BioOne.org will be down briefly for maintenance on 17 December 2024 between 18:00-22:00 Pacific Time US. We apologize for any inconvenience.
Open Access
How to translate text using browser tools
2 May 2022 Seasonal population dynamics and movement patterns of a critically endangered, cave-dwelling bat, Miniopterus orianae bassanii
Emmi van Harten, Ruth Lawrence, Lindy F. Lumsden, Terry Reardon, Andrew F. Bennett, Thomas A. A. Prowse
Author Affiliations +
Abstract

Context. Seasonal migration and movements of bats have important implications for their conservation. The southern bent-winged bat (Miniopterus orianae bassanii), a critically endangered cave-dwelling taxon in Australia, has been described as undertaking regional-scale migration between maternity and non-breeding caves.

Aims. To describe the seasonal cycle of movements by the southern bent-winged bat, including migration and congregation events of different sex- and age-classes in the population.

Methods. We tagged a total of 2966 southern bent-winged bats with passive integrated transponder (PIT) tags. Antennas were used to detect bats in flight at a major maternity cave and a key non-breeding cave in south-east South Australia, from January 2016 to August 2019. We used capture–resight histories to visualise population patterns and model the daily encounter probability for each sex- and age-class at the respective roost sites.

Key results. Bats congregated at the maternity cave for most of the year, with different seasonal patterns among sex- and age-classes. Seasonal movements were associated with behaviour over winter months: most of the population dispersed from the maternity cave from May and a staged return occurred among population classes from July through September. A previously undescribed movement occurred in adult females and juveniles each year: these classes left the maternity cave in late summer, when juveniles became independent, and returned in early mid-autumn, later undertaking winter dispersal. Complex underlying movements of individuals occurred throughout the year, with individuals able to fly 72 km between roosting caves in just a few hours.

Conclusions. Seasonal movements are a key aspect of the life history of this taxon. The newly reported movement of adult females and juveniles conforms to the maternal guidance hypothesis, whereby mothers guide their young to suitable non-breeding caves and hibernation sites. In addition to seasonal movements, some individuals moved 72 km between caves multiple times over short time periods, including on successive nights. This 72-km overnight flight distance more than doubles the previous distance used to inform management buffer zones. Extended congregation of bats at the maternity cave highlights resource limitation in the surrounding area as a potential threat to this population.

Implications. The dynamic nature of the population has implications for the management of emerging risks, including mortality at windfarms and potential rapid spread of the exotic white-nose syndrome.

Introduction

Migration biology provides a ‘grand challenge’ in organismal biology, with many aspects of the phenomena poorly understood (Bowlin et al. 2010). In addition to being challenging to study, migrating animals also provide challenges for conservation: they often have complex habitat requirements and a tendency to congregate in restricted areas (Fleming and Eby 2003). In bats, migration has been defined as the seasonal movement of populations from one location to another, typically as a two-way movement of >50 km and involving a return to the starting location, to seek conditions that are climatically or energetically more favourable (Fleming and Eby 2003). However, migratory behaviour in small insectivorous bats in Australia is known only for a few species. For example, the regional seasonal migration of the eastern bent-winged bat (Miniopterus orianae oceanensis) often has adult females travelling distances of >160 km to maternity caves (Dwyer 1966). Here, we examine the seasonal population patterns, migration and movements of the southern bent-winged bat (Miniopterus orianae bassanii), a critically endangered taxon in south-eastern Australia.

Study of migration and movement in small insectivorous bats has traditionally involved long-term deployment of forearm bands (Hutterer 2005), but recapture rates are low. Studies using stable isotopes and comparing genetic structure have helped to determine area of origin and migration direction (Petit and Mayer 2000; Voigt et al. 2012). Short-term deployment of transmitters and loggers allows the recording of detailed information on movement patterns, but limitations include the short duration that transmitters remain attached (O’Mara et al. 2014), and that devices need to be <5% of body mass (Aldridge and Brigham 1988). The use of passive integrated transponder (PIT) tags is an approach that allows for the passive detection of individuals for their lifetime (Gibbons and Andrews 2004). By using antennas at roost sites, or other regularly used locations, information can be gleaned about movement, activity and survival patterns of PIT-tagged individuals over time. PIT-tagging has been used as a wildlife marking tool since the 1980s (Gibbons and Andrews 2004), but its potential for investigating seasonal movement patterns in insectivorous bats has not yet been tested.

In this study, we use PIT-tag technology and monitoring to discover seasonal population patterns, migration, and movements of the critically endangered southern bent-winged bat to enhance its conservation. In large bent-winged bats (M. orianae, previously M. schreibersii) in Australia, regional migration of adult females has been attributed to the need to move to and from maternity caves that have suitable microclimatic conditions; those selected provide stable, high humidity and temperatures necessary for the development of young (Dwyer 1963; Dwyer and Hamilton-Smith 1965; Baudinette et al. 1994). Non-breeding caves have more variable, cooler temperatures and may facilitate the use of torpor in cooler months (Hall 1982). Regional inter-cave movements are largely centred on maternity caves, but also include a number of non-breeding caves typically associated with a maternity population (Dwyer 1969). However, most knowledge of seasonal movements of bent-winged bats in Australia has been documented from populations now described as the eastern bent-winged bat (M. orianae oceanensis).

The southern bent-winged bat is thought to undertake similar seasonal movements (Churchill 2008; DELWP 2020); although, unlike the eastern bent-winged bat subspecies, many adult males also congregate at maternity caves (Dwyer and Hamilton-Smith 1965). The southern bent-winged bat has undergone serious population decline since the 1960s (DELWP 2020). Survival rates assessed in 2016–2019 show lowered seasonal survival during summer (December–February) and autumn for juveniles and lactating females, with the lowest survival rates coinciding with drought in early 2016 (van Harten 2020). Population modelling predicts a continued population decline (van Harten 2020), the cause of which remains uncertain, though resource limitation due to loss of foraging habitat and drought is suspected as a key threat (Allinson et al. 2006; Bourne and Hamilton-Smith 2007; DELWP 2020; van Harten 2020). Health surveys have not revealed pathogenic factors that could explain the severe population decline (Holz et al. 2018a , 2018b , 2018c , 2019a , 2020).

The southern bent-winged bat faces two emerging threats, both influenced by migration and movement patterns. First, there are numerous windfarms within its restricted range, and many more are proposed (Moloney et al. 2019; DELWP 2020). Globally, collision with wind turbines is the leading cause of multiple mortality events in bats (O’Shea et al. 2016), and migrating bats appear most at risk (Cryan and Barclay 2009). In Australia, although deceased bats are recovered at windfarms (Hull and Cawthen 2013), there is a high degree of uncertainty around mortality estimates and population level impacts are unknown (Moloney et al. 2019). A second emerging threat is the potential introduction of the pathogen causing white-nose syndrome (Holz et al. 2019b ), which has decimated bat populations in North America (Cheng et al. 2021). A risk assessment found that it is ‘very likely/almost certain’ that white-nose syndrome will be inadvertently introduced to Australia and ‘likely’ that it will come into contact with bats in the coming decade (Holz et al. 2019b ). Eight species of Australian bats are considered most at risk, including the southern bent-winged bat (Turbill and Welbergen 2020). Knowledge of the seasonal activity cycle of the southern bent-winged bat is critical to inform both species recovery (DELWP 2020) and sustainable windfarm development, and strengthen potential responses to the threat of white-nosed syndrome in Australia (Holz et al. 2019b ; Turbill and Welbergen 2020). To address these knowledge gaps, we installed PIT antennas at a major maternity cave and a key non-breeding cave of the southern bent-winged bat in South Australia, and continuously monitored activity of the PIT-tagged bat population over 3.5 years (van Harten et al. 2019). We used these data to address three predictions: first, that there are two annual migration events, to and from the maternity cave in spring and autumn respectively, with ‘virtually all’ bats present at the maternity cave for the summer breeding season (Dwyer and Hamilton-Smith 1965); second, that the timing of movements will vary by age and sex class; and third, that there is little activity in winter when individuals are expected to disperse to non-breeding caves and undertake periods of torpor (Hall 1982).

Methods

PIT-tagging

Southern bent-winged bats were trapped and PIT-tagged at Bat Cave within the Naracoorte Caves National Park, South Australia (37°2′1″S, 140°47′42″E), a major maternity and summer congregation site (current population estimated at approximately 30 000 individuals). Trapping occurred over six nights in 2016, and four nights in each of 2017 and 2018, at the end of the breeding season (January and February), timed to coincide with juveniles commencing flying and becoming independent. To reduce disturbance, only two consecutive trapping nights were undertaken at a time. Bats were trapped with 10–14 Austbat harp traps (Faunatech, Mount Taylor, Vic., Australia), set exterior to the fencing surrounding the cave entrance. Trapping continued from dusk until the early hours of the morning, catching bats as they left or re-entered the cave.

Sex and age were recorded for each of 2966 PIT-tagged bats. Age was described as juvenile (first year) or adult, based on the presence or absence of a cartilaginous core in the metacarpal–phalangeal joints (Brunet-Rossinni and Wilkinson 2009). The PIT-tag (Biomark HPT 12, 12.5 mm, <0.1 g) was subcutaneously injected dorsally using a sterilised 12-gauge needle and applicator (Biomark MK10 implanter and N125 needles in 2016, Biomark MK 25 Implant Guns and HPT12 Pre-load Trays in 2017–2018). The injection site was sealed with a drop of surgical adhesive (3M™ VetBond™) to minimise tag loss (Lebl and Ruf 2010), and allowed to dry prior to release (van Harten et al. 2020). All PIT-tags were checked for correct function using a hand-held PIT-tag scanner (Trovan LID560 and Biomark 601), both before and after insertion. During handling and tagging, bats typically remained calm and were able to fly within minutes of the procedure. Re-captured individuals were in good physical condition, with no sign of infection or other detrimental effects (van Harten et al. 2020).

Monitoring of PIT-tagged individuals and data collection

PIT-tagged bats were monitored using large PIT-tracking systems (Biomark IS1001) installed at two study sites. The first system was installed within a cave passage at the Bat Cave maternity site from January 2016. The second was installed at the entrance to a key non-breeding cave located near Glencoe, 72 km south of Bat Cave. This second system was trialled short-term (e.g. 2–3 nights at a time) in February 2017, with long-term monitoring commencing in April 2017 (though with intermittent power outages until June 2017). The antenna systems detected any tagged individuals as they flew through the loop formed with the flexible, 15- m long antenna (van Harten et al. 2019). When the systems were working optimally, there was a large read-range (up to 105 cm) before and after the antennas, and high detection success (van Harten et al. 2019). The system recorded data directly to USB flash drives plugged into the data logger board of the Biomark IS1001 system.

Data recorded included individual PIT-tag detections (date, time and PIT-tag number) and noise reports. Noise is a measure of total interference, or unwanted signal, being received by the detection system, and is known to affect detection success (van Harten et al. 2019). Data were downloaded from the systems regularly (approximately monthly) by manually retrieving the flash drives until 16 August 2019, with over 2.1 million unique detections recorded.

Analysis of population patterns using probability of encounter

We defined probability of encounter as the probability that an individual known to be alive was both present and detected. Thus, for an age/sex class in the population, an increasing value of encounter probability (from 0 to 1) reflects an increasing proportion of that age/sex class that is likely to be present and detected at the respective cave. We used models of encounter probability data to address the three predictions: (1) that annual migration occurs to and from the maternity cave; (2) that the timing of movements varies between age and sex classes; and (3) in winter months, individuals disperse to non-breeding caves.

To prepare the data for analysis, we first created capture–resight histories for each of the 2966 PIT-tagged bats to produce a binary response variable (detected/undetected) for each individual across each day of the respective study periods for each cave. ‘Day’ was defined as the 24 h between successive middays. Plots of the capture–resight histories (detected/undetected) for each tagged individual were generated to visualise patterns at the two caves, as well as to identify when individuals were detected at both caves in a single night.

Age functions were added such that juveniles were coded as adult on 31 December in the year of tagging, when approximately 13 months old. Known to be alive (KTBA) matrices were calculated for each age by sex category (adult females, adult males, juvenile females, juvenile males). Noise readings for each antenna were averaged across each study day and were also included in the final matrices for each cave.

We used a binomial generalised additive model, implemented with the R package ‘mgcv’, to model the per-individual, daily probability of encounter as a function of noise + yday (by different sex and age class parameters; see Table 2), fitted with a cyclic cubic regression spline. Noise is daily average noise (%) and yday is day of year. The spline was included to ensure continuity in the modelled response of the last and first day of year in the model. The upper limit on the degrees of freedom of the splines is given by (k − 1): we assumed that k = 3 for the spline for noise, which allowed for some non-linearity in detection probability as a function of environmental noise; and k = 20 for the spline for yday, which permitted a flexible response due to the day of year.

The final model for each cave was selected by comparing values of the Akaike information criterion (AIC) for alternate models that incorporated different demographic variables for individuals: (1) sex, (2) age, (3) combination of sex and age classes, and (4) no demographic variable. The AIC includes a penalty for increasing complexity (i.e. number of parameters) in the model. The Akaike weight for each alternate model is a measure of the likelihood of that model being the best fit to the data among the set of models considered. The top-ranked model is the one with the lowest AIC value, and can be compared with other models by the difference in AIC values and AIC weights with the top-ranked model. Deviance explained was used as a measure of model fit. The chosen models for each cave were also modelled separately as yearly subsets to compare variation in patterns among years.

Observational data

Infra-red cameras were installed within the Bat Cave maternity cave in 1995, forming part of the tourist attractions for Naracoorte Caves National Park (Reed and Bourne 2013). Live footage of the bats, in multiple chambers of the cave, can be viewed from the Bat Observation Centre during visitor tours. We made use of these pre-existing cameras (Panasonic WV-SPN631) and tour schedule by asking the National Park staff to report any notable behaviour of the bats, such as birthing of the young. Observations were also made during visits to Bat Cave to collect PIT-tag data. The southern bent-winged bat is the only bat taxon known to roost in this cave, so there was no concern about confounding observations with other species. Observational data from the cameras and from trapping, together with presence/absence data from PIT-tag monitoring, were used to identify the phenology of the reproductive cycle.

Results

Phenology of the breeding cycle

Birthing at Bat Cave was observed in mid to late November (Table 1, Fig. 1a ). The first births occurred 8–10 days before mass birthing by pregnant females in the 2015/2016 and 2016/2017 breeding seasons. In 2017/2018, the timing of mass birthing could not be determined due to the creche being positioned out of view of the cameras. Juveniles commenced flying and began emerging from the maternity cave in January, with many juveniles captured at the maternity cave exit from mid-January.

Table 1.

Observations of births of southern bent-winged bats and juvenile development over three summer breeding seasons at Bat Cave, Naracoorte Caves National Park, South Australia.

WR21088_T1.gif

Fig. 1.

(a) A cluster of adult females beginning birthing in the maternity chamber at Bat Cave on 19 November 2016; mass birthing in the population occurred over the following day. On the centre-right of the frame (arrowed), two pups can be observed, one with umbilical cord and placenta still attached. (b) Mating and coupling behaviour observed in a smaller chamber extending off the main maternity chamber in Bat Cave, on 6 May 2018. Both observations were observed remotely via infra-red video footage. Photos: Emmi van Harten.

WR21088_F1.gif

Mating and coupling behaviour were observed during the day on the cameras in Bat Cave on 6 May 2018 (the only observation) (Fig. 1b ), with bats roosting as dispersed couples on the walls and ceiling of a smaller chamber extending from the main maternity chamber. In contrast, in the main maternity chamber that day, bats roosted in clusters or individually, the typical pattern at other times of the year.

Encounter probability

For each study site, the top-ranked model for the daily encounter probability of individuals, as assessed by AIC values and AIC weights, included the interaction of an individual’s sex and age (Table 2). That is, the model that fitted separate estimates for adult females, adult males, juvenile females and juvenile males had the lowest AIC value, much lower than alternative models that included only age class or only sex (Table 2). AIC weights clearly indicated that, for each site, this model was by far the best fit to the data among the models tested. Total deviance explained by the top-ranked models were 81.9% for Bat Cave and 52% for Glencoe, respectively. For Bat Cave, the demographic covariate (i.e. age and sex classes) accounted for 36.7% of the deviance, and for Glencoe this was 17.2%.

Table 2.

Selection table comparing alternative encounter probability models with different individual covariates included for the effects of yday.

WR21088_T2.gif

Daily encounter probability (i.e. the probability that an individual known to be alive is present and detected) at Bat Cave was high for all sex and age classes from November to February (Fig. 2a ). From February, encounter probability decreased at Bat Cave, with the lowest encounter probability for autumn months occurring in juveniles (of both sexes) and adult females in March, coinciding with a peak in encounter probability in juveniles and adult females at Glencoe (Fig. 2b ). Modelled encounter probability for these three sex and age classes was similar at both caves during this period. Activity in these classes increased again at Bat Cave around April (and decreased at Glencoe).

Fig. 2.

Daily encounter probability for age and sex classes of the southern bent-winged bats at two sites: (a) the maternity cave, Bat Cave; and (b) the non-breeding cave at Glencoe, South Australia (modelled effects of yday, where noise = 5%). The models are based on detections of 2966 bats PIT-tagged at Bat Cave over 3.5 years, 1449 of which were subsequently detected at Glencoe. Ribbon width for each class represent 95% confidence intervals. Note that (a) and (b) have a different y-axis scale.

WR21088_F2.gif

Over winter, from May, the daily encounter probability at Bat Cave fell steeply to ~0–0.05 at the beginning of June (Fig. 2a ). Compared with the other sex and age classes, encounter probability of adult males at Bat Cave decreased later and increased earlier, such that there was only approximately 1 month (~June) when few bats were detected at Bat Cave. Following an influx of bats at Glencoe in May–June, associated with dispersal from the maternity cave, the winter months also experienced a drop in encounter probability at this non-breeding cave, likely due to lowered winter activity or use of other non-breeding caves. Nevertheless, regular activity was still detected at Glencoe and it was not uncommon to detect hundreds of bats per day at the entrance of this cave in June and July. Adult males maintained higher encounter probability at Glencoe over winter (e.g. encounter probabilities >0.1) than other sex and age classes, until beginning their earlier return to Bat Cave (~July). Adult females became more active at Glencoe around the beginning of August, with the daily encounter probability for spring peaking at this site at the beginning of September. Daily encounter probability in juvenile classes began increasing approximately 1 month after that of adult females but rose faster, peaking at Glencoe in mid-September.

At Bat Cave, there was a staged increase in activity between sex and age classes in late winter and early spring, with variation in timing evident among years (Fig. 3). Encounter probability of adult females increased later than adult males, followed by the juvenile cohorts. For example, encounter probability of adult males was 0.25 at the beginning of August in each of the first 3 years, whereas adult females did not reach the same encounter probability until mid-August to early September in the same years. Both adult classes returned to Bat Cave earlier in 2019, reaching 0.25 in mid-July and the beginning of August for males and females, respectively. Caution must be taken when interpreting results for late spring due to a series of system issues and power outages (occurring around October 2016, November 2017 and November 2018, Supplementary Fig. S1), which likely influenced the drop in encounter probability during these periods – thus population patterns at this time of the year remain less clear. However, encounter probability at Glencoe also varied considerably between the 2 years of spring monitoring at this location (Fig. 3b , 2017 and 2018), and is not associated with any known system issues or outages at this time of year (Supplementary Fig. S2).

Fig. 3.

Annual variation in daily encounter probability for age and sex classes of the southern bent-winged bats over the study years at two sites: (a) the maternity cave Bat Cave; and (b) the non-breeding cave at Glencoe, South Australia (modelled effects of yday, where noise = 5%). Models are based on data collected at Bat Cave from January 2016 to August 2019 and Glencoe from May 2017 to August 2019. Ribbon width for each class represents 95% confidence intervals. Note, because no bats were tagged in 2019 only adult (≥1 year old) classes are known for that year.

WR21088_F3.gif

Despite variation in timing (Fig. 3), the general seasonal patterns among sex and age classes were maintained across years. A notable exception was in early 2016, when adult males showed a decline in encounter probability in February and March at Bat Cave that is not shown in the following 3 years. This may have been caused by detection issues at Bat Cave during this period, resolved in May 2016 (van Harten et al. 2019). This period also corresponded with severe drought conditions that may have affected movement behaviour in adult males.

Visualising individual detection histories across the tagged population demonstrated that the observed changes in encounter probability were associated with individuals moving between the two caves, with clear seasonal patterns of movement evident (Fig. 4). This includes the aforementioned synchronous patterns of encounter probability for juveniles and adult females in early autumn.

Fig. 4.

Capture–resight histories of all PIT-tagged individuals at Bat Cave (pink) and Glencoe (blue) over the 3.5-year study period. Each of the 2966 tagged bats is represented as an individual row on the y-axis, with initial capture and subsequent daily detections indicating presence at the respective caves marked in pink and blue. The data occur in blocks because individuals were tagged over 3 years and seven trapping events. The Glencoe PIT-antenna system was installed in April 2017. Some absences (white) are due to system issues such as power outages or high ‘noise’ (signal interference) – these occurrences are outlined in the Supplementary Figs S1, S2. Grey shading indicates the winter months of May to August, when little activity was expected (due to use of torpor and dispersal to numerous non-breeding caves). Occurrences where individuals were detected at both caves in a single night are marked in black. Distinct seasonal movement patterns are evident in the population. This figure also highlights the vastness of the dataset and the complexity of inter-cave movements by individuals over the study period. For an example of finer detail, see Fig. 6.

WR21088_F4.gif

Direct movements between caves

In addition to seasonal population movements, direct movements between the two monitored caves were detected throughout the year, in all seasons, even during peak occupancy periods at the respective caves (Fig. 5). Individuals were able to fly the 72 km between caves in a single night. The nightly occurrence of detecting such ‘direct flights’ peaked during the early autumn, autumn–winter and winter–spring population movements (Fig. 5). For example, 35 individuals were recorded at both caves on the same night in early May 2018, equating to just over 2% of the tagged population known to be alive at that time.

Fig. 5.

Nightly proportion of PIT-tagged southern bent-winged bats (of the total population known to be alive each night) detected at both caves on the same night. The caves, Bat Cave and Glencoe, South Australia, are located 72 km apart.

WR21088_F5.gif

Detailed analysis of individual movements is beyond the scope of this paper. However, individuals demonstrated complexity in movement patterns and seasonal inter-cave movements were not necessarily ‘one-way’ regional migrations (Fig. 6). For example, an adult female in early August (late winter) 2017 flew the 72 km from Glencoe to Bat Cave in 3.2 h, returning to Glencoe the following night in 3.5 h. This female was then not detected for two nights, then subsequently flew again from Glencoe to Bat Cave, this time in 5.5 h, and returned to Glencoe on the following night in 4.2 h.

Fig. 6.

An example of detail from Fig. 4. Rows represent the capture–resight histories for approximately 90 PIT-tagged individuals from mid-January to the beginning of May 2018. Grey shading on the right of the image indicates the start of May. Pink represents presence/detection at Bat Cave (the maternity cave), blue indicates presence/detection at Glencoe (non-breeding cave), black shows occurrences where an individual was detected at both caves on the same night and white indicates absence or lack of detection. Although clear seasonal population patterns emerged in the encounter models developed (Fig. 2), the detail in this dataset shows that individual presence/absence and movements are complex and are not confined to only two-way seasonal movements or ‘migrations’.

WR21088_F6.gif

Discussion

In this study, we have provided new insights into the phenology of the seasonal congregation and movements of the southern bent-winged bat. Using PIT-tag technology, we identified seasonal patterns among the population’s age and sex classes, and use these to bring together the full seasonal cycle of the subspecies for the first time. We interpret this knowledge in relation to the conservation of this critically endangered taxon, particularly in relation to emerging threats.

Seasonal breeding cycle and population movements

The encounter probability of PIT-tagged individuals confirmed that the population at Bat Cave peaks over the summer breeding season. Mass birthing occurred in November, and presence at the maternity cave remained high among all age and sex classes over the subsequent summer months. Juveniles began flying in January. Lactation rates decreased in early February (van Harten 2020), suggesting the bats are being weaned at this time.

Following juveniles becoming independent, a previously undescribed movement event occurred in autumn months each year. This event peaked in mid-March, with bats moving away from the maternity cave (coinciding with increased detection at Glencoe), and then returning to Bat Cave in April. This inter-cave movement was primarily undertaken by juveniles and adult females, which had almost identical encounter probability patterns at the two caves during this time. This behaviour is consistent with the maternal guidance hypothesis (Stumpf et al. 2017), whereby mothers guide their offspring to known roost sites, including hibernacula. In wild free-ranging bats, individuals use a combination of cognitive processes to localise roosts (Hernández-Montero et al. 2020). For example, the Bechstein’s bat (Myotis bechsteinii) uses spatial memory to re-localise previously occupied roosts: however, social information significantly improves success in localising unfamiliar roosts (Hernández-Montero et al. 2020). Maternal guidance of young to roosts has long been proposed (e.g. Fenton 1969), and the hypothesis has been supported for several northern hemisphere species by observations from proximity sensors (Ripperger et al. 2019) and genetic studies (Stumpf et al. 2017).

After this short-term movement to the non-breeding cave in late summer to early autumn, most adult females (daily encounter probability >0.7) and many juveniles (daily encounter probability >0.5) returned to the maternity cave in April through to May. An opportunistic observation of mating behaviour at Bat Cave in early May suggests that adult females return to mate with adult males; this coincides with the timing of conception recorded in the population (Crichton et al. 1989). Miniopterus orianae are thought to not reach reproductive maturity until their second year (Dwyer 1963; van Harten 2020). It is possible that many first-year bats return to Bat Cave as part of their socialisation and learning, or due to attachment to their mothers or social group. Migrating bat species are commonly documented mating at, or on route to, ‘swarming’ sites and hibernacula (Fleming and Eby 2003). In this population, autumn swarming (see Parsons et al. 2003) has not been observed, and the presence of males at maternity caves could explain the mating behaviour described. For example, in Daubenton’s bats (Myotis daubentonii), mating behaviour varied depending on the proportion of males at maternity caves: at roosts with few males, females mated at swarming sites, whereas at mixed maternity roosts, females mated with males at the maternity site (Angell et al. 2013). Further observation of mating in southern bent-winged bats is needed to draw conclusions, because they may also mate at non-breeding caves and at other times.

The southern bent-winged bat has been described as entering periods of torpor over winter months from mid-May to mid-September, including deeper hibernation from June to mid-August (based on observations at caves when collecting specimens during these months) (Crichton et al. 1989). We anticipated near-zero detection of PIT-tagged bats over June and July, but contrary to expectation it was not uncommon to detect hundreds of bats per day active at Glencoe during these months. Encounter probability was significantly reduced from mid-June through July (Fig. 2), though adult males remained more active than adult females, possibly to increase mating opportunities and due to males having no need to conserve body condition for spring pregnancy (Turbill 2006; Czenze et al. 2017).

In spring, the return to Bat Cave was gradual and staged among age and sex classes: adult males returned first, then adult females, and finally juveniles from the previous breeding season. By October, daily encounter probability approached similar levels to that observed before winter dispersal for all groups, suggesting that natal philopatry in the population is high in both sexes. There was just 1 month at Bat Cave (~June) when few bats were detected at the maternity cave.

Although this research re-shapes understanding of seasonal population patterns in the southern bent-winged bat, there are elements consistent with other observations over the last ~50 years. For example, Dwyer and Hamilton-Smith (1965) reported that juveniles had dispersed from Bat Cave by the end of February in 1962 and 1963, timing that coincides with our observation of late summer–early autumn movement in juveniles and adult females before returning to Bat Cave. Codd et al. (2003) reported a decline in bats at Bat Cave through May, coinciding with winter dispersal – and Hamilton-Smith’s cave journal records (unpubl. data) noted that the low number of bats present in mid-August 1964 were all males, which aligns with the observation in this study of adult males returning to Bat Cave before females.

Inter-cave movement and flight distance

Movements between roosts, and daily/nightly movements to and from foraging areas by insectivorous bats are typically less than several kilometres (Kunz and Lumsden 2003). For example, tracking individuals of the large-eared pied bat (Chalinolobus dwyeri) showed commutes of less than 700 m from cliff roosts to foraging areas (Williams and Thomson 2019), and lactating eastern cave bats (Vespadelus troughtoni) regularly undertake inter-cave movements of less than 1.5 km (Law et al. 2005). However, some studies have recorded maximum nightly flight distances from 10 to 35 km (Barclay et al. 2000; O’Donnell 2001; Lumsden et al. 2002; Bourne 2010), particularly in fragmented habitats. In this study, we recorded numerous movements between the two caves (72 km) in the same night, with individuals able to fly this distance in just a few hours. These flight distances more than double the previously recorded maximum flight distance by the southern bent-winged bat (35 km, Bourne 2010), which has been used to inform buffer zones around caves for conservation.

Dwyer and Hamilton-Smith (1965) suggested that almost all southern bent-winged bats in this region congregate at Bat Cave for the breeding season. This was supported by observations of the approximate equivalence in adult sex ratios and apparent desertion of non-breeding caves (Dwyer and Hamilton-Smith 1965). Our results show that most bats do congregate at Bat Cave, but there is an underlying turnover occurring within the population. In addition to the main seasonal movements, inter-cave movements between the maternity cave and Glencoe non-breeding cave occur all year-round. Thus, not all movement detected was consistent with the definition of seasonal migration (e.g. Fleming and Eby 2003), notably the movements by some individuals back and forth between the caves on successive nights. There are ~80 non-breeding caves known in the southern bent-winged bat’s distribution, including at least 48 caves in south-east South Australia (Thompson 2017; DELWP 2020). Similar movements probably also occur between Bat Cave and some of these caves. Preliminary PIT-tag data from other non-breeding caves in the lower south-east of South Australia demonstrate movement occurring between these sites and Glencoe (unpubl. data). Simultaneous monitoring of a number of non-breeding caves is needed to characterise these movement patterns. We suggest that a shift in terminology from regional ‘migration’ to ‘movement’ is appropriate for the southern bent-winged bat.

The drivers for inter-cave movements are not clear. Maternity caves provide warm, humid microclimatic conditions for raising young (Dwyer and Hamilton-Smith 1965; Baudinette et al. 1994). However, southern bent-winged bats use the Bat Cave maternity cave for much of the year, so it likely also fulfills other population requirements; for example, acting as a ‘social hub’, and at certain times of the year, a mating site. The use of non-breeding sites has been attributed to cooler microclimates that facilitate torpor (Hall 1982); however, resource availability may also be a driver. Codd et al. (2003) suggested that dispersal away from Bat Cave for the winter may be associated with decreased prey in the local area. The non-breeding cave at Glencoe is close to vegetated areas and wetlands that may provide important foraging resources. This may explain continued movement to this key non-breeding cave (previously assumed to be a ‘wintering cave’), even during summer months when the regional population was thought to remain at the Bat Cave maternity site (Dwyer and Hamilton-Smith 1965).

Implications for emerging threats and conservation

The extended congregation of the southern bent-winged bat at Bat Cave highlights the importance of adequate resources in the vicinity of this major maternity cave to support a large population almost year-round. Drought and loss of foraging habitat have been identified as key threats to the southern bent-winged bat (DELWP 2020). Approximately 90% of native vegetation in its distribution has been cleared (DELWP 2020), and lower survival rates for juveniles and lactating females occur in the drier seasons of summer and autumn, with highest mortality during drought (van Harten 2020). These times of lower survival in summer and autumn coincide with the timing of significant seasonal movements, undertaken predominately by juveniles and adult females. Any additional mortality associated with such movements (e.g. due to collisions with wind turbines) would further disadvantage these vulnerable population classes.

Population congregation and movement patterns have important implications for the development of windfarms within the range of the southern bent-winged bat, and their mitigation strategies (Peste et al. 2015). For example, the risk associated with bat activity in the vicinity of proposed windfarms may be underestimated if pre-construction monitoring is undertaken only short-term, or during summer when juveniles still depend on adult females at maternity caves. Autumn months are when bats are more frequently found dead at windfarms, both in Australia (Hull and Cawthen 2013; Moloney et al. 2019) and internationally (Cryan and Barclay 2009). If pre-construction surveys target the autumn period, but for only a short period (e.g. only in April, when many bats returned to the maternity cave), significant levels of bat activity could be missed. Monitoring over a full seasonal cycle would provide greater understanding of bat activity and more comprehensively inform mitigation strategies.

The high level of movement also has implications for potential responses to the risk of white-nose syndrome. If the pathogen causing white-nose syndrome is inadvertently introduced to Australia and comes into contact with southern bent-winged bats, it will likely spread quickly through the entire distribution. Hibernating bats are susceptible because infection causes a cascade of physiological effects which lead to bats arousing more frequently from torpor, and thereby depleting fat reserves (Reeder et al. 2012; Verant et al. 2014). It has been suggested that bat species that are ‘shallow hibernators’, with relatively high levels of winter activity (e.g. characterised by more frequent arousals from torpor), have a lower susceptibility to white-nose syndrome (Johnson et al. 2012). Our finding of higher than expected winter activity parallels results in other studies that some species of temperate bats are more active in winter than previously thought (Hope and Jones 2012; Johnson et al. 2016), including in subzero temperatures (Christie and Simpson 2006; Lausen and Barclay 2006). Further knowledge of the length, frequency and other characteristics of torpor bouts in the southern bent-winged bat, and other Australian bats, is needed to adequately assess their hibernation ecology, associated susceptibility to white-nose syndrome and appropriate response strategies (Holz et al. 2019b ; Turbill and Welbergen 2020).

Globally, many species of bats are threatened with extinction (Frick et al. 2020): in Australia, 62% of cave-dwelling bats are listed as threatened or near-threatened (van Harten in press). The seasonal population dynamics and movement patterns of the critically endangered southern bent-winged bat highlight the conservation challenges associated with highly mobile species, particularly a reliance on congregating in specific and restricted areas, combined with complex and broadscale habitat needs (Fleming and Eby 2003; Welbergen et al. 2020). The higher than expected mobility of the southern bent-winged bat is consistent with other studies of dynamic movement in some bat species, across regional, state and international jurisdictional boundaries (Hutterer 2005; Voigt et al. 2012; Welbergen et al. 2020). This highlights the need for conservation and management initiatives to be distribution-wide if they are to adequately address threats such as habitat loss (Frick et al. 2020), the risk of mortality from windfarm development (O’Shea et al. 2016; Frick et al. 2017) and white-nose syndrome (Frick et al. 2015; Holz et al. 2019b ; Turbill and Welbergen 2020), and the need to ensure effective conservation into the future.

Data availability

The data that support this study will be shared upon reasonable request to the corresponding author.

Conflicts of interest

Thomas Prowse is an Associate Editor of Wildlife Research. Despite this relationship, he did not at any stage have editor-level access to this manuscript while in peer review, as is the standard practice when handling manuscripts submitted by an editor of this journal. The authors have no further conflicts of interest to declare.

Declaration of funding

This work was financially supported by an Australian Government Research Training Scholarship and funded by the Holsworth Wildlife Research Endowment, Australian Speleological Federation Karst Conservation Fund, Department of Environment and Water (South Australia), Natural Resources South East, and Lirabenda Endowment Fund. A solar panel was donated by My Energy Engineering.

Ethics approval

All animal capture and handling procedures and data collection were carried out under ethics approval from the La Trobe University Animal Ethics Committee (Project Number AEC15-67) and in accordance with relevant guidelines and regulations prescribed by the South Australian Department of Environment and Water (Research Permit Number U26453).

Supplementary material

Supplementary material is available  online.

Acknowledgements

This study would not have been possible without the help of many people, especially the 70+ volunteers who worked throughout the nights during trapping and tagging. A special thanks to Rose Thompson and Dennis Matthews, who generously assisted with fieldwork throughout the study. We are grateful for the continued time and in-kind support from the staff at Naracoorte Caves National Park, in particular Andrew Hansford and Tom Shortt. Many thanks also to Matt Seeliger for providing continued access.

References

1.

Aldridge HDJN, Brigham RM (1988) Load carrying and maneuverability in an insectivorous bat: a test of the 5% ‘rule’ of radio-telemetry. Journal of Mammalogy 69, 379–382. https://doi.org/10.2307/1381393 Google Scholar

2.

Allinson G, Mispagel C, Kajiwara N, Anan Y, Hashimoto J, Laurenson L, Allinson M, Tanabe S (2006) Organochlorine and trace metal residues in adult southern bent-wing bat (Miniopterus schreibersii bassanii) in southeastern Australia. Chemosphere 64, 1464–1471. https://doi.org/10.1016/j.chemosphere.2005.12.067 Google Scholar

3.

Angell RL, Butlin RK, Altringham JD (2013) Sexual segregation and flexible mating patterns in temperate bats. PLoS One 8, e54194. https://doi.org/10.1371/journal.pone.0054194 Google Scholar

4.

Barclay RMR, Chruszcz BJ, Rhodes M (2000) Foraging behaviour of the large-footed myotis, Myotis moluccarum (Chiroptera: Vespertilionidae) in south-eastern Queensland. Australian Journal of Zoology 48, 385–392. https://doi.org/10.1071/zo00036 Google Scholar

5.

Baudinette RV, Wells RT, Sanderson KJ, Clark B (1994) Microclimatic conditions in maternity caves of the bent-wing bat, Miniopterus schreibersii: an attempted restoration of a former maternity site. Wildlife Research 21, 607–619. https://doi.org/10.1071/wr9940607 Google Scholar

6.

Bourne S (2010) Bat research at Naracoorte. The Australasian Bat Society Newsletter 34, 24–29. Google Scholar

7.

Bourne S, Hamilton-Smith E (2007) Miniopterus schreibersii bassanii and climate change. The Australasian Bat Society Newsletter 28, 67–69. Google Scholar

8.

Bowlin MS, Bisson I-A, Shamoun-Baranes J, Reichard JD, Sapir N, Marra PP, Kunz TH, Wilcove DS, Hedenstrom A, Guglielmo CG, Akesson S, Ramenofsky M, Wikelski M (2010) Grand challenges in migration biology. Integrative and Comparative Biology 50, 261–279. https://doi.org/10.1093/icb/icq013 Google Scholar

9.

Brunet-Rossinni AK, Wilkinson GS (2009) Methods for age estimation and the study of senescence in bats. In‘Ecological and Behavioral Methods for the Study of Bats’. (Eds TH Kunz, S Parsons) pp. 315–325. (Johns Hopkins University Press: Baltimore, MD, USA) Google Scholar

10.

Cheng TL, Reichard JD, Coleman JTH, Weller TJ, Thogmartin WE, Reichert BE, Bennett AB, Broders HG, Campbell J, Etchison K, Feller DJ, Geboy R, Hemberger T, Herzog C, Hicks AC, Houghton S, Humber J, Kath JA, King RA, Loeb SC, Massé A, Morris KM, Niederriter H, Nordquist G, Perry RW, Reynolds RJ, Sasse DB, Scafini MR, Stark RC, Stihler CW, Thomas SC, Turner GG, Webb S, Westrich BJ, Frick WF (2021) The scope and severity of white-nose syndrome on hibernating bats in North America. Conservation Biology 35, 1586–1597. https://doi.org/10.1111/cobi.13739 Google Scholar

11.

Christie JE, Simpson W (2006) Influence of winter weather conditions on lesser short-tailed bat (Mystacina tuberculata) activity in Nothofagus forest, Fiordland. New Zealand Journal of Zoology 33, 133–140. https://doi.org/10.1080/03014223.2006.9518437 Google Scholar

12.

Churchill S (2008) ‘Australian Bats’, 2nd edn. (Allen and Unwin: Sydney, NSW, Australia) Google Scholar

13.

Codd JR, Sanderson KJ, Branford AJ (2003) Roosting activity budget of the southern bent-wing bat (Miniopterus schreibersii bassanii). Australian Journal of Zoology 51, 307–316. https://doi.org/10.1071/zo01079 Google Scholar

14.

Crichton EG, Seamark RF, Krutzsch PH (1989) The status of the corpus luteum during pregnancy in Miniopterus schreibersii (Chiroptera: Vespertilionidae) with emphasis on its role in developmental delay. Cell and Tissue Research 258, 183–201. https://doi.org/10.1007/bf00223157 Google Scholar

15.

Cryan PM, Barclay RMR (2009) Causes of bat fatalities at wind turbines: hypotheses and predictions. Journal of Mammalogy 90, 1330–1340. https://doi.org/10.1644/09-mamm-s-076r1.1 Google Scholar

16.

Czenze ZJ, Jonasson KA, Willis CKR (2017) Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate. Physiological and Biochemical Zoology 90, 502–511. https://doi.org/10.1086/692623 Google Scholar

17.

DELWP (2020) National recovery plan for the southern bent-wing bat Miniopterus orianae bassanii. Victorian Government, Melbourne, Vic., Australia. Google Scholar

18.

Dwyer PD (1963) The breeding biology of Miniopterus schreibersii blepotis (Termminck) (Chiroptera) in north-eastern NSW. Australian Journal of Zoology 11, 219–240. https://doi.org/10.1071/zo9630219 Google Scholar

19.

Dwyer PD (1966) The population pattern of Miniopterus schreibersii (Chiroptera) in north-eastern New South Wales. Australian Journal of Zoology 14, 1073–1137. https://doi.org/10.1071/zo9661073 Google Scholar

20.

Dwyer PD (1969) Population ranges of Miniopterus schreibersii (Chiroptera) in south-eastern Australia. Australian Journal of Zoology 17, 665–686. https://doi.org/10.1071/zo9690665 Google Scholar

21.

Dwyer PD, Hamilton-Smith E (1965) Breeding caves and maternity colonies of the bent-winged bat in south-eastern Australia. Helictite 4, 3–21. Google Scholar

22.

Fenton MB (1969) Summer activity of Myotis lucifugus (Chiroptera: Vespertilionidae) at hibernacula in Ontario and Quebec. Canadian Journal of Zoology 47, 597–602. https://doi.org/10.1139/z69-103 Google Scholar

23.

Fleming TH, Eby P (2003) Ecology of bat migration. In‘Bat Ecology’. (Eds TH Kunz, MB Fenton) pp. 156–208. (The University of Chicago Press: Chicago, IL, USA) Google Scholar

24.

Frick WF, Puechmaille SJ, Hoyt JR, Nickel BA, Langwig KE, Foster JT, Barlow KE, Bartonička T, Feller D, Haarsma A-J, Herzog C, Horáček I, van der Kooij J, Mulkens B, Petrov B, Reynolds R, Rodrigues L, Stihler CW, Turner GG, Kilpatrick AM (2015) Disease alters macroecological patterns of North American bats. Global Ecology and Biogeography 24, 741–749. https://doi.org/10.1111/geb.12290 Google Scholar

25.

Frick WF, Baerwald EF, Pollock JF, Barclay RMR, Szymanski JA, Weller TJ, Russell AL, Loeb SC, Medellin RA, McGuire LP (2017) Fatalities at wind turbines may threaten population viability of a migratory bat. Biological Conservation 209, 172–177. https://doi.org/10.1016/j.biocon.2017.02.023 Google Scholar

26.

Frick WF, Kingston T, Flanders J (2020) A review of the major threats and challenges to global bat conservation. Annals of the New York Academy of Sciences 1469, 5–25. https://doi.org/10.1111/nyas.14045 Google Scholar

27.

Gibbons JW, Andrews KM (2004) PIT tagging: simple technology at its best. BioScience 54, 447–454. https://doi.org/10.1641/0006-3568(2004)054[0447:ptstai]2.0.co;2 Google Scholar

28.

Hall LS (1982) The effect of cave microclimate on winter roosting behaviour in the bat, Miniopterus schreibersii blepotis. Austral Ecology 7, 129–136. https://doi.org/10.1111/j.1442-9993.1982.tb01586.x Google Scholar

29.

Hernández-Montero JR, Reusch C, Simon R, Schöner CR, Kerth G (2020) Free-ranging bats combine three different cognitive processes for roost localization. Oecologia 192, 979–988. https://doi.org/10.1007/s00442-020-04634-8 Google Scholar

30.

Holz PH, Lumsden LF, Druce J, Legione AR, Vaz P, Devlin JM, Hufschmid J (2018a) Virus survey in populations of two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in south-eastern Australia reveals a high prevalence of diverse herpes-viruses. PLos One 13, e0197625. https://doi.org/10.1371/journal.pone.0197625 Google Scholar

31.

Holz PH, Lumsden LF, Hufschmid J (2018b) Ectoparasites are unlikely to be a primary cause of population declines of bent-winged bats in south-eastern Australia. International Journal for Parasitology: Parasites and Wildlife 7, 423–428. https://doi.org/10.1016/j.ijppaw.2018.10.006 Google Scholar

32.

Holz PH, Lumsden LF, Marenda MS, Browning GF, Hufschmid J (2018c) Two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in southern Australia have diverse fungal skin flora but not Pseudogymnoascus destructans. PLos One 13, e0204282. https://doi.org/10.1371/journal.pone.0204282 Google Scholar

33.

Holz PH, Lumsden LF, Legione AR, Hufschmid J (2019a) Polychromophilus melanipherus and haemoplasma infections not associated with clinical signs in southern bent-winged bats (Miniopterus orianae bassanii) and eastern bent-winged bats (Miniopterus orianae oceanensis). International Journal for Parasitology: Parasites and Wildlife 8, 10–18. https://doi.org/10.1016/j.ijppaw.2018.11.008 Google Scholar

34.

Holz P, Hufschmid J, Boardman WSJ, Cassey P, Firestone S, Lumsden LF, Prowse TAA, Reardon T, Stevenson M (2019b) Does the fungus causing white-nose syndrome pose a significant risk to Australian bats? Wildlife Research 46, 657–668. https://doi.org/10.1071/wr18194 Google Scholar

35.

Holz PH, Clark P, McLelland DJ, Lumsden LF, Hufschmid J (2020) Haematology of southern bent-winged bats (Miniopterus orianae bassanii) from the Naracoorte Caves National Park, South Australia. Comparative Clinical Pathology 29, 231–237. https://doi.org/10.1007/s00580-019-03049-z Google Scholar

36.

Hope PR, Jones G (2012) Warming up for dinner: torpor and arousal in hibernating Natterer's bats (Myotis nattereri) studied by radio telemetry. Journal of Comparative Physiology B 182, 569–578. https://doi.org/10.1007/s00360-011-0631-x Google Scholar

37.

Hull C, Cawthen L (2013) Bat fatalities at two wind farms in Tasmania, Australia: bat characteristics, and spatial and temporal patterns. New Zealand Journal of Zoology 40, 5–15. https://doi.org/10.1080/03014223.2012.731006 Google Scholar

38.

Hutterer R (2005) ‘Bat Migrations in Europe: A Review of Banding Data and Literature.’ (Federal Agency for Nature Conservation: Bonn) Google Scholar

39.

Johnson JS, Lacki MJ, Thomas SC, Grider JF (2012) Frequent arousals from winter torpor in Rafinesque's big-eared bat (Corynorhinus rafinesquii). PLoS One 7, e49754. https://doi.org/10.1371/journal.pone.0049754 Google Scholar

40.

Johnson JS, Treanor JJ, Lacki MJ, Baker MD, Falxa GA, Dodd LE, Waag AG, Lee EH (2016) Migratory and winter activity of bats in Yellowstone National Park. Journal of Mammalogy 98, 211–221. https://doi.org/10.1093/jmammal/gyw175 Google Scholar

41.

Kunz TH, Lumsden LF (2003) Ecology of cavity and foliage roosting bats. In‘Bat Ecology’. (Eds TH Kunz, MB Fenton) pp. 3–89. (University of Chicago Press: Chicago, IL, USA) Google Scholar

42.

Lausen CL, Barclay RMR (2006) Winter bat activity in the Canadian prairies. Canadian Journal of Zoology 84, 1079–1086. https://doi.org/10.1139/z06-093 Google Scholar

43.

Law B, Chidel M, Mong A (2005) Life under a sandstone overhang: the ecology of the eastern cave bat Vespadelus troughtoni in northern New South Wales. Australian Mammalogy 27, 137–145. https://doi.org/10.1071/am05137 Google Scholar

44.

Lebl K, Ruf T (2010) An easy way to reduce PIT-tag loss in rodents. Ecological Research 25, 251–253. https://doi.org/10.1007/s11284-009-0629-y Google Scholar

45.

Lumsden LF, Bennett AF, Silins JE (2002) Location of roosts of the lesser long-eared bat Nyctophilus geoffroyi and Gould's wattled bat Chalinolobus gouldii in a fragmented landscape in south-eastern Australia. Biological Conservation 106, 237–249. https://doi.org/10.1016/s0006-3207(01)00250-6 Google Scholar

46.

Moloney, PD, Lumsden, LF, and Smales, I (2019). Investigation of existing post-construction mortality monitoring at Victorian wind farms to assess its utility in estimating mortality rates. Arthur Rylah Institute for Environmental Research Technical Report Series No. 302. Department of Environment, Land, Water and Planning, Melbourne, Vic., Australia. Google Scholar

47.

O'Donnell CFJ (2001) Advances in New Zealand mammalogy 1990–2000: long-tailed bat. Journal of the Royal Society of New Zealand 31, 43–57. https://doi.org/10.1080/03014223.2001.9517638 Google Scholar

48.

O'Mara MT, Wikelski M, Dechmann DKN (2014) 50 years of bat tracking: device attachment and future directions. Methods in Ecology and Evolution 5, 311–319. https://doi.org/10.1111/2041-210x.12172 Google Scholar

49.

O'Shea TJ, Cryan PM, Hayman DTS, Plowright RK, Streicker DG (2016) Multiple mortality events in bats: a global review. Mammal Review 46, 175–190. https://doi.org/10.1111/mam.12064 Google Scholar

50.

Parsons KN, Jones G, Davidson-Watts I, Greenaway F (2003) Swarming of bats at underground sites in Britain – implications for conservation. Biological Conservation 111, 63–70. https://doi.org/10.1016/s0006-3207(02)00250-1 Google Scholar

51.

Peste F, Paula A, da Silva LP, Bernardino J, Pereira P, Mascarenhas M, Costa H, Vieira J, Bastos C, Fonseca C, Pereira MJR (2015) How to mitigate impacts of wind farms on bats? A review of potential conservation measures in the European context. Environmental Impact Assessment Review 51, 10–22. https://doi.org/10.1016/j.eiar.2014.11.001 Google Scholar

52.

Petit E, Mayer F (2000) A population genetic analysis of migration: the case of the noctule bat (Nyctalus noctula). Molecular Ecology 9, 683–690. https://doi.org/10.1046/j.1365-294x.2000.00896.x Google Scholar

53.

Reed L, Bourne S (2013) ‘Old’ cave, new stories: the interpretative evolution of Blanche Cave, Naracoorte, South Australia. Journal of the Australasian Cave and Karst Management Association 90, 11–28. Google Scholar

54.

Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, Britzke ER, Vodzak ME, Darling SR, Stihler CW, Hicks AC, Jacob R, Grieneisen LE, Brownlee SA, Muller LK, Blehert DS (2012) Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One 7, e38920. https://doi.org/10.1371/journal.pone.0038920 Google Scholar

55.

Ripperger S, Günther L, Wieser H, Duda N, Hierold M, Cassens B, Kapitza R, Koelpin A, Mayer F (2019) Proximity sensors on common noctule bats reveal evidence that mothers guide juveniles to roosts but not food. Biology Letters 15, 20180884. https://doi.org/10.1098/rsbl.2018.0884 Google Scholar

56.

Stumpf M, Meier F, Grosche L, Halczok TK, Schaik JV, Kerth G (2017) How do young bats find suitable swarming and hibernation sites? Assessing the plausibility of the maternal guidance hypothesis using genetic maternity assignment for two European bat species. Acta Chiropterologica 19, 319–327. https://doi.org/10.3161/15081109acc2017.19.2.008 Google Scholar

57.

Thompson, R (2017). Review and revision of the Southern Bent-wing Bat (Miniopterus orianae bassanii) Regional Action Plan for the South East of South Australia: 2017–2027. Report prepared for the Department of Environment, Water and Natural Resources, Government of South Australia. Nature Glenelg Trust, Mount Gambier, SA, Australia. Google Scholar

58.

Turbill C (2006) Thermoregulatory behavior of tree-roosting chocolate wattled bats (Chalinolobus morio) during summer and winter. Journal of Mammalogy 87, 318–323. https://doi.org/10.1644/05-mamm-a-167r1.1 Google Scholar

59.

Turbill C, Welbergen JA (2020) Anticipating white-nose syndrome in the Southern Hemisphere: widespread conditions favourable to Pseudogymnoascus destructans pose a serious risk to Australia's bat fauna. Austral Ecology 45, 89–96. https://doi.org/10.1111/aec.12832 Google Scholar

60.

van Harten E (2020) Population dynamics of the critically endangered, southern bent-winged bat Miniopterus orianae bassanii. PhD thesis, La Trobe University, Melbourne, Vic., Australia. Available at  https://doi.org/10.26181/60f76319cf701 Google Scholar

61.

van Harten E (in press) Cave-dwelling bats in Australia. In‘Australian Cave and Karst Systems’. (Eds J Webb, S White) (Springer Nature: Cham, Switzerland) Google Scholar

62.

van Harten E, Reardon T, Lumsden LF, Meyers N, Prowse TAA, Weyland J, Lawrence R (2019) High detectability with low impact: optimizing large PIT tracking systems for cave-dwelling bats. Ecology and Evolution 9, 10916–10928. https://doi.org/10.1002/ece3.5482 Google Scholar

63.

van Harten E, Reardon T, Holz PH, Lawrence R, Prowse TAA, Lumsden LF (2020) Recovery of southern bent-winged bats (Miniopterus orianae bassanii) after PIT-tagging and the use of surgical adhesive. Australian Mammalogy 42, 216–219. https://doi.org/10.1071/am19024 Google Scholar

64.

Verant ML, Meteyer CU, Speakman JR, Cryan PM, Lorch JM, Blehert DS (2014) White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiology 14, 10. https://doi.org/10.1186/s12899-014-0010-4 Google Scholar

65.

Voigt CC, Popa-Lisseanu AG, Niermann I, Kramer-Schadt S (2012) The catchment area of wind farms for European bats: a plea for international regulations. Biological Conservation 153, 80–86. https://doi.org/10.1016/j.biocon.2012.04.027 Google Scholar

66.

Welbergen JA, Meade J, Field HE, Edson D, McMichael L, Shoo LP, Praszczalek J, Smith C, Martin JM (2020) Extreme mobility of the world's largest flying mammals creates key challenges for management and conservation. BMC Biology 18, 101. https://doi.org/10.1186/s12915-020-00829-w Google Scholar

67.

Williams ER, Thomson B (2019) Aspects of the foraging and roosting ecology of the large-eared pied bat (Chalinolobus dwyeri) in the western Blue Mountains, with implications for conservation. Australian Mammalogy 41, 212–219. https://doi.org/10.1071/am17064 Google Scholar
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Emmi van Harten, Ruth Lawrence, Lindy F. Lumsden, Terry Reardon, Andrew F. Bennett, and Thomas A. A. Prowse "Seasonal population dynamics and movement patterns of a critically endangered, cave-dwelling bat, Miniopterus orianae bassanii," Wildlife Research 49(7), 646-658, (2 May 2022). https://doi.org/10.1071/WR21088
Received: 8 June 2021; Accepted: 27 February 2022; Published: 2 May 2022
KEYWORDS
bats
encounter probability
mark–recapture
migration
Miniopterus
PIT tags
population modelling
Back to Top