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The activity time of the lesser bamboo bat, Tylonycteris pachypus (Chiroptera: Vespertilionidae)

Li-Biao Zhang Fu-Min Wang Qi Liu Li Wei About the authors

Abstract

The activity time of the lesser bamboo bat, Tylonycteris pachypus (Temminck, 1840), was investigated at two observation locations in southern China: Longzhou and Guiping. Two bouts of activity (post dusk and predawn), with an intervening period of night roosting at diurnal roosts, were identified. The period of activity within each bout was usually less than 30 minutes. The activity periods of individuals belonging to the Longzhou population right after dusk and just before dawn lasted longer than those of the the Guiping population. We also found that the nocturnal emergence time of T. pachypus from the Longzhou population happened earlier than in the Guiping population. These findings indicate that the activity time of T. pachypus was quite short at night, and that different locations may affect the nocturnal activity rhythm of this species.

Activity period; emergence; return; Tylonycteris pachypus


Most bats are nocturnal, foraging at night and resting in roosts during the day. Between activity bouts, they also spend time in night roosts (Anthony & Kunz 1997Anthony ELP, Kunz TH (1997) Feeding strategies of the little brown bat, Myotis lucifugus, in southern New Hampshire. Ecology 58: 775-786. doi: 10.2307/1936213
https://doi.org/10.2307/1936213...
). The patterns of nocturnal activity vary dramatically among different species. O'Shea & Vaughan (1977O'Shea TJ, Vaughan TA (1977) Nocturnal and seasonal activities of the pallid bat, Antrozous pallidus. Journal of Mammalogy 58: 269-284. doi: 10.2307/1379326
https://doi.org/10.2307/1379326...
) have reported that the pallid bat Antrozous pallidus (Le Conte, 1856) utilizes two foraging periods with an intervention period of night roosting. Some other species, such as Euderma maculatum (J.A. Allen, 1891), spend the entire night flying and foraging (Wai-Ping & Fenton 1988Wai-Ping V, Fenton MB (1988) Ecology of spotted bat (Euderma maculatum): roosting and foraging behavior. Journal of Mammalogy 70: 617-622. doi: 10.2307/1381434
https://doi.org/10.2307/1381434...
). Likewise, the duration of bouts has also been found to be different. For instance, Eptesicus fuscus (Beauvois, 1796) spends only 2 hours flying each night (Brigham 1991Brigham RM (1991) Flexibility in foraging and roosting behavior by the big brown bat (Eptesicus fuscus). Canada Journal of Zoology 69: 117-121. doi: 10.1139/z91-017
https://doi.org/10.1139/z91-017...
), while Nacteris grandis spends even less time in this activity (Fenton et al. 1990Fenton MB, Swanepoel CM, Brigham RM, Cebek E, Hickey MB (1990) Foraging behavior and prey selection by large slit-faced bats (Nycteris grandis; Chiroptera: Nycteridae). Biotropica 22: 2-8. doi: 10.2307/2388713
https://doi.org/10.2307/2388713...
).

The timing and pattern of bat nocturnal activity may be influenced by environmental factors such as light levels (Lee & McCracken 2001Lee Y-F, McCracken GF (2001) Timing and variation in the emergence and return of Mecican free-tailed bat, Tadarida brasiliensis mexicana. Zoological Study 40: 309-316.), prey abundance (Erkert 1982Erkert HG (1982) Ecological aspects of bat activity rhythms, p. 201-242. In: Kunz TH (Ed.). Ecology of bats. New York, Plenum Press. doi: 10.1007/978-1-4613-3421-7-5
https://doi.org/10.1007/978-1-4613-3421-...
), temperature (Catto et al. 1995Catto CMC, Racey PA, Stephenson PJ (1995) Activity patterns of the serotine bat (Eptesicus serotinus) at a roost in southern England. Journal of Zoology (London) 235: 635-644. doi: 10.1111/j.1469-7998.1995.tb01774.x
https://doi.org/10.1111/j.1469-7998.1995...
), cloud (Kunz & Anthony 1996Kunz TH, Anthony ELP (1996) Variation in the timing of nightly emergence behavior in the little brown bat, Myotis lucifugus (Chiroptera: Vespertilionidae), p. 225-235. In: Genoways HH, Baker RJ (Eds.). Contribution in Mammalogy: a memorial volume honoring Dr. J. Knox. Lubbock, The Museum of Texas Tech University, 315p.) and rain (Mcaney & Fairley 1988Mcaney CM, Fairley JS (1988) Activity patterns of the lesser horseshoe bat Rhinolophus hipposideros at summer roosts. Journal of Zoology (London) 216: 325-338. doi: 10.1111/j.1469-7998.1988.tb02433.x
https://doi.org/10.1111/j.1469-7998.1988...
). Moreover, intrinsic biological factors such as predation risk (McWilliam 1989McWilliam AM (1989) Emergence behavior of the bat Tadarida (Chaerephon) pumila (Chiroptera: Molossidae) in Ghana, West Africa. Journal of Zoology (London) 219: 698-701. doi: 10.1111/j.1469-7998.1989.tb02615.x
https://doi.org/10.1111/j.1469-7998.1989...
, Speakman 1991Speakman JR (1991) Why do insectivorous bats in Britain not fly in daylight more frequently? Functional Ecology 5: 518-524. doi: 10.2307/2389634
https://doi.org/10.2307/2389634...
), colony size, age, sex, the reproductive status of individuals (Avery 1986Avery MI (1986) Factors affecting the emergence times of Pipistrelle bats. Journal of Zoology (London) 209: 293-296. doi: 10.1111/j.1469-7998.1986.tb03589.x
https://doi.org/10.1111/j.1469-7998.1986...
, Rydell 1989Rydell J (1989) Feeding activity of the northern bat Eptesicus nilssoni during pregnancy and lactation. Oecologica 80: 562-565. doi: 10.1007/BF00380082
https://doi.org/10.1007/BF00380082...
, Korine et al. 1994Korine C, Izhaki I, Makiin D (1994) Population structure and emergence order in the fruit-bat (Rousettus aegyptiacus: Mammalia, Chiroptera). Journal of Zoology (London) 232: 163-174. doi: 10.1111/j.1469-7998.1994.tb01566.x
https://doi.org/10.1111/j.1469-7998.1994...
, Clark et al. 2002Clark BS, Clark BK, Lesie Jr DM (2002) Seasonal variation in activity patterns of the endangered Ozark big-eared bat (Corynorhinus townsendii ingens). Journal of Mammalogy 83: 590-598. doi: 10.1644/1545-1542
https://doi.org/10.1644/1545-1542...
, O'Donnell 2002O'Donnell CFJ (2002) Influence of sex and reproductive status on nocturnal activity of long-tailed bats (Chalinolobus tuberculatus). Journal of Mammalogy 83: 794-803. doi: 10.1644/1545-1542
https://doi.org/10.1644/1545-1542...
), and interspecific competition (Swift & Racey 1983Swift SM, Racey PA (1983) Resource partitioning in two species of vespertilionid bats (Chiroptera) occupying the same roost. Journal of Zoology (London) 200: 249-2593. doi: 10.1111/j.1469-7998.1983.tb05787.x
https://doi.org/10.1111/j.1469-7998.1983...
, Bonaccorso et al. 2006Bonaccorso FJ, Winkelmann JR, Shin D, Agrawal CI, Aslami N, Bonney C, Hsu A, Jekielek PE, Knox AK, Kopach SJ, Jennings TD, Lasky JR, Menesale SA, Richards JH, Rutland JA, Sessa AK, Zhaurova L, Kunz TH (2006) Evidence for exploitative competition: comparative foraging behavior and roosting ecology of short-tailed fruit bats (Phyllostomidae). Biotropica 39: 249-256. doi: 10.1111/j.1744-7429.2006.00251.x
https://doi.org/10.1111/j.1744-7429.2006...
) may also impact the nocturnal activity of bats. The intensity of competition between or among sympatric related species is expected to be greater because they are morphologically similar, which is assumed to reflect niche similarity (Findley & Black 1983Findley JS, Black H (1983) Morphological and dietary structuring of a Zambian insectivorous bat community. Ecology 64: 625-630. doi: 10.2307/1937180
https://doi.org/10.2307/1937180...
, Aldridge & Rautenbach 1987Aldridge HDJN, Rautenbach IL (1987) Morphology, echolocation and resource partitioning in insectivorous bats. Journal of Animal Ecology 56: 763-778. doi: 10.2307/4947.
https://doi.org/10.2307/4947....
, Arita 1997Arita E (1997) Species composition and morphological structure of the bat fauna of Yucatan, Mexico. Journal of Animal Ecology 66: 83-97. doi: 10.2307/5967
https://doi.org/10.2307/5967...
). When common resources are limited, the niche theory predicts that resource partitioning (such as spatial and temporal niche) is necessary for species to coexist within a guild. They may forage in different habitats (Arlettaz 1999Arlettaz R (1999) Habitat selection as a major resource partitioning mechanism between the two sympatric sibling bat species Myotis myotis and Myotis blythii. Journal of Animal Ecology 68: 460-471. doi: 10.1046/j.1365-2656.1999.00293.x
https://doi.org/10.1046/j.1365-2656.1999...
) and then feed on different diet items (Arlettaz et al. 1997Arlettaz R, Perrin N, Hausser J (1997) Trophic resource partitioning and competition between the two sibling bat species Myotis myotis and Myotis blythii. Journal of Animal Ecology 66: 897-991. doi: 10.2307/6005
https://doi.org/10.2307/6005...
), or forage during different times (Bonaccorso et al. 2006Bonaccorso FJ, Winkelmann JR, Shin D, Agrawal CI, Aslami N, Bonney C, Hsu A, Jekielek PE, Knox AK, Kopach SJ, Jennings TD, Lasky JR, Menesale SA, Richards JH, Rutland JA, Sessa AK, Zhaurova L, Kunz TH (2006) Evidence for exploitative competition: comparative foraging behavior and roosting ecology of short-tailed fruit bats (Phyllostomidae). Biotropica 39: 249-256. doi: 10.1111/j.1744-7429.2006.00251.x
https://doi.org/10.1111/j.1744-7429.2006...
). In contrast, when their shared resources are not limited, species may forage concomitantly and for longer periods.

The lesser bamboo bat, Tylonycteris pachypus (Temminck, 1840) (Chiroptera: Vespertilionidae), and its sibling species, Tylonycteris robustula Thomas, 1915, are genetically closely related. The two species have similar morphological features (Medway & Marshall 1978Medway L, Marshall AG (1978) Roost-site selection among flat-headed bats (Tylonycteris spp.). Journal of Zoology (London) 161: 237-245. doi: 10.1111/j.1469-7998.1970.tb02038.x
https://doi.org/10.1111/j.1469-7998.1970...
). According to our field observations, which have been published in another contribution, the two species rarely roost together in the same internode, although they overlap in distribution. Also, they can alternate their use of the same internodes at different times or seasons (Zhang et al. 2004Zhang L-B, Liang B, Zhou S-Y, Lu L-R, Zhang S-Y (2004) Group structure of lesser flat-headed bat Tylonycteris pachypus and greater flat-headed bat T. robustula. Acta Zoology Sinica 50: 326-333.) and forage on similar categories of insects that occur sympatrically (Zhang et al. 2005aZhang L-B, Jones G, Rossiter S, Ades G, Liang B, Zhang S-Y (2005a) Diet of flat-headed bats, Tylonycteris pachypus and T. robustula, in Guangxi, South China. Journal of Mammalogy 86: 61-66. doi: 10.1644/1545-1542
https://doi.org/10.1644/1545-1542...
).

The nocturnal activity rhythm of T. pachypus and T. robustula is still poorly known. In the present study we investigated the activity time (emergence time and foraging duration) of the lesser bamboo bat, T. pachypus, in two populations inhabiting Longzhou and Guiping Counties, Guangxi, south China, approximately 250 km apart from each other. T. pachypus is sympatric with T. robustula in Longzhou County, but occurs alone in Guiping County.

MATERIAL AND METHODS

The study was carried out from March to November, in 2008 in Guangxi Province, south China. Two locations (Longzhou County, 21°10'N, 106°50'E, 116 m in elevation, and Guiping County, 23°09'N, 110°10'E, 68 m in elevation) were selected. Zhang et al. (2005aZhang L-B, Jones G, Rossiter S, Ades G, Liang B, Zhang S-Y (2005a) Diet of flat-headed bats, Tylonycteris pachypus and T. robustula, in Guangxi, South China. Journal of Mammalogy 86: 61-66. doi: 10.1644/1545-1542
https://doi.org/10.1644/1545-1542...
) had previously described the climate and vegetation of Longzhou County as having average annual temperature of 22.8°C and average annual precipitation of 1,180 mm (Fang 1995Fang WZ (1995) Natural resource of Guangxi, China. Beijing, China Environment Science Press, 369p.). Guiping County has a similar climate but the habitat is hilly rather than the typical karst of Longzhou County, with average annual temperature of 21.4°C and average annual precipitation of 1,727 mm (Fang 1995Fang WZ (1995) Natural resource of Guangxi, China. Beijing, China Environment Science Press, 369p.). Within both study areas, the bamboo, Bambusa spinosa Roxb, is abundant. This plant has enough internodes to provide enough suitable roost sites for both bat species. During data collection, T. pachypus and T. robustula were never found in the same roost at the same time, except on one occasion, when a single T. pachypus male and a single T. robustula male roosted in the same internode. In Longzhou County, bamboo is found in and around villages, while in Guiping County it is distributed along streams in areas that are somewhat far from villages.

Nocturnal observations were conducted from dusk to the next morning. Observers were split into two groups (two persons per group) and each group observed the activity time of T. pachypus in the two locations, at the same time. Normally, bamboo bats are faithful to their bamboo internodes for a short period (Zhang et al. 2004Zhang L-B, Liang B, Zhou S-Y, Lu L-R, Zhang S-Y (2004) Group structure of lesser flat-headed bat Tylonycteris pachypus and greater flat-headed bat T. robustula. Acta Zoology Sinica 50: 326-333.), which allowed us to continuously observe groups in the same internode from dusk to dawn. We selected a fixed bamboo forest in each location to conduct our observations. The bamboo bat colony in each forest had more than two hundred individuals. We swapped among different bamboo internodes on different days during the same month, and the size of the group in each of these internodes was normally over eight bats. In each location, the time of emergence and returning were recorded, respectively. Emergence time was defined as the time when the first bat individual flied out of its bamboo internode; the returning time was defined as the time when the first bat individual flied back into the bamboo roost, or attempted to do so. If no bat emerged from a bamboo internode after 20 minutes (confirmed by using a wire to check bat lairs), we terminated the observation on emergence time. Likewise, if no bat returned back to its bamboo internode we terminated the observation on returning time. The duration of activity was defined as the time period between emergence and returning, since it is difficult to observe the entire behavior of the bat after it flies out. Additionally, T. pachypus forages around or over their roost bamboo forest; for example, their foraging sites are nearby their roosts (Zhang et al. 2007Zhang L-B, Liang B, Jones G, Parsons S, Wei L, Zhang S-Y (2007) Morphology, echolocation and foraging behavior in two sympatric sibling species of bat (Tylonycteris pachypus and T. robustula) (Chiroptera: Vespertilionidae). Journal of Zoology (London) 271: 344-351. doi: 10.1111/j.1469-7998.2006.00210.x
https://doi.org/10.1111/j.1469-7998.2006...
). We also recorded air temperature at sunset and sunrise, and position of the roost site (via GPS, eTrex, Garmin Corp., Taiwan). The time of sunset and sunrise were read from a GPS. During the observation period, nocturnal observations were conducted for at least one week per month, normally in the middle of the month. Since T. pachypus is sympatric with T. robustula in Longzhou, we identified and confirmed the identify of T. pachypus using characteristics of its echolocation calls using a sound detector (D-980, Petterson Electronic AB, Uppsala) when individuals flied out or returned. This study was conducted according to the protocols approved by the Guangdong Entomological Institute Administrative Panel on Laboratory Animal Care.

A total of 75 night observations were conducted both in Longzhou and Guiping. When it was raining during the bat's normal activity period, the data of the corresponding night were omitted from both sites in the analysis. As a result, data on twelve night observations were discharged, and 63 night observations, one week per month, were analyzed. All data were tested for normality and homogeneity of variances using Kolmogorov-Smirnov test and Bartlett test. We conducted Independent-Samples t-test for comparisons of emergence time, returning time and duration of activity between the Longzhou and Guiping populations, respectively. Then for comparisons of monthly variations in activity duration, we used One-Way ANOVA. Regression was used to analyze activity time and local air temperature. All statistical analyses were performed in SPSS 17.0 for Windows. Descriptive data were expressed as Mean ± SD, and the significant difference at 95% confidence level was calculated by Central Limit Theorem.

RESULTS

Based on our observations, the lesser bamboo bat T. pachypus normally feeds in and around bamboos in the forests in which they roost, and fly to foraging sites directly from their roost. The activity time of T. pachypus individuals in the two populations was characterized by two distinct bouts, one immediately after dusk and the second just before dawn. The duration of the activity within each bout was usually less than 30 minutes. The dusk (23.7 ± 8.39 min) and predawn (27.9 ± 14.79 min) activity periods of T. pachypus individuals were significantly longer in Longzhou than in Guiping (dusk: 21.2 ± 8.09 min; predawn: 25.4 ± 14.43 min) (dusk: t = 2.374, p < 0.05; predawn: t = 2.857, p < 0.05) (Fig. 1). A strong positive correlation was also observed between activity duration and air temperature at dusk and predawn in the two populations, respectively (Longzhou: rdusk = 0.891, rpredawn = 0.904, respectively, both p < 0.001; Guiping: rdusk = 0.881, rpredawn = 0.837, both p < 0.001) (Figs. 2-3). In addition, we found that the durations of activity of T. pachypus varied significantly in both populations from one month to another (Longzhou: F = 4.069, p < 0.001; Guiping: F = 3.619, p < 0.001) (Figs. 2-3).

Figure 1.
The foraging time of dusk (n = 63) and predawn (n = 63) periods of Tylonycteris pachypus in Longzhou County (empty column) and Guiping County (grey column), Guangxi, south China. All data are expressed as Mean ± SD. *p < 0.05.

Figure 2-3.
The total foraging time over one night (average value of seven nights for each month) of Tylonycteris pachypus in Longzhou County (2) and Guiping County (3). Solid portions indicate dusk foraging periods while hollow portions indicate dawn foraging periods. The dots indicate the average temperature.

Figure 4.
Time of dusk emergence (n = 63) and predawn returning (n = 63) of Tylonycteris pachypus in Longzhou County (empty column) and Guiping County (grey column), Guangxi, south China. All data are expressed as Mean ± SD. *p < 0.05.

The time of emergence obtained for the Longzhou population at post dusk (12.7 ± 0.62 min after sunset) was significantly earlier than for the Guiping population (14.7 ± 0.48 min) (t = 2.37, p < 0.05), but the returning time at predawn did not significantly differ between them (Longzhou: 17.3 ± 0.94 min before sunrise, Guiping: 17.5 ± 0.62 min) (t = 1.38, p > 0.05) (Fig. 4). We also found that there is a significant correlation between the time of evening emergence and the average air temperature at sunset, and between time of predawn return and average air temperature at sunrise for both populations, respectively (Longzhou: remergence = 0.882, rreturn = -0.915, respectively, both p < 0.001; Guiping: remergence = 0.735, rreturn = -0.826, both p < 0.001).

DISCUSSION

Mammals that are characterized by energetically expensive modes of locomotion and which encounter limited (temporally) food supply tend to regulate their foraging behavior. Bat species usually emerge to feed after sunset and return before sunrise (Bateman & Vaughan 1974Bateman GC, Vaughan TA (1974) Nightly activities of mormoopid bats. Journal of Mammalogy 55: 45-65. doi: 10.2307/1379256
https://doi.org/10.2307/1379256...
, O'Shea & Vaughan 1977O'Shea TJ, Vaughan TA (1977) Nocturnal and seasonal activities of the pallid bat, Antrozous pallidus. Journal of Mammalogy 58: 269-284. doi: 10.2307/1379326
https://doi.org/10.2307/1379326...
, Duvergé et al. 2000Duvergé PL, Jones G, Rydell J, Ransome RD (2000) Functional significance of emergence timing in bats. Ecography 23: 32-40. doi: 10.1034/j.1600-0587.2000.230104.x
https://doi.org/10.1034/j.1600-0587.2000...
). The timing of these activity bouts correspond to the time at dusk and predawn when insects are most abundant (Kunz 1974Kunz TH (1974) Feeding ecology of a temperate insectivorous bat (Myotis velifer). Ecology 55: 693-711., Racey 1982Racey PA (1982) Ecology of bat reproduction, p. 335-427. In: Kunz TH (Ed.). Ecology of bats. New York, Plenum Publishing. doi: 10.1007/978-1-4613-3421-7_2
https://doi.org/10.1007/978-1-4613-3421-...
, Racey & Swift 1985Racey PA, Swift SM (1985) Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. I. Foraging behavior. Journal of Animal Ecology 54: 205-215. doi: 10.2307/4631
https://doi.org/10.2307/4631...
, Rydell 1993Rydell J (1993) Variation in foraging activity of an aerial insectivorous bat during reproduction. Journal of Mammalogy 74: 503-509. doi: 10.2307/1382411
https://doi.org/10.2307/1382411...
, Swift 1997Swift SM (1997) Roosting and foraging behavior of Natterer's bats (Myotis nattereri) close to the northern border of their distribution. Journal of Zoology (London) 242: 375-384. doi: 10.1111/j.1469-7998.1997.tb05809.x
https://doi.org/10.1111/j.1469-7998.1997...
). Based on previous studies, most bat species spend more than one hour each night in predation activities, and their nocturnal activity rhythm can be highly variable among different species. For instance, O'Shea & Vaughan (1977O'Shea TJ, Vaughan TA (1977) Nocturnal and seasonal activities of the pallid bat, Antrozous pallidus. Journal of Mammalogy 58: 269-284. doi: 10.2307/1379326
https://doi.org/10.2307/1379326...
) have reported that the activity of pallid bats was characterized by two foraging periods with an intervening period of night roosting. Anthony et al. (1981Anthony ELP, Stack MH, TH Kunz (1981) Night roosting and the nocturnal time budget of the little brown bat, Myotis lucifugus: effects of reproductive status, prey density, and environmental conditions. Oecologia 51: 151-156. doi: 10.1007/BF00540593
https://doi.org/10.1007/BF00540593...
) have also reported that the little brown bat typically has two foraging periods at night, which are divided by a short break in night roost. In the present study, we found that the night foraging time patterns of T. pachypus were characterized by two bouts: dusk and predawn, respectively. Within each bout, activity duration (time period from emergence to returning) was remarkably short, less than 30 minutes. This may be correlated with the fact that the lesser bamboo bat is one of the smallest bat species, and therefore individuals can spend relatively short periods of activity time to balance energy intake and the costs to maintain their high metabolic rate during flight (Speakman 2005Speakman JR (2005) Body size, energy metabolism and lifespan. Journal of Experimental Biology 208: 1717-1730. doi: 10.1242/jeb.01556
https://doi.org/10.1242/jeb.01556...
). On the other hand, the roosting behavior of T. pachypus may also contribute to their short activity time. T. pachypus roosts within bamboo internodes, and these restricted spaces may limit the activity of bats and subsequently reduce their energy consumption. Moreover, the short foraging distance away from their internode roosts decrease flight time as well as energy consumption (Zhang et al. 2007Zhang L-B, Liang B, Jones G, Parsons S, Wei L, Zhang S-Y (2007) Morphology, echolocation and foraging behavior in two sympatric sibling species of bat (Tylonycteris pachypus and T. robustula) (Chiroptera: Vespertilionidae). Journal of Zoology (London) 271: 344-351. doi: 10.1111/j.1469-7998.2006.00210.x
https://doi.org/10.1111/j.1469-7998.2006...
).

Our results indicate that in Longzhou County T. pachypus emerges earlier and forages for longer periods of time than that in Guiping County. On average, the activity time of individuals in Longzhou each night is approximately five minutes, which is longer than that in Guiping. Although this increase is small in magnitude, it represents a 10% increase in average activity time. The different activity behavior in different locations may have resulted from many factors such as the effect of interspecific competition (Swift & Racey 1983Swift SM, Racey PA (1983) Resource partitioning in two species of vespertilionid bats (Chiroptera) occupying the same roost. Journal of Zoology (London) 200: 249-2593. doi: 10.1111/j.1469-7998.1983.tb05787.x
https://doi.org/10.1111/j.1469-7998.1983...
, Bonaccorso et al. 2006Bonaccorso FJ, Winkelmann JR, Shin D, Agrawal CI, Aslami N, Bonney C, Hsu A, Jekielek PE, Knox AK, Kopach SJ, Jennings TD, Lasky JR, Menesale SA, Richards JH, Rutland JA, Sessa AK, Zhaurova L, Kunz TH (2006) Evidence for exploitative competition: comparative foraging behavior and roosting ecology of short-tailed fruit bats (Phyllostomidae). Biotropica 39: 249-256. doi: 10.1111/j.1744-7429.2006.00251.x
https://doi.org/10.1111/j.1744-7429.2006...
), variations in prey abundance (Erkert 1982Erkert HG (1982) Ecological aspects of bat activity rhythms, p. 201-242. In: Kunz TH (Ed.). Ecology of bats. New York, Plenum Press. doi: 10.1007/978-1-4613-3421-7-5
https://doi.org/10.1007/978-1-4613-3421-...
), predation risk (McWilliam 1989McWilliam AM (1989) Emergence behavior of the bat Tadarida (Chaerephon) pumila (Chiroptera: Molossidae) in Ghana, West Africa. Journal of Zoology (London) 219: 698-701. doi: 10.1111/j.1469-7998.1989.tb02615.x
https://doi.org/10.1111/j.1469-7998.1989...
, Speakman 1991Speakman JR (1991) Why do insectivorous bats in Britain not fly in daylight more frequently? Functional Ecology 5: 518-524. doi: 10.2307/2389634
https://doi.org/10.2307/2389634...
), and colony size (Avery 1986Avery MI (1986) Factors affecting the emergence times of Pipistrelle bats. Journal of Zoology (London) 209: 293-296. doi: 10.1111/j.1469-7998.1986.tb03589.x
https://doi.org/10.1111/j.1469-7998.1986...
, Rydell 1989Rydell J (1989) Feeding activity of the northern bat Eptesicus nilssoni during pregnancy and lactation. Oecologica 80: 562-565. doi: 10.1007/BF00380082
https://doi.org/10.1007/BF00380082...
, Korine et al. 1994Korine C, Izhaki I, Makiin D (1994) Population structure and emergence order in the fruit-bat (Rousettus aegyptiacus: Mammalia, Chiroptera). Journal of Zoology (London) 232: 163-174. doi: 10.1111/j.1469-7998.1994.tb01566.x
https://doi.org/10.1111/j.1469-7998.1994...
, Clark et al. 2002Clark BS, Clark BK, Lesie Jr DM (2002) Seasonal variation in activity patterns of the endangered Ozark big-eared bat (Corynorhinus townsendii ingens). Journal of Mammalogy 83: 590-598. doi: 10.1644/1545-1542
https://doi.org/10.1644/1545-1542...
, O'Donnell 2002O'Donnell CFJ (2002) Influence of sex and reproductive status on nocturnal activity of long-tailed bats (Chalinolobus tuberculatus). Journal of Mammalogy 83: 794-803. doi: 10.1644/1545-1542
https://doi.org/10.1644/1545-1542...
). Both T. pachypus and T. robustula eat similar categories of insects when they occur sympatrically, although the prey of the later is somewhat larger than that of the former (Zhang et al. 2005aZhang L-B, Jones G, Rossiter S, Ades G, Liang B, Zhang S-Y (2005a) Diet of flat-headed bats, Tylonycteris pachypus and T. robustula, in Guangxi, South China. Journal of Mammalogy 86: 61-66. doi: 10.1644/1545-1542
https://doi.org/10.1644/1545-1542...
). In conclusion, in Longzhou where both sibling species are sympatric, the activity time of T. pachypus may be affected by T. robustula.

Many authors have documented seasonal fluctuations in emergence and returning time of bats (Bateman & Vaughan 1974Bateman GC, Vaughan TA (1974) Nightly activities of mormoopid bats. Journal of Mammalogy 55: 45-65. doi: 10.2307/1379256
https://doi.org/10.2307/1379256...
, O'Shea & Vaughan 1977O'Shea TJ, Vaughan TA (1977) Nocturnal and seasonal activities of the pallid bat, Antrozous pallidus. Journal of Mammalogy 58: 269-284. doi: 10.2307/1379326
https://doi.org/10.2307/1379326...
, Duvergé et al. 2000Duvergé PL, Jones G, Rydell J, Ransome RD (2000) Functional significance of emergence timing in bats. Ecography 23: 32-40. doi: 10.1034/j.1600-0587.2000.230104.x
https://doi.org/10.1034/j.1600-0587.2000...
). Pallid bats emerge earlier in the summer sunset when compared with spring and autumn sunsets (O'Shea & Vaughan 1977O'Shea TJ, Vaughan TA (1977) Nocturnal and seasonal activities of the pallid bat, Antrozous pallidus. Journal of Mammalogy 58: 269-284. doi: 10.2307/1379326
https://doi.org/10.2307/1379326...
). Lee & McCracken (2001Lee Y-F, McCracken GF (2001) Timing and variation in the emergence and return of Mecican free-tailed bat, Tadarida brasiliensis mexicana. Zoological Study 40: 309-316.) have also reported that the timing of evening emergence and returning of the Mexican free-tailed bats, Tadarida brasiliensis (I. Geoffroy, 1824), are correlated with the time of sunset and sunrise, and that bats are more likely to emerge earlier in relation to earlier sunset time during late summer, when compared with spring to early summer. They also return progressively later at dawn, which is associated with sunrise in the entire season. We found that the dawn returning times of T. pachypus were correlated with sunrise from March to November. In this study, T. pachypus emerged only 5-10 minutes after sunset during summer, but 10-20 minutes during spring and autumn. Pallid bats emerged 20-40 minutes after sunset (O'Shea & Vaughan 1977O'Shea TJ, Vaughan TA (1977) Nocturnal and seasonal activities of the pallid bat, Antrozous pallidus. Journal of Mammalogy 58: 269-284. doi: 10.2307/1379326
https://doi.org/10.2307/1379326...
) and greater horseshoe bats emerged 45-53 minutes after sunset (Duvergé et al. 2000Duvergé PL, Jones G, Rydell J, Ransome RD (2000) Functional significance of emergence timing in bats. Ecography 23: 32-40. doi: 10.1034/j.1600-0587.2000.230104.x
https://doi.org/10.1034/j.1600-0587.2000...
). Kunz et al. (1995)Kunz TH, Whitaker Jr JO, Wadanoli MD (1995) Dietary energetics of the insectivorous Mexican free-tailed bats (Tadarida brasiliensis) during pregnancy and lactation. Oecologica 101: 407-415. doi: 10.1007/BF00329419
https://doi.org/10.1007/BF00329419...
have pointed out that increased energetic demands during pregnancy and lactation could cause females, especially those lactating, to spend twice or even three times as much time foraging than bats that are neither pregnant nor lactating. As a result, emerging earlier in the evening and returning later at dawn will give these bats more time to feed, but at the cost of a greater danger of predation (Fenton 1995Fenton MB (1995) Constraint and flexibility-bats as predators, bats as prey. Symposium of the Zoological Society of London 67: 277-290., Speakman et al. 1995Speakman JR, Stone RE, Kerslake JE (1995) Temporal patterns in the emergence behavior of pipistrelle bats, Pipistrellus pipistrellus, from maternity colonies are consistent with an anti-predator response. Animal Behavior 50: 1147-1156. doi: 10.1016/0003-3472(95)80030-1
https://doi.org/10.1016/0003-3472(95)800...
, Rydell et al. 1996Rydell J, Entwistle A, Racey PA (1996) Timing of foraging flights of three species of bats in relation to insect activity and predation risk. Oikos 76: 243-252. doi: 10.2307/3546196
https://doi.org/10.2307/3546196...
). Our results indicate that the activity time of flat-headed bats is longer in summer than in spring and in autumn. This may be influenced by prey activity, reproductive status and energy demands (Richards 1989Richards GC (1989) Nocturnal activity of insectivorous bats relative to temperature and prey availability in tropical Queensland. Austra lian Wildlife Research 16: 151-158. doi: 10.1071/WR9890151
https://doi.org/10.1071/WR9890151...
). Female flat-headed bats usually become pregnant in May, and give birth and lactate in June (Zhang et al. 2005bZhang L-B, Jones G, Parsons S, Liang B, Zhang S-Y (2005b) Development of vocalizations in the flat-headed bats, Tylonycteris pachypus and T. robustula (Chiroptera: Vespertilionidae). Acta Chiropterologica 7: 91-99. doi: 10.3161/1733-5329
https://doi.org/10.3161/1733-5329...
). During this time, reproductive females would require more energy to maintain the increased physiological requirements of pregnancy and lactation, which is reflected in their increased activity time.

Seasonal fluctuations in activity patterns can be influenced by many factors, such as ambient temperature and/or prey availability (Anthony et al. 1981Anthony ELP, Stack MH, TH Kunz (1981) Night roosting and the nocturnal time budget of the little brown bat, Myotis lucifugus: effects of reproductive status, prey density, and environmental conditions. Oecologia 51: 151-156. doi: 10.1007/BF00540593
https://doi.org/10.1007/BF00540593...
, Rydell 1989Rydell J (1989) Feeding activity of the northern bat Eptesicus nilssoni during pregnancy and lactation. Oecologica 80: 562-565. doi: 10.1007/BF00380082
https://doi.org/10.1007/BF00380082...
, Maier 1992Maier C (1992) Activity patterns of pipistrelle bats (Pipistrellus pipistrellus) in Oxfordshire. Journal of Zoology (London) 116: 396-435. doi: 10.1111/j.1469-7998.1992.tb04433.x
https://doi.org/10.1111/j.1469-7998.1992...
). In the present study, the bamboo bats emerged earlier and returned latter when the ambient temperature was higher, which resulted in a positive association between high ambient temperature and increased activity. In March and November, when temperatures were relatively low, the activity periods of bamboo bats were obviously short than from April to October. Reduced activity in lower temperatures has also been demonstrated for many other insectivorous bat species (e.g., Anthony et al. 1981Anthony ELP, Stack MH, TH Kunz (1981) Night roosting and the nocturnal time budget of the little brown bat, Myotis lucifugus: effects of reproductive status, prey density, and environmental conditions. Oecologia 51: 151-156. doi: 10.1007/BF00540593
https://doi.org/10.1007/BF00540593...
, Kronwitter 1988Kronwitter F (1988) Population structure, habitat use, and activity patterns of the noctule bat, Nyctalus noctula Schreib. 1774 (Chiroptera: Vespertilionidae) revealed by radio-tracking. Myotis 26: 23-85., Rydell 1989Rydell J (1989) Feeding activity of the northern bat Eptesicus nilssoni during pregnancy and lactation. Oecologica 80: 562-565. doi: 10.1007/BF00380082
https://doi.org/10.1007/BF00380082...
, Maier 1992Maier C (1992) Activity patterns of pipistrelle bats (Pipistrellus pipistrellus) in Oxfordshire. Journal of Zoology (London) 116: 396-435. doi: 10.1111/j.1469-7998.1992.tb04433.x
https://doi.org/10.1111/j.1469-7998.1992...
, Catto et al. 1995Catto CMC, Racey PA, Stephenson PJ (1995) Activity patterns of the serotine bat (Eptesicus serotinus) at a roost in southern England. Journal of Zoology (London) 235: 635-644. doi: 10.1111/j.1469-7998.1995.tb01774.x
https://doi.org/10.1111/j.1469-7998.1995...
). This negative influence may be a reflection of decreased food availability, because insect activity throughout the night is positively correlated with temperatures (Taylor 1963Taylor LR (1963) Analysis of the effect of temperature on insects in flight. Journal of Animal Ecology 32: 99-117., Lewis & Taylor 1964Lewis T, Taylor LR (1964) Diurnal periodicity of flight by insects. Transactions of the Entomological Society of London 116: 396-435. doi: 10.1111/j.1365-2311.1965.tb02304.x
https://doi.org/10.1111/j.1365-2311.1965...
).

In conclusion, our findings suggest that the lesser bamboo bat spends relatively short time being active, even less than half hour each bout. This behavior may be correlated with the high-energy demand for this tiny mammal to be able to fly. Secondly, our findings suggest that the activity behavior of the lesser bamboo bat, including emergence time and activity duration, varies in different locations. The variation in activity may result from many factors such as the effect of sibling sympactric species, and variations in prey abundance, predation risk, and colony size in different locations. Further studies should be conducted to confirm the factors that influence the variations in bat activity.

ACKNOWLEDGEMENTS

We thank Hui Qin, Shen-Ming Huang (Guangxi Normal University) for their assistance in the field, and Stuart Parsons (University of Auckland) and Yi Chen for assistance in writing this manuscript. This study was financed by the Special Planning of Major Scientific and Technological Production (Cultivation Project), Guangdong Academy of Sciences (ZDCCYD201307), Special Foundation for Innovative Scientists of Guangdong Entomological Institute (GDEI-cxrc201303), and Science & Technology Planning Project of Guangdong (2013B050800024) . Li-Biao Zhang and Fu-Min Wang contributed equally to this paper.

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Publication Dates

  • Publication in this collection
    May-Jun 2015

History

  • Received
    09 June 2014
  • Reviewed
    24 Apr 2015
  • Accepted
    02 May 2015
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