785
POSTNATAL GROWTH, AGE ESTIMATION, AND SEXUAL
MATURITY IN THE FORMOSAN LEAF-NOSED BAT
(HIPPOSIDEROS TERASENSIS)
H. C. CHENG ANDL. L. LEE*
Taiwan Endemic Species Research Institute, Nantou, Taiwan, ROC (HCC) Department of Zoology, National Taiwan University, Taipei, Taiwan, ROC (LLL)
Changes in body mass, length of forearm, and length of total epiphyseal gaps of young Formosan leaf-nosed bats (Hipposideros terasensis) were monitored by marking and re-capturing at a maternity colony in central Taiwan. Length of forearm and body mass of 1-day-old neonates averaged 43.3 mm6 2.7 SD and 15.9 g 6 3.3 SD, respectively. Increase in forearm length and body mass was fastest in the 1st week after birth, but rate of increase decreased thereafter. Length of total epiphyseal gap increased to its maximum size at about 10 days after birth and subsequently decreased linearly. Growth constants derived from the logistic growth model were 0.096 and 0.114 for the increase in length of forearm and body mass, respectively. Age of H. terasensis between 1 and 44 days can be estimated either by length of forearm when forearm length is #91 mm or by length of total epiphyseal gap when forearm length is .91 mm. Subsequent monitoring suggested that males of H.
ter-asensis are capable of reaching sexual maturity in their 1st year and females in their 2nd
year. When compared with other bats, growth rate of H. terasensis was faster than that of many tropical species but slower than that of most temperate species.
Key words: body mass, growth constant, Hipposideridae, length of forearm, subtropical insectivo-rous bat, total epiphyseal gap
Studies on sizes of animals at birth and on subsequent postnatal growth are impor-tant for understanding the aspects of their life history (Kunz and Robson 1995) and for understanding a wide range of ecologi-cal, behavioral, and developmental patterns (Habersetzer and Marimuthu 1986; Powers et al. 1991; Studier and Kunz 1995). Many studies on postnatal growth and develop-ment of bats have been conducted under natural conditions (Baptista et al. 2000; Hoying and Kunz 1998; Isaac and Mari-muthu 1996; Koehler and Barclay 2000; Kunz and Anthony 1982; Kunz and Robson 1995) because such studies provide the most ecologically meaningful data. Tuttle and Stevenson (1982) reported that 14 of the 19 chiropteran families lack data on * Correspondent: leell@ccms.ntu.edu.tw
postnatal growth, and #3% of known bat species have been investigated regarding their growth and development. Eighty per-cent of studies on postnatal growth are re-stricted to the family Vespertilionidae, par-ticularly bats of the temperate zone. Our study on Hipposideros terasensis is the 1st to report postnatal growth of a subtropical insectivorous member of the family Hip-posideridae.
Members of the family Hipposideridae, or the Old World leaf-nosed bats, inhabit tropical and subtropical regions of Africa, Asia, and Australia (Nowak 1994). The Formosan leaf-nosed bat (H. terasensis) is the largest insectivorous bat endemic to Tai-wan. Average body mass of an adult is about 60 g. H. terasensis generally roosts in caves, abandoned tunnels, and buildings
at elevations of #1,000 m, and individuals assemble at a distance of about 5–10 cm from each other. Pregnant females usually give birth to a single young each year be-tween May and early June (Chen 1995; Cheng 1999; Lin et al. 1997). H. terasensis was once regarded as a subspecies of H.
armiger (Kishida 1924; Nowak 1994).
However, some scholars consider H.
tera-sensis as a separate species on the basis of
its distinct morphological characteristics (Bogdanowicz and Owen 1998; Yoshiyuki 1991).
Postnatal growth period, which is defined as the time from birth until the epiphyses of long bones become visibly closed (Kunz 1987; Kunz and Anthony 1982), may ex-tend from several weeks up to several months in bats. The period can be opera-tionally divided into 3 distinct stages: pre-flight, early flight and weaning, and post-flight (Kunz 1987). Body mass, length of forearm, and length of total epiphyseal gap have been shown to be important variables for estimating age of young at different growth stages on the basis of mark–recap-ture data of known-age young (Baptista et al. 2000; Isaac and Marimuthu 1996; Kunz and Anthony 1982; Kunz and Robson 1995; Rajan and Marimuthu 1999). Reli-able equations for estimating age of young bats can be derived by combining mean changes in length of forearm during the pre-flight period with changes in the 4th meta-carpal–phalangeal epiphyseal gap during the early flight and weaning period. Body mass is not a good character for estimating age because of its sensitivity to nutritional input, energy expenditure, and water flux (Kunz 1987), but it is ideal for interspecific comparison of growth rates throughout the postnatal growth period among species from different regions (Kunz and Stern 1995). Kunz and Hood (2000) reviewed and compared growth rates of postnatal body mass in 41 species of bats, including 31 microchiropterans from temperate and tropical regions. They found that growth rates of young bats decreased linearly with
increasing asymptotic body mass. When the effect of body mass was removed, latitude (tropical or temperate) became the only var-iable that had a significant effect on post-natal growth rates, with temperate species growing faster than tropical species.
In this study we measured the size of H.
terasensis at birth. We describe the pattern
of their postnatal growth under natural con-ditions from birth to the postflight period and derive equations for estimating their ages. We also describe the trend in changes in body mass and length of forearm for young H. terasensis using recapture data in subsequent months until the subjects mi-grated to winter hibernacula. In addition, we monitor changes in the percentage of sexually mature individuals in a cohort in subsequent years to determine age of sexual maturity of both males and females. Finally, we compare the growth constant and age of sexual maturity of H. terasensis with that of other bats described by Kunz and Hood (2000), Kunz and Stern (1995), and Tuttle and Stevenson (1982). Because H.
terasen-sis is a large microchiropteran species
in-habiting subtropical regions, we predict that postnatal growth rate of H. terasensis will be slower than that of most temperate bats but faster than that of most tropical species and that age of sexual maturity of H.
tera-sensis will be later than that of most
tem-perate bats but earlier than that of most tropical species.
MATERIALS AND METHODS
Our study was conducted at a roost of H.
ter-asensis inside an abandoned tunnel at
Chung-liao, Nantou County, in central Taiwan (1208449E, 238549N). The tunnel, which has 2 entrances facing east and west, is 300 m long, 3.7 m wide, and 4 m high and is surrounded by betel nut (Areca catechu L.) plantations and or-chards. A stream flows adjacent to the south side of the tunnel. Approximately 300 individuals roosted in this tunnel during the breeding season from 1997 to 1999. Bats usually arrive in late February or early March and depart in late No-vember or December each year.
hand-cap-tured young H. terasensis by plucking them off the wall inside the tunnel immediately after the nightly emergence of adults at 2- to 9-day inter-vals. Infants with an attached umbilical cord were assumed to be 1 day old (Hoying and Kunz 1998; Isaac and Marimuthu 1996; Kunz and An-thony 1982; Kunz and Robson 1995). We placed the young in cloth-holding bags after they were caught and processed them as follows. We weighed individuals to the nearest 0.05 g using a portable electronic balance (Acculab, Hunting-don Valley, Pennsylvania) and measured the length of forearm and total epiphyseal gap of the 4th metacarpal–phalangeal joint to the nearest 0.05 mm using dial calipers (Mitutoyo, Japan; Kunz and Anthony 1982; Kunz and Robson 1995). When measuring the length of epiphyseal gap, we placed a lamp under the wing of the subject so that the cartilaginous band would show up clearly. We marked each young by fit-ting a uniquely numbered aluminum band (5.2 by 5.5 mm; Lambournes Ltd., Birmingham, United Kingdom) to the right arm of females and to the left arm of males. Then, we returned the young by hand to the site of capture inside the tunnel. We completed the whole task within 1 h to minimize disturbance. Lactating females generally return to the roost about 1 h after they emerge. Within the hour, we captured and mea-sured as many young as possible (usually 10– 15 pups each time).
We continued to recapture young until they approached adult size and could fly indepen-dently. We estimated age of sexual maturity of the 1997 cohort by recapturing and examining their reproductive characteristics every month from August 1997 to May 1999, except in win-ter. Females were considered mature if they were pregnant or showed signs of parturition or nurs-ing, i.e., swollen and elongated nipples or pubic nipples (or both), which are a special tissue sit-uated in the pubic region in species of
Hippos-ideros and which can be observed easily on
nursing females (Racey 1988). Males were con-sidered mature if they had enlarged testes or ep-ididymides (or both), indicating active genesis. During the period of active spermato-genesis, which generally begins in April, peaks in June, and ceases in September (Chen 1998), the sizes of testes may increase from 12.1–24.2 mm3 in the nonspermatogenesic stage to 38.4–
96.1 mm3and can be easily diagnosed from the
outside. We mist-netted postpartum females at
tunnel entrances and measured their body mass and length of forearm in late May of 1997 to provide a measurement of the sizes of standard adults.
We used a linear regression model to derive equations of age estimation for young H.
tera-sensis on the basis of changes in length of
fore-arms and epiphyseal gaps (Kunz and Anthony 1982; Kunz and Robson 1995). We used data only from those young that were captured more than once during the analysis of growth and age estimation. We used an unpaired t-test to com-pare length of forearm and body mass of males and females at birth and chi-square test to eval-uate whether sex ratio at birth was different from unity. The logistic model was applied to derive growth curves and growth constants of young (Kunz and Robson 1995; Stern and Kunz 1998). We also compared growth rate of H. terasensis with that of other microchiropteran bats, de-scribed by Kunz and Hood (2000), by compar-ing growth constants of these bats.
RESULTS
Ten young H. terasensis were captured and marked on the 1st night of this study on 20 May 1997. Length of forearm of the largest young without an attached umbilicus was 57.5 mm, and body mass was 24.5 g. According to the age-estimation equation given subsequently, this young bat was about 6–7 days old. During this study the last young with an attached umbilicus was captured on 27 May 1997. In June we did not capture any young with attached um-bilici. These results reveal that H. terasensis in this roost gave birth from mid- to late May in 1997, which coincides with the be-ginning of warm and wet season in the Nantou area (Fig. 1).
A total of 63 young (33 females and 30 males) were captured and measured be-tween 20 May and 2 July, during the pre-flight stage. The sex ratio (1 female : 0.91 males) did not differ significantly from uni-ty (x2 5 0.14, d.f. 5 1, P . 0.05). Only 9
of these young had an attached umbilicus. Length of forearm of these 1-day-old young ranged from 40.0 to 47.1 mm (X¯ 5 43.3 6 2.7), and their body mass ranged from 11.2
FIG. 1.—Climatic conditions throughout the year at study site in Nantou, central Taiwan. A) Mean daily temperature and B) total rainfall in the Nantou area in 1961–1990 (open symbols) and 1997 (closed symbols). Data from Sun Moon Lake weather station. Arrow indicates be-ginning of parturition of Hipposideros
terasen-sis.
to 20.2 g (X¯ 5 15.9 6 3.3). No significant difference was found between length of forearm of male (X¯ 5 47.0 6 0.1, n 5 2) and female (X¯ 5 42.2 6 2.3, n 5 7; t 5 0.03, d.f. 5 6, P . 0.05) young, although average length of forearm of males is lon-ger. Similarly, body masses of male (X¯ 5 18.5 6 2.4, n 5 2) and female (X¯ 5 15.3 6 3.0, n 5 7) young were not significantly different (t5 0.21, d.f. 5 6, P . 0.05).
Newborns are naked with a gray dorsal part and a pink ventral part. Their eyes are closed, and ears are folded. Eye slits appear within 1 week after birth, and eyes are com-pletely open after 2 weeks. Ears become erect at about 1 week of age. When roosting inside tunnel, young often firmly attach to 1 of the 2 pubic nipples on the ventral side
of their mothers, in a head-up position. Af-ter mothers emerge to forage, the young that are left behind generally hang on the wall in a loose group. They can fly a short distance inside the tunnel when 3–4 weeks old. Some mothers carry their young to for-age even when the young are already fairly large in size (41–43 g). On 7 July 1997 a mother–young pair was captured, and the young was estimated to be about 6 weeks old. When young are about 1 month old, their fur is similar to that of adults but dark-er in color, which makes them easily distin-guishable from their mothers’ brown-col-ored fur. The young could fly independently at about 7 weeks old, but most of those caught in early August still had a visible epiphyseal gap on the metacarpal–phalan-geal joint.
Of the 63 young captured during this study, 7 were recaptured once, 9 were re-captured twice, 3 were rere-captured thrice, and 5 were recaptured 4 times, for a total of 54 recaptures before they could fly in-dependently. Therefore, only 24 young (38.1%) were recaptured 1 or more times during the growth period. The recapture in-tervals of these young ranged from 2 to 28 days. To increase sample size for deriving postnatal growth curve, those young with a forearm length ,47.1 mm, but without an attached umbilicus, were regarded as 2 days old.
By examining recaptured young, we found that rate of increase in body mass was highest in the 1st week (2.06 g/day), after which growth rate decreased (Fig. 2a). The rate of increase was reduced to 0.62 g/ day in the 2nd week and then to 0.38, 0.27, 0.21, and 0.17 g/day in subsequent weeks. Average body mass of neonates is about 23% of that of their mother (60.33 6 3.21 g, n 5 3) and approaches 70% of their mother’s mass when they are 6 weeks of age.
Length of forearm also increased contin-uously during the 6-week period of post-natal growth (Fig. 2b). During the 1st week, rate of increase in length of forearm was
FIG. 2.—Postnatal growth patterns of young
Hipposideros terasensis based on measurement
of a) body mass, b) length of forearm, and c) length of total epiphyseal gap of 4th metacarpal– phalangeal joint.
FIG. 3.—Age-predictive relationships between a) length of forearm and age (1–22 days) and b) length of total epiphyseal gap and age (14–44 days) in Hipposideros terasensis. The age-pre-dictive equation in a) is valid when length of forearm# 91 mm and the age-predictive equa-tion in b) is valid when length of forearm. 91 mm.
highest (4.21 mm/day), with length of fore-arm nearly doubling in the 1st week. There-after, rate of increase reduced to 1.27 mm/ day in the 2nd week and then to 0.77, 0.56, 0.44, and 0.36 mm/day in subsequent weeks. Length of forearm of newborn H.
terasensis was about 40% of that of an
adult female (93.66 0.17 mm, n 5 3). By 14 days of age, length of forearm averaged about 80% of the adult size. By 44 days, length of forearm was almost the same as that of an adult female. Length of total epiphyseal gap increased linearly for about 10 days and then decreased linearly from 10 to 44 days (Fig. 2c).
We derived logistic equations to describe postnatal growth patterns of young H.
ter-asensis by fitting a sigmoidal curve to
growth data (see Kunz and Robson 1995; Stern and Kunz 1998). Equations are as fol-lows: forearm length5 93.91[e20.096(t21.51)2
1]21 and body mass 5 40.7[e20.114(t23.33) 2
1]21, where t is age in days, and 0.096 and
0.114 are growth constants.
To derive regression equations for pre-dicting age on the basis of length of fore-arms and total epiphyseal gaps, we divided the postnatal growth period into 2 stages over which linear regressions could be computed. Regression analysis indicates that length of forearm can be used to reli-ably estimate age of young H. terasensis up to 21 days. The equation for estimating age on the basis of length of forearm is valid if this dimension is #91 mm (Fig. 3a), i.e., age (days)5 0.42 (forearm length) 2 17.49 (r25 0.89, d.f. 5 48, P , 0.05). To estimate
TABLE 1.—Sexual maturation of male and female Hipposideros terasensis as shown by recapture of bats from the newborn cohort of 1997 in 1997, 1998, and 1999.
Year 1997 Female Male 1998 Female Male 1999 Female Male Number recaptured
Number sexually mature Percent sexually mature
42 0 0 42 0 0 15 0 0 16 10 62.5 14 8 57.1 4 4 100
age of young when length of forearm is .91 mm, length of total epiphyseal gap was used (Fig. 3b). By reversing the axes of regression analysis for age versus length of epiphyseal gaps (see Kunz and Anthony 1982), the equation for age estimation on the basis of length of total epiphyseal gap was derived, i.e., age (days)5 20.71 (total epiphyseal gap)1 64.60 (r2 5 0.86, d.f. 5
33, P, 0.05). Age estimation by this equa-tion is valid for young that are 22–44 days old when length of forearm is .91 mm. Together, these 2 equations allow us to pre-dict the age of young H. terasensis from 1 to 44 days after birth.
From May to November 1997, a total of 84 young bats (42 females and 42 males) were captured. Of these, 31 bats (15 fe-males and 16 fe-males) were recaptured in 1998 and 18 (14 females and 4 males) in 1999. In 1997 none of the recaptured fe-males or fe-males had reached sexual maturity (Table 1). In 1998 none of the recaptured females had the status of pregnancy, par-turition, or nursing, but 62.5 % of the re-captured males had enlarged testes or epi-didymides (or both); these males were re-garded as sexually mature. We found the 1st young male with enlarged testes on 21 April 1998. This finding showed that young males could reach sexual maturity within 12 months of birth. In 1999, 57.1% of the recaptured females had elongated pubic nipples, which are signs of sexual maturity. All the recaptured males showed evidence of spermatogenesis. Results indicated that some male H. terasensis are capable of reaching sexual maturity in their 1st year,
whereas females do not become sexually mature until their 2nd year or later.
DISCUSSION
Altringham (1996) showed that megachi-ropterans can fly at an age of 9–12 weeks, with weaning at 15–20 weeks, whereas in microchiropterans these traits occur at 2–6 weeks and 5–10 weeks, respectively. Young vespertilionid bats become volant at ages between 2 weeks and 2 months, mostly at 3–4 weeks, and weaning occurs between 5 and 8 weeks (Tuttle and Stevenson 1982). Young H. terasensis born in mid- to late May begin to fly at ages of 3–4 weeks and emerge to feed independently at about 7 weeks of age. This coincides with the time of weaning, when their diet consists mainly of insects (Chiu 2000). However, most of the young caught in early August still had a visible epiphyseal gap on the metacarpal– phalangeal joint. According to the defini-tion of Kunz and Anthony (1982), postnatal growth period of H. terasensis might extend to 2.5 months before their metacarpal–pha-langeal joints consolidate. Habersetzer and Marimuthu (1986) found that young H.
speoris became volant when 25–30 days
old. Weaning is initiated at about 2 months of age, and young are able to fend for them-selves at 3 months of age. H. commersoni is weaned at an age of 20 weeks (Brosset 1969). H. speoris and H. commersoni are both tropical species from India. The time at which young H. terasensis become vo-lant does not seem to be much different from that of tropical Hipposideridae and Vespertilionidae, but their weaning time is
earlier than that of some tropical species of
Hipposideros. The phenomenon of early
weaning time in young H. terasensis is sim-ilar to that of some temperate species (hi-bernating bats), such as Lasiurus cinereus and Rhinolophus ferrumequinum nippon. Young of these species are weaned when they are 4 and 7 weeks old (Koehler and Barclay 2000; Sano 2000). One of the rea-sons H. terasensis has an earlier weaning time may be related to the survival strategy for their 1st winter. To deposit enough en-ergy (fat) to be used throughout hiberna-tion, an earlier weaning time and long post-flight period may be necessary for young hibernating bats in the subtropics, as it is for the temperate species (Hoying and Kunz 1998; Kunz and Hood 2000; Kunz and Stern 1995) but not for nonhibernating trop-ical species.
The young of most microchiropterans weigh around 20–30%, mostly about 25%, of their mother’s weight at birth (Altring-ham 1996; Kurta and Kunz 1987). From the perspective of relative body mass at birth, bats are clearly precocial because they are generally heavier than the young of other mammals having comparable litter size (Kurta and Kunz 1987), which average only 5–10% of adult weight (Altringham 1996). However, bats are highly altricial with re-spect to development of forelimb and lo-comotive function (Powers et al. 1991). Most microchiropteran bats cannot fly be-fore they attain 90% of adult wing dimen-sions (Barclay 1995). In our study, average length of forearm of H. terasensis at birth was 43.3 mm and about 40% of the mean value of postpartum females, and average body mass at birth was 15.9 g and about 23% of the size of adult females. They could fly for a short distance at 3–4 weeks of age when their length of forearm was about 89% of that of an adult female, but they rarely emerged from their roost inde-pendently before they were 6 weeks old. In
R. ferrumequinum (a larger member of
Rhinolophidae in the temperate region, with an adult body mass of 23.6 g), body mass
at birth is 5.8 g (Ransome et al., in litt., cited in Kunz and Hood 2000), which is much less than that of H. terasensis. Length of forearm of neonates averages 25.2 mm, which increases rapidly to reach 90.4% of adult size in just 16–18 days, when they start to fly (Sano 2000). In H. speoris (a smaller tropical Hipposideros) average length of forearm and body mass of new-born are 16 mm and 2.3 g, which are about 31% and 21% of that of their mother, re-spectively (Habersetzer and Marimuthu 1986). Young of H. speoris are also much smaller than those of H. terasensis, and they cannot fly for a short distance before they are 5–6 weeks old, when their length of forearm is only about 70% of that of the mother. These results indicate that, although
H. terasensis is a much larger insectivorous
bat, its growth rate is still greater than that of its smaller tropical counterpart and less than that of temperate species.
Kunz and Hood (2000) reviewed and compared postnatal growth rates of body mass of 41 species of bats, including 31 microchiropterans from temperate and trop-ical regions, by means of the logistic growth equation. They found a significant negative correlation between postnatal growth rate and asymptotic body mass. Af-ter the effect of body mass was removed, latitude (tropical or temperate) was the only extrinsic variable that affected postnatal growth rates, i.e., temperate species grow faster than tropical species. On the basis of reviews by Kunz and Hood (2000) and Kunz and Stern (1995), growth constants of body mass of all megachiropterans (K 5 0.01 to 0.04, n 5 10) and tropical micro-chiropterans (K5 0.04 to 0.11, n 5 11) are lower than that of H. terasensis (K 5 0.114). In contrast, most temperate micro-chiropteran species have a higher growth constant (K 5 0.12 to 0.25, n 5 13), and only 4 species have a lower growth constant (K 5 0.04 to 0.10) than that of H.
terasen-sis. This demonstrates, again, that postnatal
growth of H. terasensis (a subtropical mi-crochiropteran) is faster than that of tropical
bats but slower than that of most temperate bats. The fact that young of H. terasensis, which are larger in size at birth, grow faster than smaller bats in the tropics and slower than bats in the temperate regions suggests that latitude is a stronger factor than body size in affecting postnatal growth rate of young bats.
Ages of sexual maturity are highly vari-able among taxa, between males and fe-males of a single species, and sometimes even between individuals of the same sex (Tuttle and Stevenson 1982). In both micro-bats and megamicro-bats, sexual maturity is nor-mally reached within 1–2 years (Altringh-am 1996). In some species, females may be sexually mature within a few months, for instance 5–6 months for Hypsignathus
monstrosus and Rousettus leschenaulti in
megachiropterans and 3 months for R.
hip-posideros in microchiropterans (Tuttle and
Stevenson 1982). Churchill (1995) com-pared 8 tropical species of Hipposideridae and found that both males and females gen-erally reach sexual maturity at 16–24 months, except for females of H. speoris,
H. ater, and Rhinonycteris aurantius, which
mature at 6–8 months. Male and female H.
terasensis become sexually mature in their
1st and 2nd years after birth (mostly ,12 months), which was earlier than in the case of most tropical species of Hipposideros re-ported by Churchill (1995). The result seems to agree with the conclusion of Kunz and Stern (1995), that climate (latitude) is also important in affecting age of sexual maturity and that temperate species mature earlier than subtropical species, which ma-ture earlier than tropical species.
Few species of bats have been studied regarding the relationship between postna-tal growth rate and age of sexual maturity. By comparing results of our study with the available information in Kunz and Stern (1995) and Tuttle and Stevenson (1982), it appeared that species with a higher post-natal growth rate tend to mature earlier than those that have a lower postnatal growth rate, especially in females. However,
Pip-istrellus mimus, a tropical species from
In-dia that undergoes parturition 3 times a year and gives birth to 2 young per litter has a slower growth rate than most other vesper-tilionids have; but these females reach sex-ual maturity at only 4 months after birth (Isaac and Marimuthu 1996). Therefore, more information on various species is needed to examine the relationship between postnatal growth rate and age of sexual ma-turity in bats.
ACKNOWLEDGMENTS
We thank Y. L. Chen, K. L. Huang, and S. L. Liou for helping with fieldwork, and C. Chiu for helping with statistical analysis. We also thank 2 anonymous reviewers for providing helpful comments on the manuscript and valuable ref-erences. Taiwan Endemic Species Research In-stitute supported this study.
LITERATURECITED
ALTRINGHAM, J. D. 1996. Reproduction and develop-ment. Pp. 133–153 in Bats: biology and behaviour. Oxford University Press, Oxford, United Kingdom. BAPTISTA, T. L., C. S. RICHARDSON,ANDT. H. KUNZ. 2000. Growth rates and age estimation in free-rang-ing bats: a comparison of longitudinal and cross-sectional sampling methods. Journal of Mammalogy 81:709–718.
BARCLAY, R. M. R. 1995. Constraints in reproduction by flying vertebrates: energy and calcium. American Naturalist 144:1021–1031.
BOGDANOWICZ, W.,ANDR. D. OWEN. 1998. In the Mi-notaur’s labyrinth: phylogeny of the bat family Hip-posideridae. Pp. 27–42 in Bat biology and conser-vation (T. H. Kunz and P. A. Racey, eds.). Smith-sonian Institution Press, Washington, D.C. BROSSET, A. 1969. Recherches sur la biologie des
Chi-ropte`res troglophiles dans le nord-est du Gabon. Biologie of Gabon 5:93–116 (not seen, cited in Tut-tle and Stevenson 1982).
CHEN, S. F. 1995. Activity pattern and food habit of sympatric Formosan leaf-nosed bat (Hipposideros
armiger) and Formosan horseshoe bat (Rhinolophus monoceros) in Yangmingshan area. M.S. thesis,
Na-tional Taiwan University, Taipei, Taiwan (in Chi-nese, English summary).
CHEN, C. W. 1998. Reproductive ecology of Taiwan leaf-nosed bat (Hipposideros terasensis) in Chun-gliau area, Nantou County. M.S. thesis, Tunghai University, Taichung, Taiwan (in Chinese, English summary).
CHENG, H. C. 1999. Population dynamics and activity pattern of Formosan leaf-nosed bat (Hipposideros
terasensis) in Nantou area. Endemic Species
Re-search (Taiwan) 1:1–11 (in Chinese, English sum-mary).
leaf-nosed bat (Hipposideros terasensis). B.S. thesis, Na-tional Taiwan University, Taipei, Taiwan (in Chi-nese, English summary).
CHURCHILL, S. H. 1995. Reproductive ecology of the orange horseshoe bat, Rhinonycteris aurantius (Chi-roptera: Hipposideridae), a tropical cave-dweller. Wildlife Research 22:687–698.
HABERSETZER, J.,ANDG. MARIMUTHU. 1986. Ontogeny of sounds in the echolocating bat Hipposideros
speoris. Journal of Comparative Physiology, A.
Sen-sory, Neural, and Behavioral Physiology 158:247– 257.
HOYING, K. M., ANDT. H. KUNZ. 1998. Variation in size at birth and post-natal growth in the insectivo-rous bat Pipistrellus subflavus (Chiroptera: Vesper-tilionidae). Journal of Zoology (London) 245:15–27. ISAAC, S. S., AND G. MARIMUTHU. 1996. Postnatal growth and age estimation in the Indian pygmy bat
Pipistrellus mimus. Journal of Mammalogy 77:199–
204.
KISHIDA, K. 1924. On the Formosan Chiroptera. Zoo-logical Magazine (Tokyo) 36:30–49 (in Japanese). KOEHLER, C. E.,ANDR. M. R. BARCLAY. 2000.
Post-natal growth and breeding biology of the hoary bat (Lasiurus cinereus). Journal of Mammalogy 81: 234–244.
KUNZ, T. H. 1987. Postnatal growth and energetics of suckling bats. Pp. 395–420 in Recent advances in the study of bats (M. B. Fenton, P. Racey, and J. M. V. Rayner, eds.). Cambridge University Press, Cam-bridge, United Kingdom.
KUNZ, T. H.,ANDE. L. P. ANTHONY. 1982. Age esti-mation and post-natal growth in the bat Myotis
lu-cifugus. Journal of Mammalogy 63:23–32.
KUNZ, T. H.,ANDW. H. HOOD. 2000. Parental care and postnatal growth in the Chiroptera. Pp. 415–468 in Reproductive biology of bats (E. G. Greighton and P. H. Krutzsch, eds.). Academic Press, New York. KUNZ, T. H., AND S. K. ROBSON. 1995. Postnatal
growth and development in the Mexican free-tailed bat, Tadarida brasiliensis mexicana: birth size, growth rates, and age estimation. Journal of Mam-malogy 76:769–783.
KUNZ, T. H.,ANDA. A. STERN. 1995. Maternal invest-ment and post-natal growth in bats. Symposia of the Zoological Society of London 67:123–138. KURTA, A.,ANDT. H. KUNZ. 1987. Size of bats at birth
and maternal investment during pregnancy. Sym-posia of the Zoological Society of London 57:79– 106.
LIN, L. K., L. L. LEE,ANDH. C. CHENG. 1997. Bats of Taiwan. National Nature and Science Museum, Tai-chung, Taiwan (in Chinese, English summary and remarks).
NOWAK, R. N. 1994. Old World leaf-nosed bats. Pp. 110–114 in Walker’s bats of the world. The Johns Hopkins University Press, Baltimore, Maryland. POWERS, L. V., S. C. KANDARIAN, AND T. H. KUNZ.
1991. Ontogeny of flight in the little brown bat,
My-otis lucifugus: behavior, morphology, and muscle
histochemistry. Journal of Comparative Physiology, B. Biochemical, Systematic, and Environmental Physiology 168:675–685.
RACEY, P. A. 1988. Reproductive assessment in bats. Pp. 31–45 in Ecological and behavioral methods for the study of bats (T. H. Kunz, ed.). Smithsonian In-stitution Press, Washington, D.C.
RAJAN, K. E., AND G. MARIMUTHU. 1999. Postnatal growth and age estimation in the Indian false vam-pire bat (Megaderma lyra). Journal of Zoology (London) 248:529–534.
SANO, A. 2000. Postnatal growth and development of thermoregulative ability in the Japanese greater horseshoe bat, Rhinolophus ferrumequinum nippon, related to maternal care. Mammal Study (Japan) 25: 1–15.
STERN, A. A.,ANDT. H. KUNZ. 1998. Intraspecific var-iation in postnatal growth in the great spear-nosed bat. Journal of Mammalogy 79:755–763.
STUDIER, E. H.,ANDT. H. KUNZ. 1995. Nitrogen and mineral accretion in suckling bats, Tadarida
brasi-liensis and Myotis velifer. Journal of Mammalogy
76:32–42.
TUTTLE, M. D.,ANDD. STEVENSON. 1982. Growth and survival of bats. Pp. 105–150 in Ecology of bats (T. H. Kunz, ed.). Plenum Press, New York.
YOSHIYUKI, M. 1991. Taxonomic status of
Hipposide-ros terasensis Kishida, 1924 from Taiwan
(Mam-malia, Chiroptera, Hipposideridae). Journal of the Mammalogical Society of Japan 16:27–35.
Submitted 16 July 2001. Accepted 11 September 2001. Associate Editor was William L. Gannon.
