same trend of significant declines during summer.

Perimyotis subflavus - Canadian Data

Results in parts of Canada where WNS has been reported for >2 years are similar to those reported in the US, although the generally low numbers of P. subflavus makes it harder to establish if a decline occurred, or animals were missed in a survey (see details below).

In eastern Ontario, Perimyotis subflavus were recorded in the monitored hibernacula (i.e., 12 at Hunt Mine; L. Hale, pers. comm.) but specific numbers for P. subflavus are not available. It is assumed that the 93% decline in Myotis indicates a similar mortality level in P. subflavus.

In Quebec, 15-21 Perimyotis subflavus were recorded in three of 11 hibernacula per year during the two preceding pre-WNS years (Mainguy et al. 2011). There are data for only one of the three sites (Mine-aux-Pipistrelles) after the arrival of WNS; the number of P. subflavus declined from 17 in March 2010 to one in November 2011, a 94% decline.

In NB, Perimyotis subflavus were recorded in five sites (range of 1-9 per site) with a decline from 20 (pre-WNS) to 14 P. subflavus (- 30%), and none recorded at three sites in 2011 (D. McAlpine and K. Vanderwolf, unpub. data). Individuals did not show signs of WNS in 2011. A single P. subflavus found dead in Berryton Cave in March 2011 and submitted to Atlantic Veterinary College tested positive for Pd (S. McBurney, CCWHC unpub. data). In mid-winter 2012/13,Pd spores were first recorded on hibernaculum walls (as distinct from swabs taken from bats), suggesting that Pd spores were  then well distributed in hibernacula. By April 2013, the number of P. subflavus was five bats (-75% since 2010), and all remaining bats were infected with WNS (D. McAlpine, pers. comm.).

In Nova Scotia, 47 Perimyotis subflavus (0.8% of 5,974 total bats) had been captured at the entrance of the five hibernacula being monitored (H. Broders, unpub. data). No carcasses have been found as of winter 2012/13. Based on mortality of P. subflavus in adjacent NB, the 91% decline in NS bats in 2012/13 likely includes P. subflavus.

Systematic monitoring of summer populations of Perimyotis subflavus in Canada has not been conducted.

Rescue Effect

There is no expectation of a rescue effect, given the presence of WNS because: 1) immigrants to previously infected areas likely would not survive; and 2) uninfected subpopulations are expected to become infected. The northern part of Myotis lucifugus and M. septentrionalis range presently is uninfected but it is unlikely that mortality levels will be different than those recorded southward. Bats in northern hibernacula may hibernate in relatively colder conditions (i.e., 2-3˚C in NT; J. Wilson, pers. comm.) and thus may be less susceptible to WNS because Pd does not grow as well at that temperature (Gargas et al. 2009). However, bats in laboratories exposed to WNS at <4°C still eventually died (Grieneisen 2011) and the longer period of hibernation in the north will likely result in higher mortality rates. WNS has been spreading into colder regions; to date, the most northerly mortality associated with WNS (M. lucifugus and M. septentrionalis, 2013) is near Chibougamou, Quebec, 700 km north of Montréal (G. Lupien, pers. comm.).

There is an expectation that mortality levels will be lower in the southern US because infected bats that are forced to look for water and food are likely to find both, and overall hibernation periods are shorter (Hallam and Fedrico 2011; Maher et al. 2012). Similarly, the coast of BC is milder and mortality will be lower. However, Pd spores persist in soil in hibernacula (see Transmission and Risk of Infection section) and it is likely that any bat subpopulations expanding northward from the southern US, or eastward from BC, would be impacted by Pd when they enter infected hibernacula in Canada.

Although evidence to date is lacking, if the population develops resistance to WNS (see Resistance section), and Pd spores are not viable indefinitely (see Transmission and Risk of Infection section), then the long-distance movements that helped spread WNS could also facilitate rescue.

Threats and Limiting Factors

Number of Locations

WNS constitutes the single most serious and plausible threatening event for the three species. Six years post-arrival, most known hibernacula in the northeastern US and the Maritimes have experienced massive declines. Hibernacula conditions are similar across the range of each species in Canada and at present there is no evidence that WNS will not grow in western caves. A single location could apply. However, the IUCN/COSEWIC guidelines on locations is based on the main threatening event rapidly affecting all individuals, which to date has not occurred for the two Myotis species. Therefore, the number of locations at present would instead be ‘many’ for the two Myotis, because each hibernaculum or maternity colony across the species’ range presently is subject to varying risk of extermination or disturbance from recreation, mining, etc. For Perimyotis subflavus, on the other hand, a single location is plausible because most of the Canadian range of the species is already coincident with the range of WNS within a three-year period.

White-nose Syndrome

Cause and Impact on Bats

Small-bodied bat species that winter in caves or mines are dying from WNS, caused by a dermatophyte fungus, Pseudogymnoascus destructans (Minnis and Lindner 2013) (previously called Geomyces destructans), believed to have originated in Europe (Lindner et al. 2011; Pikula et al. 2012; Ren et al. 2012; Warnecke et al. 2012). It was first detected in North America (NA) in 2006 (Lorch et al. 2011) and there is no evidence that the fungus was present in NA prior to this time; Pd was absent in samples of soil, walls, and bats in locations prior to the appearance of WNS on bats (Lorch et al. 2013;Vanderwolf et al. 2013). The fungus grows in cold environments >0°C, with optimum growth between 12-16°C, and no growth >19.8°C (Gargas et al. 2009; Blehert et al. 2009; 2012, Langwig et al. 2012; Verant et al. 2012). The fungus grows in the same conditions that the three species inhabit during winter (see Physiology section). Pd colonizes the bat’s epidermis and damages sweat glands, muscle, connective tissue, blood vessels, and hair follicles (Meteyer et al. 2009; Cryan et al. 2010). The muzzle often turns white and appears fuzzy while wings and ears have white-gray blotches on the surface (Figure 1; cover of report).

The actual cause of death is under investigation. It is suspected that irritation and dehydration associated with the fungal growth causes bats to arouse from torpor, resulting in increased grooming, premature depletion of fat reserves, and a need to forage for water and food (Warnecke et al. 2012, 2013; Brownlee-Bouboulis and Reeder 2013). Large numbers of bats seen flying during winter can be an indicator of WNS. Insect prey generally is absent in winter and bat mortality is hypothesized to be caused by starvation, dehydration, and exposure for those leaving the hibernaculum (Reeder et al. 2012; Willis et al. 2011; see Physiology section). Bats that survive until spring may have damaged wings (numerous holes) and are either too physiologically stressed to successfully birth or feed offspring (Meteyer et al. 2009; Reichard and Kunz 2009; Reeder and Turner 2008; Powers et al. 2012), or they may die during summer because their immune system reactivates in spring (Bouma et al. 2010) and an intense neutrophilic inflammatory response results in cell pathology and death (Meteyer et al. 2012). A comparison of pre- and post-WNS changes in reproduction behaviour associated with stress noted shifts in timing and shortening in duration of pregnancy and lactation rates, and the proportion of juveniles of Myotis lucifugus were 40% lower, and M. septentrionalis 50% lower, when compared to pre-WNS data in West Virginia (Francl et al. 2012).

Six species are recorded as dying in significant numbers from WNS: Myotis lucifugus, M. septentrionalis, M. sodalis, M. leibii, Perimyotis subflavus, and Eptesicus fuscus (NWHC 2013). Not all cave-dwelling species appear equally vulnerable; Eptesicus fuscus has experienced mortality but some populations may be increasing (Francl et al. 2012), possibly because of more active immune systems than other species (Reeder et al. 2012).Moreover, Pd has been recorded on three additional hibernating species--M. grisescens, M. austroriparius, andM. velifer--but large mortality events have not been observed to date (Foley et al. 2011). Five affected species occur in Canada; M. lucifugus, M. septentrionalis, M. leibii, P. subflavus, and E. fuscus. The species most affected to date in the northeastern US are M. lucifugus, M. septentrionalis, and P. subflavus (Herzog and Reynolds 2012).

WNS was first recorded in February 2006 in Howes Cave near Albany, New York and significant mortality was recorded the following winter (Frick et al. 2010a; Figure 5). The prevalence of infected hibernacula was 5% in the second year (2007), then 49 and 59% in the next two years in the northeastern US (Frick et al. 2010a). As of fall 2012, it is believed that all known underground hibernacula in the northeastern region of the US are infected with WNS, based on numerous surveys conducted across multiple states as part of the US monitoring program for WNS (Herzog and Reynolds 2012; C. Herzog, pers. comm.). Not all hibernacula have been surveyed but infection has been found in almost all that have been surveyed. For example, in New York, 59 of 100 hibernacula with >10 bats have been surveyed as of 2012, and all are infected (suspected, or confirmed with histopathology). Similar results exist for West Virginia, Virginia, and Pennysylvania where a subsample of the thousands of hibernacula has been surveyed; nearly all were infected (C. Herzog, pers. comm.).

Rate of Spread

The spread of WNS is presented in two stages that recognize positive detection of Pd and the actual occurrence of WNS. In the first few years of the outbreak, evidence of WNS was based on the characteristic and externally visible white muzzle (see Cause and Impact on Bats section). Since then, PCR-based testing (i.e., Lorch et al. 2010) of swabbed bats hibernating in unaffected areas has provided evidence of Pd on individuals that lack visible signs of WNS. Based on trends to date, it is believed that these ‘positive Pd’, or ‘suspected cases’ (Figure 5) likely forecast future declines for the site. In many of the northeastern states, as well as in NS, NB, Quebec, and Ontario, infection and mortality rates were lower (i.e., 20%) in year one of detection, followed by high levels (i.e., >70%) within two years (see below). It is suspected that similar trends are occurring at the western edge of the outbreak. For example, in 2010, Pd was recorded at two sites in Missouri but significant mortality events or changes in number of bats per hibernacula had not been detected afterwards. In 2012/13, 11 new hibernacula showed signs of WNS and based on trends in eastern jurisdictions, significant mortality is predicted for next winter (A. Elliot, pers. comm.).

As of September 2013, Pd/WNS had been recorded in 23 US states and five Canadian provinces (Figure 5). In some jurisdictions (e.g., NY, NB; McAlpine et al. 2011), first detection was coupled with numerous carcasses found in the hibernaculum. Generally, however, bats would be absent from previously populated hibernacula; it is suspected that bats were dying outside hibernacula and not being discovered. WNS was first detected in PEI in February 2013, with 15 confirmed cases as of March 15, 2013 (CCWHC 2013). Additional sites within the existing range of WNS in Canada and the US are being detected each year (e.g., northern NB, central Ontario [Figure 5]), with the most recent (spring 2013) detection of Pd in northeastern Minnesota, the first record west of the northern end of the Great Lakes, and 100 km from the Canadian border (MNDNR 2013).

When using data only from sites with known mortality from WNS, the rate of spread was approximately 200-250 km per year in Canada. WNS was first detected in Ontario and Quebec in winter 2009-2010, in NB and NS in 2010-2011, and in PEI in 2012-2013 (Figure 5). The movement rate from the Albany, NY epicentre to NB was 200 km/yr, and 250 km/yr to the westernmost Canadian site (Wawa, Ontario). The first event in Ontario (Cochrane) was 1,000 km from the epicentre (250 km/yr), which may indicate Pd can spread in large leaps, either by bat or human movement, or that Pd was already present but undetected in Ontario sites that are closer to Albany. When using data from sites with Pd (but no evidence of WNS), the rate of spread was more rapid (i.e., 400 km/yr to Missouri; 600 km/yr to Oklahoma; 333 km/yr to Minnesota). Cases of Pd or WNS were recorded in eastern Iowa in spring 2012 (268 km/yr) and northern Georgia in March 2013 (215 km/yr).

Transmission and Risk of Infection

The transmission dynamics of WNS within hibernacula are not understood but likely are related to the density of bats and frequency of contact between infected bats and walls, and potentially by people visiting multiple caves (Foley et al. 2011).

Laboratory experiments showed bat-to-bat contact spreads Pd spores (Lorch et al. 2011). The amount of physical contact among hibernating bats varies by species. Myotis lucifugus typically roost in clusters, M. septentrionalis roost in clusters and by themselves, while Perimyotis subflavus typically roost by themselves (see Adaptability section). Langwig et al. (2012) modelled infection rates and concluded that M. septentrionalis populations are not viable in the northeastern US because the density levels and proximity of M. septentrionalis within northeastern hibernacula are high enough to facilitate transmission of Pd spores. Larger populations of M. septentrionalis experienced larger declines than smaller populations but smaller populations still experienced high mortality rates. M. lucifugus populations declined, regardless of density, apparently because they cluster in large groups and the transmission of fungal spores continued, even as populations declined. A change in behaviour toward single roosting was noted for this species following the onset of WNS, which may increase the chances of survival. For P. subflavus, the modelling by Langwig et al. (2012) suggests that <6 P. subflavus in a hibernaculum may be below a threshold of risk of transmission. However, the model was based on data as of April 2010 when some hibernacula still had higher survival rates and some caves were uninfected. Now, however, there are no known uninfected, large hibernacula in the northeastern US (Herzog and Reynolds 2012) and results likely would differ.

Recent evidence suggests that contact with infected substrates may be a more significant transmission factor than bat-to-bat contact (Kilpatrick 2013). The amount of physical contact among hibernating bats varies by species, and has not correlated well with infection rates. For example, despite the minimal clustering by Perimyotis subflavus, this species has suffered high mortality rates; members of this species existed in low numbers of only several individuals per hibernaculum in NB, but still became infected (see Perimyotis subflavus - Canadian data section). It is expected that transmission to uninfected bats will increase as more of the hibernacula surface retains Pd spores. There is evidence that the fungus resides in the soil and walls of caves (Chaturvedi et al. 2012; Lindner et al. 2011; Puechmaille et al. 2011), even in summer when bats are absent (Lorch et al. 2013). The viability of spores over time is unknown.

Hence, though the dynamics of transmission are unclear, evidence suggests that WNS eventually causes significant mortality in hibernacula with different bat densities, and on species with different clustering behaviour.

At a regional scale, bats themselves are the likely transporters of Pd, although more research is needed. Spores of Pd have been found on bats during summer, and in bat boxes (Dobony et al. 2012) but it is unknown if transmission occurs during summer. Extensive bat-to-bat contact during swarming during autumn may be instrumental in the spread of WNS (B. Fenton, pers. comm.). Swarming behaviour shows young bats where to hibernate and also heralds the start of the mating season; bats may enter caves during swarming (Thomas et al. 1979), potentially picking up Pd spores from one another.

Infection of Remaining Canadian Range of Myotis lucifugus and M. septentrionalis

Although there is some uncertainty (see below), Pd is expected to continue to spread throughout Canada and the western US because: 1) most of the population of Myotis lucifugus and M. septentrionalis in the western range hibernates in same range of abiotic conditions found in WNS-affected sites in the east; 2) there is no evidence of containment ofPd and WNS events; and 3) bats hibernating in low numbers still appear to be susceptible to WNS (see Transmission and Risk of Infection section).

Population declines are expected because most hibernating bats hibernate within the growth range of Pd even though there is some variation in both microclimate used by hibernating bats and growth rates of Pd at different temperatures (see Cause and Impact on Batssection). Based on growing conditions for Pd (minimum and maximum temperatures in hibernacula), and the relationship between temperature and lipid reserves in Myotis lucifugus, Hallam and Federico (2011) predicted that much of the US has the conditions necessary for growth of WNS. Recent suitability modelling based on presence of environmental variables at sites with Pd in Europe predicts that all of the current Canadian bat range is susceptible to Pd, with highest suitability existing in the Great Lakes region and BC (Puechmaille 2013).

Much of the initial spread of Pd/WNS was along a northeast to southwest direction of the Appalachian mountain chain, and northward and eastward into Canada (Figure 5). Infection westward in the US occurred in the Ozark Mountains area and across the Mississippi River in 2011. The disease is approaching less forested regions of central North America but the amount of bat movement along an east-west axis, or from forest to prairie is unknown. The relative dryness, few trees, and hibernacula in the Prairies suggests transmission might occur with less speed across the region, but Myotis lucifugus are common in the Prairies (see Distribution section) and it is possible that the Prairies would slow, but not prevent, the spread of WNS. Alternatively, WNS may spread westward by routes south and north of the Prairies. The most westerly Pd confirmed sites to date (Arkansas, Missouri) are 1,200-1,300 km from the Rocky Mountains (Denver, Colorado), and one possible pathway is for Pd/WNS to move northward into Canada after reaching the US section of the Rocky Mountains. To the north, Pd/WNS would be expected to move westward across the forested sections of the Prairie provinces because this habitat is similar to forests in infected regions of central Quebec and Ontario, and the Minnesota detection of Pd may be indicative of westward spread. In spite of some evidence of genetic structure (see Designatable Units), enough genetic similarities exist among Myotis lucifugus in the Rocky Mountains to suggest that the mountains have not served as a physical barrier to gene flow, and will therefore not prevent WNS from reaching the Pacific Ocean (Russell et al. 2012).

If the recorded average rate of spread (200-250 km/yr) is applied under the assumption that the spread will continue at this rate, WNS could occur on the west coast of North America within 12-15 years (i.e., 3,000 km from Lincoln County, Missouri to San Francisco, California). Starting from Wawa, Ontario (the most westerly record of WNS in Canada), WNS could reach the BC coast (the western extent of M. lucifugus) in 14-17 years at the same rate. The western edge of the Canadian range of M. septentrionalis (approximately, Trout Lake, BC to southeastern Yukon) could be reached in 12-15 years. The detection of Pd in northeastern Minnesota (800 km west of Wawa) may mean that the fungus is already closer to the Rockies than the Wawa starting point.

In the US, simulation modelling based on dispersal, cave location, climate, and distance predicted that WNS will first reach the Rocky Mountains in 2015 and Pacific coast in 2031 (18 yrs), with the slowest infection along Mexican border (Maher et al. 2012). The study did not address Canada because of a lack of data on cave number and location. There is no evidence to suggest different results between Canada and US.

There also is the possibility that WNS will reach western populations faster than the prediction based on the movement of bats. It is suspected that Pd was accidently brought to North America by tourists who had visited caves in Europe; the original site of detection was in Howes Cave, a non-commercial part of the Howes Caverns that receives >200,000 visitors per year (Howes Caverns 2013). Pd spores have been detected on clothing of people exiting a cave (Okoniewski et al. 2010). The possibility of WNS transmission by people raises concern that Pd will be transmitted to western hibernacula by tourists or spelunkers who visit multiple sites. The movement of bats from Asia to western North America on ships may also be a conduit for WNS (Wright and Moran 2011).

Limited understanding of the dynamics of transmission increases uncertainty regarding vulnerability of western bats to WNS. The rates of east-west bat movement are unknown, and less is known about hibernating bats in the west than east. There is long-distance, north-south bat movement in Manitoba (see Migration section) but such movement may be atypical, resulting in only a small number of bats present to carry Pd (Norquay et al. 2013). The number of infected bats required to infect a new site is unknown. Although the site in NT has >3,000 bats, it is suspected that bats in the western range are hibernating at many sites and in small numbers (see Abundance section). It is possible, but unproven, that Pd/WNStransmission rates could be slower if there are different density- or frequency-dependent factors in western hibernacula that affect the severity of WNS.

WNS and Perimyotis subflavus

The impact of WNS on Perimyotis subflavus requires additional discussion because the effect of WNS on P. subflavus is not as straightforward as it is for the other two species. There are fewer data on P. subflavus in Canada than for the other two species and there is some debate on where they hibernate.

Fewer than 30 P. subflavus are typically recorded in any US hibernaculum (Fujita and Kunz 1984;Trombulak et al. 2001; but see Davis (1959) where 800 P. subflavus were banded in two West Virginia caves) and less than 20 in Canada. For Canadian P. subflavus, this observation may be because: 1) few exist in Canada during summer and thus there is no discrepancy between winter and summer data sets; 2) more P. subflavus actually are present in hibernacula but they are harder to detect; 3) they have migrated southward and winter underground, within WNS range and thus are vulnerable to WNS; or 4) they have migrated southward and are not vulnerable to WNS because they have gone beyond WNS range, or hibernate where WNS is not present (i.e., above ground). In scenario 4, if a significant proportion migrate south (see Migration section), and overwinter above ground in southern areas (Davis 1959) it raises doubt as to the severity of WNS on this species (i.e., if only a small proportion of the species are in caves, then few are vulnerable to WNS) (B. Fenton, pers. comm.).

There is evidence for the first three scenarios. Records of Perimyotis subflavus in summer are very low and similar to the number of winter records (see Abundance section). Also, they are believed to be hard to detect in hibernacula; it is suspected that most hibernating P. subflavus are in the caves but cannot be seen (A. Hicks, pers. comm. 2011) because they often hibernate singly, and deep in caves where human access is limited (Hitchcock 1949; Fujita and Kunz 1984; Sandel et al. 2001).

There is evidence of southward autumnal movement, with distances that could take them into WNS range (northeastern US) and the only records of the species in winter within WNS range are underground. The evidence that P. subflavus overwinter above ground anywhere is limited; in Texas, P. subflavus hibernate above ground in road culverts (Sandel et al. 2001) but 93% of all observation records in the US are in caves or mines (Ellison et al. 2003). And the species is considered an obligate hibernator in the US. In Florida, a jurisdiction where insects and temperature may be sufficient to minimize the need for hibernation, P. subflavus still hibernate, and are only known from underground caves (McNab 1974).

In summary, evidence suggests that Perimyotis subflavus are hibernating underground in Canada, and most likely in the northeastern US within the range of WNS. Importantly, populations in summer show marked decline (see Population Trends section), concurrent with recorded declines in the other bats impacted by WNS; thus it seems likely that P. subflavus populations are affected by WNS, regardless of the uncertainty with hibernating behaviour.

In addition, Perimyotis subflavus already are a rare species in Canada, and there is evidence that individuals hibernating within WNS range are particularly susceptible. P. subflavus hibernate at a temperature that is optimum for the growth of Pd, they hibernate for the longest period of time of the three species, and they have essentially no immune activity while hibernating (Raesly and Gates 1987; D. Reeder, pers. comm.). The range of P. subflavus in Canada occurs within the present distribution of WNS and refugia are unlikely (Figure 4).

Resistance to WNS

At the early stages of the spread of WNS, it was hoped that only some hibernacula would be vulnerable to WNS. If the spread of WNS was strongly density-dependent, then hibernacula with small populations might escape WNS (Wilder et al. 2011). Instead, as of spring 2012, 6-7 winters after first detection, WNS infects virtually all hibernacula in the northeastern US (Herzog and Reynolds 2012; see Cause and Impact on Bats section).

A few sites seem resistant to WNS. In Maryland, for example, bats in three abandoned railway tunnels have not shown signs of WNS. These sites have high air flow, fluctuating temperatures, and creosote-covered framing, factors that might inhibit growth of Pd (D. Feller, unpub. data). In general, however, these unique and artificial sites contain small numbers of bats and if they persist, likely will not play a significant role in recovery of the regional population.

Hope for any recovery of the species is based on the likelihood that some small percentage of the population across the range will have a genetically based resistance to the effects of Pd. These survivors would pass on this resistance to their offspring and populations would increase. It is suspected that such a situation occurred in Europe because even though Pd has been recorded on several species of bats, mortality levels are low (Wibbelt et al. 2010); in central Europe, 62-64% of 100 hibernacula, and 50% of Myotis myotis tested positive for Pd, but no mass mortality or aberrant flight behaviour has been recorded (Horacek et al. 2012).

There is evidence that some individuals exposed to WNS can survive, based on laboratory data (Meteyer et al. 2011) and banding studies (Dobony et al. 2011), presumably because the fungus ceases growing as body and ambient temperature increases after bats leave hibernacula (Meteyer et al. 2011). In the Dobony study, a small number (i.e., <20) of banded Myotis lucifugus in Ft. Drum, NY had wing damage (suggesting exposure to WNS) but had survived and were recaptured the following summer. Five females were recaptured after two years, and some were lactating, suggesting reproduction in some survivors. One cave in NY has populations of approximately 1,000 bats for four years in succession, suggesting stabilization (Turner et al. 2011). These results suggest some hope for eventual recovery. It is noted, however, that declines at these sites were 88% (Ft. Drum) and 93% (NY) and apparent stability at some hibernacula may be due to movements of uninfected bats from other areas; lactation does not mean that pups survived if adults are physiologically stressed (Dobony et al. 2011). Research designed to evaluate the extent of movement between caves has begun using a large population of banded bats (Hicks et al. 2012).

The populations of affected species are not expected to recover quickly because bats have slow population growth rates. Mortality is high in yearlings while adults are long-lived and only produce 1-2 young annually. The population growth rate over 16 years was 1.008 in a recent, pre-WNS study from New Hampshire (Frick et al. 2010b), and 0.98-1.2 in 22 populations in the northeastern US (Frick et al. 2010a). The rate for Myotis septentrionalis and Perimyotis subflavus was estimated to be 1.03 and 1.04, respectively (Langwig et al. 2012). Such a life-history strategy heightens the vulnerability of these bat species to high adult mortality rates.

Wind Turbines

Turbines cause mortality in bats by direct striking of a bat in flight, or barotrauma associated with acute differences in air pressure near the turbines (Baerwald et al. 2008). It is not possible to determine the significance of mortality because total population of the three species is unknown. Also, estimates of mortality are difficult because carcasses are hard to locate due to vegetation, decomposition, scavengers, and size of area to be surveyed (Kunz et al. 2007). Regulatory agencies often require a correction factor be applied to the number of carcasses found per site (e.g., OMNR 2011). For example, in one 86-turbine site in southeastern Ontario (Wolfe Island), correction factors estimated that 1,920 bats were killed in one year, based on 118 actual carcasses found (Note: the correction factors are for all species combined but only one of the 118 was identified as either Myotis lucifugus or M. septentrionalis (Stantec 2010; 2011). Overall, it is not possible to adequately quantify total estimated mortality across the species’ range because some data are not available and correction factors are not available by species, or have not been consistently applied or provided.

Long-distance migrant bat species, such as Hoary, Red and Silver-haired (Lasionycteris noctivagans) comprised approximately 75-80% of known fatalities at turbines (reviews by Arnett et al. 2008; Johnson 2005). Myotis bats were not as commonly killed by turbines (e.g., 0-13%; Arnett et al. 2008) likely because they migrate shorter distances, and, during summer, generally fly below turbine height (Reynolds 2006). Mortality of M. lucifugus in 2010 was estimated at 4,720 bats in 10 northeastern states (Kunz and Reichard 2010).

In Canada, a summary of 1,423 bat carcasses collected from 638 turbines at 16 sites from seven provinces between 2006-2009 (Environment Canada et al. 2011) noted nine species, with Myotis lucifugus the third most common (21% nationally, 27% in Ontario). Carcasses of M. septentrionalis and Perimyotis subflavus were found the least, but numbers were not provided. Correction factors that estimate actual mortality were not provided in the review.

Low numbers of Myotis lucifugus, and virtually no M. septentrionalis and Perimyotis subflavus, carcasses have been collected in Canadian jurisdictions: NS (1 M. lucifugus from two sites in 2011; M. Elderkin, pers. comm.), NB (4 M. lucifugus of 7 total bats at two sites in 2011;M. Sabine, pers. comm.), Manitoba (1 M. lucifugus, 0 M. septentrionalis from 98 total bats from four turbines at 63 turbine sites over a three-year period; Jameson and Willis 2012); Saskatchewan (0 Myotis of 85 bats, Golder 2008; 2 M. lucifugus of 46 bats, Golder 2011). In PEI, 9 Myotis (6 M. lucifugus; remainder too decomposed) were killed at four turbines near Summerside in 2010, suggesting a corrected mortality rate of 2.47 bats/turbine/year (Fundy Engineering 2012). Of 62 carcassses collected from 2005-2011 at six wind farms on the Gaspé Peninsula, Quebec, there were 6 M. septentrionalis, 1 M. lucifugus, and 0 P. subflavus (A. Massé, pers. comm.). In Alberta, neither Myotis typically is recorded (Baerwald 2008; R. Barclay, pers. comm.). In BC, Myotis (numerous species combined) comprised 44% of fatalities at the first wind development in the province (Hemmera 2011).

Although migratory bats are most vulnerable, there is evidence that relatively large numbers of Myotis are killed at some sites, indicating that siting of wind turbines is an important factor in assessing their threat (Arnett et al. 2008). A few sites in Tennessee and West Virginia recorded Perimyotis subflavus to represent as much as 25% of mortalities, and Myotis lucifugus in one site in Alberta as 23% of total mortalities (Arnett et al. 2008). In Ontario, M. lucifugus comprised 4-60% of mortalities at 16 sites monitored between 2006-2010, and 306 (27%) of 1,133 total bats from nine sites (474 turbines) (Environment Canada et al. 2011). An estimated 7,000 M. lucifugus, 310 M. septentrionalis, and 52 Perimyotis subflavus were killed annually, based on correction factors and data from 44 wind farms (2,955 turbines) across Canada (R. Zimmerling, pers. comm.).

Migration distance and proportion of a population that migrates are important factors but we know little of the extent of movement within Canada, or by Canadian bats into US jurisdiction. Most mortality documented in Canada has occurred in August, which corresponds to migration (Johnson 2005). Movement by Myotis lucifugus has been recorded between Ontario and NY (Davis and Hitchcock 1965; Fenton 1970a) but the impact of any increase in wind turbines in the US is unknown.

A significant increase in the number of wind farms in North America is expected. The US Department of Energy forecasts 241 GW will be needed to meet their goal of 20% energy from wind by 2030; as of March 2010, the total online was 36 GW (Kiesecker et al. 2011). The Canadian Wind Energy Association estimates Canada presently has 5,403 MW (approximately 3,063 turbines) with as many being constructed again in the next five years; Ontario alone is proposing increasing capacity by 5,600 MW by 2018 (CWEA 2012).

Predicting the impact of turbines to bats in the future is confounded by potential mitigation activities. In Ontario, for example, turbines are turned off when mortality levels exceed certain thresholds (McGuiness et al. 2011) and since most bat strikes occur during low wind speed, there may be an economic threshold on power generation that also minimizes bat mortality (Baerwald et al. 2009).

In summary, mortality levels from wind turbines are unknown because only a small subsample of turbines have been sampled, the number of mortalities varies by location, height, and speed of turbine, and correction factors are of mixed application. Moreover, total bat population size is unknown, making it impossible to assess population-level impacts. Where data exist, evidence to date suggests mortality levels at a national scale are relatively low for Myotis septentrionalis and Perimyotis subflavus. Mortality levels of M. lucifugus can be high in certain locations and total mortality likely will increase with proposed increases in the number of wind farms. Because mortality levels will vary depending on location it is not possible to assess the extent of the threat on each species. The impact of additional mortality from wind turbines on bat populations already decreased by WNS is unknown.

Colony Eradication

Some maternity colonies of bats in buildings are exterminated due to fears of contacting histoplasmosis and rabies, and because of noise and the accumulation of feces. The number of exterminations in Canada is unknown, but likely in the hundreds; a dozen requests are made annually in the Yukon alone (T. Jung, pers. comm.). Most data are anecdotal (e.g. 30,000 exterminated in a Quebec church in mid-1980s; Wells 1986). Colony removal can be significant to local populations because maternity colonies often contain most of the breeding females and offspring for a large area. For example, the only known colony on PEI was in a house and all bats were removed (Brown et al. 2007). If maternity colonies have multiple roosts, such as in the Yukon (B. Slough and T. Jung, unpub. data), exclusion from one colony could be mitigated by moving to the other colony.

Eradication programs used chemicals (i.e., dichlorodiphenyltrichloroethane [DDT]) on maternity and overwintering populations in much of the species’ southern range (Geluso et al. 1976). Pesticides (chlordane and DDT) applied to a New Hampshire maternity colony of Myotis lucifugus caused approximately 50% mortality in newborns and decreased the population, but did not eradicate it (Kunz et al. 1977). At 11 sites in Ontario, small colonies of Eptesicus fuscus were eradicated with DDT, but larger ones persisted (Barclay et al. 1979). DDT was commonly used to control bats in Ontario, at least through 1978 (Barclay et al. 1979).

Non-lethal methods involve sealing the entrances to a maternity colonyto restrict access before females arrive, or after pups have dispersed. Sealing entrancesproved the most successful method, as compared to application of DDT and sticky deterrants (Barclay et al. 1979).Sealing entrances may cause abandonment of the area, and not just the maternity colony; Neilson and Fenton (1994) found breeding females abandoned the study area when their site was sealed and did not use available bat houses, or move to other nearby maternity colonies in a complex of buildings. Data are unavailable on the extent of non-lethal versus lethal removal in Canada. The closing of abandoned mines also may be a threat to bats if the site was a hibernaculum and most local bats had switched from natural hibernacula to the mine. In some jurisdictions (i.e., Ontario), swarming bat surveys are conducted at sites to be closed (P. Davis, pers. comm.) but the number of mines containing bats that have been sealed is unknown.

Disturbance of Hibernating Bats

In eastern (and possibly western) North America, bat species that hibernate are at risk because most of the population overwinters in only a few sites (see Space Use section) and a high proportion of the population could be affected by single events. Bats enter the hibernation period with a finite fat reserve and a considerable amount of fat is consumed every time they are aroused (see Physiology section). Handling of hibernating bats will result in arousal from torpor (Speakman et al. 1991) and even without touching them, visitation by people causes arousal; in one study, bats flew above normal rates for up to eight hours after visits that had been <2 hours in length (Thomas 1995). When in deep torpor, bats are generally unaffected by ambient noise (Harrison 1965) but it appears that some individuals are closer to arousal and are the first to respond to noise and light, and begin to fly. Their tactile activities (i.e., attempted copulation, rejoining the cluster of bats) causes a cascade of arousal that can result in additional flying bats (Thomas 1995). Frequent and extended visits increase the severity of fat consumption; if the number of arousal events exceed natural rates, bats will consume fat reserves and die (Gaisler et al. 1981). Repeated visits over several days likely have severe impacts (Boyles and Brack 2009). Body mass of Myotis sodalis was lower at sites with increased levels of human visitation (Johnson et al. 1998) and M. velifer were disturbed the most from hibernation when tour groups were close, loud, and used lights (Mann et al. 2002). Restricting access and the enforcement of these regulations appeared to explain the increased number of M. lucifugus documented at Cadomin Cave in Alberta (Olson et al. 2011).

Visitation to hibernacula is not recommended (Hutson and Mickleburgh 1988) and some caves and mines are gated to limit liability from injury, but also to minimize disturbance of bats (Sherwin et al. 2009). Bats may avoid gated hibernacula and gates and barriers can be a problem for hibernating bats if airflow is restricted (Richter et al. 1993). Maintaining gates is a problem in some sites because people repeatedly remove them to gain access. Visitation to caves occurs in four categories; tourists, spelunkers, partiers, and researchers. Most of the visitation occurs in the summer and likely has relatively less impact on bats because they can replenish fat reserves, or are not using the site during summer. The number of visits in winter is unknown for any hibernacula in Canada. Many jurisdictions have local spelunking societies, and webpages identifying cave location and characteristics, as well as guidelines to minimize spread of WNS (e.g., US National Speleological Society). Prior to WNS, bat researchers were required to minimize the number of visits and duration, either though ethical code of practice or university animal care and government permit guidelines. Since WNS, researchers in US and Canada are expected to follow government protocols (USFWS 2012), which include single-use hazardous material coveralls, and fungicide application to equipment and clothing. In summary, the role of people in the spread of WNS within North America is a potentially significant issue but the impact has not been quantified.

Habitat Loss

Habitat for bats is composed of winter hibernacula, foraging habitat, and summer roost and maternity colony structures (see Habitat section). The use of buildings and bat boxes for maternity colonies by Myotis lucifugus may represent a benefit to the population, but likely less so in remote parts of their range where natural roosts may predominate. The forest structures most associated with maternity colonies for M. septentrionalis are numerous, difficult to identify, and have not been inventoried. Declines in amount of older age class forests (i.e., late successional, ‘old-growth’) could be a threat if these forests are preferentially used for foraging and roosting. Alternatively, clearcut harvest creates edge habitat that is widely used for foraging, and forest harvest practices that create forest remnants in harvest area, retain snags, and involve partial cut harvest may mitigate impacts of forestry. Overall, the extent of habitat loss (or gain) cannot be quantified because of the species’ large range and the varied intensity of forest harvest and practices across the range. The intensity and extent of this threat is unknown.

Chemical Contaminants

The threat of contaminants is threefold: direct impact on physiology of the bat either through intake of contaminated food, mortality from eradication programs (see Colony Eradication section), and indirectly through reduction of a food source. Toxic levels of organochlorines (i.e., dieldrin, polychlorinated biphenyl, DDT, DDE) derived from insect pest spray programs have been recorded in organ tissue in several species of bats (Reidinger 1976) and shown to cause fatality in fetuses and newborn Eptesicus fuscus (Clark and Lamont 1976). Lukens and Davis (1964) determined bats likely are more sensitive to DDT than other mammals. Geluso (1976) demonstrated mortality in young bats that metabolized fat containing toxic levels of DDT and surmised drastic declines in Tadarida brasiliensis were due to agricultural use of pesticides. The application of some of these chemicals has declined or been banned (i.e., DDT) but the impact of pesticides that remain in use today is not well studied.

Few studies have been made on the impacts of heavy metals on bats but one study in Ontario and Quebec (Hickey et al. 2001) found elevated levels of mercury, zinc, selenium, and lead in Myotis lucifugus, and mercury and zinc in M. septentrionalis. The levels of mercury were high enough to cause sub-lethal biological effects. Bats were likely ingesting heavy metals by feeding on insects (i.e., Trichoptera) that emerged from metal-laden sediments in agricultural areas.

The impact to bats from decreases in insects due to pesticide spraying is unknown. Bats consume a wide range of insects over wide areas; a localized application for a short period likely does not impact a population. Widespread and continuous application of pesticides likely would be a significant impact. In much of forested regions of Canada, forest Lepidopterans often are controlled with a naturally occurring bacteria, Bt (Bacillus thuringiensis) that kills all Lepidopteran species at a certain larval development stage; the impact on bats is unknown.

Other Threats

Frick et al. (2010b) concluded that annual female survival declined because of drier summers, suggesting climate change may be a concern if the amount of summer precipitation declines. Precipitation is associated with insect production, and lower insect abundance would affect a female’s ability to recover from producing pups and accumulate fat reserves needed to survive hibernation. Data on bat response for much of the range are unavailable.

The impact of mining activities, during exploration and extraction stages, may be a concern if noise and vibration disturb hibernating bats (N. Gougeon, pers. comm.). Closure of mines that excludes bats or reactivation of abandoned mines containing hibernating bats represents habitat loss. However, data on the extent of such activities are unavailable and the significance of any activity is unknown because the total number of hibernacula or bats is unknown.

Noise from road traffic will cause foraging bats to alter travel routes, and thus increased road density presumably decreases foraging area (Bennet and Zurcher 2012). The severity is not known and much of species’ range is in relatively roadless areas.

Protection, Status, and Ranks

Legal Protection and Status

Until recently, both Myotis were relatively common throughout much of their range and protection within many jurisdictions was limited to basic protection as a recognized wildlife species. Many mines have been closed, and the use of gates to allow bat access is variable. The construction of gates is most associated with sites where the presence of endangered species, such as Myotis sodalis, has been established. Permits are required in some jurisdictions for pest control activities at maternity colonies. Some protection for the species is derived from shared use of sites that are mainly protected for endangered cave bat species in the US, such as Myotis sodalis and M. grisescens.

The three species had not been previously assessed by COSEWIC before the 2012 emergency assessment, and a listing decision by the Minister is pending, as of this writing (see Preface section). M. lucifugus and M. septentrionalis in Ontario were listed as Endangered in January 2013 (OMNR 2013) and those species, plus P. subflavus, are in the process of being listed in Quebec (N. Desrosiers and I. Gauthier, pers. comm.). All three species were listed as Endangered in NB in June 2013 (M. Sabine, pers. comm.) and were added to to the list of animals and plants protected under the Nova Scotia Endangered Species Act in July 2013.

Following petition and preliminary review, M. septentrionalis was added to the US Endangered Species Act in October 2013 (Federal Register 2013). A petition was made for emergency listing of M. lucifugus in 2010 (Kunz and Reichard 2010) and an assessment process by the US Fish and Wildlife Service is underway (K. Tinsley, pers. comm.). Information requests have been initiated as the first part of an assessment process for Perimyotis subflavus (K. Tinsley, pers. comm.).

In 2009-2010, as part of a national response to minimize the spread of WNS, caves in numerous national forests in western US and all caves in the National Wildlife Refuges system were closed to the public (Kunz and Reichard 2010). Numerous states have similar programs established. An extensive research program is underway in the US to document the biology of WNS and mitigation strategies.

Non-Legal Status and Ranks

NatureServe Canada ranks for Myotis lucifugus are N3, and N2N3 for M. septentrionalis. National rankings had been N5 and N4 for M. lucifugus and M. septentrionalis, respectively, and were changed in September 2012 due to concerns of WNS. Ranks for Perimyotis subflavus are N2N3 (assessed January 2012). P. subflavus occurs in four Canadian jurisdictions, with ranks of S1? To S3?. M. lucifugus and M. septentrionalis are found in most Canadian jurisdictions and generally were ranked as secure (S4 or S5) until recent reviews related to WNS resulted in imperiled status (S1) in NS, NB, and Quebec (Table 14). In PEI, both species were already at high risk status. Outside of WNS range (Table 15), both species are ranked as secure, except in NT and Yukon, where they are ranked S1S2 because of small presumed numbers, and existence at the northern edge of the species’ range.

The global NatureServe ranks were changed from a status of secure-apparently secure (G5, G4) in July 2012 due to WNS and are now ranked as G3 (vulnerable) for Myotis lucifugus and Perimyotis subflavus, and G1G3 (critically imperiled to vulnerable) for M. septentrionalis. The US national rank for the three species changed from N5 (secure) to N3 (M. lucifugus, P. subflavus) and N1N3 (M. septentrionalis). Most jurisdictions within the range of WNS rank the three species as Secure (S5) or Apparently Secure (S4) but status is changing; of the 15 jurisdictions within the range of WNS that responded to a request for an update on their ranking process, 13 jurisdictions are reviewing the status due to WNS (Table 14). Several states recently have listed one or all three species as endangered (e.g., Massachusetts, Vermont) or threatened (Wisconsin), or are in the process of a review that may result in listing under some higher category of risk (e.g., Maine, Maryland, Ohio). NatureServe ranks for jurisdictions beyond WNS range are presented in Table 15.

Perimyotis subflavus is found in four jurisdictions, and each of their ranks indicated some concern (e.g., S2?, S3? status) existed for the species before WNS. In 2012-2013, NS, NB, and Quebec uplisted the species to S1?, S1, and S1 respectively, due to WNS (Table 14).

A national strategy for coordinating the management of and response to WNS in Canada is under development (Inter-agency WNS Committee 2012). The strategy parallels the American plan and includes goals for communication to the public and decision-makers about WNS, standardized monitoring, diagnostics, database management, and conservation practices.

Habitat Protection and Ownership

Protection levels vary across Canada. Bats are listed as wildlife under provincial wildlife acts, (except for PEI; R. Curley, pers. comm.), and cannot be hunted or harmed without permit. Some jurisidictions allow the removal of colonies on private property. Known hibernacula may have special protection related to development and resource extraction (i.e., in Manitoba, a 200 m radius buffer from forest harvest is required; Manitoba 2010; in NF, development is restricted within 200 m of the main large hibernaculum; S. Moores, pers. comm.). A policy requiring surveys to determine presence of bats in mines scheduled for closure does not exist in most jurisdictions. Jurisdictions have begun to respond to WNS by restricting access and/or recommending that the public stay out of hibernacula and avoid using the same clothes and equipment if travelling to multiple sites. For example, in NS, all mines on public land are off-limits due to safety concerns, as are several natural caves, one of which (Hayes Cave) is the main provincial hibernaculum. Four sites are gated (M. Elderkin, pers. comm.). In NB, one site has restricted access because it is in a protected natural area (M. Sabine, pers. comm.). The main hibernaculum in Manitoba (St. George Cave) is a protected ecological reserve (Dubois and Monson 2007). Some jurisdictions outside WNS range have restricted access as a precaution; hibernating bats in Cadomin Cave, Alberta, for example, have been protected from disturbance with the Alberta Wildlife Act since 1984 but the site remained heavily visited and was closed year-round to the public in May 2010 (Olson et al. 2011). The efficacy of restrictions in limiting the spread of WNS is unknown. Many known hibernacula in southern parts of the Canadian range are on private land where restrictions may not apply. The hibernaculum in NT is on Aboriginal property.

Ownership of habitat is not as significant an issue because these wide-ranging species are found in a variety of urban, rural and forest landscapes, and overwintering in hundreds of hibernacula. Southern hibernacula could be at risk on private lands if restrictions did not apply and landowners impacted the site. The species are found in most national and provincial protected areas within their range. Hibernacula are located on private, public, and Aboriginal property. Protection of the species resides with multiple landowners.

Acknowledgements and Authorities Contacted

This report (and the preceding document used in the emergency assessment) was written with input from numerous researchers and managers involved with bats and White-nose Syndrome in North America, and was in part facilitated by discussions held during the North American Bat Research Conference in Toronto (October 2011).

• Anions, Marilyn. Director, Natureserve Canada. Ottawa, Ontario.
• Barclay, Robert. Biological Sciences, University of Calgary, Calgary, Alberta.
• Barker, Ian. Ontario Veterinary College, University of Guelph, Guelph, Ontario.
• Bowman, Jeff. Research Scientist, Ontario Ministry Natural Resources, Peterborough, Ontario.
• Brauning, Daniel. Wildlife Diversity, Game Commission. Harrisburg, Pennsylvania.
• Brigham, Mark. Department of Biology, University of Regina. Regina, Saskatchewan.
• Britzke, Eric. US Army Engineer Research and Development Center, Vicksburg, Mississippi.
• Broders, Hugh. Department of Biology. St. Marys University, Halifax, Nova Scotia.
• Brunkhurst, Emily. New Hampshire Fish and Game Department, Concord, New Hampshire.
• Butchkoski, Calvin. Pennsylvania Game Commission, Harrisburg, Pennsylvania.
• Butler, Dororthy. Heritage Coordinator, Department of Conservation. Jefferson City, Missouri.
• Carrière, Suzanne. Biologist (Biodiversity), Department of Environment and Natural Resources, Yellowknife, Northwest Territories.
• Coleman, Jeremy. National White-nose Syndrome Coordinator. US Fish and Wildlife Service, Hadley, Massachusetts.
• Curley, Rosemary. Program Manager, Protected Areas and Biodiversity Conservation
• Forests, Dept. of the Environment, Energy and Forestry, Charlottetown, Prince Edward Island.
• Darling, Scott. Wildlife Management Program Director. Rutland, Vermont.
• Davis, Peter. Northeast Region Wildlife Biologist, Ontario Ministry of Natural Resources.
• Delorme, M. Ministère du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec. Québec, Québec.
• DePue, John. Furbearer/Small Mammal Biologist. Department of Inland Fisheries and Wildlife. Bangor, Maine.
• Desrosiers, Nathalie. Ministère du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec. Québec, Québec.
• Elderkin, Mark. Species at Risk Biologist. Department of Natural Resources, Kentville, Nova Scotia.
• Elliot, Anthony. Wildlife Ecologist, Department of Conservation, Kirksville, Missouri.
• Feller, Dan. Western Region Ecologist. Department of Natural Resources, Frostburg, Maryland.
• Fenton, Brock. Department of Biology, University of Western Ontario, London, Ontario.
• Fraser, Erin. Department of Biology, University of Western Ontario, London, Ontario.
• Gauthier, Isabelle. Ministère du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec. Québec, Québec.
• Gifford, Krishna. Endangered Species Program. US Fish and Wildlife Service, Hadley, Massachusetts.
• Goquen, Nicole. Secrétaire-trésorière. Comité conjoint de chasse, de pêche et de piégeage. Montréal, Québec.
• Gregg, David. Rhode Island Natural History Survey. Kingston, Rhode Island.
• Haggery, Sarah. Information Manager, Division of Fisheries and Wildlife. Westborough, Massachusetts.
• Hale, Lesley. Ministry of Natural Resources, Peterborough, Ontario.
• Hallam Sr., Tom. Department of Biology, University of Tennessee, Knoxille, Tennessee.
• Hellmich, Ron. Natural Heritage Data Center. Indiana.
• Herzog, Carl. Wildlife Biologist. Department of Environmental Conservation. Albany, New York.
• Hicks, Alan. 2011. Reseacher on white-nose syndrome. Retired biologist, New York State Department, Vesper Environmental.
• Hobson, Dave. Wildlife Biologist, Fish and Wildlife Division, Edson, Alberta.
• Johnson, Catherine. USDA Forest Service. Elkins, West Virginia.
• Jung, Thomas. Senior Wildlife Biologist, Environment Yukon, Whitehorse, Yukon Territory.
• Kent, Don. Department of Resources and Economic Development, Concord, New Hampshire
• Kieninger, Tara. Database Program Manager, Department of Natural Resources. Springfield, Illinois.
• Klymko, John. Atlantic Canadian Conservation Data Centre. Sackville, New Brunswick.
• Lausen, Cori. Wildlife Conservation Society Canada, Kaslo, BC.
• Leighton, Ted. Canadian Cooperative Wildlife Health Centre, Atlantic Veterinary College, University of Saskatchewan, Regina, Saskatchewan.
• Lupien, Gilles. Ministère du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec. Québec.
• Mainguy, Julien. Ministère du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec. Québec, Québec.
• Massé, Ariane. Ministère du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec. Québec, Québec.
• McBurney, Scott. Canadian Cooperative Wildlife Health Centre, Atlantic Region. Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island.
• Maher, Tom. Senior Environmental Assessment Administrator. Ministry of Environment. Regina, Saskatchewan.
• Moores, Shelley. Endangered Species and Biodiversity, Wildlife Division. Corner Brook, Newfoundland and Labrador.
• McAlpine, Don. Zoologist. New Brunswick Museum. Saint John, New Brunswick.
• Niederriter, Holly. Division of Fish and Wildlife, Dover, Delaware.
• Oldham, Mike. Ontario Ministry of Natural Resources. Peterborough, Ontario.
• Reeder, DeeAnn. Department of Biology, Bucknell University, Lewisburg, Pennsylvania.
• Reynolds, Rick. Department of Game and Inland Fisheries, Virginia.
• Rodrigues, Bruce. Wildlife Division. Government of Newfoundland and Labrador.
• Rogers, Rebecca. Michigan Natural Features Program. Michigan.
• Sabine, Mary. Species at Risk Biologist. Department of Natural Resources. Fredericton, New Brunswick
• Schneider, Gregg. Biodiversity Database Program. Department of Natural Resources. Columbus, Ohio.
• Simard, Anouk. Ministère du Développement durable, de l’Environnement, de la Faune et des Parcs du Québec. Québec, Québec.
• Stihler, Craig. West Virginia Department of Natural Resources, West Virginia.
• Stipec, Katrina. BC Conservation Data Centre. Ministry of the Environment, Victoria British Columbia.
• Tinsley, Karl. United States Fish and Wildlife Service. Fort Snelling, Minnesota.
• Turner, Greg. Endangered Mammal Specialist, Pennsylvania Game Commission, Pennsylvania.
• Vanderwolf, Karen. New Brunswick Museum. Saint John, New Brunswick.
• Watkins, Bill. Wildlife Branch, Manitoba Conservation and Water Stewardship. Winnipeg, Manitoba.
• Withers, David. Tennessee Natural Heritage Program. Nashville, Tennessee.
• Welch, Michael. Division of Natural Resources. Elkin, West Virginia.
• Willis, Craig. University of Winnipeg, Winnipeg, Manitoba.
• Wilson, Joanna. Wildlife Biologist (Species at Risk). Department of Environment and Natural Resources, Yellowknife, Northwest Territories.
• Zimmerling, Ryan. Canadian Wildlfie Service, Ottawa, Ontario.
• Zyko, Karen. Bureau of Natural Resources. Hartford, Connecticut.

Information Sources

• Alaska Department of Fish and Game. 2013. Terrerstrial Mammals - Appendix 4 [PDF, 435KB]; South coastal Bats. [accessed March 2013].
• Amelon, S. and D. Burhans. 2006. Conservation assessment: Myotis septentrionalis (Northern Long-eared Bat) in the eastern United States. Pp. 69-82 in Thompson, F. (ed.). Conservation Assessments for Five Forest Bat Species in the Eastern United States. United States Department of Agriculture General Technical Report NC-260. 83 pp.
• Anderson, J., and C. Robert. 1971. A new unipolar electrode for electrocardiography in small mammals. Journal of Mammalogy 52:469-471.
• Anthony, E., and T. H. Kunz. 1977. Feeding strategies of the little brown bat, Myotis lucifugus, in southern New Hampshire. Ecology 58:775–786.
• Arnett, E. (and 13 co-authors). 2008. Patterns of bat fatalities at wind energy facilities in North America. Journal of Wildlife Management 71:61-78.
• Arnold. B. 2007. Population structure and sex-biased dispersal in the forest-dwelling Vespertilionid bat, Myotis septentrionalis. American Midland Naturalist 157:374-384.
• Avery, M.I. 1985. Winter activity of Pipistrelle bats. Journal of Animal Ecology 54: 721-738.
• Baerwald, E. 2008. Variation in the Activity and Fatality of Migratory Bats at Wind Energy Facilities in Southern Alberta: Causes and Consequences. MSc. Thesis, University of Calgary, Calgary, Alberta.
• Baerwald, E., G. D’Amours, B. Klug, and R. Barclay. 2008. Barotrauma is a significant cause of bat fatalities at wind turbines. Current Biology 18:695-696.
• Baerwald, E., J. Edworthy, M. Holder and R. Barclay. 2009. A large-scale mitigation experiment to reduce bat fatalities at wind energy facilities Journal of Wildlife Management 73:1077-1081.
• Baker, R. 1978. The Evolutionary Ecology of Animal Migration. Holmes and Meier, New York. 1012 pp.
• Ballmann, A. 2012. Update on submissions to the North American WNS diagnostic laboratory network. Abstract. 5th Annual White-nose Syndrome Symposium, June 4-7, 2012, Madison, Wisconsin.
• Barbour, R. and W. Davis. 1969. Bats of America. University Press Kentucky, Lexington, KY. 286 pp.
• Barclay, R. 1982. Night roosting behavior of little brown bat, Myotis lucifugus. Journal of Mammalogy 63:464-474.
• Barclay, R., and M. Brigham. 1996. Bats and Forests Symposium, October 19-21, 1995, Victoria, BC. Paper 23/1996, BC Ministry of Forests, Victoria BC. 292 pp.
• Barclay, R., D. Thomas, and B. Fenton. 1979. Comparison of methods used for controlling bats in buildings. Journal of Wildlife Management 44:502-506.
• Barclay, R.M.R., (and 7 co-authors). 2004. Variation in the reproductive rate of bats. Canadian Journal Zoology 82: 688-693.
• Bat Population Data Project. 2013. USGS. https://my.usgs.gov/bpd/.
• Bennett, V., and A. Zurcher. 2012. When corridors collide: road-related disturbance to commuting bats. Journal of Wildlife Management 77:93-101.
• Blehert, D., (and 12 co-authors). 2009. Bat white-nose syndrome: An emerging fungal pathogen. Science 323:227.
• Blehert, D. (and 14 co-authors). 2012. An overview ofongoing bat white-nose syndrome research at the US Geological Survey- National Wildlife Health Center. Abstract. 5th Annual White-nose Syndrome Symposium, June 4-7, 2012, Madison Wisconsin.
• Bouma, H., H. Carey, and F. Kroese. 2010. Hibernation: The immune system at rest? Journal of Leucocyte Biology 88:1-6.
• Boyles, J., and V. Brack Jr. 2009. Modeling survival rates of hibernating mammals with individual-based models of energy expenditure. Journal of Mammalogy 90:9-16.
• Boyles, J., P. Cryan, G. McCracken, and T. Kunz. 2011. Economic importance of bats in agriculture. Science 332:41-42.
• Boyles, J., and A. McKechnie. 2010. Energy conservation in hibernating endotherms: Why ‘suboptimal’ temperatures are optimal. Ecological Modelling 221:1644-1647.
• Boyles, J., J. Storm, and V. Brack Jr. 2008. Thermal benefits of clustering during hibernation: a field test of competing hypotheses on Myotis sodalis. Functional Ecology 22:632-636.
• Brack, V. and J. Twente. 1985. The duration of the period of hibernation of vespertilionid bats. 1. Field studies. Canadian Journal of Zoology 63:2952-2954.
• Briggler, J., and J. Prather. 2003. Seasonal use and selection of caves by the eastern pipistrelle bat (Pipistrellus subflavus). American Midland Naturalist 149:406-412.
• Brigham, R.M., E.K.V. Kalka, G. Jones, S. Parsons, H.J.G.A. Limpens (eds). 2002. Bat Echolocation Research: tools, techniques and analysis. Bat Conservation International, Austin, Texas.
• Britzke, E., C. Herzog, and B. Ewing. 2011. Observations and initial results from 3 years of sampling bats along acoustic transects. Abstract. 41st North American Bat Research Meeting, Toronto, Canada. October 2011.
• Broders. H., L. Burns, and S. McCarthy. 2013. First records of the northern myotis (Myotis septentrionalis) from Labrador and summer distribution records and biology of little brown bats (Myotis lucifugus) in southern Labrador. Canadian Field-Naturalist 127:266-269.
• Broders, H., and G. Forbes. 2004. Interspecific and intersexual variation in roost-site selection of northern long-eared and little brown bats in the Greater Fundy National Park Ecosystem. Journal of Wildlife Management 68:602-610.
• Broders, H., D. McAlpine, and G. Forbes. 2001. Status of the eastern pipistrelle (Pipistrellus subflavus) in New Brunswick. Northeastern Naturalist 8:331-336.
• Broders, H., G. Quinn and G. Forbes. 2003. Species status, and the spatial and temporal patterns of activity of bats in southwest Nova Scotia, Canada. Northeastern Naturalist 10:383-398.
• Broders, H., G. Forbes, S. Woodley and I. Thompson. 2005. Range extent and stand selection for roosting and foraging in forest dwelling Myotis septentrionalis and M. lucifugus in the Greater Fundy Ecosystem, New Brunswick. Journal Wildlife Management 70(5):1174-1184.
• Brooks, R. 2009. Habitat-associated and temporal patterns of bat activity in a diverse forest landscape of southern New England, USA. Biodiversity Conservation 18:529-545 DOI 10.1007/s10531-008-9518-x.
• Brooks, R. 2011. Decline in summer bat activity in central New England 4 years following initial detection of White-nose Syndrome. Biodiversity Conservation 20:2537-2541.
• Brown, J., D. McAlpine, and R. Curley. 2007. Northern long-eared bat, Myotis septentrionalis (Chiroptera: Vespertilionidae), on Prince Edward Island: First records of occurrence and overwintering. Canadian Field-Naturalist 121:208-209.
• Brownlee-Bouboulis, S., and D. Reeder. 2013. White nose syndrome-affected little brown myotis (Myotis lucifugus) increase grooming and other activity behavior during arousal from hibernation. Journal of Wildlife Diseases 49:850-859.
• Burles, D.W., M.B. Fenton, R.M.R. Barclay, R.M. Brigham, and D. Volkers. 2014. Aspects of the winter ecology of bats on Haida Gwaii, British Columbia. Northwestern Naturalist 95(2): in press.
• Burnett, C., and T. Kunz. 1982. Growth rates and age estimation in Eptesicus fuscus and comparison with Myotis lucifugus. Journal of Mammalogy 63:33-41.
• Butchkoski, C. 2011. Project Annual Job Report; Indiana Bat Summer Roost Investigations. Pennsylvania Game Commission Bureau of Wildlife Management. Unpublished government report. 21 pp.
• Caceres, C. 1998. The summer ecology of Myotis species bats in the interior wet-belt of British Columbia. MSc. Thesis. University of Calgary, Calgary, Alberta. 107 pp.
• Caceres, C., and R. Barclay. 2000. Myotis septentrionalis. Mammalian Species. 634:1-3. American Society Mammalogists.
• Cagle, F.R. and L. Cockrum. 1943. Notes on a summer colony of Myotis lucifugus. Journal of Mammalogy 24: 474-492.
• Caire, W., R. K. LaVal, M. L. LaVal, and R. Clawson. 1979. Notes on the ecology of Myotis keenii (Chiroptera, Vespertilionidae) in eastern Missouri. American Midland Naturalist 102(2):404-7.
• Canadian Cooperative Wildlife Health Centre. 2013. Inter-Agency Bat White-nose Syndrome Survey Update. [accessed April 2013].
• Canadian Wind Energy Association. 2012. Wind Energy web page. [accessed July 15, 2012].
• Carstens, B., and T. Dewey. 2010. Species delimitation using a combined coalescent and information-theoretic approach: An example form North American Myotis bats. Systematic Biology 59:400-414.
• Chaturvedi, V., (and 7 co-authors). 2012. Identifying the natural habitat of Geomyces destructans, the etiological agent of bat geomycosis. Abstract. 5th Annual White-nose Syndrome Symposium, June 4-7, 2012, Madison Wisconsin.
• Clark, D., and T. Lamont. 1976. Organochlorine residues and reproduction in the big brown bat. Journal of Wildlife Management 40:249-254.
• Cleveland, C., (and 12 co-authors). 2006. Economic value of the pest control service provided by Brazilian free-tailed bats in southcentral Texas. Frontiers in Ecology and the Environment 4:238-243.
• Coleman, J., and R. Barclay. 2011. Influence of urbanization on demography of little brown bats (Myotis lucifugus) in the prairies of North America. PLoS ONE 6(5): e20483.doi:10.1371/journal.pone.0020483.
• Crampton, L., and R. Barclay. 1996. Habitat selection by bats in fragmented and unfragmented aspen mixedwood stands of different ages. Pp. 238-259 in M. Brigham and R. Barclay (eds.). Bats and Forests Symposium, October 19-21, 1995, Victoria, BC. Paper 23/1996, BC Ministry of Forests, Victoria BC. 292 pp.
• Cryan P., C. Meteyer, J. Boyles, and D. Blehert. 2010. Wing pathology of white-nosed syndrome in bats suggests life-threatening disruption of physiology. BMC Biology 2010, 8:135.
• Czenze, Z., and H. Broders. 2011. Ectoparasite community structure of two bats (Myotis lucifugus and M. septentrionalis) from the Maritimes of Canada. Journal of Parasitology Research. Doi:10.1155/2011/341535. 9 pages.
• Dalton, V. 1987. Distribution, abundance, and status of bats hibernating in caves in Virginia. Virginia Journal of Science 38:369-379.
• Darling, S., and R. Smith. 2011. Assessment of Vermont cave bat populations and proposal to list bat species. Vermont Fish and Wildlife Department report. 15 pp.
• Daoust, P-Y., A. Wanderler, and G. Casey. 1996. Cluster of rabies cases of probable bat origin among red foxes in Prince Edward Island. Jounral of Wildlife Diseases 32:403-406.
• Davis, W. 1959. Disproportionate sex ratios in hibernating bats. Journal of Mammalogy 40:16-19.
• Davis, W. 1966. Homing performance and homing ability in bats. Ecological Monographs 36:201-237.
• Davis, W. 1970. Hibernation: ecology and physiological ecology. Pp. 265-300 in W. Wimsatt (ed.). Biology of Bats, Volume 1. Academic Press, New York, NY.
• Davis, W., and H. Hitchcock. 1965. Biology and migration of the bat, Myotis lucifugus, in New England. Journal of Mammalogy 46:296-313.
• Davis, W., and R. Mumford. 1962. Ecological notes on the bat Pipistrellus subflavus. American Midland Naturalist 68:394-398.
• DeBlase, A., S. Humphrey, and K. Drury. 1965. Cave flooding and mortality in bats in Wind cave, Kentucky. Journal of Mammalogy 46:96.
• Dewey, T. A. 2006. Systematics and phylogeography of North American Myotis (Chiroptera: Vespertilionidae). PhD. Dissertation, University of Michigan, Ann Arbor.
• Dixon, M. 2011. Population genetic structure and natal philopatry in the widespread North American bat Myotis lucifugus. Journal of Mammalogy 92:1343-1351.
• Dobony, C., A. Hicks, K. Langwig, R. von Linden, J. Okoniewski, and R. Rainbolt. 2011. Little Brown Myotis persist despite exposure to white-nose syndrome. Journal of Fish and Wildlife Management. 2:190-195.
• Dobony, C., (and 6 co-authors). 2012. White-nose syndrome: Lessons learned at Ft. Drum Military Installation. Abstract. 5th Annual White-nose Syndrome Symposium, June 4-7, 2012, Madison Wisconsin.
• Dubois, J., and K. Monson. 2007. Recent distribution records of the little brown bat, Myotis lucifugus, in Manitoba and northwestern Ontario. Canadian Field-Naturalist 121:57-61.
• Dunbar M., and R.M. Brigham. 2010. Thermoregulatory variation among populations of bats along a latitudinal gradient. Journal of Comparative Physiology B 180:885-893.
• Dzal, Y., L. McGuire, N. Veselka, and B. Fenton. 2011. Going, going, gone: the impact of white-nose syndrome on the summer activity of the little brown bat (Myotis lucifugus). Biology Letters 7:392-394.
• Ellison, T., T. O’Shea, M. Bogan, A. Everette, and D. Schneider. 2003. Existing data on colonies of bats in the United States: Summary and analysis of the U.S. Geological Survey’s bat population database. Pp. 127-239 in T. O’Shea, and M. Brogan (eds.). Monitoring Trends in Bat Populations of the United States and Territories: Problems and Prospects. United States Geological Service Information and Technology Report. USGS/BRD/ITR-2003-0003. 274 pp.
• Environment Canada, Canadian Wind Energy Association, Bird Studies Canada and Ontario Ministry of Natural Resources. 2011. Wind energy bird and bat monitoring database: Summary of the findings from post-construction monitoring reports. 17 pp. Bird Studies Canada. [accessed July 14, 2012].
• Fabianek, F., D. Gagnon, and M. Delorme. 2011. Bat distribution and activity in Montreal Island green spaces: Responses to multi-scale habitat effects in a densely urbanized area. Ecoscience 18:9-17.
• Farrow, L., and H. Broders. 2011. Loss of forest cover impacts the distribution of the forest-dwelling tri-colored bat (Perimyotis subflavus). Mammalian Biology 76:172-179.
• Federal Register. 2013. Endangered and Threatened Wildlife and Plants; 90-Day Finding on a Petition To List the Eastern Small-Footed Bat and the Northern Long-Eared Bat as Threatened or Endangered. Vol. 78, No. 191 Part III.
• Fenton, M. B. 1969. Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Québec. Canadian Journal of Zoology 47:597-602.
• Fenton, M. B. 1970a. Population studies of Myotis lucifugus (Chiroptera: Vespertilionidae) in Ontario. Royal Ontario Museum Life Sciences Contribution 77:1-34.
• Fenton, M. B. 1970b. A technique for monitoring bat activity with results obtained from different communities in southern Ontario. Canadian Journal of Zoology 48:817-820.
• Fenton, M. B. 1997. Science and the conservation of bats. Journal of Mammalogy 78:1-14.
• Fenton, M. B. 2012. Bats and white-nose syndrome. Proceedings National Academy of Sciences 109:6794-6795.
• Fenton, M. B. and R. Barclay. 1980. Myotis lucifugus. Mammalian Species No. 42 pp. 1-8. American Society Mammalogists.
• Fenton. M. B., and G. Bell. 1991. Recognition of bats by their echolocation calls. Journal of Mammalogy 62:233-243.
• Fenton, M. B., C. G. van Zylle de Jong, G. Bell, D. Campbell, and M. Laplante. 1980. Distribution, parturition dates, and feeding of bats in south-central British Columbia. Canadian Field-Naturalist 94:416-420.
• Firman M.C., C. Godwin, and R.M.R. Barclay. 1995. Bat fauna of the west Shuswap and south Thompson River region, BC. Report prepared for Wildlife Branch, Ministry of Environment, Lands and Parks, Victoria, BC.
• Foley, K., D. Clifford, K. Castle, P. Cryan, and R. Ostfeld. 2011. Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats. Conservation Biology 25:223-231.
• Ford, W., E. Britzke, C. Dobony, J. Rodrigue, and J. Johnson. 2011. Patterns of acoustical activity of bats prior to and following white-nose syndrome occurrence. Journal of Fish and Wildlife Management 2:125-134.
• Foster, R., and A. Kurta. 1999. Roosting ecology of the northern bat (Myotis septentrionalis) and comparisons with endangered Indiana bat (Myotis sodalis). Journal of Mammalogy 80:659-672.
• Francl, K., M. Ford, D. Sparks, and V. Brack Jr. 2012. Capture and reproductive trends in summer bat communities in West Virginia: Assessing the impact of White-nose Syndrome. Journal of Fish and Wildlife Management 3:33-42.
• Fraser, E., L. McGuire, J. Eger, F. Longstaffe, and B. Fenton. 2012. Evidence of latitudinal migration in tri-colored bats, Perimyotis subflavus. PLoS ONE 7:e31419.doi:10.1371/journal.pone.0031419.
• Frick, W., (and 7 co-authors). 2010a. An emerging disease causes regional population collapse of a common North American bat species. Science 329:679-682.
• Frick, W., Reynolds, and T. Kunz. 2010b. Influence of climate and reproductive timing on demography of little brown bat, Myotis lucifugus. Journal of Animal Ecology 79:128-136.
• Fujita, M., and T. Kunz. 1984. Pipistrellus subflavus. Mammalian Species 228:1-6.
• Fundy Engineering. 2012. City of Summerside Wind Farm Project: Year 1 Post-development Avian and Bat Monitoring Report. 98 pp.
• Furlonger, C., H. Dewar, and M. B. Fenton. 1987. Habitat use by foraging insectivorous bats. Canadian Journal of Zoology 65:284-288.
• Gaisler, H., V. Hanak, and I. Horacek. 1981. Remarks on the current status of bat populations in Czechoslovakia. Myotis 18/19:68-75.
• Gargas, A., M. Trest, M. Christensen, T. Volk, and D. Blelhert. 2009. Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108:147-154.
• Garroway, C., and H. Broders. 2008. Day roost characteristics of northern long-eared bats (Myotis septentrionalis) in relation to female reproductive status. Ecoscience 15:89-93.
• Geluso, K., J. S. Altenbach, and D. Wilson. 1976. Bat mortality: pesticide poisoning and migratory stress. Science194:184–186.
• Geluso, K., T. Mollhagen, J. Tigner, and M. Brogan. 2004. Westward expansion of the eastern pipistrelle (Pipistrellis subflavus) in the United States, including new records from New Mexico, South Dakota, and Texas. Western North American Naturalist. 65:405-409.
• Gillman, K., (and 9 co-authors). 2011. Myotis lucifugus at maternity colonies in Massachusetts: Assessing impacts of White-nose Syndrome. Abstract. 41st North American Bat Research Meeting, Toronto, Canada, October 2011.
• Girard, K., H. Hitchcock, G. Edsall, and R. MacCready. 1965. Rabies in bats in southern New England. New England Journal of Medicine 272:75-80.
• Golder 2008. SaskPower International Centennial Wind Power Facility: Bird-Bat Monitoring Program Final Report. Submitted to SaskPower International. Golder Associates. 293 pp.
• Golder 2011. Red Lily Wind Farm: Post-construction Monitoring Program 2011. Submitted to SaskPower International. Golder Associates. 35 pp.
• Grieneisen, L. 2011. Hibernacula Microclimate and White-nose Syndrome Susceptibility in the Little Brown Myotis (Myotis lucifugus). MSc Thesis, Bucknell University, Lewisburg ,PA.
• Griffin, D. R. 1934. Marking bats. Journal of Mammalogy 15:202-207.
• Griffin, D. R. 1940. Migrations of New England bats. Bulletin Museum of Comparative Zoology 86:217-246.
• Griffin, D. R. 1945. Travels of banded cave bats. Journal of Mammalogy 26:15-23.
• Grindal, S., and M. Brigham. 1999. Impacts of forest harvesting on habitat use by foraging insectivorous bats at different spatial scales. Ecoscience 6:25-34.
• Grindal, S.D., C.I. Stefan, and C. Godwin-Sheppard. 2011. Diversity, distribution, and relative abundance of bats in the oil sands regions of Northeastern Alberta. Northwestern Naturalist, 92(3):211-220.
• Hall, J., R. Cloutier, and D. Griffin. 1957. Longevity records and notes on toothwear in bats. Journal of Mammalogy 38:407-409.
• Hallam, T., and P. Federico. 2011. The panzootic white-nose syndrome: An environmentally constrained disease? Transboundary and Emerging Diseases. 1-10. doi:10.1111/j.1865-1682.2011.01268x.
• Harrison, J. 1965. Temperature effects on responses in the auditory system of the little brown bat, Myotis lucifugus. Physiological Zoology 38:34-48.
• Hayes, J., and S. Loebb. 2007. The influences of forest management on bats in North America. Pp. 207-236 in M. Lacki, J. Hayes, and A. Kurta (eds.). Bats in Forests: Conservation and Management. Johns Hopkins Univeristy Press, Baltimore. 329 pp.
• Hemmera. 2011. Raptor and migratory bird and bat monitoring and follow-up report 2010 and recommendations for 2011. Prepared by Hemmera Consulting, Vancouver, BC for Bear Mountain Wind Limited Partnership, AltaGas, Calgary.
• Henderson, L., and H. Broders. 2008. Movements and resource selection of the northern long-eared Myotis (Myotis septentrionalis) in a forest-agriculture landscape. Journal of Mammalogy 89:952-963.
• Henderson, L., L. Farrow, and H. Broders. 2008. Intra-specific effects of forest loss on the distribution of the forest-dependant northern long-eared bat (Myotis septentrionalis). Biological Conservation 141:1819-1828.
• Henderson, L., L. Farrow, and H. Broders. 2009. Summer distribution of the bats of Prince Edward Island, Canada. Northeastern Naturalist 16:131-140.
• Henry, M., D. Thomas, R. Vaudry, and M. Carrier. 2002. Foraging distances and home range of pregnant and lactating little brown bats (Myotis lucifugus). Journal of Mammalogy 83:767-774.
• Henshaw, R.E. and G.E. Folk. 1966. Relation of thermoregulation to seasonally changing microclimate in two species of bats (Myotis lucifugus and M. sodalis). Physiological Zoology 39:223-236.
• Herzog, C., and R. Reynolds. 2012. Epicenter regional update. Abstract. 5th Annual White-nose Syndrome Symposium, June 4-7, 2012, Madison Wisconsin.
• Hicks, A. (and 12 co-authors). 2012. Banding begins to determine if WNS survivors occur in the Northeast.Abstract. 5th Annual White-nose Syndrome Symposium, June 4-7, 2012, Madison Wisconsin.
• Hickey, M., M. B. Fenton, K. MacDonald, and C. Soulliere 2001. Trace elements in the fur of bats (Chiroptera: Vespertilionidae) from Ontario and Québec, Canada. Bulletin of Environmental Contamination and Toxicology 66:699-706.
• Hitchcock, H. 1940. Keeping tracks of bats. Canadian Field-Naturalist 59:55-56.
• Hitchcock, H. 1949. Hibernation of bats in southeastern Ontario and adjacent Québec. Canadian Field-Naturalist 63:47-59.
• Hitchcock, H. 1965. Twenty-three years of bat banding in Ontario and Québec. Canadian Field-Naturalist 79:4-14.
• Hock, R. J., 1951. The metabolic rates and body temperatures of bats. Biological Bulletin 101:289-299.
• Hogberg, L., K. Patriquin, and R. Barclay. 2002. Use by bats of patches of residual trees in logged areas of the boreal forest. American Midland Naturalist 148:282-288.
• Holloway, G., and R. Barclay. 2000. Importance of prairie riparian zones to bats in southeastern Alberta. Ecoscience 7:115-122.
• Holroyd, S.L., R.M.R. Barclay, L.M. Merk and R.M. Brigham. 1993. A survey of the bat fauna of the dry interior of British Columbia: A summary by species with recommendations for future work. Report prepared for Ministry of the Environment, Wildlife Branch, Victoria, British Columbia.
• Hoofer, S. R., R. Van Den Bussche, and I. Horacek. 2006. Generic status of the American pipistrelles (Vespertilionidae) with description of a new genus. Journal of Mammalogy 87(5):981-992.
• Horacek, I., J. Zukal, T. Bartonika, and N. Martinkova. 2012. Ecology of geomycosis in central Europe. Abstract. 5th Annual White-nose Syndrome Symposium, June 4-7, 2012, Madison Wisconsin.
• Howes Caverns. 2013. Howes Caverns tour company.
• Humphrey, S., and J. Cope. 1976. Population ecology of the little brown bat, Myotis lucifugus, in Indiana and north-central Kentucky. American Society Mammalogists Special Publication 4:1-81.
• Humphries, M., J. Speakman, and D. Thomas. 2006. Temperature, hibernation energetic, and the cave and continental distributions of little brown Myotis. Pp. 23-37 in Functional and Evolutionary Ecology of Bats. A. Zubaid, G. McCracken, and T. Kunz (eds.). Oxford University Press. 342 pp.
• Huynh, H. 2010. Taxonomic studies on the tri-colored bat, Perimyotis subflavus, in southwestern Nova Scotia, Canada. MSc Thesis. Acadia University, Nova Scotia. 82 pp.
• Hutson, A., and S. Mickleburgh. 1988. Bats underground: a conservation code. Flora and Fauna Preservation Society. London, U.K. 30 pp.
• Inter-agency White-nose Syndrome Committee. 2012. A National Plan to Manage White-nose Syndrome in Bats. February 12, 2012 Draft Report for Canadian Wildlife Directors Committee. 15 pp.
• IUCN 2011. Guidelines for Using the IUCN Red List Categories and Criteria [PDF, 3,42 MB]. (Version 9.0 September 2011). Prepared by the Standards and Petitions Subcommittee.
• Jameson, J., and C. Willis. 2012. Bat mortality at a wind power facility in central Canada. Northwestern Naturalist 93:194-202.
• Johnson, C. and C. Sanders. 2012. Using long-term mist netting to assess the impact of WNS on summer bat populations. Poster presentation. 5th Annual WNS Symposium [PDF, 687 KB]. Madison, Wisconsin. [accessed August 2012].
• Johnson, G. 2005. A review of bat mortality at wind-energy developments in the United States. Bat Research News 46:45-49.
• Johnson, S., V. Brack Jr, and R. Rolley. 1998. Overwinter weight loss of Indiana bats (Myotis sodalis) from hibernacula subject to human visitation. American Midland Naturalist 139: 255-261.
• Jonasson, K.A., and C.K.R. Willis. 2011. Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome. PLoS One. 6: 1-8. doi:10.1371/journal.pone.0021061.
• Jonasson K.A., and C.K.R. Willis. 2012. Hibernation energetics of little brown bats. Journal of Experimental Biology 215:2141-2149.
• Jones K., D. Armstrong, R. Hoffmann and C. Jones. 1983. Mammals of the Northern Great Plains. University of Nebraska Press, Lincoln, Nebraska. 379 pp.
• Jung, T.S. 2013. Estimating little brown bat (Myotis lucifugus) colony size in southern Yukon: a mark-recapture approach. Yukon Fish and Wildlife Branch Technical Report TR-13-13: 17 pp.
• Jung, T., I. Thompson, R. Titman, and A. Applejohn. 1999. Habitat selection by forest bats in relation to mixed-wood stand types and structure in central Ontario. Journal of Wildlife Management 63:1306-1319.
• Jung, T., B. Slough, D. Nagorsen, T. Dewey, and T. Powell. 2006. First records of the northern long-eared bat, Myotis septentrionalis, in the Yukon. Canadian Field-Naturalist 120:39-42.
• Jung, T., I. Thompson, and R. Titman. 2004. Roost site selection by forest-dwelling male Myotis in central Ontario, Canada. Forest Ecology and Management 202:325-335.
• Jutras, J., M. Delorme, J. McDuff, and C. Vasseur. 2011. Le suivi des chauves-souris du Québec. Le Naturalsite Canadien 136:48-52.
• Kalcounis, M., K. Hobson, M. Brigham, and K. Hecker. 1999. Bat activity in the boreal forest: Importance of stand type and vertical strata. Journal of Mammalogy 80:673-682.
• Kalka, M., A. Smith, and E. Kalko. 2008. Bats limit arthropods and herbivory in a tropical forest. Science 320:71.
• Kiesecker, J. (and 8 co-authors). 2011. Win-win for wind and wildlife: A vision to facilitate sustainable development. PLoS ONE 6(4): e17566.doi:10.1371/journal.pone.0017566.
• Keen, R., and H. Hitchcock. 1980. Survival and longevity of the little brown bat (Myotis lucifugus) in southeastern Ontario. Journal of Mammalogy 61:1-7.
• Kilpatrick, M. 2013. Transmission of Geomyces destructans between bats and the environment. International Bat Research Conference, San Jose, Costa Rica, 11 – 15 Aug.
• Krusic, R., M. Yamasaki, C. Neefus, and P. Pekins. 1996. Bat habitat use in White Mountain National Forest. Journal of Wildlife Management 60:625-631.
• Kunz, T. H. 1973. Resource utilization: temporal and spatial components of bat activity in central Iowa. Journal of Mammalogy 54:14-32.
• Kunz, T. H., E. L. P. Anthony, and W. T. Rumage. 1977. Mortality of little brown bats following multiple pesticide applications. Journal of Wildlife Management 41: 476-483.
• Kunz, T., (and 8 co-authors). 2007. Assessing impacts of wind-energy development on nocturnally-active birds and bats: a guidance document. Journal of Wildlife Management 71:2449-2486.
• Kunz, T.H., and J.D. Reichard. 2010. Status review of the little brown Myotis (Myotis lucifugus) and determination that immediate listing under the endangered species act is scientifically and legally warranted [PDF, 451 KB].
• Kunz, T., and M. Tuttle. 2009. White-nose syndrome science strategy meeting II.
• Kurta, A., G. Bell, K. Nagy, and T. Kunz. 1989. Energetics of lactation and pregnancy in free ranging little brown bats (Myotis lucifugus). Physiological Zoology 62:804-818.
• Kurta, A., and J. Teramino. 1994. A novel hibernaculum and noteworthy records of the Indiana bat and eastern pipistrelle (Chiroptera: Vespertilionidae). American Midland Naturalist 132:410-413.
• Langwig, K., W. Frick, J. Bried, A. Hicks, T. Kunz, and A. Kilpatrick. 2012. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecology Letters doi:10.1111/j.1461-0248.2012.1829.x
• Lancaster, P., J. Bowman, and B. Pond. 2008. Fishers, farms and forests in eastern North America. Environmental Management 42:93-101.
• Lausen, C. L. 2009. Status of Northern Myotis (Myotis septentrionalis) in Alberta: 2009 Update. Alberta Wildlife Status Report No. 3, Government of Alberta. 34 pp.
• Lausen, C. L. 2011. Late summer survey of bat hibernacula and bat diversity in South Slave Region, Northwest Territories and Wood Buffalo National Park, Alberta. Unpublished report submitted to Parks Canada and NT Government. 34 pp.
• Lausen, C. L., and R. Barclay. 2006. Winter bat activity in the Canadian prairies. Canadian Jounral of Zoology 84:1079-1086.
• Lausen, C.L., I. Delisle, R.M.R. Barclay, and C. Strobek. 2008. Beyond mtDNA: nuclear gene flow suggest taxonomic oversplitting in the little brown bat (Myotis lucifugus). Canadian Journal of Zoology 86:700-713.
• Lausen, C., and T. Hill. 2010. A summary of bat work in 2009 in the Columbia Basin as part of the provincial taxonomic study of long-eared bats in B.C. Fish and Wildlife Compensation Program - Columbia Basin, Nelson, B.C.
• Lausen, C., T.S. Jung, and J. Talerico. 2008. Range extension of the northern long-eared bat (Myotis septentrionalis) in the Yukon. Northwestern Naturalist 89:115-117.
• Lindner, D.L., (and 6 co-authors). 2011. DNA-based detection of the fungal pathogen Geomyces destructans in soils from bat hibernacula. Mycologia 103(2): 241-246.
• Lorch, J., A. (and 7 co-authors). 2010. Rapid polymerase chain reaction diagnosis of white-nose syndrome in bats. Journal of Veterinary Diagnostic Investigations 22:224-230.
• Lorch, J., (and 10 co-authors). 2011. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature. October 26, 2011 (online version).
• Lorch, J., L. Muller, R. Russell, M. O’Connor, D. Lidner, and D. Blehert. 2013. Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula in the eastern United States. Applied Environmental Microbiology 79(4):1293. Doi 10.1128/AEM.02939-12.
• Lukens, M., and W. Davis. 1964. Bats: sensitivity to DDT. Science 146:948.
• Luszcz, T., (and 7 co-authors). 2003. Comparisons of morphology, echolocation call structure, and genetics of Myotis lucifugus and Myotis yumanensis. Bat Research News 44: 156.
• MacDonald, K., E. Matsui, R. Stevens, and M. B. Fenton. 1994. Echolocation calls and field identification of the eastern pipistrelle (Pipistrellus subflavus: Chiroptera: Vespertilionidae), using ultrasonic bat detectors. Journal of Mammalogy 75:462-465.
• Maher, S., et al. 2012. Spread of white-nose syndrome on a network regulated by geography and climate. Nature Communications 3:1306/DOI:10.1038/ncomms2301.
• Mainguy, J., N. Desrosiers, and F. Lelièvre. 2011. Cave-dwelling bats in the province of Québec: historical data about hibernacula population surveys. Unpublished report. Ministère des Ressources naturelles et de la Faune. 7pp.
• Manitoba 2010. Forest Management Guidelines for Terrestrial Buffers [PDF, 348 KB]. Manitoba Conservation, Winnipeg, MB. 20 pp. [accessed December 2012].
• Mann, S., R. Steidl, and V. Dalton. 2002. Effects of cave tours on breeding Myotis velifer. Journal of Wildlife Manangement 66:618-624.
• Martinez, F., A. Menzies, and Z. Czenze. 2012. Bat Hibernacula Survey Report 2012 for the Northwestern Ontario Area. Unpublished report submitted to Ontario Ministry of Natural Resources. 7 pp.
• McAlpine, D., K. Vanderwolf, G. Forbes and D. Malloch. 2011. Consumption of bats (Myotis spp.) by raccoons (Procyon lotor) during an outbreak of white-nose syndrome in New Brunswick, Canada: implications for estimates of bat mortality. Canadian Field-Naturalist 125:257-260.
• McGuiness, F., P. Carter, and L. Hale. 2011. Ontario’s science based approach to bat protection for wind power projects. Abstract. 41st Annual North American Society for Bat Research. October 26-29, 2011. Toronto, Ontario.
• McNab, B. 1974. The behavior of temperate bats in a subtropical environment. Ecology 55:943-958.
• Messenger, S., C. Rupprecht, and J. Smith. 2003. Bats, emerging virus infections, and the rabies paradigm. Pp. 622-657 in Bat Ecology. T. Kunz and B. Fenton (eds.) University of Chicago Press, Chicago, Illinois. 779 pp.
• Meteyer, C., M. Valent, J. Kashmer, E. Buckles, J. Lorch, D. Blehert, A. Lollar, D. Berndt, E. Wheeler, C. White, and A. Ballmann. 2011. Recovery of Little Brown Bat (Myotis lucifugus) from natural infection with Geomyces destructans, White-nose Syndrome. Journal of Wildlife Diseases 47:618-626.
• Minnis, A., and D. Lindner. 2013. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biology 117:638-649.
• Minnesota Department of Natural Resources. 2013. Fungus dangerous to bats detected at two Minnesota state parks. News Release; August 9, 2013. News.dnr.state.mn.us/2013/08/09/fungus
• Mohr, C.E. 1952. A survey of bat banding in North America, 1932-1951. National Speleological Society News 14: 3-13.
• Nagorsen, D. 1980. Records of hibernating big brown bats (Eptesicus fuscus) and little brown bats (Myotis lucifugus) in northwestern Ontario. Canadian Field-Naturalist 94:83-85.
• Nagorsen, D., and M. Brigham. 1993. Bats of British Columbia. Royal British Museum, Victoria, BC. 170 pp.
• National Foresty Database. 2012. [accessed July 26, 2012].
• National Wildlife Health Center. 2013. White-nose Syndrome. [accessed April 2013].
• Neilson, A., and M. B. Fenton. 1994. Responses of little brown Myotis to exclusion and to bat houses. Wildlife Society Bulletin 22:8-14.
• Nordquist. G. 2000. Winter use of subterranean cavities by bats in and near Minnesota. MSc. Thesis. University of Minnesota. St. Paul, Minnesota.
• Norquay, K., F. Martinez-Nunez, J. Dubois, K. Monson, and C. Willis. 2013. Long-distance movements of little brown bats (Myotis lucifugus). Journal of Mammalogy 94:506-515.
• O’Donnell, C. 2009. Population dynamics and survivorship in bats. Pp. 158-176 in T. Kunz and S. Parsons (eds.) Ecological and Behavioral Methods for the Study of Bats. 2nd. Edition. John Hopkins University Press. Baltimore. MD. 901 pp.
• Okoniewski, J., J. Haines, A. Hicks, K. Langwig, R. VonLinden, and C. Dobony. 2010. Detection of the conidia of Geomyces destructans in northeast hibernacula, at maternal colonies, and on gear – some findings based on microscopy and culture. Abstract from 2010 WNS Symposium, Pittsburg Pennsylvania. p. 18.
• Ontario Ministry of Natural Resources. 2011. Bats and Bat Habitat: Guidelines for Wind Power Projects. OMNR, Peterborough, Ontario. 24 pp.
• Ontario Ministry of Natural Resources. 2013. E-laws; Species at Risk. [accessed November 2013]
• O’Shea, T., L. Ellison, and T. Stanley. 2004. Survival estimation in bats: Historical overview, critical appraisal, and suggestions for new approaches. Pp. 297 - 336 in W. Thompson (ed.). Sampling Rare and Elusive Species. Island Press, Washington, D.C. 429 pp.
• Olson, C., D. Hobson, and M. Pybus. 2011. Changes in population size of bats at a hibernaculum in Alberta, Canada, in relation to cave disturbance and access restrictions. Northwestern Naturalist 92:224-230.
• Owen, S., (and 6 co-authors). 2003. Home-range size and habitat used by the northern Myotis (Myotis septentrionalis). American Midland Naturalist 150:352-359.
• Park, A., and H. Broders. 2012. Distribution and roost selection of bats on Newfoundland. Northeastern Naturalist 19:165-176.
• Patriquin, K. 2001. Ecology of a bat community in harvested boreal forest in northwestern Alberta. MSc. Thesis. University of Calgary, Calgary, Alberta. 106 pp.
• Patriquin, K., and R. Barclay. 2003. Foraging by bats in cleared, thinned and unharvested boreal forest. Journal of Applied Ecology 40:646-657.
• Perry, R., and R. Thill. 2007. Tree roosting by male and female eastern pipistrelles in a forested landscape. Journal of Mammalogy 88:974-981.
• Pierson, E. 1998. Tall trees, deep holes, and scarred landscapes: Conservation biology of North American bats. Pp. 309-325 in Kunz, T., and P. Racey (eds.), Bat Biology and Conservation. Smithsonian Institution Press, Washington, DC. 365 pp.
• Pikula, J., H. (and 7 co-authors). 2012. Histopathology confirms White-nose Syndrome in Europe. Journal Wildlife Diseases 48:207-211.
• Poissant, J., and H. Broders. 2008. Ectoparasite prevalence in Myotis lucifugus and M. septentrionalis (Chiroptera: Vespertilionidae) during fall migration at Hayes Cave, Nova Scotia. Northeastern Naturalist 15: 515-522.
• Poissant, J., H. Broders, and G. Quinn. 2010. Use of lichen as a roosting substrate by Perimyotis subflavus, the tricolored bat, in Nova Scotia. Ecoscience 14: 372-378.
• Powers, L., E. Pritchard, K. Lau, and B. Francis. 2012. Does Geomyces destructans infection reduce female fertility in Myotis lucifugus? North America Symposium on Bat Research, Puerto Rico.
• Puechmaille, S. 2013. Modelling Geomyces destructans distribution in North America and Eurasia using ecological niche modeling: What can we learn? International Bat Research Conference, San Jose, Costa Rica, 11- 15 Aug.
• Puechmaille, S.E., (and 26 co-authors). 2011. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoSONE 6: e19167. doi:10.1371/journal.pone.0019167.
• Pybus, M., D. Hobson, and D. Onderka. 1986. Mass mortality of bats due to probable  blue-green algal toxicity. Journal of Wildlife Diseases 22: 449–450.
• Raesly, R., and E. Gates. 1987. Winter habitat selection by north temperate bats. American Midland Naturalist 118:15-31.
• Randall, L., R. Barclay, M. Reid, and T. Jung. 2011. Recent infestation of forest stands by spruce beetles do not predict habitat use by little brown bats (Myotis lucifugus) in southwestern Yukon, Canada. Forest Ecology and Management 261:1950-1956.
• Randall, L., T.S. Jung, and R.M.R. Barclay. in press. Roost-sites and movements of little brown bats (Myotis lucifugus) in southwestern Yukon. Northwestern Naturalist 95: in press.
• Reeder, D.M., and G. R. Turner. 2008. Working together to combat White-nose Syndrome: A report of a meeting on 9-11 June 2008, in Albany, New York. Bat Research News 49:75-78.
• Reeder, D., (and 14 co-authors). 2012. Frequent arousal from hibernation linked to severity of infection and mortality in bats with White-Nose Syndrome. PLoS ONE 7(6): e38920. doi:10.1371/journal.pone.0038920.
• Reichard, J., and T. Kunz. 2009. White-nose syndrome inflicts lasting injuries to the wings of Little Brown Bats (Myotis lucifugus). Acta Chiropterologica 11:457-464.
• Reidinger, R. 1976. Organchlorine residues in adults of six suthwestern bat species. Journal of Wildlife Management 40:677-680.
• Reimer, J., and L. Kaupas. 2013. South Slave region bat research summary 2013. Unpub. report submitted to Environment and Natural Resources, Northwest Territories. 8 pp.
• Ren P., Haman K., Last L., Rajkumar S., Keel M., and Chaturvedi, V. 2012. Clonal spread of Geomyces destructans among bats, midwestern and southern United States [letter]. Emerging Infectious Disease Journal [serial on the Internet]. May 2012.
• Reynolds, S. 2006. Monitoring the potential impact of a wind development site on bats in the northeast. Journal of Wildlife Management 70:1219-1227.
• Richter, A., S. Humphrey, J. Cope, and V. Brack Jr. 1993. Modified cave entrances: thermal effect on body mass and resulting decline of endangered Indiana bats (Myotis sodalis). Conservation Biology 7:407-415.
• Russell, A., M. Vonhof, and E. Claire. 2012. Phylogeographic analyses reveal cryptic subdivisions and unexpected connections among Myotis lucifugus populations. North America Symposium on Bat Research, Puerto Rico.
• Roche, N. (and six co-authors). 2011. A car-based monitoring method reveals new information on bat populations and distributions in Ireland. Animal Conservation doi: 10.1111/j.1469-1795.2011.00470.x.
• Sandel, J., G. Benatar, K. Burke, C. Walker, T. Lacher, and R. Honeycutt. 2001. Use and selection of winter hibernacula by the eastern pipistrelle (Pipistrellus subflavus) in Texas. Journal of Mammalogy 82:173-178.
• Sasse, D., and P. Pekins. 1996. Summer roosting ecology of northern long-eared bats (Myotis septentrionalis) in the White Mountain National Forest. Pp. 91-101 in Bats and Forests Symposium. R. Barclay and M. Brigham (eds.). Research Branch, British Columbia Ministry of Forests Working Paper 23/1996. 291 pp.
• Sasse, D., and P. Pekins. 2000. Ectoparasites observed on northern long-eared bats, Myotis septentrionalis. Bat research News 41:69-71.
• Schowalter, D, 1980. Swarming, reproduction, and early hibernation of Myotis lucifugus and M. volans in Alberta. Journal of Mammalogy 61:347-350.
• Schowalter, D., J. Gunson, and L. Harder. 1979. Life history characteristics of little brown bats (Myotis lucifugus) in Alberta. Canadian Field-Naturalist 93:243-251.
• Scott, F., and A. Hebda. 2004. Annotated list of the mammals of Nova Scotia. Proceedings of the Nova Scotia Institute of Science 42:189-208.
• Sherwin, R., S., Altenbach, and D. Waldien. 2009. Managing abandoned mines for bats. Bat Conservation International.
• Slough, B., and T. Jung. 2007. Diversity and distribution of the terrestrial mammals of the Yukon Territory: A review. Canadian Field-Naturalist 121:119-127.
• Slough, B., and T. Jung. 2008. Observations on the natural history of bats in the Yukon. The Northern Review 29:127-150.
• Speakman, J., P. Webb, and P. Racey. 1991. Effects of disturbance on the energy expenditure of hibernating bats. The Journal of Applied Ecology 28:1087-1104.
• Stantec 2010. Wolfe Island Wind Plant Post-construction Follow-up Plan: Bird and Bat Resources Monitoring Report No. 4. July-December 2010. 104 pp.
• Stantec 2011. Wolfe Island Wind Plant Post-construction Follow-up Plan: Bird and Bat Resources Monitoring Report No. 5. January-June 2011. 166 pp.
• Studier, E., and D. Howell. 1969. Heart rate of female big brown bats in flight. Journal of Mammalogy 50:842-845.
• Talerico, J. 2008. The behaviour, diet and morphology of the little brown bat (Myotis lucifugus) near the northern extent of its range in Yukon Canada. MSc. Thesis, University of Calgary, Calgary, AB.
• Thomas, D. 1995. Hibernating bats are sensitive to non-tactile human disturbance. Journal of Mammalogy 76:940-946.
• Thomas, D., and D. Cloutier. 1992. Evaporative water loss by hibernating little brown bats, Myotis lucifugus. Physiological Zoology 65:443-456.
• Thomas, D., M. Dorais, and J-M. Bergeron. 1990. Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. Journal of Mammalogy 71:475-479.
• Thomas, D. W., M. B. Fenton, and R. Barclay. 1979. Social behaviour of the little brown bat, Myotis lucifugus. Behavioural Ecology and Sociobiology 6:129–136.
• Thomas, D., and F. Geiser 1997. Periodic arousals in hibernating mammals: Is evaporative water loss involved? Functional Ecology 11:585-591.
• Trombulak S., P. Higuera, and M. DesMeules. 2001. Population trends of wintering bats in Vermont. Northeastern Naturalist 8:51-62.
• Turner, G., D. Reeder, and J. Coleman. 2011. A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and a look to the future. Bat Research News 52:13-27.
• Tuttle, M. 2003. Estimating population size of hibernating bats in caves and mines. Pp. 31-40 in Monitoring Trends in Bat Populations of the United States and Territories: Problems and Propsects. T. O’Shea, M. Bogan (eds.). USGS/BRD/ITR- 2003. 287 pp.
• Twente, J., J. Twente, and V. Brack Jr. 1985. The duration of the period of hibernation of vespertilionid bats. 2. Laboratory studies. Canadian Journal of Zoology 63:2955-2961.
• United States Fish and Wildlife Service. 2012. White-nose syndrome decontamination protocol: Version 03.15.2012 [PDF, 342 KB]. [Accessed March 16, 2012].
• Vanderwolf, K., D. McAlpine, G. Forbes, and D. Malloch. 2012. Bat populations and cave microclimate prior to and at the outbreak of White-nose Syndrome in New Brunswick. Canadian Field-Naturalist 126:125-134.
• Vanderwolf, K., D. McAlpine, D. Malloch, and G. Forbes. 2013. Ectomycota associated with hibernating bats in eastern Canadian caves prior to the emergence of White-nose Syndrome. Northeastern Naturalist 20:115-130.
• van Zyll de Jong, C. 1979. Distribution and systematic relationships of long-eared Myotis in western Canada. Canadian Journal of Zoology 57:987-994.
• van Zyll de Jong, C. 1985. Handbook of Canadian Mammals: Bats. Canadian Museum of Nature, Ottawa, Canada. 212 pp.
• Veilleux, J., J. Whitaker, and S. Veilleux. 2003. Tree-roosting ecology of reproductive female eastern pipistrelles, Pipistrellus subflavus, in Indiana. Journal of Mammalogy 84:1068-1075.
• Veilleux, J., and S. Vielleux. 2004. Intra-annual and interannual fidelity to summer roost areas by female eastern pipistrelles, Pipistrellus subflavus. American Midland Naturalist 152:196-200.
• Verant, M., Boyles J., Waldrep W., Wibbelt G., and Blehert D. (2012) Temperature-dependent growth of Geomyces destructans, the fungus that causes bat White-Nose Syndrome. PLoS ONE 7(9): e46280. doi:10.1371/journal.pone.0046280.
• Walley, H., and W. Jarvis. 1971. Longevity record for Pipistrellus subflavus. Illinois Academy of Science. 64:305.
• Warnecke, L. J. Turner, T. Bollinger, J. Lorch, V. Misra, P. Cryan, G. Wibbelt, D. Blehert, and C. Willis. 2012. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proceedings National Academy of Sciences. doi/10.1073/pnas.1200374109.
• Warnecke, L. ( and 7 co-authors). 2013. Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biology Letters 9:20130177. doi.org/10.1098/rsbl.2013.0177.
• Watt, E., and B. Fenton 2008. DNA fingerprinting provides evidence of discriminate suckling and non-random mating of little brown bat, Myotis lucifugus. Molecular Ecology 4:261-264.
• Webb, P., J. Speakman, and P. Racey. 1996. How hot is a hibernaculum? A review of the temperature at which bats hibernate. Canadian Journal of Zoology 74:761-765.
• Weller, T.J., S.A. Scott, T.J. Rodhouse, P.C. Ormsbee, and J.M. Zinck. 2007. Field identification of the cryptic vespertilionid bats, Myotis lucifugus and M. yumanensis. Acta Chiropterologica 9(1): 133–147.
• Wells, E. 1986. 30,000 chauves-souris chassées des églises. Echo Dimanche 3(18):3.
• Whitaker, J., and L. Rissler. 1993. Winter activity of bats at a mine entrance in Vermillion County, Indiana. American Midland Naturalist 127:52-59.
• Wibbelt, G. A., (and 13 co-authors). 2010. White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerging Infectious Diseases 16:1237–1243.
• Wilder, A., W. Frick, K. Langwig, and T. Kunz. 2011. Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. Biology Letters 7:950-953.
• Williams-Guillen, K., I. Perfecto, and J. Vandermeer. 2008. Bats limit insects in a neotropical agroforestry system. Science 320:70.
• Willis, C.K. R. 2006. Daily heterothermy by temperate bats using natural roosts. Pp. 38-55 in Functional and Evolutionary Ecology of Bats. A. Zubaid, G. McCracken and T. Kunz (eds.). Oxford University Press. 342 pp.
• Willis, C., A. Menzies, J. Boyles, and M., Wojciechowski. 2011. Evaporative water loss is a plausible explanation for mortality of bats from White-Nose Syndrome. Integrative and Comparative Biology 51:364–373.
• Wilson, J. and R.M.R. Barclay. 2006. Consumption of caterpillars by bats during an outbreak of western spruce budworm. American Midland Naturalist 155:244-249.
• Wilson, D., and D. Reeder. 2005. Mammal Species of the World. 3rd edition. Johns Hoplkins University Press, Baltimore, Md.
• Wright, S., and J. Moran. 2011. Ocean-going vessels: a possible conduit for the introduction of white-nose fungus (Geomyces destructans) into bats in Alaska. Northwestern Naturalist 92:133-135.
• Zimmerman, G., and W. Glanz. 2000. Habitat use by bats in eastern Maine. Journal of Wildlife Management 64:1032-1040.

Biographical Summary of Report Writer(s)

Graham Forbes (PhD) received graduate degrees from the University of Waterloo, Waterloo, Canada and is a cross-appointed professor in the Faculty of Forestry and Environmental Management, and the Department of Biology at the University of New Brunswick, Fredericton, NB. He is Director of the NB Cooperative Fish and Wildlife Research Centre and the Sir James Dunn Wildlife Research Centre, UNB and is presently serving as Co-Chair of the Terrestrial Mammal Sub-committee of COSEWIC.

Collections Examined

No collections were examined.

Appendix 1. Threats Assessment Worksheet.

Population trend data are derived from two periods (overwintering and summer), with the majority of data from the overwintering period. Most winter data are of counts of bats in hibernacula, but not all hibernacula are monitored. Perimyotis subflavus are relatively easy to identify because of their size and colour (Tuttle 2003). The separation of Myotis species by sight is more difficult; Myotis septentrionalis and M. lucifugus can be separated based on the pointed tragus of M. septentrionalis, but only if they are near (e.g., <1 m, such as in low, flat-ceiling mines). In Quebec and many US jurisdictions, surveyors are confident they can separate the two species at certain sites because of their proximity to bats, and/or use of high-resolution photography (see below). However, there is a lack of consensus among jurisdictions on whether the two species should be combined or separated in surveys. Data on Myotis species are combined in Ontario (L. Hale, pers. comm. 2012), New Brunswick (D. McAlpine, pers. comm.) and Nova Scotia (H. Broders, pers. comm.).

The most complete summary of population change in bats in hibernacula impacted by WNS is a compilation of survey efforts by five state agencies (New York, Pennsylvania, Vermont, Virginia, West Virginia) as of winter 2010-2011, using sites with >1 year of post-WNS exposure (Turner et al. 2011; G. Turner, pers. comm.). The Turner et al. (2011) paper does not list effort (e.g., how species are separated, % of sites surveyed, number of observers, observer training), which makes it difficult to compare surveys. To address this issue, the report author contacted state biologists regarding effort and confidence associated with identifying species in their surveys. In New York, high resolution photography is used to identify Myotis to species, in part because of need to identify all endangered M. sodalis (C. Herzog, pers. comm.). Some monitoring of bats in the northeastern US has been standardized as part of the American WNS monitoring program, and it was standard practice in Vermont to minimize bias associated with effort, or not include such data (Darling and Smith 2011).

Identifying a species is more difficult as distance from the observer increases. The highest counts for M. septentrionalis in the northeastern US sites are in hibernacula with the lowest ceilings, suggesting an increased confidence that data recorded as M. septentrionalis are actually correct (C. Herzog, pers. comm.). Assuming that detection probability is constant pre- and post-WNS, and any identification bias is constant, a decline recorded in these sites likely represents an actual decline. In Tables 1, 8, only the sites with low ceilings in Vermont were included for Myotis data (S. Darling, pers. comm.).

Although there may be a concern about actual numbers of Myotis lucifugus and M. septentrionalis in US hibernacula, there is confidence that both species are present in the hibernacula; Griffin (1940a) identified 589 Myotis septentrionalis in 10 of 11, and 2,998 M. lucifugus in 11 of 11 hibernacula, while banding bats in four northeastern states (Connecticut, Massachusetts, New York, Vermont). Recent data suggest M. septentrionalis have maintained a significant presence in the northeast; 41% of 11,734 bats caught in West Virginia between 1998-2007 were M. septentrionalis (compared to 25% M. lucifugus) (Francl et al. 2012) and M. septentrionalis were regularly captured throughout the northeast in the last 10 years (Brooks 2009).

Another issue with data on declines is that declines may have resulted from inter-cave movement, rather than mortality. This issue is being studied but the winter declines are considered real because declines in summer mirror declines in winter. Also, accuracy of species identification is not an issue because most summer data comes from captures.

Finally, the issue of species identification is somewhat moot. Both Myotis species are present and the decline is so extensive that few, or no bats, remain. As of 2011, in 19 (66%) of the 29 sites where Myotis data were separated into M. lucifugus or M. septentrionalis, populations declined to <50 bats, and in six sites (21%), populations declined to zero bats (Turner et al. 2011). Additional sites have been infected and declines continue. Declines in the Maritimes have been as extensive as in the US northeast. In summary, even though exact numbers of each species are debated, the issue of species identification is at least partially addressed and much data on M. septentrionalis in Turner et al. (2011) clearly reflects observed trends. A compilation of population counts by hibernaculum is in development but to date does not include post-WNS data (BPD 2013).