Do Bats Need Trees? Habitat Use of Two Mala- Gasy Hipposiderid Bats Triaenops Furculus and T

Hystrix It. J. Mamm. (n.s.) 22(1) 2011: 81-92

Pag. 80 disegno DO BATS NEED TREES? HABITAT USE OF TWO MALA- GASY HIPPOSIDERID BATS TRIAENOPS FURCULUS AND T. MENAMENA IN THE DRY SOUTHWEST

1†* 2 2 LAURA BAMBINI , AMYOT F. KOFOKY , TSIBARA MBOHOAHY , 2 3 MAHEFATIANA RALISATA , THEODORE MANJOAZY , DAVID J. 1 2,4 HOSKEN , RICHARD K.B. JENKINS

1Centre for Ecology and Conservation, University of Exeter in Cornwall, Tremough Cam- pus, TR10 9EZ, UK; †Current address: Mauritian Wildlife Foundation, Grannum Road, Vacoas, Mauritius; *Corresponding author, E-mail: [email protected] 2 Madagasikara Voakajy, B. P. 5181, Antananarivo (101), Madagascar 3 Département de Biologie, Faculté des Sciences, Université de Toliara, Toliara (601), Madagascar

4School of Biological Sciences, University of Aberdeen, Aberdeen, AB24 2TZ, UK

Received 25 August 2010; accepted 27 March 2011

ABSTRACT - Habitat degradation and loss threaten the survival of many bat species. Re- cent studies in Madagascar however have found some species are present in areas of low forest cover even though their echolocation calls and wing morphology suggest they are able to forage in forests. The present study investigated habitat use and prey selection in two sympatric hipposiderid bats, Triaenops furculus and T. menamena, in the dry southwest of Madagascar. The study colony occupied a cave in limestone karst surrounded by intact spiny bush and several secondary or degraded habitats. We used bat detectors and radiotracking to determine habitat use, and faecal analysis and invertebrate sampling to assess prey selection. Spiny bush, the dominant habitat type in the study area, was used less than predicted from its availability, based on satellite imagery and ground-based habitat mapping. Areas containing large trees were used by radiotracked bats in approximate proportion to their availability and acoustic sampling revealed highest bat activity in this habitat. The radio-tracked individuals used agricultural land more than expected from its availability. A significant difference was found in the proportion of Lepidoptera in the faeces of the two species, with T furculus showing a preference for moths. Triaenops furculus also selected Coleoptera, whereas T. menamena preferred mainly Hemiptera. While this study did not identify a strong association with forested habitats in T. furculus or T. menamena, it remains to be established whether the bats forage in a sub-optimal habitat due to their preference for roosting in the nearby karst caves.

Key words: habitat use, prey selection, hipposiderid bats, radiotracking, Madagascar

RIASSUNTO - I pipistrelli necessitano di alberi? Uso dello habitat di Triaenops furculus e T. menamena in ambienti secchi del Madagascar sud occidentale. Il degrado e la perdi- ta di habitat minacciano la sopravvivenza di molte specie di pipistrelli. Recenti studi in Madagascar hanno trovato che alcune specie sono presenti in aree con scarsa copertura forestale, anche se le loro ecolocalizzazioni e la loro morfologia alare suggeriscono che sono in grado di utilizzare i boschi per il foraggiamento. Nel presente studio sono esaminati

81 Bambini et al. l'uso dell’habitat e la selezione delle prede di due pipistrelli simpatrici, Triaenops furculus e T. menamena., in ambienti secchi del Madagascar sud occidentale. La colonia studiata occupava una grotta carsica calcarea, circondata da boscaglia spinosa intatta e diversi habitat secondari o degradati. Il bat detector e la tecnica del radio-tracking erano utilizzati per valutare l’uso dell’habitat, mentre la selezione delle prede era determinata sulla base dei dati ottenuti dall’analisi delle feci e dai campionamenti sulla disponibilità di invertebrati. Le zone con cespugli spinosi bassi (< 2 m), habitat dominante nell'area di studio, erano sottoutilizzate rispetto alla loro disponibilità. Le aree con grandi alberi erano usate dai pipistrelli radiomarcati approssimativamente in proporzione alla loro disponibilità, mentre i rilevamenti delle ecolocalizzazioni evidenziavano una più elevata attività in questo ambiente. I pipistrelli radiomarcati utilizzavano l’ambiente agricolo in proporzione maggiore alla sua disponibilità. Il consumo di Lepidotteri differiva tra le due specie, con T. furculus che mostrava preferenza per le tarme. T. furculus selezionava anche i Coleotteri, T. menamena preferiva principalmente gli Emitteri. Anche se questo studio non ha evidenziato una marcata associazione tra le due specie di pipistrelli e gli habitat forestali, resta da stabilire se entrambe foraggiano in habitat sub-ottimali a causa della vicinanza di grotte carsiche utilizzate come roost.

Parole chiave: uso dell’habitat, selezione delle prede, pipistrelli ipposideridi, radiotracking, Madagascar

DOI: 10.4404/Hystrix-22.1-4467

INTRODUCTION ties for conservation action (Scott et al. 2006). Deforestation has been identified as The southern dry forests of Madagascar one of the biggest threats to global have been identified as high priority biodiversity (Brooks et al. 2002; Se- areas for conservation, although it is abloom et al. 2002; Gaston et al. 2003). feared that for many animal popula- Biodiversity hotspots, areas of great tions this may come too late as many species diversity and richness with ecosystems have degraded beyond the often high levels of endemism, tend to possibility of recovery (Seddon et al. coincide with poverty and anthropo- 2000; Ganzhorn et al. 2001). The im- genic pressure on natural resources pact of forest degradation on bats in (Fisher and Christopher 2007). Mada- Madagascar is poorly understood; some gascar, one of the hottest hotspots for authors have suggested a low depend- biodiversity, is no exception (Ganzhorn ence on intact forest (Goodman et al. 2001). Although estimates vary, at least 2005), but there is evidence that cer- 40% and perhaps even over 80% of the tain species require forested habitats to original forest cover has been lost (Du forage (Randrianandriananina et al. Puy and Moat 1998; Harper et al. 2007; 2006; Kofoky et al. 2007). Randrianan- Hanski et al. 2007). In order to mitigate driaina et al. (2006) also found that the impacts of deforestation on biodi- even though taxon richness was great- versity, it is important to identify spe- est in forest habitats (in eastern Mada- cies that are most susceptible and to gascar), bat activity was highest in determine those that should be priori- plantations and on agricultural land.

82 Bambini et al. Malagasy hipposiderid bats l'uso dell’habitat e la selezione delle prede di due pipistrelli simpatrici, Triaenops furculus e Bat species richness varies regionally and Russ 2001), and could therefore be T. menamena., in ambienti secchi del Madagascar sud occidentale. La colonia studiata in Madagascar, with the highest num- expected to fly close to vegetation. occupava una grotta carsica calcarea, circondata da boscaglia spinosa intatta e diversi ber of species reported from the dry Kofoky et al. (2007) found T. mena- habitat secondari o degradati. Il bat detector e la tecnica del radio-tracking erano utilizzati region of the western domain rather mena foraging close to forest edges, per valutare l’uso dell’habitat, mentre la selezione delle prede era determinata sulla base dei than from the humid east (Bayliss and and in clearings. Surveys carried out in dati ottenuti dall’analisi delle feci e dai campionamenti sulla disponibilità di invertebrati. Le zone con cespugli spinosi bassi (< 2 m), habitat dominante nell'area di studio, erano Hayes 1999; Goodman 1999; Goodman the dry regions of Madagascar found T. sottoutilizzate rispetto alla loro disponibilità. Le aree con grandi alberi erano usate dai et al. 2005; Randrianandriananina et al. furculus and T. menamena roosting in pipistrelli radiomarcati approssimativamente in proporzione alla loro disponibilità, mentre i 2006). This is possibly because of the caves in areas without extensive forma- rilevamenti delle ecolocalizzazioni evidenziavano una più elevata attività in questo greater availability of roosting sites tions of intact forest and this led to the ambiente. I pipistrelli radiomarcati utilizzavano l’ambiente agricolo in proporzione associated with the limestone karst suggestion that neither species is forest maggiore alla sua disponibilità. Il consumo di Lepidotteri differiva tra le due specie, con T. regions of the west (Eger and Mitchell dependant (Goodman et al. 2005). furculus che mostrava preferenza per le tarme. T. furculus selezionava anche i Coleotteri, T. 2003; Goodman et al. 2005). Another The aim of the present study was to menamena preferiva principalmente gli Emitteri. Anche se questo studio non ha evidenziato suggested reason is that the availability investigate the habitat use and preferred una marcata associazione tra le due specie di pipistrelli e gli habitat forestali, resta da of insect prey may be greater in the dry prey of T. furculus and T. menamena, stabilire se entrambe foraggiano in habitat sub-ottimali a causa della vicinanza di grotte in an attempt to identify some of the carsiche utilizzate come roost. forests and spiny bush than in the eastern humid forests (Eger and Mitchell conservation needs of these species in Parole chiave: uso dell’habitat, selezione delle prede, pipistrelli ipposideridi, radiotracking, 2003). the dry southwest of Madagascar. Madagascar Three insectivorous species in the ge- nus Triaenops (Hipposideridae) have STUDY AREA DOI: 10.4404/Hystrix-22.1-4467 been described from Madagascar: T. auritus, T. furculus and T. menamena This study was conducted over two periods INTRODUCTION ties for conservation action (Scott et al. (previously T. rufus) (Peterson et al. in the field (six weeks in April-May and 2006). 1995; Goodman and Ranivo 2009). five weeks in June-July 2006) in and The southern dry forests of Madagascar Triaenops auritus is limited to the around the village of St Augustin (S23˚34’ Deforestation has been identified as E43˚46’) in the Toliara province of south- one of the biggest threats to global have been identified as high priority northernmost part of Madagascar areas for conservation, although it is whilst T. furculus occurs in the west western Madagascar. The study area ex- biodiversity (Brooks et al. 2002; Se- periences a dry, tropical climate with most abloom et al. 2002; Gaston et al. 2003). feared that for many animal popula- and south west. Triaenops menamena rain falling between December and March Biodiversity hotspots, areas of great tions this may come too late as many is more widely distributed, occurring and an average daily temperature of 20-25 species diversity and richness with ecosystems have degraded beyond the throughout the west and into the humid ˚C during the austral winter (May- often high levels of endemism, tend to possibility of recovery (Seddon et al. regions of the northeast (Peterson et al. September). St. Augustin lies on the edge coincide with poverty and anthropo- 2000; Ganzhorn et al. 2001). The im- 1995; Bennett and Russ 2001; Good- of the deciduous, dry southern forest and pact of forest degradation on bats in man et al. 2005). The precise habitat scrubland. This vegetation type encom- genic pressure on natural resources 2 (Fisher and Christopher 2007). Mada- Madagascar is poorly understood; some requirements for many Malagasy bat passes over 100000 km , retains substantial gascar, one of the hottest hotspots for authors have suggested a low depend- species are poorly understood, however primary vegetation cover, and is poorly protected (Du Puy and Moat 1998). The biodiversity, is no exception (Ganzhorn ence on intact forest (Goodman et al. wing morphology and the characteristic 2 study was limited to a 3 km area with the 2001). Although estimates vary, at least 2005), but there is evidence that cer- echolocation calls can provide an indi- cation to the structure of the preferred day roost located in a limestone cave at its 40% and perhaps even over 80% of the tain species require forested habitats to centre. Of this, dry forest and scrub (‘spiny original forest cover has been lost (Du forage (Randrianandriananina et al. habitat and prey types (Barclay 1986; bush’) with a canopy height of < 2 m was Puy and Moat 1998; Harper et al. 2007; 2006; Kofoky et al. 2007). Randrianan- Jones 1990; Norberg 1998). Triaenops the dominant habitat type, encompassing Hanski et al. 2007). In order to mitigate driaina et al. (2006) also found that bats have a relatively low aspect ratio approximately 65% of the surface area. the impacts of deforestation on biodi- even though taxon richness was great- and wing-loading (Peterson et al. Other prominent habitats were ‘mangroves’ versity, it is important to identify spe- est in forest habitats (in eastern Mada- 1995), and emit low energy frequency (5%), a riparian zone (8%) mostly compris- cies that are most susceptible and to gascar), bat activity was highest in modulated (FM) calls with maximum ing of, and here grouped together under, determine those that should be priori- plantations and on agricultural land. amplitude at around 100 kHz (Bennett ‘agricultural land’ (5%) dominated by rice

83 Bambini et al. paddies, and ‘forest’ habitat (7%) contain- bats were commonly observed foraging at ing taller trees that form a non-continuous the height of 3-5 metres, but it was not canopy > 3 m high, found on the edge of possible to suspend the traps at such a the limestone karst formation and in the height due to the lack of suitable trees and valleys. The remaining area comprised of the difficulty in securing tall poles in the bare sand (5%) and the ‘village’ itself hard substrate. Instead, the hem of the trap (10%). Extent of each habitat was assessed was set at a height of one metre, and the using satellite imagery (Google Earth, trap was deployed from 18.00 to 23.00 h in ©DigitalGlobe, Terrametrics, Google) and the vicinity of each acoustic recording ground-based habitat mapping. The village point. The invertebrates were stored in 70% of St. Augustin has a dense concentration ethanol and later identified to the level of of simple dwellings and a few outlying order using Scholtz and Holm (1985) and houses; there is very little vegetation in the Chinery (1993). One-way ANOVA was village itself, apart from some fruit trees. used to compare numbers of insects caught The study area experiences continuous, low between the two collecting periods, and level anthropogenic impact in the form of from the different habitat types. fire-wood gathering and goat grazing, and The number and duration of Triaenops all of the natural habitat can be described as calls was later noted from each recording, moderately degraded. and an attempt was made to differentiate between T. furculus and T. menamena calls METHODS by measuring the frequency of maximum amplitude, using BatSound v 3.1 software Bat activity in the different habitat types (Petterson Elektronik AB, Uppsala, Swe- was measured using acoustic recording den). In Madagascar, the call frequencies of stations. Over a total of 42 nights of re- Triaenops spp. overlap, and there appears cording, 14 recordings (each consisting of to be some regional variation. For this five 15 minute blocks) were made in the reason, calls were recorded from known ‘spiny bush’ habitat; 14 recording were individuals to determine the parameters for made in the ‘forest’ habitat, as this type of identifying the species: T. furculus fre- habitat was scattered around the study area quency of maximum amplitude (FMA) in small disconnected patches. Six to seven 100.2 ± 0.2 kHz (n = 18), T. menamena recordings were made in each of the other FMA 95.8 ± 0.1 kHz (n = 21). An attempt habitats (mangroves, n = 6; village, n = 6; was made to separate the frequency divi- agriculture, n = 7). No recordings were sion Triaenops calls recorded at the acous- made in the ‘bare sand’ habitat, as no bats tic sampling sites into T. furculus and T. were observed foraging in this habitat dur- menamena so that those with a FMA at or ing reconnaissance walks conducted carry- below 97 kHz were identified as T. mena- ing a bat detector. Bat calls were recorded mena calls, and those above as T. furculus. onto a minidisk (Sony Minidisk, Tokyo, A total of 71 randomly selected calls were Japan) in 15 minute blocks, hourly between thus analysed. Count data on Triaenops 18.00 and 22.15 hours using a Batbox Duet passes, determined as a distinct sequence of (Stag Electronics, UK) heterodyne and calls, were used to investigate habitat pref- frequency division bat detector set on the erences of the bats. As the data were not frequency of Triaenops calls (100 kHz) and normally distributed, the non-parametric secured onto a pole, at a height of 1.5 m. In Kruskal-Wallis test was performed on the addition, aerial insects were caught simul- total number of Triaenops passes (recorded taneously to the acoustic sampling on 37 in each type of habitat), using habitat as a occasions, using a Malaise trap. Triaenops factor. The resulting H statistic was ad-

84 Bambini et al. Malagasy hipposiderid bats paddies, and ‘forest’ habitat (7%) contain- bats were commonly observed foraging at justed for ties to account for the large num- strength of the signal, or where two observ- ing taller trees that form a non-continuous the height of 3-5 metres, but it was not ber of zero values. A linear regression ers were present, by using standard triangu- canopy > 3 m high, found on the edge of possible to suspend the traps at such a model was used to determine whether there lation techniques (White and Garrott 1990). the limestone karst formation and in the height due to the lack of suitable trees and was a correlation between the number To record the locations, eTrex Venture® valleys. The remaining area comprised of the difficulty in securing tall poles in the (abundance) of insects caught and that of GPS device (Garmin Ltd., Hampshire, UK) bare sand (5%) and the ‘village’ itself hard substrate. Instead, the hem of the trap bat passes recorded. An ANOVA was used was used. The observed animal locations (10%). Extent of each habitat was assessed was set at a height of one metre, and the to determine the significance of the model were then assigned to different habitat using satellite imagery (Google Earth, trap was deployed from 18.00 to 23.00 h in findings. categories (see above), using satellite im- ©DigitalGlobe, Terrametrics, Google) and the vicinity of each acoustic recording In order to obtain individuals for radio- agery (Google Earth, ©DigitalGlobe, Ter- ground-based habitat mapping. The village point. The invertebrates were stored in 70% tracking, a 6-metre mist net was deployed rametrics, Google) and ground-based habi- of St. Augustin has a dense concentration ethanol and later identified to the level of at the entrance to the cave on nine separate tat mapping carried out in the field. Chi- of simple dwellings and a few outlying order using Scholtz and Holm (1985) and occasions between April and July 2006. square test was used to compare observed houses; there is very little vegetation in the Chinery (1993). One-way ANOVA was The cave had two entrances, the larger one animal locations with expected ones based village itself, apart from some fruit trees. used to compare numbers of insects caught 2.5 m high and 4 m wide, and the smaller on proportional availability of each habitat The study area experiences continuous, low between the two collecting periods, and one as high but only 2 m wide. The interior type. level anthropogenic impact in the form of from the different habitat types. of the cave consisted of a large hall around Faecal pellets were collected from caught fire-wood gathering and goat grazing, and The number and duration of Triaenops 4-5 m high and 6x4 m in area; at one end of bats held in cotton bags. The pellets were all of the natural habitat can be described as calls was later noted from each recording, the cave, at a height of 2 m, was a small placed in sample vials filled with ethanol moderately degraded. and an attempt was made to differentiate opening leading to the main roosting area. 90% and stored for later analysis. A total of between T. furculus and T. menamena calls The bats presumably roosted deep inside 200 faecal pellets, collected from 10 indi- METHODS by measuring the frequency of maximum this cavity, as no signal was received from viduals from each species (T. furculus and amplitude, using BatSound v 3.1 software the transmitters once the bats had entered T. menamena) were analysed for dietary composition. The arthropod fragments Bat activity in the different habitat types (Petterson Elektronik AB, Uppsala, Swe- inside. Outside the cavity, a large mound of were identified to the level of order with was measured using acoustic recording den). In Madagascar, the call frequencies of guano had been deposited, suggesting ei- the aid of several identification guides stations. Over a total of 42 nights of re- Triaenops spp. overlap, and there appears ther that the roost had been in use for a (Scholtz and Holm 1985; Delvare and cording, 14 recordings (each consisting of to be some regional variation. For this long time, or that it once contained many Aberlenc 1989; Shiel et al. 1997; Rana- five 15 minute blocks) were made in the reason, calls were recorded from known more bats. The total number of bats in this ivoson and Andrianaivoarivelo 2004). ‘spiny bush’ habitat; 14 recording were individuals to determine the parameters for roost was estimated to be 200-250 indi- The dietary preference of the bats was made in the ‘forest’ habitat, as this type of identifying the species: T. furculus fre- viduals; in addition to Triaenops furculus assessed using Ivlev’s electivity index (E ). habitat was scattered around the study area quency of maximum amplitude (FMA) and T. menamena, Myotis gleni and M. i This gives a measure of the level of prefer- in small disconnected patches. Six to seven 100.2 ± 0.2 kHz (n = 18), T. menamena manavi were captured in the mist net. In ence or avoidance the bats are showing for recordings were made in each of the other FMA 95.8 ± 0.1 kHz (n = 21). An attempt total, nine male and two female T. furculus each insect order consumed, and was calcu- habitats (mangroves, n = 6; village, n = 6; was made to separate the frequency divi- were fitted with LB-2N transmitters for lated using the formula: agriculture, n = 7). No recordings were sion Triaenops calls recorded at the acous- bats (Holohil Systems Ltd., Ontario, Can- made in the ‘bare sand’ habitat, as no bats tic sampling sites into T. furculus and T. ada) with a battery-life of 12 days. The were observed foraging in this habitat dur- menamena so that those with a FMA at or transmitters were attached between the r n shoulder blades of the bats using skin-bond i i ing reconnaissance walks conducted carry- below 97 kHz were identified as T. mena- E  mena calls, and those above as T. furculus. (Torbot Bonding Cement, Torbot Group i  ing a bat detector. Bat calls were recorded ri ni A total of 71 randomly selected calls were Inc., Cranston (RI), USA). The weight of onto a minidisk (Sony Minidisk, Tokyo, thus analysed. Count data on Triaenops the transmitter (0.37 g) did not exceed 5% Japan) in 15 minute blocks, hourly between where r = percentage of order i in the diet, 18.00 and 22.15 hours using a Batbox Duet passes, determined as a distinct sequence of of the body weight of the animals, each of i and n = percentage of order i in the envi- (Stag Electronics, UK) heterodyne and calls, were used to investigate habitat pref- them weighing 7.5 g or more. The tagged i ronment. This measure (E ) takes a value frequency division bat detector set on the erences of the bats. As the data were not individuals were tracked from emergence i ranging from -1 (strong avoidance) through frequency of Triaenops calls (100 kHz) and normally distributed, the non-parametric to when they returned to roost, or were lost, to +1 (strong preference) (Krebs 1989). secured onto a pole, at a height of 1.5 m. In Kruskal-Wallis test was performed on the each night while the battery on the trans- The Mann-Whitney test was used to assess addition, aerial insects were caught simul- total number of Triaenops passes (recorded mitters lasted. Location of the tracked ani- whether the diets of the two species dif- taneously to the acoustic sampling on 37 in each type of habitat), using habitat as a mal was determined either by estimating fered significantly. occasions, using a Malaise trap. Triaenops factor. The resulting H statistic was ad- direction and distance to observer from the

85 Bambini et al.

RESULTS searches conducted in the surrounding area did not reveal additional roosting A total of 515 Triaenops calls were sites. Of the recorded bat locations, 10 recorded across the 47 recording sta- were on a boundary between two habi- tions over 42 nights. Separating the tat types, and were therefore excluded calls into T. furculus and T. menamena from the analysis. When all data were was not possible in 40% of cases; of grouped together, a chi-square test the 71 calls downloaded for analysis, revealed that the bat locations differed only 42 were identified as belonging to significantly from expected (X2 = one or the other species. Of the 42 264.86, p < 0.001, df = 93). Tracked identified calls, 30 belonged to T. fur- bats were located in the spiny bush less culus, and were recorded in all sampled frequently than expected, more loca- habitats. Triaenops menamena calls (n tions were recorded in agricultural ar- = 12) were only recorded in habitats eas than expected,and visits to forest containing trees, or in the mangroves. habitats were recorded approximately In the statistical analysis, all calls were corresponding to availability (Tab. 1). grouped together. The majority (n = The maximum distance travelled by the 403) of all calls recorded came from bats from the roost was 1681 m and one station, located in a small clearing was recorded for one of the males; the surrounded by trees (‘forest’). Overall, other bats travelled to a distance of the stations located in ‘forest’ habitat 670-1486 m from the roost. (N = 14) had the highest number of The difference in numbers of insects calls recorded (90% of the total num- caught during the two collecting ber, or 57% if the station with most periods was not statistically significant recordings is excluded from the sam- (F = 2.85, df = 36, p = 0.100) and these ple). However, the Kruskal-Wallis test data were combined in subsequent revealed no significant difference in analyses. The number of insects caught number of bat passes recorded in dif- during the different nights of sampling ferent habitats (H = 8.31, p = 0.081 varied greatly (Fig. 1), and the (adjusted for ties), df = 4). No correla- difference in numbers collected from tion was found between insect abun- different habitat types was not dance and bat passes (r = 0.062, F = statistically significant (F = 1.073, df = 0.139, p = 0.223 df = 37). 36, p = 0.385). In over 60 nights of tracking, a total of The faecal analysis indicated that T. 104 data points were obtained on the furculus and T. menamena consume location of five of the 11 individuals insect prey mainly from the same three fitted with transmitters. The remaining orders (Coleoptera, Hemiptera and six bats were lost during the first night Lepidoptera). A significant difference of tracking, and never found again. It was found in the proportion of Lepi- was thought these individuals may have doptera in their diet, which was much switched to a different day roost, and higher in T. furculus (W = 134.5, df = despite nightly searches none of them 9, p = 0.028). Also, T. furculus was returned to the day roost cave while the found to consume prey from the order transmitters remained viable. Day-time Diptera which was absent in the faecal

86 Bambini et al. Malagasy hipposiderid bats

RESULTS searches conducted in the surrounding samples collected from T. menamena DISCUSSION area did not reveal additional roosting (Fig. 2). No differences were apparent A total of 515 Triaenops calls were sites. Of the recorded bat locations, 10 in the diet of males and females. The Radio tracking bats at St. Augustin in recorded across the 47 recording sta- were on a boundary between two habi- Ivlev’s electivity index based on the southern Madagascar proved to be dif- tions over 42 nights. Separating the tat types, and were therefore excluded percentage of each order in the diet and ficult and only 3 of the 11 individuals calls into T. furculus and T. menamena from the analysis. When all data were its availability in the environment sug- provided us with enough data to ana- was not possible in 40% of cases; of grouped together, a chi-square test gested that T. furculus strongly selected lyse. Notwithstanding the caveat of a the 71 calls downloaded for analysis, revealed that the bat locations differed for Coleoptera, whereas T. menamena small sample size, it appeared that the only 42 were identified as belonging to significantly from expected (X2 = showed high preference for Hemiptera bats spent little time in the dry bush one or the other species. Of the 42 264.86, p < 0.001, df = 93). Tracked (Tab. 2). habitat, despite it being the most com- identified calls, 30 belonged to T. fur- bats were located in the spiny bush less culus, and were recorded in all sampled frequently than expected, more loca- habitats. Triaenops menamena calls (n tions were recorded in agricultural ar- Table 1 - Proportional availability of the different habitat types in the study area, and ob- = 12) were only recorded in habitats eas than expected,and visits to forest served use by the radio-tracked individuals (proportion of total number of fixes recorded). containing trees, or in the mangroves. habitats were recorded approximately In the statistical analysis, all calls were corresponding to availability (Tab. 1). Habitat type Available Observed use grouped together. The majority (n = The maximum distance travelled by the Spiny bush 65.0 19.10 403) of all calls recorded came from bats from the roost was 1681 m and one station, located in a small clearing was recorded for one of the males; the Mangrove 5.00 0.00 surrounded by trees (‘forest’). Overall, other bats travelled to a distance of Agriculture 8.00 47.90 the stations located in ‘forest’ habitat 670-1486 m from the roost. (N = 14) had the highest number of The difference in numbers of insects Forest 7.00 6.40 calls recorded (90% of the total num- caught during the two collecting Sand 5.00 22.30 ber, or 57% if the station with most periods was not statistically significant Village 10.00 4.30 recordings is excluded from the sam- (F = 2.85, df = 36, p = 0.100) and these ple). However, the Kruskal-Wallis test data were combined in subsequent revealed no significant difference in analyses. The number of insects caught number of bat passes recorded in dif- during the different nights of sampling 140 ferent habitats (H = 8.31, p = 0.081 varied greatly (Fig. 1), and the 120 (adjusted for ties), df = 4). No correla- difference in numbers collected from tion was found between insect abun- different habitat types was not 100 dance and bat passes (r = 0.062, F = statistically significant (F = 1.073, df = 80 0.139, p = 0.223 df = 37). 36, p = 0.385). In over 60 nights of tracking, a total of The faecal analysis indicated that T. 60 104 data points were obtained on the furculus and T. menamena consume 40 location of five of the 11 individuals insect prey mainly from the same three Number of insects fitted with transmitters. The remaining orders (Coleoptera, Hemiptera and 20 six bats were lost during the first night Lepidoptera). A significant difference 0 of tracking, and never found again. It was found in the proportion of Lepi- Forest Spiny bush Mangrove Agriculture Village was thought these individuals may have doptera in their diet, which was much switched to a different day roost, and higher in T. furculus (W = 134.5, df = Figure 1 - Number of insects (± SE) caught over a total of 37 nights, using Malaise traps, in despite nightly searches none of them 9, p = 0.028). Also, T. furculus was different habitat types. returned to the day roost cave while the found to consume prey from the order transmitters remained viable. Day-time Diptera which was absent in the faecal

87 Bambini et al.

T. furculus T. menamena 80 70 % 60 50 40 30 20 10 0 Coleoptera Diptera Hemiptera Lepidoptera Other

Figure 2 - Mean percentage of insect fragments (± SE) by Order, found in a total of 200 faecal pellets analysed for prey items. ‘Other’ includes remains of Homoptera and Heterop- tera. Total number of fragments identified in T. furculus and T. menamena samples were 446 and 332, respectively.

Table 2 - Dietary selection by T. furculus and T. menamena, comparing prey consumption determined from faecal analysis on pellets collected from 20 individuals to prey availability, determined by invertebrate sampling over 37 nights of trapping. A high positive D value indicates strong selection for a prey order.

Ivlev’s electivity index (D) Insect Order T. furculus T. menamena Coleoptera 0.836 0.187 Diptera -0.960 - Hemiptera 0.760 0.857 Lepidoptera 0.329 -0.026 mon vegetation type in the study T. furculus feeding in the spiny bush area,and areas of farmland were used habitat might be explained by the low disproportionately by the bats. Tri- availability of prey in these areas. Two aenops furculus has an echolocation of the tracked bats were found foraging and wing morphology typical of a bat in the spiny bush habitat each night of that is adapted to fly and forage in or tracking; two bats foraged almost ex- near vegetation. The low incidence of clusively in the agricultural and ripar-

88 Bambini et al. Malagasy hipposiderid bats

ian habitat, and visited areas with tall habitat, whereas T. menamena may trees on their way to and from their have a preference for habitats contain- T. furculus T. menamena foraging sites. Similarly, bats located in ing trees. However, the small sample 80 the bare sand habitats were commuting size makes this inconclusive. In addi- 70 from the roost to their foraging sites, tion to being flexible in the types of % 60 probably foraging opportunistically on habitat they use, Triaenops bats may the way; the high incidence of ‘fixes’ also be able to switch prey according to 50 recorded in this type of habitat can be seasonal changes in abundance. 40 explained by the fact that it was the Razakarivony et al. (2005) analysed common habitat in the vicinity of the stomach contents of T. menamena and 30 day roost. While no bats were observed found remains of insects from the or- 20 foraging in this habitat during the re- ders Isoptera, Hymenoptera, Coleoptera connaissance walks using bat detectors, and Lepidoptera. They suggest that 10 acoustic sampling of the ‘bare sand’ Isoptera may be a seasonally abundant 0 habitat in areas further away from the food source that the bats exploit oppor- Coleoptera Diptera Hemiptera Lepidoptera Other day roost and in areas not connected to tunistically (Razakarivony et al. 2005). known foraging habitats may have In the present study, comparison be- Figure 2 - Mean percentage of insect fragments (± SE) by Order, found in a total of 200 clarified whether or not the bats chose tween dietary compositions in the two faecal pellets analysed for prey items. ‘Other’ includes remains of Homoptera and Heterop- to forage in this habitat. species revealed a significant differ- tera. Total number of fragments identified in T. furculus and T. menamena samples were ence only in the proportion of Lepidop- 446 and 332, respectively. The apparent difference in foraging habitat selection between the tracked tera, which was higher in T. furculus. bats may reflect individual preference, Diptera were the most common order Table 2 - Dietary selection by T. furculus and T. menamena, comparing prey consumption or a difference in food availability, as found in the Malaise trap samples, and determined from faecal analysis on pellets collected from 20 individuals to prey availabil- the bats found foraging in the fields although both species seemed to avoid ity, determined by invertebrate sampling over 37 nights of trapping. A high positive D were tracked in June-July, during the it, T. furculus faecal pellets contained value indicates strong selection for a prey order. some remains of Diptera whereas these austral winter. Riparian zones are known for being an abundant food were completely absent in T. mena- Ivlev’s electivity index (D) Insect Order source for insectivorous bats, even in mena faeces. The apparent selection of T. furculus T. menamena disturbed habitats (Lloyd et al. 2006). Coleoptera by T. furculus may present a bias in the sampling method used for Coleoptera 0.836 0.187 However, insect abundance did not appear to fluctuate between the two the capture of invertebrates; further- Diptera -0.960 - periods in the field, although tempera- more, the hard chitinous remains of Hemiptera 0.760 0.857 tures were noticeably higher and more Coleoptera are better preserved and thunderstorms and heavy rain occurred easily identified in faecal samples. Lepidoptera 0.329 -0.026 during April-May. Based on the findings of the present In contrast, the acoustic sampling re- study, it appears that T. furculus con- sults did not reflect a preference for sumes prey from various different or- mon vegetation type in the study T. furculus feeding in the spiny bush agricultural or riparian habitats; highest ders, and is less selective in its choice area,and areas of farmland were used habitat might be explained by the low numbers of bat passes were recorded in of foraging habitat than T. menamena disproportionately by the bats. Tri- availability of prey in these areas. Two spiny bush and habitats containing tall which was observed only in habitats aenops furculus has an echolocation of the tracked bats were found foraging trees. Although the number of recorded containing trees and found selecting and wing morphology typical of a bat in the spiny bush habitat each night of calls that were assigned to each species prey mainly from the Order Hemiptera. that is adapted to fly and forage in or tracking; two bats foraged almost ex- was low, the results suggest that T. While the findings of the present study near vegetation. The low incidence of clusively in the agricultural and ripar- furculus is less selective of its foraging do not indicate a strong forest depend-

89 Bambini et al. ency in T. menamena or T. furculus, it support throughout the project. WWF remains unknown how the continuing Madagascar and the Mayor of Saint habitat degradation around the St Au- Augustin were kind to allow the field work gustin area will affect the long term to take place in the area surrounding the survival of the colony. Further, more village of Saint Augustin. This work was made possible by the generous support in-depth studies are required to estab- received from Bat Conservation Inter- lish the relative importance of the dif- national (LB), Conservation International, ferent habitat types to the bats. Often, the Darwin Initiative, The Rufford the impact of habitat degra-dation and Foundation (AK), and the School of loss on animals can only be detected Biosciences at University of Exeter (LB). after considerable time has elapsed We wish to thank Professor Paul Racey, Dr (Brooks et al. 1999; Ewers and Didham Nik Cole and Dr Nicolas Zuel, and two 2006). It is certain that soil erosion anonymous referees who provided helpful brought on by the grazing goats and comments. tree felling, as well as the overall degradation and loss of the spiny bush REFERENCES habitat will have a negative impact on Barclay R.M.R. 1986. The echolocation the diversity and abundance of wildlife, calls of hoary (Lasiurus cinereus) and as well as reduce the resource base silver-haired (Lasionycteris noctiva- available to the inhabitants of St Au- gans) bats as adaptations for long vs gustin. In order to mitigate the impact short-range foraging strategies and the of goat grazing, some areas would consequences for prey selection. Can. benefit from fencing to exclude the J. Zool 64: 2700-2705. goats. To obtain fuel wood from a sus- Bayliss J., Hayes B. 1999. The status and tainable source, and to reduce the de- distribution of bats, primates and but- sertification in the area surrounding the terflies from the Makira Plateau, Madagascar. Unpublished Report. village of St. Augustin, trees should be University of Aberdeen. planted around the surviving shrubbery. Bennett D., Russ J. (Eds.) 2001. The Bats Coppicing could be introduced to en- of Madagascar: A Field Guide with sure a continuous supply of wood. descriptions of echolocation calls. Vi- per Press, Glossop, UK. 96 pp. ACKNOWLEDGEMENTS Brooks T.M., Pimm S.L., Oyugi J.O. 1999. Time lag between and bird extinction in tropical forest fragments. Cons. We wish to thank the Ministère de Biol. 13: 1140-1150. l’Environnement, des Eaux et Forêts for Brooks T.M., Mittermeier R.A., Mitter- issuing permits to conduct this research. meier C.G., de Fonseca G.A.B., Ry- Daniel Rakotondravony (Département de lands A.B., Konstant W.R., Flick P., Biologie Animale, Université d’Antana- Pilgrim J., Oldfield S., Magin G., Hil- narivo), Anne Marie Randriatompoinarivo ton-Taylor C. 2002. Habitat loss and (Département des Sciences Biologiques, extinction in the hotspots of biodiver- Université de Toliara) and Félicitée Rejo- sity. Cons. Biol. 16(4): 909-923. Fienena (Direction Inter-Régionale de Chinery M. 1993. Insects of Britain & Toliara, Ministère de l’Environment, des Northern Europe. 3rd Edn. Harper Col- Eaux et Forêts) provided us with excellent lins Publishers, London.

90 Bambini et al. Malagasy hipposiderid bats ency in T. menamena or T. furculus, it support throughout the project. WWF Delvare G., Aberlenc H-P. 1989. Les in- Goodman S.M., Andriafidison D., Andri- remains unknown how the continuing Madagascar and the Mayor of Saint sectes d’Afrique et d’Amérique tropi- anaivoarivelo R., Cardiff S.G., Ifticene habitat degradation around the St Au- Augustin were kind to allow the field work cal - Clés pour la reconnaissance des E., Jenkins R.K.B., Kofoky A.F., gustin area will affect the long term to take place in the area surrounding the familles. PRIFAS/CIRAD, Montpel- Mbohoahy T., Rakotondravony D., lier, France. Ranivo J., Ratrimomanarivo F., survival of the colony. Further, more village of Saint Augustin. This work was made possible by the generous support Du Puy D.J., Moat J. 1998. 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