Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T11:18:19.108Z Has data issue: false hasContentIssue false

Dietary resource overlap among three species of frugivorous bat in Costa Rica

Published online by Cambridge University Press:  03 May 2019

Lauren D. Maynard*
Affiliation:
Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA
Ariana Ananda
Affiliation:
John Muir College, University of California San Diego, La Jolla, CA 92092, USA
Maria Fernanda Sides
Affiliation:
Escuela de Ciencias Biológicas, Universidad Nacional de Costa Rica, Heredia, Costa Rica
Hannah Burk
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
Susan R. Whitehead
Affiliation:
Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
*

Abstract

The maintenance of biodiversity in tropical forests is thought to be dependent on fine-scale mechanisms of niche partitioning that allow species to coexist. This study examined whether three species of short-tailed fruit bat that co-occur at a lowland tropical forest site in Costa Rica (Carollia castanea, C. perspicillata, C. sowelli) avoid inter- and intraspecific competition through dietary specialization on species in the genus Piper. First, dietary composition was examined using faecal samples (N = 210), which yielded three main findings: (1) bat species and sexes vary in overall reliance on fruits of Piper, with a higher percentage of seeds of Piper detected in the diets of C. castanea (98.2%) and females (91.5%); (2) adults and juveniles partition species of Piper by habitat, with a lower percentage of mid- to late-successional species of Piper detected in adults (20.8%); and (3) overall, there is a strong dietary overlap among and within the three species of Carollia. Second, controlled choice experiments were conducted with individual bats (N = 123) to examine preferences for different species of Piper. These results indicated few differences in Piper preference based on bat species, sex, age class or reproductive status, suggesting preference is not the primary mechanism shaping the observed differences in dietary composition. Overall, the dietary composition and preference similarities suggest there is strong competition both among and within the three species of Carollia for food resources.

Type
Research Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature cited

Banack, SA (1998) Diet selection and resource use by flying foxes (Genus Pteropus). Ecology 79, 19491967.10.2307/176701CrossRefGoogle Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.10.18637/jss.v067.i01CrossRefGoogle Scholar
Bonaccorso, 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 and Kunz, TH (2007) Evidence for exploitative competition: comparative foraging behavior and roosting ecology of short-tailed fruit bats (Phyllostomidae). Biotropica 39, 249256.10.1111/j.1744-7429.2006.00251.xCrossRefGoogle Scholar
Brown, S and Lugo, A (1990) Tropical secondary forests. Journal of Tropical Ecology 6, 132.10.1017/S0266467400003989CrossRefGoogle Scholar
Charles-Dominique, P (1991) Feeding strategy and activity budget of the frugivorous bat Carollia perspicillata (Chiroptera: Phyllostomidae) in French Guiana. Journal of Tropical Ecology 7, 243256.10.1017/S026646740000540XCrossRefGoogle Scholar
Clark, DA (1980) Age- and sex-dependent foraging strategies of a small omnivore. Journal of Animal Ecology 49, 549563.10.2307/4263CrossRefGoogle Scholar
Clarke, KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117143.10.1111/j.1442-9993.1993.tb00438.xCrossRefGoogle Scholar
Cloyed, CS and Eason, PK (2017) Niche partitioning and the role of intraspecific niche variation in structuring a guild of generalist anurans. Royal Society Open Science 4, 170060.10.1098/rsos.170060CrossRefGoogle ScholarPubMed
Crawley, MJ (2007) Statistical modelling. In Crawley, MJ (ed.), The R Book. Chichester: Wiley, pp. 323386.10.1002/9780470515075.ch9CrossRefGoogle Scholar
Emmons, LH (1980) Ecology and resource partitioning among nine species of African rain forest squirrels. Ecological Monographs 50, 3154.10.2307/2937245CrossRefGoogle Scholar
Fleming, TH (1991) The relationship between body size, diet, and habitat use in frugivorous bats, genus Carollia (Phyllostomidae). Journal of Mammalogy 72, 493501.10.2307/1382132CrossRefGoogle Scholar
Fleming, TH (2004) Dispersal ecology of Neotropical Piper shrubs and treelets. In Dyer, LA and Palmer, ADN (eds), Piper: A Model Genus for Studies of Phytochemistry, Ecology, and Evolution, 1st Edition. Boston, MA: Springer, pp. 5877.10.1007/978-0-387-30599-8_4CrossRefGoogle Scholar
Giannini, NP and Kalko, EKV 2004. Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105, 209220.10.1111/j.0030-1299.2004.12690.xCrossRefGoogle Scholar
Herrera, LG, Gutierrez, E, Hobson, KA, Altube, B, Diaz, WG and Sanchez-Cordero, V (2002) Sources of assimilated proteins in five species of New World frugivorous bats. Oecologia 133, 280287.10.1007/s00442-002-1036-zCrossRefGoogle Scholar
Hieu, LD, Thang, TD, Hoi, TM and Ogunwande, IA (2014) Chemical composition of essential oils from four Vietnamese species of Piper (Piperaceae). Journal of Oleo Science 63, 211217.10.5650/jos.ess13175CrossRefGoogle Scholar
Hutchinson, GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? American Naturalist 93, 145159.10.1086/282070CrossRefGoogle Scholar
Jaramillo, MA and Callejas, R (2004) Current perspectives on the classification and phylogenetics of the genus Piper L. In Dyer, LA and Palmer, ADN (eds), Piper: A Model Genus for Studies of Phytochemistry, Ecology, and Evolution, 1st Edition. Boston, MA: Springer, pp. 179198.10.1007/978-0-387-30599-8_10CrossRefGoogle Scholar
Jaramillo, MA and Manos, PS (2001) Phylogeny and patterns of floral diversity in the genus Piper (Piperaceae). American Journal of Botany 88, 706716.10.2307/2657072CrossRefGoogle Scholar
Kartzinel, TR, Chen, PA, Coverdale, TC, Erickson, DL, Kress, WJ, Kuzmina, ML, Rubenstein, DI, Wang, W and Pringle, RM (2015) DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proceedings of the National Academy of Sciences USA 112, 80198024.10.1073/pnas.1503283112CrossRefGoogle ScholarPubMed
Kato, MJ and Furlan, M (2007) Chemistry and evolution of the Piperaceae. Pure and Applied Chemistry 79, 529538.10.1351/pac200779040529CrossRefGoogle Scholar
Kunz, TH, Hodgkison, R and Weise, CD (2009) Methods of capturing and handing bats. In Kunz, TH and Parsons, S (eds), Ecological and Behavioral Methods for the Study of Bats, Second Edition. Baltimore, MD: Johns Hopkins University Press, pp. 335.Google Scholar
Lewis, R, O’Connell, TC, Lewis, M, Campagna, C and Hoelzel, AR (2006) Sex-specific foraging strategies and resource partitioning in the southern elephant seal (Mirounga leonina). Proceedings of the Royal Society B: Biological Sciences 273, 29012907.10.1098/rspb.2006.3642CrossRefGoogle Scholar
Lopez, JE and Vaughan, C (2007) Food niche overlap among neotropical frugivorous bats in Costa Rica. Revista de Biología Tropical 55, 301313.Google ScholarPubMed
MacArthur, R and Levins, R (1967) The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101, 377385.10.1086/282505CrossRefGoogle Scholar
McNab, BK (1971) The structure of tropical bat faunas. Ecology 52, 352358.10.2307/1934596CrossRefGoogle Scholar
Minchin, PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69, 89107.10.1007/BF00038690CrossRefGoogle Scholar
Mott, R, Herrod, A and Clarke, RH (2017) Resource partitioning between species and sexes in Great Frigatebirds and Lesser Frigatebirds. The Auk 134, 153167.10.1642/AUK-16-184.1CrossRefGoogle Scholar
Pacala, S and Roughgarden, J (1982) Resource partitioning and interspecific competition in two two-species insular Anolis lizard communities. Science 217, 444446.Google ScholarPubMed
Phillips, H, Newbold, T and Purvis, A (2017) Land-use effects on local biodiversity in tropical forests vary between continents. Biodiversity and Conservation 26, 22512270.10.1007/s10531-017-1356-2CrossRefGoogle Scholar
Pianka, ER (1973) The structure of lizard communities. Annual Review of Ecology and Systematics 4, 5374.10.1146/annurev.es.04.110173.000413CrossRefGoogle Scholar
Roughgarden, J (1976) Resource partitioning among competing species– a coevolutionary approach. Theoretical Population Biology 9, 388424.10.1016/0040-5809(76)90054-XCrossRefGoogle ScholarPubMed
Samarah, CK (2017) Chao, jackknife and bootstrap estimators of species richness. International Journal of Applied Mathematical Analysis and Applications 12, 715.Google Scholar
Tamsitt, JR (1967) Niche and species diversity in Neotropical bats. Nature 213, 784786.10.1038/213784a0CrossRefGoogle Scholar
Thies, W and Kalko, EKV (2004) Phenology of Neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae). Oikos 104, 362376.10.1111/j.0030-1299.2004.12747.xCrossRefGoogle Scholar
Thies, W, Kalko, E and Schnitzler, H (2006) Influence of environment and resource availability on activity patterns of Carollia castanea (Phyllostomidae) in Panama. Journal of Mammalogy 87, 331338.10.1644/05-MAMM-A-161R1.1CrossRefGoogle Scholar
Whitehead, SR and Bowers, MD (2014) Chemical ecology of fruit defence: synergistic and antagonistic interactions among amides from Piper. Functional Ecology 28, 10941106.10.1111/1365-2435.12250CrossRefGoogle Scholar
Whitehead, SR, Jeffrey, CS, Leonard, MD, Dodson, CD, Dyer, LA and Bowers, MD (2013) Patterns of secondary metabolite allocation to fruits and seeds in Piper reticulatum. Journal of Chemical Ecology 39, 13731384.10.1007/s10886-013-0362-4CrossRefGoogle ScholarPubMed
Whitehead, SR, Obando-Quesada, MF and Bowers, MD (2016) Chemical tradeoffs in seed dispersal: defensive metabolites in fruits deter consumption by mutualist bats. Oikos 125, 927937.10.1111/oik.02210CrossRefGoogle Scholar
York, HA and Billings, SA (2009) Stable-isotope analysis of diets of short-tailed fruit bats (Chiroptera: Phyllostomidae: Carollia). Journal of Mammalogy 90, 14691477.10.1644/08-MAMM-A-382R.1CrossRefGoogle Scholar
York, HA and Papes, M (2007) Limiting similarity and species assemblages in the short-tailed fruit bats. Journal of Zoology 273, 249256.10.1111/j.1469-7998.2007.00321.xCrossRefGoogle Scholar