Abstract
Many plant species have seeds embedded in their fleshy pulp to attract frugivores, which enhances the chance of seed dispersal. However, some tropical plants are evolved with sharp spines to avoid herbivores and/or to prevent water loss, which makes foraging by frugivores difficult. Such plants receive frugivores’ attention, either because of resource scarcity or adaptive behavioural plasticity. We have a limited understanding of how fruit-eating animals access fruits protected by spines. In this 1-year study, we describe bat foraging on a spiny tropical shrub, Ziziphus mauritiana (Rhamnaceae) whose dried branches are often used by the local people to capture bats in caves that inevitably damage their wing membranes. The greater short-nosed fruit bat, Cynopterus sphinx was the only visitor to this spiny plant during its fruiting season and predominantly extracted fruits using a hovering tactic (on 81% observations) without damaging wing membranes. The hovering enabled them to extract fruits quicker than when alighting on the tree. Bats carried all the fruits away from the parent tree to feeding roosts for consumption. Bat foraging has thus effectuated short-distance seed dispersal (range 11–70 m radii) in which most seeds (30.73%) were found at the distance of 31–40 m in our search up to 150 m. Although bats extracted both ripe and unripe fruits, ripe-fruit extraction was 4.5 × higher than the unripe fruits. This study shows the tradeoff between getting a good meal and contending with spines in a resource-scarce habitat. Besides, this study describes the adaptive foraging tactics of greater short-nosed fruit bats that facilitate short-distance seed dispersal.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
All the data and materials used in the study are original and no metadata has been used in this study.
Data availability
All data generated or analysed during this study are included in this article.
Code availability
Not applicable.
References
Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149. https://doi.org/10.1890/0012-9658(2006)87[132:PDS]2.0.CO;2
Alpízar P, Schneider J, Tschapka M (2020) Bats and bananas: simplified diet of the nectar-feeding bat Glossophaga soricina (Phyllostomidae: Glossophaginae) foraging in Costa Rican banana plantations. Glob Ecol Conserv 24:e01254. https://doi.org/10.1016/j.gecco.2020.e01254
Alves RJV, Pinto AC, da Costa AVM, Rezende CM (2005) Ziziphus mauritiana Lam. (Rhamnaceae) and the chemical composition of its floral fecal odor. J Braz Chem Soc 16:654–656. https://doi.org/10.1590/S0103-50532005000400027
Armani M, Charles-Dominique T, Barton KE, Tomlinson KW (2019) Developmental constraints and resource environment shape early emergence and investment in spines in saplings. Ann Bot 124:1133–1142. https://doi.org/10.1093/aob/mcz152
Aziz SA, McConkey KR, Tanalgo K, Sritongchuay T, Low M-R, Yong JY, Mildenstein TL, Nuevo-Diego CE, Lim VC, Racey PA (2021) The critical importance of Old World fruit bats for healthy ecosystems and economies. Front Ecol Evol 9:641411. https://doi.org/10.3389/fevo.2021.641411
Balasingh J, Ronald J, Nathan PT, Isaac SS (1999) Occurrence of Cynopterus brachyotis (Chiroptera: Pteropodidae) in Kalakad Mundanthurai Tiger Reserve, southern India. Curr Sci 76:1542
Baldwin JW, Dechmann DKN, Thies W, Whitehead SR (2020) Defensive fruit metabolites obstruct seed dispersal by altering bat behavior and physiology at multiple temporal scales. Ecology 101:e02937. https://doi.org/10.1002/ecy.2937
Belwood JJ, Morris GK (1987) Bat predation and its influence on calling behavior in neotropical katydids. Science 238:64–67. https://doi.org/10.1126/science.238.4823.64
Burrows FM (1986) The aerial motion of seeds, fruits, spores and pollen. In: Murray DR (ed) Seed dispersal. Academic Press, Sydney, pp 2–48
Cazetta E, Schaefer HM, Galetti M (2008) Does attraction to frugivores or defense against pathogens shape fruit pulp composition? Oecologia 155:277–286. https://doi.org/10.1007/s00442-007-0917-6
Chan AAQ, Aziz SA, Clare EL, Coleman JL (2021) Diet, ecological role and potential ecosystem services of the fruit bat, Cynopterus brachyotis, in a tropical city. Urban Ecosyst 24:251–263. https://doi.org/10.1007/s11252-020-01034-x
Chapman CA, Chapman LJ (1996) Frugivory and the fate of dispersed and non-dispersed seeds of six African tree species. J Trop Ecol 12:491–504. https://doi.org/10.1017/S026646740000972X
Chapman CA, Chapman LJ, Wangham W, Hunt K, Lebo D, Gardner L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531. https://doi.org/10.2307/2389015
Chattopadhyay B, Garg KM, Kumar AK, Doss DP, Rheindt FE, Kandula S, Ramakrishnan U (2016) Genome-wide data reveal cryptic diversity and genetic introgression in an Oriental cynopterine fruit bat radiation. BMC Evol Biol 16:41. https://doi.org/10.1186/s12862-016-0599-y
Corlett RT (2011) How to be a frugivore (in a changing world). Acta Oecol 37:674–681. https://doi.org/10.1016/j.actao.2011.01.005
Dhileepan K (2017) Biological control of Ziziphus mauritiana (Rhamnaceae): feasibility, prospective agents and research gaps. Ann Appl Biol 170:287–300. https://doi.org/10.1111/aab.12338
Drake DR, McConkey KR (2021) Novel diplochory: native bats and non-native rats disperse seeds of an island tree. Acta Oecol 111:103719. https://doi.org/10.1016/j.actao.2021.103719
Elangovan V (2000) Foraging behavior of a frugivorous bat Cynopterus sphinx. PhD Dissertation, Madurai Kamaraj University, Madurai, India
Elangovan V, Marimuthu G, Kunz TH (2000) Nectar feeding behaviour in the short-nosed fruit bat Cynopterus sphinx (Pteropodidae). Acta Chiropterol 2:1–5
Elangovan V, Marimuthu G, Kunz TH (2001) Temporal patterns of resource use by the short-nosed fruit bat, Cynopterus sphinx. J Mammal 82:161–165. https://doi.org/10.1644/1545-1542(2001)08
Elangovan V, Priya EYS, Marimuthu G (2006) Olfactory discrimination ability of the short-nosed fruit bat Cynopterus sphinx. Acta Chiropterol 8:247–253. https://doi.org/10.3161/1733-5329(2006)8[247:ODAOTS]2.0.CO;2
Fleming TH, Breitwisch R, Whitesides GH (1987) Patterns of tropical vertebrate frugivore diversity. Ann Rev Ecol Syst 18:91–109. https://doi.org/10.1146/annurev.es.18.110187.000515
Frick WF, Heady PA III, Hayes JP (2009) Facultative nectar-feeding behavior in a gleaning insectivorous bat (Antrozous pallidus). J Mammal 90:1157–1164. https://doi.org/10.1644/09-MAMM-A-001.1
Frick WF, Price RD, Heady PA, Kay KM (2013) Insectivorous bat pollinates columnar cactus more effectively per visit than specialized nectar bat. Am Nat 181:137–144. https://doi.org/10.1086/668595
Gelmi-Candusso TA, Hämäläinen AM (2019) Seeds and the city: the interdependence of zoochory and ecosystem dynamics in urban environments. Front Ecol Evol 7:41. https://doi.org/10.3389/fevo.2019.00041
Geluso K, Keele EC, Pauley NM, Gomez IR, Tye SP (2018) Night roosting behaviors for the Northern Long-eared Myotis (Myotis septentrionalis) under a bridge revealed by time-lapse photography. Am Midl Nat 179:287–293. https://doi.org/10.1674/0003-0031-179.2.287
Grice AC (1996) Seed production, dispersal and germination in Cryptostegia grandiflora and Ziziphus mauritiana, two invasive shrubs in tropical woodlands of northern Australia. Aust J Ecol 21:234–331
Hocking D (1993) Trees for Drylands. Oxford & IBH Publishing Co Pvt. Ltd., New Delhi, India
Hodgkison R, Ayasse M, Häberlein C, Schulz S, Zubaid A, Mustapha WAW, Kunz TH, Kalko EKV (2013) Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behavior of bats in the New and Old World tropics. Funct Ecol 27:1075–1084. https://doi.org/10.1111/1365-2435.12101
Howe HF (1986) Seed dispersal by fruit-eating birds and mammals. In: Murray DR (ed) Seed dispersal. Academic Press, Sydney, pp 123–190
Jordano P, Garcia C, Godoy JA, Garcia-Castano JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. PNAS 104:3278–3282. https://doi.org/10.1073/pnas.0606793104
Karuppudurai T, Sripathi K (2018) Foraging and roosting ecology of the Lesser Dog-faced fruit bat Cynopterus brachyotis (Mammalia: Chiroptera: Pteropodidae) in southern India. J Threat Taxa 10:12163–12172. https://doi.org/10.11609/jott.3850.10.9.12163-12172
Knight T, Jones G (2009) Importance of night roosts for bat conservation: roosting behavior of the lesser horseshoe bat Rhinolophus hipposideros. Endanger Species Res 8:79–86. https://doi.org/10.3354/esr00194
Korine C, Kalko EKV (2005) Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction. Behav Ecol Sociobiol 59:12–23. https://doi.org/10.1007/s00265-005-0003-1
Kunz TH, De Torrez EB, Bauer DM, Lobova TA, Fleming TH (2011) Ecosystem services provided by bats. Ann NY Acad Sci 1223:1–38. https://doi.org/10.1111/j.1749-6632.2011.06004.x
Leisler-Miller LB, Kaliszewska ZA, Lauterbur ME, Mann B, Rifell JA, Santana SE (2020) A fruitful endeavor: scent cues and echolocation behavior used by Carollia castanea to find fruit. Integr Organism Biol. https://doi.org/10.1093/iob/obaa007
Loumassine HE, Bonnot N, Allegrini B, Bendjeddou ML, Bounaceur F, Auglagnier S (2020) How arid environments affect spatial and temporal activity of bats. J Arid Environ 180:104206. https://doi.org/10.1016/j.jaridenv.2020.104206
Mahandran V, Raghuram H, Nathan PT (2016) Geophagy by the Indian short-nosed fruit bat, Cynopterus sphinx (Pteropodidae) while foraging on Madhuca latifolia (Sapotaceae) in Tamil Nadu, India. Acta Ethol 19:95–99. https://doi.org/10.1007/s10211-015-0227-7
Mahandran V, Murugan CM, Nathan PT (2017) Effect of female group size on harem male roosting behavior of the Indian short-nosed fruit bat Cynopterus sphinx. Acta Ethol 21:43–49. https://doi.org/10.1007/s10211-017-0276-1
Mahandran V, Murugan CM, Marimuthu G, Nathan PT (2018) Seed dispersal of a tropical deciduous Mahua tree, Madhuca latifolia (Sapotaceae) exhibiting bat-fruit syndrome by pteropodid bats. Glob Ecol Conserv 14:e00396. https://doi.org/10.1016/j.gecco.2018.e00396
Mahandran V, Murugan CM, Wang G, Chen J, Nathan PT (2021) Multimodal cues facilitate ripe-fruit localization and extraction in free-ranging pteropodid bats. Behav Process 189:104426. https://doi.org/10.1016/j.beproc.2021.104426
Milne DJ, Fisher A, Rainey I, Pavey CR (2005) Temporal patterns of bats in the top end of the northern territory, Australia. J Mammal 86:909–920. https://doi.org/10.1644/1545-1542(2005)86[909:TPOBIT]2.0.CO;2
Muchhala N (2006) Nectar bat stows huge tongue in rib cage. Nature 444:701–702. https://doi.org/10.1038/444701a
Muchhala N, Thomson JD (2009) Going to great lengths: selection for long corolla tubes in an extremely specialized bat-flower mutualism. Proc R Soc B 276:2147–2152. https://doi.org/10.1098/rspb.2009.0102
Murray DR (1986) Seed dispersal by water. In: Murray DR (ed) Seed dispersal. Academic Press, Sydney, pp 49–86
Murugan CM, Saravana-Bhavan P, Nathan PT, Mahandran V (2020) Hunting bats for bushmeat despite Nipah concerns in Idukki, Kerala, India. Ecotropica 22:202006. https://doi.org/10.30427/ecotrop202006
Nathan PT, Raghuram H, Elangovan V, Karuppudurai T, Marimuthu G (2005) Bat pollination of Kapok tree, Ceiba pentandra. Curr Sci 88:1679–1681
Nathan PT, Karuppudurai T, Raghuram H, Marimuthu G (2009) Bat foraging strategies and pollination of Madhuca latifolia (Sapotaceae) in Southern India. Acta Chiropterol 11:435–441. https://doi.org/10.3161/150811009X485657
Noble JC (1991) On ratites and their interactions with plants. Rev Chil De Hist Nat 64:85–118
Parameswaran K (2014) Roosting ecology and conservation status of bats in and around Salem, Tamil Nadu. MSc Dissertation, Periyar University, Salem, India
Rajive S (2017) Foraging and feeding ecology of Indian short-nosed fruit bat, Cynopterus sphinx through mist-netting and observation at foraging ground and feeding roosts. MSc Dissertation, Periyar University, Salem, India
Ripperger SP, Rehse S, Wacker S, Kalko EKV, Schulz S, Rodriguez-Herrera B, Ayasse M (2019) Nocturnal scent in a ‘bird-fig’: a cue to attract bats as additional dispersers? PLoS One 14:e0220461. https://doi.org/10.1371/journal.pone.0220461
Shilton LA, Altringham JD, Compton SG, Whittaker RJ (1999) Old World fruit bats can be long-distance seed dispersers through extended retention of viable seeds in the gut. Proc R Soc Lond B 266:219–223. https://doi.org/10.1098/rspb.1999.0625
Singaravelan N (2002) Foraging behavior of fruit bats in orchards. PhD Dissertation, Madurai Kamaraj University, Madurai, India
Singaravelan N, Marimuthu G (2004) Nectar feeding and pollen carrying from Ceiba pentandra by pteropodid bats. J Mammal 85:1–7. https://doi.org/10.1644/1545-1542(2004)085%3c0001:NFAPCF%3e2.0.CO;2
Singaravelan N, Marimuthu G (2006) Muntingia calabura—an attractive food plant of Cynopterus sphinx—deserves planting to lessen orchard damage. Acta Chiropterol 8:239–245. https://doi.org/10.3161/1733-5329(2006)8[239:MCAAFP]2.0.CO;2
Singaravelan N, Marimuthu G (2008) In situ feeding tactics of short-nosed fruit bats (Cynopterus sphinx) on mango fruits: evidence of extractive foraging in a flying mammal. J Ethol 26:1–7. https://doi.org/10.1007/s10164-007-0044-1
Spoelstra K, van Grunsven RHA, Ramakers JJC, Ferguson KB, Raap T, Donners M, Veenendaal EM, Visser ME (2017) Response of bats to light with different spectra: light-shy and agile bat presence is affected by white and green, but not red light. Proc R Soc B 284:20170075. https://doi.org/10.1098/rspb.2017.0075
Tang ZH, Xu JL, Flanders J, Ding XM, Ma XF, Sheng LX, Cao M (2012) Seed dispersal of Syzygium oblatum (Myrtaceae) by two species of fruit bat (Cynopterus sphinx and Rousettus leschenaulti) in South-West China. J Trop Ecol 28:255–261. https://doi.org/10.1017/S0266467412000156
Tschapka M, Gonzalez-Terrazas TP, Knörnschild M (2015) Nectar uptake in bats using a pumping-tongue mechanism. Sci Adv 1:e1500525. https://doi.org/10.1126/sciadv.1500525
Valiente-Banuet A, Arizmendi MC, Martinez AR, Dominguez-Canseco L (1996) Ecological relationship between columnar cacti and nectar feeding bats in Mexico. J Trop Ecol 12:103–119. https://doi.org/10.1017/S0266467400009330
Voigt CC (2013) Bat flight with bad wings: is flight metabolism affected by damaged wings? J Exp Biol 216:1516–1521. https://doi.org/10.1242/jeb.079509
Voigt CC, Capps KA, Dechmann DKN, Michener RH, Kunz TH (2008) Nutrition or detoxification: why bats visit mineral licks of the Amazonian rainforest. PLoS One 3:e2011. https://doi.org/10.1371/journal.pone.0002011
Wenny DG (2000) Seed dispersal, seed predation and seedling recruitment of a Neotropical mountain tree. Ecol Monogr 70:331–351. https://doi.org/10.2307/2657180
Zhang SY, Wang LX (1995) Fruit consumption and seed dispersal of Ziziphus cinnamomum (Rhamnaceae) by two sympatric primates (Cebus apella and Ateles paniscus) in French Guiana. Biotropica 27:397–401. https://doi.org/10.2307/2388926
Acknowledgements
We are grateful to two anonymous reviewers for constructive criticisms on the earlier version of this manuscript. We extend our thanks to Ms. Dona Maria (for language improvement), Mr. K. Chandhirasekar, Mr. R. Dheebarasu and Mr. P. Arulmani (for field assistance).
Funding
This study received financial supports from the Periyar University, Salem (Ref. no. PU/AD-3/URF/2016 and 2018) to DS and CMM, National Natural Science Foundation of China (International Cooperation and Exchange Project no. 31950410559) and XTBG postdoctoral fellowship to VM, and Indian National Science Academy, New Delhi, India to GM.
Author information
Authors and Affiliations
Contributions
DS and CMM conducted the fieldwork and equally contributed to this study, VM analysed the data and led the writing of the manuscript, PTN designed and supervised the study and GM edited the manuscript. All the authors contributed substantially to the draft and gave consent for the publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose. The authors have no conflicts of interest to declare that are relevant to the content of this article. All authors certify that they have no affiliations with or involvement in any organisation or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript. The authors have no financial or proprietary interests in any material discussed in this article.
Ethics approval
Animals were not captured in this study hence ethical clearance from the animal use committee was not required for this study.
Consent to participate
Not applicable.
Consent for publication
All authors read the final draft and gave consent for the publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Below is the link to the electronic supplementary material.
About this article
Cite this article
Sangavi, D., Murugan, C.M., Mahandran, V. et al. Adaptive foraging tactics of greater short-nosed fruit bats on a spiny shrub and its effect on seed dispersal. J Ethol 39, 353–361 (2021). https://doi.org/10.1007/s10164-021-00711-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-021-00711-4