Acta Chiropterologica, 19(1): 161–174, 2017 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS doi: 10.3161/15081109ACC2017.19.1.013

Social activity of lesser horseshoe (Rhinolophus hipposideros) at nursery roosts and a hibernaculum in North Wales, U.K.

MARGARET M. ANDREWS1, 4, AMELIA M. HODNETT2, and PETER T. ANDREWS 3

1Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, United Kingdom 2Gavia Environmental, Perth, PH1 3FX, United Kingdom 3Department of Physics, Liverpool University, Liverpool L69 5BX, United Kingdom 4Corresponding author: E-mail: [email protected]

To better understand the importance of social activity, ultrasonic calls made by lesser horseshoe bats (Rhinolophus hipposideros) in North Wales, U.K. were recorded during extended pre-set periods since 2010 inside and outside nursery roosts from May to July and in a hibernaculum in October. Ultrasonic calls with fundamental frequencies between 15–42 kHz were identified as seven categories of infant development calls and 15 categories of adult ultrasonic social calls according to the frequency and duration of the fundamental, the number of harmonics and the number of calls in a sequence. Activities were monitored remotely using infrared video cameras with simultaneous time expansion sound recorders. Distinctive polyharmonic isolation calls of newborn R. hipposideros enabled timing of births to be determined and infant echolocation marked the time when they started to . Trill advertisement calls in the hibernaculum indicated mating behaviour in October. Comparison of call-triggered recording times enabled variable levels of activity to be determined quickly. The longest sonogram times were in July (50.2 min/h) and in June (49.1 min/h). During these recordings, 95 and 90 adults returned to the roost after foraging and there were 16 and 42 babies, respectively. In May sound and video recordings outside a nursery roost revealed ultrasonic social calls during the emergence of 200 adult R. hipposideros when the light level was low at two lux, which showed that R. hipposideros were engaged in social activity, not light sampling. Surveys of ten nursery roosts showed that this social behaviour was typical of R. hipposideros in Wales.

Key words: lesser horseshoe , infant, ultrasonic, social calls, roosts

INTRODUCTION in populations (Bontadina et al., 2001; P. Sinnaduri, in litt.). Population trends for the U.K. from 1999 to The lesser Rhinolophus hippo - 2013 showed an annual increase but the average hi- sideros is one of the most endangered species in bernacula count in 2014 were lower than predicted Europe (Stebbings, 1988) and is extinct in the (P. Briggs, personal communication) and there has Netherlands (Schofield, 1999; Bontandina et al., been a 30% reduction in maternity roost counts in 2001). Distribution in the U.K. is limited to Wales, Pembrokeshire from 2005–2015 (Haycock and Hay - The West Midlands, south-eastern England and the cock, 2015). West Coast of Ireland (Schofield and McAney, Conservation initiatives would benefit from 2008). This species is no longer found in Yorkshire more site studies because R. hipposideros form or the south coast of England (Schofield, 2008) and summer roosts with as few as 16 bats, but in 1993 it is an endangered species in the U.K. (Hutson, the average was 49 bats (Halliwell and Matthews, 1993; Walsh et al., 2001). More than 50% of the 2004). The broad scale National Bat Monitoring U.K. population of R. hipposideros occurs in Wales Programme, involving nursery roost exit counts and (Harris et al., 1995; Halliwell and Matthews, 2004) hibernacula counts in the U.K. (Walsh et al., 2001; where there are well established maternity roosts Schofield, 2008; Hayes et al., 2009) could be used and many suitable hibernation sites including dis- as the basis to search for new sites. Alternative- used mines (P. Sinnaduri, in litt.). Destruction of ly, radio-tracking of R. hipposideros with small roosting and hibernation sites, loss or fragmentation radio emitters (Bontandina et al., 2002) could be of , and the effects of pesticides on insect productive in finding maternity roosts within a 10 prey are considered the main causes of the decline km radius of a known hibernaculum (P. Sinnaduri, 162 M. M. Andrews, A. M. Hodnett, and P. T. Andrews in litt.). Jones et al. (2000) and Parsons and Szew - MATERIALS AND METHODS czak (2009) have defined non-invasive techniques for monitoring bats using sound recordings but weak Sound Recording and Method of Analysis and highly directional R. hipposideros echoloca- tion calls make them difficult to detect in the Sound recordings of adult R. hipposideros were made in a nursery roost in the loft of an old barn attached to a private field (P. Sinnaduri, in litt.). Extended sampling peri- house in the Rhuddlan area of Denbighshire (53°11’7.135N, ods and deploying automated static detectors within 3°26’3.699W), Wales, U.K., during five selected periods a confined area is recommended for field sur- from June to September 2010 and in a nearby ice house veys of R. hipposideros (Collins, 2016) and Scott converted into a hibernaculum in October 2010. Adult R. hip- and Altringham (2014) recommended that at least posideros were also recorded in the Llanrwst area of Con- wy (53°11’7.135N, 3°49’5.667W), Wales, U.K., in May 2015 four field surveys of R. hipposideros should be in an underground passage (44.5 m long) leading from a nurs- made. ery roost in a cellar of a private mansion to a grilled gate and Monitoring through the use of ultrasonic record- garden outside. Infant and adult ultrasonic calls were record- ings at roost sites is a valuable aid to the conserva- ed using a modified Tranquility III time expansion bat detector tion of bat populations. Recent developments in (Bale, Courtpan Design Ltd., U.K.) with external batteries so that recordings could be made for 24 hour periods, using remote time expansion recordings enabled the iden- the methods described by Andrews and Andrews (2006). The tification of adult Rhinolophus ferrumequinum in ultrasonic calls were analysed with BatSound (Pettersson underground sites during extended pre-set periods Elektronik AB, Uppsala, Sweden) with a Hanning window (R. D. Ransome, in litt.). The direct method of and a FFT size of 512. Frequency and duration measure- recording inside nursery roosts has shown that infant ments were made according to a method described by Pettersson (2001), Russ (1999) and Altringham (2003). Ultra - R. hipposideros make ultrasonic calls (Kay and sonic social calls were identified according to the categories Pickvance, 1963; Konstantinov, 1973; Konstantinov described by Andrews and Andrews (2003), Andrews and et al., 1990). Initial investigations of time expansion An drews (2006) and Andrews et al. (2011), in which the fre- recordings of adult R. hipposideros calls at the quency, duration and number of components characterise each entrance of a roost at Glynllifon in North Wales call. Recordings of the ultrasonic calls were collected in June, July and October 2010. Regressions of the call-activated sono- in October showed that there were ultrasonic calls gram times (min/h) and the number of ultrasonic calls (uc/h) with fundamental frequencies in the range of 15–49 were performed using SSPS software (IBM Analytics, kHz and harmonic frequencies above 30 kHz Portsmouth, Hants, U.K.) to assess whether there were sig- (P. T. An drews, in litt.). The fundamental frequen- nificant relationships between those parameters in the periods cies of R. hipposideros echolocation calls are in the monitored. range of 55–57 kHz (Schofield and McAney, 2008). Therefore, the calls recorded were below the echolo- Bat Activity cation frequency. These calls warranted further in- Inside a nursery roost vestigation because adult R. ferrumequinum social A CCD camera (YD66, Maplin Electronics, U.K.) was calls have been recorded inside and outside a nurs- placed inside the nursery roost in Denbighshire with infrared il- ery roost (Andrews and Andrews, 2003, 2016) and lumination (Alana Ecology, U.K.) after the nightly exodus and in a hibernaculum (Andrews et al., 2006). Specific subsequent activity was recorded remotely on a VHS video social vocalisations have also been identified in recorder (V242 UK, Toshiba, U.K.). VHS tapes (TDK 180) were analysed in detail to monitor activity at selected periods in a captive colony of adult R. ferrumequinum tragatus June and July 2010. (Ma et al., 2006; Liu et al., 2013). The overall aim of this study was to use remote Outside a nursery roost recordings of ultrasonic calls made by adult and in- Three low light/infrared cameras (Pro-642, 746 and fant R. hipposideros as a simple and non-invasive 880, Swann, Southampton, U.K.) recorded bat exits from the method of identifying nursery roosts to aid in the nursery roost into an underground passage and emergence at conservation of this species. Initially this study the grilled exit gate that lead into the garden of the mansion in Conwy. The cameras were connected to a Medusa 960 aimed to make extended pre-set non-invasive re- DVR (QVIS, Hampshire, U.K.) and digital AVI files were mote recordings of R. hipposideros ultrasonic calls. analysed with a remote computer. Flight excursions in the This was supplemented with infrared video record- passage towards the garden exit and return flights towards ings in and around nursery roosts and a hibernacu- the nursery roost were counted visually with the number of lum. Consequently, this study also investigated the bats in the cluster and the number of flights into and out of the cluster. The cameras and video were operated by mains use of R. hipposideros ultrasonic calls, with funda- electricity or by a 12-volt battery supply (Maplin Electro- mental frequencies in the range 15–49 kHz, to deter- nics, Rotherham, U.K.) on three consecutive nights in May mine if sites were nursery or mating roosts. 2015. Social activity of lesser horseshoe bats at roosts 163

Environmental conditions during recording periods

Extended recording periods inside and around the nursery 1 roost and in the hibernaculum were pre-set and controlled re- motely. The Met Office (Exeter) and Natural Resources Wales (Cardiff) supplied local weather data. Ambient temperatures at the nursery roosts during the extended recording periods in 2010 and 2015 were similar in the fourth week of May (16.0 ± 2.4°C), third week of June (16.1 ± 0.4°C) and first and second

week of July (16.1 ± 0.4°C and 16.3 ± 0.6°C) and there was no callsTotal Event/ rain. The ambient temperature at the hibernaculum in the third week of October (11.3 ± 1.0°C) was lower. At the beginning of $ each recording session the ambient temperature was measured with an AZ-8709 Temperature Meter (Orion Air Conditioning 3.2 658 A Ltd. Kempston, U.K.). Light levels were measured with Pre - cision Gold N76CC digital light meter (Maplin, Rotherham, U.K.) with a range of 0.01–50,000 lux. Light meter readings were calibrated with light intensity records measured with – 10.4 677 – , A, B 1.3 48 – , A, B 5.6 159 – 1 a CdS photoresistor (Andrews, 1995b) and light meter records 2 were compared with voltage readings. Photocell records of 1.4–3.0 V were comparable with 1.0–600 lux and records below 1.36 V corresponded with zero light meter readings. in a nursery roost and hibernaculum Denbighshire, North –

Surveys of nursery roosts in Wales callsTotal Event/ Calls time In order to investigate R. hipposideros social activity a sur- vey was carried out at ten nursery roosts from May to Septem- $ ber 2010–2016. The locations of the roost sites listed as 1–10 are shown in Table 5. Surveys of the nursery roosts in Denbigh - R. hipposideros shire, site 2, and in Conwy, site 8, were surveyed in 2010 and — 1st, 2nd — adult ultrasonic social call activity, A return to the roost after foraging,

2015 respectively. Roost sites 3 and 6 in Denbighshire, site 1 in _ , Conwy, site 4 in Wrexham, and sites 5 and 10 in Gwynedd were 2

surveyed between 2015 and 2016. The remaining roost sites , R – 21.9 1,392 R 1 A, B 4.5 837 A

7 and 9 in Pembrokeshire were surveyed in 2014 and 2015. 1

RESULTS – Video Recording of Activity Total callsTotal Event/ Calls time

In May 2015 adult R. hipposideros emerged from $ the nursery roost in the cellar of a mansion in Con - wy into a service passage where they flew around – and formed a cluster of 28 bats six metres from the grilled gate exit that lead into a garden (Fig. 1B).

During emergence from the gate into the garden the 1 light level was below two lux and the temperature was 8°C (Fig. 1A). In June and July 2010 adult bats flew in and out of the nursery roost in Denbighshire, fed infants and clustered. Infant bats hung on the beams then flew inside the loft (Table 1). At the start 51 – 20.7 1,519 A, B – of recording in the third week of June the ambient callsTotal Event/ Calls time

temperature was 19.1°C and in the first and second $ Third week of June First week of July Second week of July Third week of October week of July it was 18°C and 19.0°C, respectively. 1.5 3.7 223 A 26.2 2,945 R 3.4 218 A 21.9 1,896 A, B 40.2 5,357 R (min/h) (n/h) Activity (min/h) (n/h) Activity (min/h) (n/h) Activity (min/h) (n/h) Activity

Sonogram Assessment of Activity Calls time

Frequency range of ultrasonic signals

During intense activity, two or three echolocation 1. Comparison of the call activated sonogram time and number ultrasonic calls made by frequencies were used simultaneously. Adult R. hip- Time GMT Time — call activated time recorded in the sonogram. Ex exit, Sr sunrise, Ss sunset; R posideros echolocation calls ranged from 110 kHz ABLE 23.00 24.00 01.00 $ 05.0006.0007.0008.0009.00 31.6 40.5 8.6 17.6 7,001 13,848 – 4,642 719 A Sr, A, C – A – – – – – – – – – – Sr – – – 21.7 – – 19.3 2,640 – 52.0 4,547 25.8 A, BA, B Sr, 12,228 24.0 2,634 A, B, C – 2.5 A, B 121 – 142 – – A – A – – – Sr – – – B — baby ultrasonic development call activity, C — cluster formed. B — baby ultrasonic development call activity, 02.0003.0004.00 3.3 4.1 49.1 253 9,974 253 A R A 13.5 – 1,202 – A, B 26.5 – 3,837 19.9 A, B 1,645 3.6 A, B 310 2.8 A 75 A 19.0020.0021.0022.00 – – 15.8 28.0 – 6,078 – 6,541 Ex – Ss – 27.2 30.4 – 17.2 8,361 4,954 1,402 Ex, A – Ss, A, B – – – – – – – – – – Ss – – 9.5 3.7 – 456 2.8 105 29.6 R – 65 2,010 Ex, Ss – Wales, U.K. Wales, T 164 M. M. Andrews, A. M. Hodnett, and P. T. Andrews to 114 kHz (112.3 ± 1.2 kHz; 0 ± SD — Fig 2I). or adult modified echolocation calls (Fig. 2E A band of frequencies between 105 kHz and 108 and 2J). In the range of 10–50 kHz, fundamental kHz in the nursery roost in July 2010 confirmed frequencies of infant development calls or adult infant R. hipposideros echolocation calls (Fig. 2E). social calls were recorded (Fig. 2A–C, 2F–H, 2K, Between 57 kHz and 108 kHz, there were infant and 2L).

FIG. 1. Activity of R. hipposideros at a nursery roost in Gwynedd, North Wales, U.K. A — bats emerging from the exit gate –× –, light level (lux) during the activity –—–. B — bat flights, out towards the exit gate –è–, out of the cluster ––, in towards the roost ––, into the cluster –£–. C — calls made during activity, echolocation calls –×–, single component social calls ––, multiple component social calls –—–, trill advertisement calls – – Social activity of lesser horseshoe bats at roosts 165

FIG. 2. Ultrasonic calls made by R. hipposideros in nursery roosts and a hibernaculum in North Wales. A–E — stages in the development of infant calls; F–J — adult social calls derived from the infant calls. Categories of adult calls: F — Type A [CF I]; G — Type B [FM II r]; H, K — Type C [FM III, FM VI]; L — Type D [FM VI t]; I, J — Type E [FM XI, CF XII]. See text and Tables 2 and 3 for details of the categories of calls 166 M. M. Andrews, A. M. Hodnett, and P. T. Andrews

Hourly sonogram recording time are summarized in Tables 3 and 4. Categories of The longest call-activated times were in the sec- single component, multiple component and modi- ond week of July (52.0 min/h) and in the third week fied echolocation calls were identified. The main of June (49.1 min/h), when there were 90 and 95 differences between infant calls and adult ultra- adult bats respectively. The shortest was in the sonic social calls were that infant calls had more third week of October (1.3 min/h) when there were than one call in a sequence and many harmonics. only 47 adult bats (Tables 1 and 2). Although the Recordings of infant R. hipposideros calls are sonogram time was long in the fourth week of May proof of the existence of a nursery roost. Stages (46.3 min/h) there were 200 adult R. hipposideros 1–5 of infant R. hipposideros calls (Fig. 2A–D active during emergence (Fig. 1C and Table 2). In and Tables 3 and 4) show the development of May 2015 there was a significant relationship be- polyharmonic isolation calls as infants attempt to tween the total number of ultrasonic calls (uc/min) echolocate. and the total number of flights (f/min) in the passage Five categories of adult R. hipposideros calls (R2 = 0.90, P ≤ 0.001). Echolocation calls were the were similar to the infant calls but occurred as majority of ultrasonic signals in each period moni- single calls and the harmonics were mainly sup- tored (Fig. 3A–E and Table 2) and each sonogram pressed. These calls have been identified accord- time (min/h) varied according to bat exits and return ing to functional types of call (Fig. 2F–J), and by to the roost (Table 1). The linear regression of sono- their frequency and duration as categories of so- gram time (min/h) versus the number of ultrasonic cial calls (Tables 3 and 4). Type A constant fre- calls (uc/h) was most significant when adult bats quency calls were often uttered as a broadband call only were in the nursery roost in the third week of that sounded like a bellow (Fig. 2F and Table 3). June (R2 = 0.88, P ≤ 0.001). Also in July, there Type B single component frequency modulated was a significant relationship (2nd week: R2 = 0.70, (FM) calls (Fig. 2G and Table 3) that sounded like P < 0.01; 1st week: R2 = 0.53, P = 0.062) when ba- whistles, when ×32 time expansion recordings bies and adults were present and in the third week of were played back, occurred during periods of in- October (R2 = 0.70, P < 0.01) there was a significant tense echolocation. Type C multiple component relationship when adults occupied the hibernacu- FM calls (Fig. 2H and Table 3) sounded like lum. Deter mination of roost activity using the sono- whistles or warbling (Fig. 2K and Table 3) and gram time (min/h) and ultrasonic call activated time occurred mainly in May (Fig. 2H and 2K) and July took approximately 10 minutes. By contrast, ultra- (Fig. 3E) when clusters of bats formed. Type D trill sonic calls/h took more than 10 hours for each period. calls (Fig. 2L and Table 3) were also made as clusters formed in May (Fig. 2L), June and July Analysis of infant and adult ultrasonic calls (Fig. 3A, 3E and Table 1). When trill calls were Ultrasonic calls made by R. hipposideros in made after bats returned to the hibernaculum the nursery roosts and hibernaculum (Fig. 2A–L) (Fig. 3D and Table 1) they were interspersed by

TABLE 2. Comparison of R. hiposideros activity inside and around nursery roosts and inside a hibernaculum in North Wales, U.K., with recordings of adult echolocation and ultrasonic social calls and infant ultrasonic development calls

Bats (n) Period Sonogram times Ultrasound Ultrasound Ratio Month/Year EL callsa (n) ABrecorded (h) (0, SD; min/h) callsc (n) infant calls (n) EL: other Fourth week 200 – 1.9 46.3, 0.0 8,245 19 – 434:1e of May 2015 Third week 90 – 12.0 17.3, 15.9 56,886 293 – 194:1e of June 2010 First week 95 16 7.0 23.3, 5.9 21,159 101 335d 209:1e 49:1f of July 2010 Second week 93 42 10.0 25.6, 12.7 34,139 121 1,013d 2,984b 282:1e 8.:1f of July 2010 Third week 47 – 11.0 6.8, 8.1 4,692 13 – 181:1e of October 2010 A — adult bats, B — baby bats, a EL — adult echolocation calls, b — baby echolocation calls, c — adult ultrasound social calls, d — baby development calls, e — ratio of EL: adult ultrasonic social calls, f — ratio of EL: adult ultrasonic social calls and infant ultrasonic with development calls Social activity of lesser horseshoe bats at roosts 167

FIG. 3. Echolocation and social calls made by R. hipposideros in Denbighshire North Wales, U.K. A, C and E — calls made by adult bats inside a nursery roost; D and F — calls made by infant bats; B — calls made by adult bats in a hibernaculum. Echolocation calls, adult –×–; baby –.–×–.–. Single component calls, adult ——, infant ––; multiple component, adult – –; infant –..––..–; modified echolocation, adult ––, infant –.––.–; trill advertisement calls –—– 168 M. M. Andrews, A. M. Hodnett, and P. T. Andrews b Total duration 6.6, 2.8 75.2, 50.2 21.9, 11.0 34.9, 5.6 45.0, 0.0 51.5, 6.7 27.2, 8.5 17.3, 4.0 39.7, 2.3 107.7, 68.4 b Duration a Frequency b Duration a in North Wales, U.K. Wales, in North $ Frequency b Duration a and in a hibernaculum * Frequency b at nursery roosts Duration a R. hipposideros Frequency b Duration — see text for locations of roosts, FM — frequency modulated, CF — constant frequency, I–VII — category of call, see text for details, r — rising I–VII — category of call, see text for details, — see text for locations of roosts, FM frequency modulated, CF constant frequency, a * $ First component Second component Third component Fourth component Fifth component Frequency — ms ( 0 , SD), b n 3. Categories of ultrasonic calls made by adult and infant kHz ( 0 , SD), of call Category ABLE CF I below 45 21.6, 4.5 21.6, 4.5 107.7, 68.4 CF IFM II rFM II fFM III 11FM IV 5VFM 8 35.7, 13.6 23.3, 2.6VIFM 8 53.6, 19.6 31.7, 19.4VIIFM 23.3, 2.6 1 21.9, 11.0 27.5, 18.4 42.9, 4.5FM III t 1 36.7, 0.0 75.2, 50.2 t V FM 6 6.6, 2.8 45.8, 5.4 4VI t FM 40.4, 0.0 38.9, 0.0 2 31.1, 12.3VII tFM 17.4, 5.2 42.8, 4.3 45.4, 0.0 5 34.0, 10.9 15.0, 00 40.4, 15.2 3 39.9, 4.5b CF I 46.6, 5.6 6.6 11.2, 29.0, 0.0 23.2, 3.6 1 48.6, 11.2b FM II r 38.9, 0.0 16.9, 3.0 17.5, 6.0 15.0, 5.7 32.5, 11.9b FM III 29.2, 0.0 41.8, 0.0 4.5, 1.3 36,1 4.3 28.7, 10.7 30.0, 0.0 12 3 30.3, 3.8 9.3, 5.9 45.2, 0.0 0.0 11.0, 25.7, 13.4 14.0, 4.6 45.6, 6.3 27.2, 6.7 3 34.0, 0.7 32.1, 5.4 32.4, 13.0 36.5, 7.8 22.0, 0.0 46.8, 0.0 30.5, 10.7 7.5, 5.5 27.2, 6.7 44.3, 0.4 13.2, 7.1 37.3, 1.0 30.5, 5.2 32.0, 20.3 29.0, 0.0 42.3, 0.0 45.3, 4.0 27.2, 8.5 46.4, 0.1 30.8, 4.8 26.3, 4.1 17.3, 4.0 53.4, 1.7 66.0, 0.0 27.0, 3.5 8.0, 7.1 58.7, 47.3 4.6 11.2, 38.6, 8.5 45.8, 0.0 41.0, 25.9 45.6, 0.3 45.1, 5.0 67.0, 0.0 23.9, 13.6 12.7, 1.2 6.8, 4.0 37.5, 0.0 47.2, 0.9 38.0, 0.0 10.0, 5.7 55.4, 0.0 27.0, 0.0 36.8, 4.3 198.0, 0.0 44.8, 6.7 128.6, 15.7 69.0, 0.0 96.6, 5.4 T frequency, f — falling frequency, b — baby calls, t trill advertisement call f — falling frequency, frequency, a __ Adult calls Infant calls Social activity of lesser horseshoe bats at roosts 169

TABLE 4. Echolocation and modified echolocation calls made by adult and infant R. hipposideros at nursery roosts* and a hibernaculum$ in North Wales, U.K.

Fundamental Harmonic 2 Category of call Frequencyx frequency Durationy n Range Start End range (kHz) Adult FM XI r [3]† 13 50–54 55.5, 3.3 53.9, 1.8 6.2, 2.0 100–109 FM XI r [2] 6 45–49 45.5, 0.6 49.7, 1.8 4.8, 2.1 90–99 FM XI r [1] 12 40–44 40.3, 1.7 43.8, 3.9 7.8, 5.4 80–89 FM XI f [1]† 4 50–54 51.7, 0.3 48.5, 1.9 9.5, 2.1 100–105 FM XI f [2] 1 45–49 50.9, 0.0 42.1, 0.0 8.0, 0.0 90–99 FM XI f [3] 2 40–44 40.3, 0.1 38.2, 0.1 8.0, 0.1 70–79 FM XI f t [1-4]‡ 4 45–55 105.5, 7.0 97.0, 7.8 4.8, 0.5 90–110 FM XI r t [5-1]‡ 5 45–55 100.6, 6.1 106.4, 6.1 5.2, 1.1 90–110 CF XII [1]† 1 55–60 56.0, 0.0 56.0, 0.0 10.0, 0.0 110–114 CF XII [2] 1 55–60 55.0, 0.0 55.0, 0.0 10.0, 0.0 110–114 CF XII [3] 1 50–54 54.0, 0.0 54.0, 0.0 10.0, 0.0 100–105 CF XII [4] 1 50–54 51.2, 0.0 51.2, 0.0 10.0, 0.0 100–105 CF XII [5] 1 35–39 38.5, 0.0 38.5, 0.0 10.0, 0.0 70–79 EL§ 100 55–60 56.2, 1.2 56.2, 1.2 22.1, 7.8 110–114 Infant b FM XI r [5]† 3 50–54 50.5, 1.7 52.9, 0.6 10.0, 1.0 100–105 b FM XI r [4] 81 45–49 45.8, 1.2 47.6, 1.1 8.8, 3.0 90–99 b FM XI r [3] 407 40–44 41.4, 1.4 43.0, 1.4 8.8, 3.9 80–89 b FM XI r [2] 118 35–39 37.5, 1.5 39.4, 1.3 7.4, 2.9 70–79 b FM XI r [1] 7 30–34 33.0, 0.9 35.0, 1.1 6.8, 1.9 60.69 b FM XI f [1]† 30 40–44 43.9, 1.4 38.8, 1.9 6.0, 3.3 80–89 b FM XI f [2] 59 35–39 39.7, 2.1 35.2, 1.5 6.6, 4.6 70–79 b FM XI f [3] 9 30–34 34.9, 1.1 24.7, 1.3 7.4, 2.8 60.69 b CF XII [5]† 1 50–54 50.5, 0.0 50.5, 0.0 15.0, 0.0 100–105 b CF XII [4] 981 45–49 46.7, 1.3 46.7, 1.3 21.6, 9.2 90–99 b CF XII [3] 701 40–44 43.7, 1.0 43.7, 1.0 20.3, 10.7 80–89 b CF XII [2] 35 35–39 38.1, 1.4 38.1, 1.4 11.9, 2.9 70–79 b CF XII [1] 2 30–34 34.0, 0.6 34.0, 0.6 9.6, 3.0 60.69 b ELγ 100 50–54 54.2, 1.6 54.2, 1.6 15.0, 0.5 100–108 * $ — see text for locations or roosts, x — kHz (0, SD), y — ms (0, SD), FM — frequency modulated, CF — constant frequency, XI–XII — see text for categories of call, r — rising frequency, f — falling frequency, b — baby calls, [n] † — order of calls in sequence, ‡ — fused cascade of calls in a falling then rising sequence, § — adult echolocation sample, γ — baby echolocation

sequences of 8–20 long echolocation calls (43.8 ± Surveys of Nursery Roosts in Wales 4.4 ms) followed by sequences of 8–24 short echolocation calls (14.5 ± 3.2 ms) (0 ± SD). All the R. hipposideros nursery roosts were lo- Echolocation calls made during the exit from cated in the roof space of stone or brick buildings the hibernaculum showed similar sequences of near deciduous woods and the number of R. hippo- long (45.5 ± 8.8 ms) and short calls (18.9 ± 3.2 ms) sideros counted during exits ranged from 57 to 282 but there were no concomitant ultrasonic social (Table 5). The average temperature outside was 18.1 calls (Tables 3 and 4). Type E modified echoloca- ± 3.1°C (0 ± SD) and ranged from 8°C to 24.7°C, tion calls sounded like sliding trombone notes which did not affect the behaviour but rain during (Fig. 2I) or like a singer humming a scale (Fig. 2J four emergence surveys did reduce social behaviour and Table 4). The cascade of modified echolocation (Table 5). There was little or no wind during the sur- calls occurred before bats flew out of a roost and veys. Video recordings of R. hipposideros showed after they returned (Fig. 3A–C, 3E and Table 1). In that flight excursions took place at all sites when July (week 14) an unusual modified echolocation there was no rain during the emergence and that this call was observed with no interval between each call behaviour took place within enclosed space outside in the cascade and that sounded like a trill call the nursery roost wherever a suitable space existed. (Table 4). At sites 1–4, 7 and 10 storage areas within stone or 170 M. M. Andrews, A. M. Hodnett, and P. T. Andrews a location Nursery roosts 9 04º55’32.438’’W 51º37’38.015’’N 1 03º48’16.493’’W 53º14’02.003’’N 6 03º18’38.810’’W 53º06’49.121’’N 5 04º18’24.791’’W 53º04’22.821’’N Site P P P P Rain d Weather C ° n ) GMT Time 95 20.00 > 22.00 18.0 – 2 03º26’03.699’’W 53º17’51.122’’N 93 00.00 > 9.00 19.0 – 2 03º26’03.699’’W 53º17’51.122’’N 57 20.38 > 21.11 17.7 – 7 04º57’33.018’’W 51º39’12.130’’N 62 20.17 > 21.12 17.9 92 19.25 > 20.45 19.0 – 10 53°03’45.367”N 04°14’12.939”W 26 15.30 > 11.30 19.1 240 20.40 > 23.10 19.6 – 8 03º49’05.667’’W 53º11’07.135’’N 282 20.40 > 22.28 17.9 – 3 03º20’52.101’’W 53º13’45.144’’N 103 19.22 > 20.42 17.2 – 4 03º05’25.239’’W 52º56’05.491’’N (240) 12.30 > 13.30 24.7 – 8 03º49’05.667’’W 53º11’07.135’’N (282) 16.30 > 11.30 18.0 – 3 03º20’52.101’’W 53º13’45.144’’N Environmental temperature outside the roost at start of recording; Ex — flight excursions in the area outside roost d in North Wales, U.K. Wales, in North –––– 200 60 225 90 19.40 > 21.40 19.45 > 21.32 19.30 > 21.40 8.0 20.00 > 22.00 19.4 18.0 – – 19.1 – – 8 6 5 03º49’05.667’’W 53º11’07.135’’N 03º18’38.810’’W 53º06’49.121’’N 2 04º18’24.791’’W 53º04’22.821’’N 03º26’03.699’’W 53º17’51.122’’N – 128 20.00 > 21.30 18.3 – 9 04º55’32.438’’W 51º37’38.015’’N P a Baby calls Adults ( Fundamental frequency; c c – – – 55 (90) 20.30 > 21.30 19.2 – – 21 (101) 20.32 > 21.49 16.0 PP PP PP PP PP P PP P P PP P PP P P PP P PP P PP P PP P PP P PP P PP P Frequency (kHz) social activity at nursery roosts 50–57 15–49 Social activity at the roost, b b Social activity 5. Surveys of R. hipposideros Month/Year ABLE See text for locations or roosts; May 2015 Ex, Cl Jun 2015Jun 2010Jun 2010Jul 2010 Ex Ex Ex Ex Jul 2010 S T Jul 2015 Ex Jul 2014 Ex Jul 2015 – Aug 2016 Ex Aug 2016 SIR Aug 2016 S Aug 2016 Ex Aug 2016 Ex Aug 2016 Ex Aug 2016 Ex Aug 2016 S Sep 2016 S exit hole, Cl — cluster; SIR ( n ) — exit count within two weeks of recording social interaction inside the roost; S — calls, sound recording only no video; Number of bats a Social activity of lesser horseshoe bats at roosts 171 brick barns were used and at sites 5, 6 and 8 flight developed to form adult echolocation pulses in the excursions were made in passageways attached to 2nd harmonic (Konstantinov, 1973; Konstantinov et the roost buildings. At site 9 a gully between two al., 1990). roofs, each of which had a roost exit hole, was used. Our study identified adult R. hipposideros ultra- The only cluster of bats was observed at site 8 sonic social calls that were similar in frequency and in May 2015 but this behaviour could also take duration to adult R. ferrumequinum calls (Andrews place earlier in the nursery roost occupancy at other and Andrews, 2003; Andrews et al., 2006), although sites. additional modified echolocation calls were ob- Adult R. hipposideros echolocation calls, in served at 50–54 kHz. Rhinolophus ferrumequinum which the fundamental frequencies of FM-constant social calls share general characteristics with ves- frequency (CF)-FM calls were in the range of 55–57 pertilionid social calls. Andrews and Andrews kHz, were recorded at all sites surveyed. Sonograms (2016) and Pfalzer and Kusch (2003) proposed that of ultrasonic calls revealed that social calls, with social calls occurred independent of species and a fundamental frequency of 15–49 kHz, were made have common functions. Therefore, R. hipposide- by adult bats at all the R. hipposideros roosts except ros threat calls, interactive calls, individual recogni- at sites 1 and 9 when it rained and at site 7, which tion calls, advertisement calls or modified echoloca- was also occupied by Rhinolophus ferrumequinum. tion calls can identify social activities inside roosts. In July, after babies were born, sonograms of record- These calls confirmed a summer nursery roost ings made inside the nursery roost at site 2 or at the and a winter hibernaculum (Hodnett, 2011) and exit hole at site 3 showed that there were ultrasonic differentiated those roosts from transient night development calls made by non-volant infants roosts used extensively by R. hipposideros (Scho - (Table 3). In August juvenile R. hipposideros flew field, 1999). with the adult bats in the areas used for social behav- A trill advertisement call of R. hipposideros in iour; and infant modified echolocation calls (Table the hibernaculum was categorised as a cascade of 4) were recorded during emergence of juvenile modified echolocation calls fused together. This call R. hipposideros. Notably, at site 3 juvenile bats flew was similar to a rippled modulated-frequency sylla- around the area used for social behaviour for one ble call made by female R. ferrumequinum tragatus hour after the adults had flown off to forage in the during copulation (Liu, et al., 2013). The sequences nearby woods. of long and short echolocation calls, identified as male R. f. tragatus copulation calls by Liu et al. DISCUSSION (2013), observed in this study with advertisement trill calls and individual recognition calls, indicated Identification of Ultrasonic Calls in a Roost a mating roost. However, sequences of long and short echolocation calls were also observed in this The development calls of infant R. hipposideros study during the exit from the hibernaculum and in parallel the development calls of R. ferrumequinum a nursery roost without social calls so further study (Andrews et al., 2011). Infant polyharmonic isola- is needed to establish their use by R. hipposideros. tion calls recorded herein are similar to those identi- Echolocation can vary with species according to fied by Konstantinov (1973) and Konstantinov et al. age, sex and body size so differences in these signals (1990) as attraction calls of newborn R. hippo si - offer the potential for intraspecific communication deros infants and the 5th harmonic at 112–114 kHz (Jones, et al., 1994; Jones and Siemers, 2011). The is in the most sensitive range of the mother’s hear- short CF pulses and large FM sweeps in rhinplophid ing (Konstantinov, 1973). The development of FM echolocation calls provide maximum information sweeps in infant R. hipposideros calls observed in about the distance of an object in front of the bat our study were similar to calls made by 2-day old (Simmons, et al., 1979; Pye, 1980; Andrews, 1995a; infant Hipposideros speoris (Harbersetzer and Mari- Tupinier, 1996). Since the short CF calls were long- muthu, 1986) and 30-day old infants call fragments er than 10 ms in this study R. hipposideros were also were similar to modified echolocation calls identi- able to detect small changes in the bat approach fied in our study. Infant R. hipposideros echolocat- velocity (Simmons et al., 1979). The individual ing in the range of 105–108 kHz that were recorded recognition and advertisement calls recorded whilst in this study, were also observed by Konstantinov R. hipposideros made flight excursions outside the et al. (1990) in 10–20 day old infants. The nasal nursery roost in Conwy in May when there was signals made by 30 day old infant R. hipposideros a minimal difference in the light level, showed 172 M. M. Andrews, A. M. Hodnett, and P. T. Andrews that this was social activity and not light sampling sites except when it rained or if R. ferrumequinum behaviour proposed by Schofield (1996). Light were present. Gaisler (1963) observed that heavy sampling behaviour was defined as the R. hippo- rain shortened R. hipposideros flight activity outside si deros response to changes in the light during a nursery roost, which began at or up to 42 min after emerg ence and return when flight excursions dusk. Also automatic monitoring of R. hipposideros around the exit hole were observed (Schofield and (Andrews, 1995b) enabled comparison of emer- McAney, 2008). Rhinolophus hipposideros behav- gence rates, which showed that the exit was slower iour observed in this study was similar to R. ferrum- when it rained and individual bats dispersed to cover equinum behaviour outside a nursery roost, which in the nearby wood without delay (M.A., personal was social interaction (Andrews and Andrews, observation). Reduction or absence of a group of 2016). R. hipposideros leaving the nursery roost together affected their overall social behaviour because it Ultrasonic Calls and Conservation was not possible or useful for individuals to interact with others. Recordings of R. hipposideros infant calls pro- The emergence of R. ferrumequinum from the vide a means of identifying not only the presence of R. hipposideros nursery roost at site 7 was unusual a nursery roost but the dates at which births occurred since cohabitation is not typical (Schofield, 2008). and when infants began flying (Konstantinov, 1973; The occurrence of juvenile R. hipposideros echolo- Konstantinov et al., 1990). If R. hipposideros are cation calls during emergence showed that they seen flying outside a possible nursery roost or possi- were leaving the roost and the absence of adult ble hibernaculum then a static survey, including time R. hipposideros ultrasonic social calls may be due expansion recordings, in a covered area just outside to a non-advertisement strategy. At R. hipposideros the entrance could reveal social behaviour sufficient nursery roost sites where R. ferrumequinum have to warrant further investigation. Record ing periods moved in, the R. hipposideros population has col- would need to be at least 30 min in duration since lapsed or deserted the roost altogether (H. W. Scho- this study showed that there were only 19 ultrasonic field, personal communication). The surveys of ten social calls in a two-hour period in May. nursery roost sites have shown that adult R. hippo - The occurrence of R. hipposideros social calls in sideros ultrasonic social calls were not unique to the June and July would identify a nursery roost. In conditions at nursery roosts at sites 2 and 8 and that Europe R. hipposideros mating takes place from populations throughout Wales exhibited the same September to November (Ransome, 1991) so trill behaviour. advertisement calls recorded in October would con- The best time to look for new sites with ultra- firm a roost as a mating site. This study showed that sound recordings would be between May and July the ideal time for static pre-set extended periods of when the adult social calls then infant development monitoring would be from 20:00 h to 08:00 h GMT. calls could be recorded. Although juvenile modified Rhinolophus hipposideros roosts could be found by echolocation calls were recorded in this study in searching for external activity from May to October August and in early September they were the late near foraging sites in broadleaf woodlands (Bonta- stages of infant development. Rhinolophus hipposi - dina et al., 2002; Motte and Libois, 2002; Schofield deros fly in early August (Gaisler, 1963) and babies et al., 2002; Schofield, 2008). Monitoring of artifi- grow to full adult size in four weeks (McAney, cial roosts after construction is an essential part of 1991) so by September they echolocate at the same mitigation for the loss of natural R. hipposideros frequencies as adults and nursery roost populations roosts (Freer et al., 2002) and the installation of non in Pembrokeshire and Denbighshire start to disperse intrusive pre-set sound recording would be the best in September (Andrews, 1995b). option, especially in remote sites. Flight activity outside R. hipposideros nursery Conclusions roosts is characteristic of the species, which has been observed by Gaisler (1963), McAney and Pre-set extended infrared video and time expan- Fairley (1988), Schofield (1996) and Schofield and sion sound recordings of R. hipposideros revealed McAney (2008). Surveys of ten R. hipposideros that in June and July nursery roosts could be identi- nursery roosts made in this study showed that adult fied by infant development calls and adult ultrasonic ultrasonic social calls occurred during excursion social calls, in addition to echolocation calls in flight. flights outside the roost during emergence at all the In October hibernacula could also be identified by Social activity of lesser horseshoe bats at roosts 173 adult ultrasonic social calls. Comparison of call-trig- BONTANDINA, F., H. W. SCHOFIELD, and B. NAEF-DAENZER. 2002. gered sonogram times per hour enabled var iable Radio-tracking reveals that lesser horseshoe bats (Rhinolo - activity levels to be determined. Recordings made phus hipposideros) forage in woodland. Journal of Zoology (London), 258: 281–290. outside ten nursery roosts in Wales revealed that COLLINS, J. 2016. 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Associate Editor: Burton Lim