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Dispersal patterns of the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae)
ARTICLE IN PRESS
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Dispersal patterns of the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae) By N. Gopukumar, T. Karuppudurai and D.P. Swami Doss Department of Animal Behaviour and Physiology, School of Biological Sciences, Madurai Kamaraj University, Madurai, India; and St. John’s College, Zoology Research Centre, Palayamkottai, India Receipt of Ms. 22.5.2003 Acceptance of Ms. 15.10.2004
Key words: Cynopterus sphinx, Pteropodidae, sex ratio, dispersal
Bats are known to exhibit varying degrees of dispersal and philopatry based on their social system (McCracken and Bradbury 1977; Gaisler 1979; Keen and Hitchock 1980; Bain and Humphrey 1986; Fleming 1988; Handley et al. 1991). The short-nosed fruit bat Cynopterus sphinx is a frugivorous, megachiropteran bat living in groups. In C. sphinx, the juveniles of both sexes are believed to disperse completely from the natal harem (Storz et al. 2000a). However, the fate of young after dispersal remains poorly understood. Do they join established harems or do they aggregate to form a new harem? The aim of this study was to answer this question. The study was carried out from February 2000 to January 2001 in an area measuring approximately 15 km in diameter in the environs of Palayamkottai, South India (81440 S, 771420 E). This region is characterized by semi-arid tropical scrubland and thorn forest (Mani 1974). We located day roosts by citing the accumulation of rejected fruits, leaf pellets, seeds, and cut branches or leaves under trees, especially Borassus flabellifer, Washigtonia filifera, Caryota urens, Areca catechu, Polyalthia longifolia, and Vernonia scandens. According to earlier studies these are the major trees commonly used by C. sphinx for roosting in this area (Balasingh et al. 1995; Storz et al. 2000b; Gopukumar et al.
2003). When any of these accumulations are seen, then it is very likely that C. sphinx bats roost in these trees inside a partially enclosed cavity structure called ‘‘tent’’. We censused 229-day roosts over a year and analysed the roosting pattern of young C. sphinx. Every week 4–6-day roosts were censused. None of the tents were resurveyed during the study period. Bats were collected using a hoop net with an extensible aluminium pole. The entire tree was enveloped with a 6 m 9 m nylon mist net (Avinet Inc. USA) to prevent bats from escaping. For each bat, sex, age, forearm length and body mass were recorded. Age determination was done following Elangovan et al. (2003). Pups: Newborn individuals with soft fur and greyish pelage, suckled by the mother and remaining attached to the mothers as they are incapable of flight. This stage marks the onset of a decline in the total epiphyseal gap (fourth metacarpal–phalangeal joint). Juveniles: This stage lasts until the disappearance of the epiphyseal gap. There is a linear increase in the forearm length. The soft fur and greyish pelage are maintained. Subadults: This stage lasts from the disappearance of the epiphyseal gap until the asymptotic level in the growth of the forearm. Data were analysed to assess for any sexbiased dispersal by applying Z-tests to check
1616-5047/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2004.10.001 Mamm. biol. 70 (2005) 2 122–125
ARTICLE IN PRESS Dispersal patterns of the short-nosed fruit bat
for the proportion of females in different age classes. We checked whether the dispersal is age-biased by comparing the forearm length and body mass of both dispersed as well as nondispersed juvenile males by using the student’s ‘t’-test. Similarly, forearm length and body mass of dispersed and nondispersed juvenile females were also analysed. Altogether, 672 C. sphinx bats were captured from 229-day-roosts. Among these only 119day-roosts were occupied by harems. We excluded adult males from the present study. Among the young, 57 bats (30 males, 27 females) were pups, 67 (24 males, 43 females) were juveniles, and 52 (10 males and 42 females) were subadults (Fig. 1). The sex ratio of pups was almost 1:1. For pups the observed female proportion 1 equals 27/57. Z-statistic is given by (27 57 2)/ ^1 (1=ð4nÞ 2) where n ¼ 57: The null hypothesis that the female proportion is 12 among pups is acceptable (Z ¼ 0:4; P ¼ 0:69). In the juvenile stage fewer males (35%) were captured than females (65%) with a sex ratio of 1:1.8. The observed female proportion equals ^1 1 (43 67 2)/(1=ð4nÞ 2) where n ¼ 67: The null hypothesis that the female proportion is 12 among juveniles is not acceptable (Z ¼ 2:32; Po0:05). In the subadult stage, of the 52 individuals only 10 individuals were males. For subadults, the observed female propor^1 1 tion equals (42 52 2)/(1=ð4nÞ 2), where n ¼ 52: A female-biased sex ratio (1:4.2) was observed (Z ¼ 4:4; Po0:01). From April to September, we came across 18 harems where the numbers of post-lactating adult females were found to be disproportionate to the number of juveniles. In May, we captured five harems with post-lactating females but without any young. Among juveniles (n ¼ 67), 18% of juvenile females (n ¼ 8) and 20% of juvenile males (n ¼ 5) were captured without adults. All these observations indicated dispersal of juveniles from natal roosts. The mean forearm length (65.3673.78 mm) and mean body mass (33.473.9 g) of dispersed juvenile males were significantly higher than the mean forearm length (61.857 2.8 mm) and mean body mass (28.5674.73 g) of nondispersed juvenile males (forearm length of dispersed male vs. nondispersed
123
male t ¼ 2:403; P ¼ 0:023; body mass of dispersed male vs. nondispersed male t ¼ 2:128; P ¼ 0:043). This indicates the possibility of an age-biased dispersal among males. Juvenile females from dispersed (forearm length 64.06371.55 mm, and body mass 31.4373.5 g) and nondispersed (forearm length 61.9773.13 mm and body mass 29.3874.57 g) individuals showed no significant difference in the morphological variables (forearm length of dispersed females vs. nondispersed female t ¼ 1:816; P ¼ 0:078; body mass of dispersed females vs. nondispersed female t ¼ 1:176; P ¼ 0:247) indicating the absence of age-biased dispersal among females. The roosting pattern of subadults showed that all 10 subadult males roosted solitarily in places near to harems. Of the 42 subadult females, eight females (19%) were found roosting solitarily, five females (11.9%) joined established harems and 29 females (69%) formed a harem of a new generation of subadult females with an adult male. The present documentation showed the complete dispersal of juveniles of both sexes from their natal group before reaching the subadult stage. This inference is based on the capture of dispersed juveniles and capture of harems consisting of post-lactating females without young bats in the study area. Especially during the period when juvenile bats were predominant, the number of juvenile bats was disproportionate to the number of post-lactating females in many of the day roosts. The juvenile females outnumbered juvenile males, which suggests early male dispersal from the natal roost. Compared to juveniles, the sex ratio was highly skewed towards females in the subadult stage. From the total of 52 subadults, only 10 were males. Moreover, not a single subadult male bat was found to be roosting in a harem. The reasons for the low capture of subadult males were not clearly known. A low rate of juvenile survivorship may be one of the reasons. However, if young males preferred to roost in dense, unmodified and previously unoccupied foliages, the probability of censusing these bats should remain low. The capture of a large number of subadult females suggests that they either joined
ARTICLE IN PRESS 124
N. Gopukumar et al.
8
Sub-adults
6
4
2
0
15 Juveniles
No. of bats captured
20
10
5
0 12 10
Pups
8 6 4 2 0 Jan
Apr
Jul
Oct
Months Fig. 1. Monthly census of pups (30 males, 27 females), juveniles (24 males, 43 females) and subadults (10 males, 42 females) in the day roosts of Cynopterus sphinx at Palayamkottai, south India. ’ Males, & Females.
established harems, formed a new harem of subadult females with an adult male or they remained alone. However, we were unable to determine whether the dispersed young bats return back to their natal harems. Yet, with a recent study carried out in a particular
population of C. sphinx in Pune, India, Storz et al. (2000a) suggested that there is neither recruitment of females to natal harems nor do they join other harems in the same or neighbouring colonies. Young females joining harems have been documented in other
ARTICLE IN PRESS Dispersal patterns of the short-nosed fruit bat
bats, e.g. Artibeus jamaicensis and Phyllostomus hastatus. In A. jamaicensis, harems contain females of all ages, suggesting that subadult females join established harems (Handley et al. 1991), whereas harems of the greater spear-nosed bat P. hastatus are formed by a new generation of subadult females (McCracken and Bradbury 1977). However, harems with females of all age classes as well as harems of only subadult females were observed to be common in C. sphinx. We conclude that young female C. sphinx become members of a harem much earlier than their male counterparts. The advantage of nonharem young females staying near to established harems is not known. But this roosting pattern may improve the chances of young females’ breeding attempts as they attain sexual maturity far earlier (ca. 7 months) than males (ca. 18 months) (Sandhu 1984).
Acknowledgements The authors thank Dr. K. Sripathi, Dr. J. Balasingh, and Dr. V. Elangovan for their critical comments and suggestions. Financial assistance from Council of Scientific and Industrial Research (CSIR), New Delhi for a Senior Research Associateship to N.G. is gratefully acknowledged.
References Balasingh, J.; Koilraj, A.; Kunz, T. H. (1995): Tent construction by the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae) in southern India. Ethology 100, 210–229. Bain, J. R.; Humphrey, S. R. (1986): Social organization and biased primary sex ratio of the evening bat, Nycticeius humeralis. Florida Sci. 49, 22–31. Elangovan, V.; Priya, E. Y. S.; Raghuram, H.; Marimuthu, G. (2003): Postnatal development in the short-nosed fruit bat (Cynopterus sphinx): growth rate and age estimation. Acta Chiropterol. 5, 107–116.
125
Fleming, T. H. (1988): The Short-Tailed Fruit Bat: A Study in Plant–Animal Interactions. Chicago: University of Chicago Press. Gaisler, J. (1979): Ecology of bats. In: Ecology of Small Mammals. Ed. by D. M. Stoddart. London: Chapman & Hall. Pp. 281–342. Gopukumar, N.; Nathan, P. T.; Doss, D. P. S.; Prakash, A.; Emmanuel, K.; Balasingh, J.; Marimuthu, G.; Kunz, T. H. (2003): Early ontogeny of foraging behaviour in the shortnosed fruit bat Cynopterus sphinx (Megachiroptera): preliminary results. Mammalia 67, 139–145. Handley Jr., C. O.; Wilson, D. E.; Gardner, A. L. (1991): Demography and Natural History of the Common Fruit Bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Washington D.C.: Smithsonian Institution Press. Keen, R.; Hitchock, H. B. (1980): Survival and longevity of the little brown bat (Myotis lucifugus) in southeastern Ontario. J. Mammalogy 61, 1–7. Mani, M. S. (1974): The flora. In: Ecology and Biogeography in India. Ed. by M. S. Mani. The Hague, Netherlands: Dr. W. Junk Publishers. Pp. 159–177. McCracken, G. F.; Bradbury, J. W. (1977): Paternity and heterogeneity in the polygynous bat, Phyllostomus hastatus. Science 198, 303–306. Sandhu, S. (1984): Breeding biology of the Indian fruit bat, Cynopterus sphinx (Vahl) in central India. J. Bombay Nat. Hist. Soc. 81, 600–611. Storz, J. F.; Bhat, H. R.; Kunz, T. H. (2000a): Social structure of a polygynous tent-making bat Cynopterus sphinx (Megachiroptera). J. Zool. (London) 251, 151–165. Storz, J. F.; Balasingh, J.; Nathan, P. T.; EmmanueL, K.; Kunz, T. H. (2000b): Dispersion and site-fidelity in a tent-roosting population of the short-nosed fruit bat (Cynopterus sphinx) in southern India. J. Trop. Ecol. 16, 117–131.
Authors’ addresses: N. Gopukumar, and T. Karuppudurai, Department of Animal Behaviour and Physiology, School of Biological Sciences, Madurai Kamaraj University, Madurai 625021, India (e-mail: gopukumar99@ hotmail.com) D. P. Swami Doss, St. John’s College, Zoology Research Centre, Palayamkottai 627002, India.
www.elsevier.de/mambio
Short communication
Dispersal patterns of the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae) By N. Gopukumar, T. Karuppudurai and D.P. Swami Doss Department of Animal Behaviour and Physiology, School of Biological Sciences, Madurai Kamaraj University, Madurai, India; and St. John’s College, Zoology Research Centre, Palayamkottai, India Receipt of Ms. 22.5.2003 Acceptance of Ms. 15.10.2004
Key words: Cynopterus sphinx, Pteropodidae, sex ratio, dispersal
Bats are known to exhibit varying degrees of dispersal and philopatry based on their social system (McCracken and Bradbury 1977; Gaisler 1979; Keen and Hitchock 1980; Bain and Humphrey 1986; Fleming 1988; Handley et al. 1991). The short-nosed fruit bat Cynopterus sphinx is a frugivorous, megachiropteran bat living in groups. In C. sphinx, the juveniles of both sexes are believed to disperse completely from the natal harem (Storz et al. 2000a). However, the fate of young after dispersal remains poorly understood. Do they join established harems or do they aggregate to form a new harem? The aim of this study was to answer this question. The study was carried out from February 2000 to January 2001 in an area measuring approximately 15 km in diameter in the environs of Palayamkottai, South India (81440 S, 771420 E). This region is characterized by semi-arid tropical scrubland and thorn forest (Mani 1974). We located day roosts by citing the accumulation of rejected fruits, leaf pellets, seeds, and cut branches or leaves under trees, especially Borassus flabellifer, Washigtonia filifera, Caryota urens, Areca catechu, Polyalthia longifolia, and Vernonia scandens. According to earlier studies these are the major trees commonly used by C. sphinx for roosting in this area (Balasingh et al. 1995; Storz et al. 2000b; Gopukumar et al.
2003). When any of these accumulations are seen, then it is very likely that C. sphinx bats roost in these trees inside a partially enclosed cavity structure called ‘‘tent’’. We censused 229-day roosts over a year and analysed the roosting pattern of young C. sphinx. Every week 4–6-day roosts were censused. None of the tents were resurveyed during the study period. Bats were collected using a hoop net with an extensible aluminium pole. The entire tree was enveloped with a 6 m 9 m nylon mist net (Avinet Inc. USA) to prevent bats from escaping. For each bat, sex, age, forearm length and body mass were recorded. Age determination was done following Elangovan et al. (2003). Pups: Newborn individuals with soft fur and greyish pelage, suckled by the mother and remaining attached to the mothers as they are incapable of flight. This stage marks the onset of a decline in the total epiphyseal gap (fourth metacarpal–phalangeal joint). Juveniles: This stage lasts until the disappearance of the epiphyseal gap. There is a linear increase in the forearm length. The soft fur and greyish pelage are maintained. Subadults: This stage lasts from the disappearance of the epiphyseal gap until the asymptotic level in the growth of the forearm. Data were analysed to assess for any sexbiased dispersal by applying Z-tests to check
1616-5047/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2004.10.001 Mamm. biol. 70 (2005) 2 122–125
ARTICLE IN PRESS Dispersal patterns of the short-nosed fruit bat
for the proportion of females in different age classes. We checked whether the dispersal is age-biased by comparing the forearm length and body mass of both dispersed as well as nondispersed juvenile males by using the student’s ‘t’-test. Similarly, forearm length and body mass of dispersed and nondispersed juvenile females were also analysed. Altogether, 672 C. sphinx bats were captured from 229-day-roosts. Among these only 119day-roosts were occupied by harems. We excluded adult males from the present study. Among the young, 57 bats (30 males, 27 females) were pups, 67 (24 males, 43 females) were juveniles, and 52 (10 males and 42 females) were subadults (Fig. 1). The sex ratio of pups was almost 1:1. For pups the observed female proportion 1 equals 27/57. Z-statistic is given by (27 57 2)/ ^1 (1=ð4nÞ 2) where n ¼ 57: The null hypothesis that the female proportion is 12 among pups is acceptable (Z ¼ 0:4; P ¼ 0:69). In the juvenile stage fewer males (35%) were captured than females (65%) with a sex ratio of 1:1.8. The observed female proportion equals ^1 1 (43 67 2)/(1=ð4nÞ 2) where n ¼ 67: The null hypothesis that the female proportion is 12 among juveniles is not acceptable (Z ¼ 2:32; Po0:05). In the subadult stage, of the 52 individuals only 10 individuals were males. For subadults, the observed female propor^1 1 tion equals (42 52 2)/(1=ð4nÞ 2), where n ¼ 52: A female-biased sex ratio (1:4.2) was observed (Z ¼ 4:4; Po0:01). From April to September, we came across 18 harems where the numbers of post-lactating adult females were found to be disproportionate to the number of juveniles. In May, we captured five harems with post-lactating females but without any young. Among juveniles (n ¼ 67), 18% of juvenile females (n ¼ 8) and 20% of juvenile males (n ¼ 5) were captured without adults. All these observations indicated dispersal of juveniles from natal roosts. The mean forearm length (65.3673.78 mm) and mean body mass (33.473.9 g) of dispersed juvenile males were significantly higher than the mean forearm length (61.857 2.8 mm) and mean body mass (28.5674.73 g) of nondispersed juvenile males (forearm length of dispersed male vs. nondispersed
123
male t ¼ 2:403; P ¼ 0:023; body mass of dispersed male vs. nondispersed male t ¼ 2:128; P ¼ 0:043). This indicates the possibility of an age-biased dispersal among males. Juvenile females from dispersed (forearm length 64.06371.55 mm, and body mass 31.4373.5 g) and nondispersed (forearm length 61.9773.13 mm and body mass 29.3874.57 g) individuals showed no significant difference in the morphological variables (forearm length of dispersed females vs. nondispersed female t ¼ 1:816; P ¼ 0:078; body mass of dispersed females vs. nondispersed female t ¼ 1:176; P ¼ 0:247) indicating the absence of age-biased dispersal among females. The roosting pattern of subadults showed that all 10 subadult males roosted solitarily in places near to harems. Of the 42 subadult females, eight females (19%) were found roosting solitarily, five females (11.9%) joined established harems and 29 females (69%) formed a harem of a new generation of subadult females with an adult male. The present documentation showed the complete dispersal of juveniles of both sexes from their natal group before reaching the subadult stage. This inference is based on the capture of dispersed juveniles and capture of harems consisting of post-lactating females without young bats in the study area. Especially during the period when juvenile bats were predominant, the number of juvenile bats was disproportionate to the number of post-lactating females in many of the day roosts. The juvenile females outnumbered juvenile males, which suggests early male dispersal from the natal roost. Compared to juveniles, the sex ratio was highly skewed towards females in the subadult stage. From the total of 52 subadults, only 10 were males. Moreover, not a single subadult male bat was found to be roosting in a harem. The reasons for the low capture of subadult males were not clearly known. A low rate of juvenile survivorship may be one of the reasons. However, if young males preferred to roost in dense, unmodified and previously unoccupied foliages, the probability of censusing these bats should remain low. The capture of a large number of subadult females suggests that they either joined
ARTICLE IN PRESS 124
N. Gopukumar et al.
8
Sub-adults
6
4
2
0
15 Juveniles
No. of bats captured
20
10
5
0 12 10
Pups
8 6 4 2 0 Jan
Apr
Jul
Oct
Months Fig. 1. Monthly census of pups (30 males, 27 females), juveniles (24 males, 43 females) and subadults (10 males, 42 females) in the day roosts of Cynopterus sphinx at Palayamkottai, south India. ’ Males, & Females.
established harems, formed a new harem of subadult females with an adult male or they remained alone. However, we were unable to determine whether the dispersed young bats return back to their natal harems. Yet, with a recent study carried out in a particular
population of C. sphinx in Pune, India, Storz et al. (2000a) suggested that there is neither recruitment of females to natal harems nor do they join other harems in the same or neighbouring colonies. Young females joining harems have been documented in other
ARTICLE IN PRESS Dispersal patterns of the short-nosed fruit bat
bats, e.g. Artibeus jamaicensis and Phyllostomus hastatus. In A. jamaicensis, harems contain females of all ages, suggesting that subadult females join established harems (Handley et al. 1991), whereas harems of the greater spear-nosed bat P. hastatus are formed by a new generation of subadult females (McCracken and Bradbury 1977). However, harems with females of all age classes as well as harems of only subadult females were observed to be common in C. sphinx. We conclude that young female C. sphinx become members of a harem much earlier than their male counterparts. The advantage of nonharem young females staying near to established harems is not known. But this roosting pattern may improve the chances of young females’ breeding attempts as they attain sexual maturity far earlier (ca. 7 months) than males (ca. 18 months) (Sandhu 1984).
Acknowledgements The authors thank Dr. K. Sripathi, Dr. J. Balasingh, and Dr. V. Elangovan for their critical comments and suggestions. Financial assistance from Council of Scientific and Industrial Research (CSIR), New Delhi for a Senior Research Associateship to N.G. is gratefully acknowledged.
References Balasingh, J.; Koilraj, A.; Kunz, T. H. (1995): Tent construction by the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae) in southern India. Ethology 100, 210–229. Bain, J. R.; Humphrey, S. R. (1986): Social organization and biased primary sex ratio of the evening bat, Nycticeius humeralis. Florida Sci. 49, 22–31. Elangovan, V.; Priya, E. Y. S.; Raghuram, H.; Marimuthu, G. (2003): Postnatal development in the short-nosed fruit bat (Cynopterus sphinx): growth rate and age estimation. Acta Chiropterol. 5, 107–116.
125
Fleming, T. H. (1988): The Short-Tailed Fruit Bat: A Study in Plant–Animal Interactions. Chicago: University of Chicago Press. Gaisler, J. (1979): Ecology of bats. In: Ecology of Small Mammals. Ed. by D. M. Stoddart. London: Chapman & Hall. Pp. 281–342. Gopukumar, N.; Nathan, P. T.; Doss, D. P. S.; Prakash, A.; Emmanuel, K.; Balasingh, J.; Marimuthu, G.; Kunz, T. H. (2003): Early ontogeny of foraging behaviour in the shortnosed fruit bat Cynopterus sphinx (Megachiroptera): preliminary results. Mammalia 67, 139–145. Handley Jr., C. O.; Wilson, D. E.; Gardner, A. L. (1991): Demography and Natural History of the Common Fruit Bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Washington D.C.: Smithsonian Institution Press. Keen, R.; Hitchock, H. B. (1980): Survival and longevity of the little brown bat (Myotis lucifugus) in southeastern Ontario. J. Mammalogy 61, 1–7. Mani, M. S. (1974): The flora. In: Ecology and Biogeography in India. Ed. by M. S. Mani. The Hague, Netherlands: Dr. W. Junk Publishers. Pp. 159–177. McCracken, G. F.; Bradbury, J. W. (1977): Paternity and heterogeneity in the polygynous bat, Phyllostomus hastatus. Science 198, 303–306. Sandhu, S. (1984): Breeding biology of the Indian fruit bat, Cynopterus sphinx (Vahl) in central India. J. Bombay Nat. Hist. Soc. 81, 600–611. Storz, J. F.; Bhat, H. R.; Kunz, T. H. (2000a): Social structure of a polygynous tent-making bat Cynopterus sphinx (Megachiroptera). J. Zool. (London) 251, 151–165. Storz, J. F.; Balasingh, J.; Nathan, P. T.; EmmanueL, K.; Kunz, T. H. (2000b): Dispersion and site-fidelity in a tent-roosting population of the short-nosed fruit bat (Cynopterus sphinx) in southern India. J. Trop. Ecol. 16, 117–131.
Authors’ addresses: N. Gopukumar, and T. Karuppudurai, Department of Animal Behaviour and Physiology, School of Biological Sciences, Madurai Kamaraj University, Madurai 625021, India (e-mail: gopukumar99@ hotmail.com) D. P. Swami Doss, St. John’s College, Zoology Research Centre, Palayamkottai 627002, India.