Bat Assemblage in an Oil Palm Plantation from the Colombian Llanos Foothills

Main Article Content

Alejandra Maria Cely-Gomez
Dennis Castillo-Figueroa
Jairo Perez

Abstract

The surge of oil palm production in the Neotropics has become a major concern about the potential impacts on biodiversity. In the Colombian Orinoquia, which has shown a massive landscape transformation due to the growth of oil palm plantations, the effects of oil palm agriculture on bats in this region have not been studied up to date. To understand the impact of habitat conversion on bat diversity, we characterized bat assemblages in secondary forest and palm plantations in the Colombian Piedmont foothills (Meta, Colombia). We captured 393 individuals (forest = 81, plantation = 312) of 18 species and three families. The forest cover presented three exclusive species while the plantation had five. Species diversity (q1) and evenness (J’) were higher in the forest compared to the plantation. These differences derived from the increase in abundances of generalist species (Artibeus sp., Carollia spp.) in the plantation. Despite the habitat simplification caused by oil palm plantations, this monoculture provides a cover that is used by some bats, decreasing their risk of predation and allowing movement between patches of forest habitat as stepping-stones. Maintaining forest cover in agricultural landscapes favors diversity by generating a “spillover effect” of the forest towards plantations, which in the case of some bats contributes to the reduction of species isolation and the maintenance of ecosystem services provided by them. It is important to improve management practices of oil palm plantations to minimize negative impacts on biodiversity, considering the expansion of this productive system and the scarcity of protected areas in this region.

Article Details

How to Cite
Bat Assemblage in an Oil Palm Plantation from the Colombian Llanos Foothills. (2021). Tropical Life Sciences Research, 32(1), 47–61. https://doi.org/10.21315/tlsr2021.32.1.3
Section
Original Article

References

Bejarano-Bonilla D A, Yate-Rivas A and Bernal-Bautista M H. (2007). Diversidad y distribución de la fauna quiróptera en un transecto altitudinal en el departamento del Tolima, Colombia. Caldasia 29(2): 297–308.

Bennett R E, Leuenberger W, Bosarreyes Leja B B, Sagone Cáceres A, Johnson K and Larkin J. (2018). Conservation of Neotropical migratory birds in tropical hardwood and oil palm plantations. PLoS ONE 13(12): e0210293. https://doi.org/10.1371/journal.pone.0210293

Bonaccorso F J and Smythe N. (1972). Punch-marking bats: An alternative to banding. Journal of Mammalogy 53(2): 389–390. https://doi.org/10.2307/1379186

Boron V, Deere N J, Xofis P, Link A, Quiñones-Guerrero A, Payán E and Tzanopoulus J. (2019). Richness, diversity, and factors influencing occupancy of mammal communities across human-modified landscapes in Colombia. Biological Conservation 232: 108–116. https://doi.org/10.1016/j.biocon.2019.01.030

Brown D E. (1994). The vampire bat in fact and fantasy. N. Mexico D.F: High-Lonesome Books. Castaño J H, Carranza J A and Pérez-Torres J. (2018). Diet and trophic structure in assemblages of montane frugivorous phyllostomid bats. Acta Oecologica 91: 81–90. https://doi.org/10.1016/j.actao.2018.06.005

Castaño J H. (2009). Murciélagos frugívoros y plantas quiropterocoras: Descubriendo la estructura de sus interacciones mutualistas en una selva semi-caducifolia. Master diss., Universidad de Los Andes, Venezuela.

Castiblanco C, Etter A and Aide T M. (2013) Oil palm plantations in Colombia: A model of future expansion. Environmental Science & Policy 27: 172–183. https://doi.org/10.1016/j.envsci.2013.01.003

Castillo-Figueroa D, Martínez-Medina D, Rodríguez-Posada M E and Bernal-Vergara S. (2019). Structural differences in mammal assemblages between savanna ecosystems of the Colombian Llanos. Papéis Avulsos de Zoologia (SPaulo) 59: e20195914. https://doi.org/10.11606/1807-0205/2019.59.14

Castillo-Figueroa D and Pérez-Torres J. (2018). Respuestas funcionales de murciélagos asociados a fragmentos de bosque seco tropical en Córdoba (Colombia): implicaciones del tipo de manejo en sistemas de ganadería extensiva. Revista Biodiversidad Neotropical 8(3): 197–211.

Cely-Gómez M A and Castillo-Figueroa D. (2019). Diet of dominant frugivorous bat species in an oil palm landscape from Colombian Llanos: Implications for forest conservation and recovery. Therya 10(2): 149–153. https://doi.org/10.12933/therya-19-682

Chao A and Hsieh T C. (2015). The online program SpadeR: Species-richness prediction and diversity estimation in R. program and user’s guide. Hsinchu, Taiwan: National Tsing Hua University.

Cleary K A, Waits L P and Finegan B. (2016). Agricultural intensification alters bat assemblage composition and abundance in a dynamic neotropical landscape. Biotropica 48(5): 667–676. https://doi.org/10.1111/btp.12327

Cleveland C, Betke M, Federico P, Frank J, Hallam T, Horn J, López J, McCracken G, Medellín R, Moreno-Valdez A, et al. (2006). Economic value of the pest control service provided by Brazilian free-tailed bats in south-central Texas. Frontiers in Ecology and the Environment 4(5): 238–243. https://doi.org/10.1890/1540-9295(2006)004 [0238:EVOTPC]2.0.CO;2

Colwell R K. (2013). EstimateS: Statistical estimation of species richness and shared species from samples (Software), Version 9.1.0. Available at: http://viceroy.colorado.edu/estimates/

Danielsen F and Heegaard M. (1995). Impact of logging and plantation development on species diversity: A case study from Sumatra. In: Sandbukt O (ed.), Management of tropical forests: Towards an integrated perspective. Oslo: University of Oslo, 73–92.

Estrada-Villegas S, Pérez-Torres J and Stevenson P. (2010). Ensamblaje de murciélagos en un bosque subandino colombiano y análisis sobre la dieta de algunas especies. Mastozoologia Neotropical 17: 31–41.

Estrada A and Coates-Estrada R. (2002). Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, México. Biological Conservation 103: 237–245. https://doi.org/10.1016/S0006-3207(01)00135-5

Estrada A, Coates-Estrada R and Meritt D. (1993). Bat species richness and abundance in tropical rain forest fragments and in agricultural habitats at Los Tuxtlas, México. Ecography 16: 309–318. https://doi.org/10.1111/j.1600-0587.1993.tb00220.x

Etter A, Sarmiento A and Romero M H. (2011). Land use changes (1970–2020) and carbon emissions in the Colombian Llanos. In: Hanan N P and Hill M J. (eds.). Ecosystem function in savannas measurement and modeling at landscape to global scales. Boca Raton, USA: CRC Press, 383–402.

Fukuda D, Tisen O B, Momose K and Sakai S. (2009). Bat diversity in the vegetation mosaic around a lowland dipterocarp forest of Borneo. The Raffles Bulletin of Zoology 57: 213–221.

Faruk A, Belabut D, Ahmad N, Knell R J and Garner T W J. (2013). Effects of oil-palm plantations on diversity of tropical Anurans. Conservation Biology 27: 615–624. https://doi.org/10.1111/cobi.12062

Federación Nacional de Cultivadores de Palma de Aceite (Fedepalma). (2019). Anuario estadístico 2019: Principales cifras de la agroindustria de la palma de aceite en Colombia. Bogotá: Fedepalma.

Freudmann A, Mollik P and Tschapka M. (2015). Impacts of oil palm agriculture on phyllostomid bat assemblages. Biodiversity and Conservation 24(14): 3583–3599. https://doi.org/10.1007/s10531-015-1021-6

Gardner A L. (2007). Mammals of South America. Volume 1: Marsupials, Xenarthrans, shrews, and bats. Chicago: University of Chicago Press. https://doi.org/10.7208/chicago/9780226282428.001.0001

Gallmetzer N and Schulze C H. (2015). Impact of oil palm agriculture on understory amphibians and reptiles: A Mesoamerican perspective. Global Ecology and Conservation 4: 95–109. https://doi.org/10.1016/j.gecco.2015.05.008

Gilroy J J, Prescott G W, Cardenas J S, Castañeda P G, Sánchez A, Rojas-Murcia L E, Medina Uribe C A, Haugassen T and Edwards D P. (2015). Minimizing the biodiversity impact of Neotropical oil palm development. Global Change Biology 21(4): 1531–1540. https://doi.org/10.1111/gcb.12696

Hammer O, Harper D A and Ryan P R. (2001). Past: Paleontological statistics software for education and data analysis. Palaeontologia Electronica 4(1): 1–9.

Heer K, Helbig-Bonitz M, Fernandes R G and Kalko E K V. (2015). Effects of land use on bat diversity in a complex plantation-forest landscape in northeastern Brazil. Journal of Mammalogy 96(4): 1–12. https://doi.org/10.1093/jmammal/gyv068

Iragorri-Valencia A. (2016). Words by the minister of agriculture and rural development. Revista Palmas 37: 155–157. Jost L. (2006). Entropy and diversity. Oikos 113: 363–375. https://doi.org/10.1111/j.2006.0030-1299.14714.x

Kasso M and Balakrishnan M. (2013). Ecological and economic importance of bats (Order Chiroptera). ISRN BIodiversity 2013: 187415. https://doi.org/10.1155/2013/187415

Kraker-Castañeda C and Pérez-Consuegra S G. (2011). Contribución de los cafetales bajo sombra en la conservación de murciélagos en la antigua Guatemala, Guatemala. Acta Zoológica Mexicana 27: 291–303. https://doi.org/10.21829/azm.2011.272754

Kunz T H and Parsons S. (1988). Ecological and behavioral methods for the study of bats. Washington: Smithsonian Institution Press. Kunz T H, Torrez E B, Bauer D, Lobova T and Fleming T H. (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223: 1–38. https://doi.org/10.1111/j.1749-6632.2011.06004.x

López-Ricaurte L, Edwards D P, Romero Rodríguez, N and Gilroy J J. (2017). Impacts of oil palm expansion on avian biodiversity in a Neotropical natural savanna. Biological Conservation 213: 225–233. https://doi.org/10.1016/j.biocon.2017.07.009

Lucey J M, Tawatao N, Senior M J M, Khen C V, Benedick S, Hamer K C, Woodcock P, Newton R J, Bottrell S H and Hill J. (2014). Tropical forest fragments contribute to species richness in adjacent oil palm plantations. Biological Conservation 169: 268–276. https://doi.org/10.1016/j.biocon.2013.11.014

McCain C M. (2007). Could temperature and water availability drive elevational species richness patterns? A global case study for bats. Global Ecology and Biogeography 16: 1–13. https://doi.org/10.1111/j.1466-8238.2006.00263.x

Ministerio de Agricultura y Desarrollo Rural. (2006). Apuesta exportadora agropecuaria 2006±2020. http://www.mincit.gov.co. (accessed on 26 October 2019).

Montaño-Centellas F, Moya M I, Aguirre L F, Galeon R, Palabrala O, Hurtado R, Galraza I and Tordoya J. (2015). Community and species-level responses of phyllostomid bats to a disturbance gradient in the tropical Andes. Acta Oecologica 62: 10–17. https://doi.org/10.1016/j.actao.2014.11.002

Morales-Martínez D, Rodríguez-Posada M, Fernández-Rodríguez C, Calderón-Capote M and Gutiérrez-Sanabria D. (2018). Spatial variation of bat diversity between three floodplain-savanna ecosystems of the Colombian Llanos. Therya 9(1): 41–52. https://doi.org/10.12933/therya-18-537

Municipio de Cumaral. (2009). Municipio de Cumaral: Información General. http://www.cumaral-meta.gov.co/municipio/nuestro-municipio (accessed on 26 October 2019).

Numa C, Verdú J R and Sánchez-Palomino P. (2005). Phyllostomid bat diversity in a variegated coffee landscape. Biological Conservation 122: 151–158. https://doi.org/10.1016/j.biocon.2004.07.013

Nur-Juliani N, Mohd Sah S, Abdul Latip N, Azman N M and Khairuddin. (2011). Diversity pattern of bats as two contrasting habitat types along Kerian River, Perak, Malaysia. Tropical Life Sciences Research 22(2): 13–22.

Ocampo-Peñuela N, García-Ulloa J, Ghazoul J and Etter A. (2018). Quantifying impacts of oil palm expansion on Colombia’s threatened biodiversity. Biological Conservation 224: 117–121. https://doi.org/10.1016/j.biocon.2018.05.024

Ortegón-Martínez D A and Pérez-Torres J. (2007). Estructura y composición del ensamblaje de murciélagos (Chiroptera) asociado a un cafetal con sombrío en la Mesa de los Santos (Santander), Colombia. Actualidades Biológicas 29(87): 215–228.

Pardo L E and Campbell M. (2019). How oil palm can become more ecologically friendly. Australasian Science 40: 35–37.

Pardo L E and Payán E. (2015). Mamíferos de un agropaisaje de palma de aceite en las sabanas inundables de Orocué, Casanare, Colombia. Biota Colombiana 16: 54–66.

Pardo L E, Campbell M, Cove M, Edwards W, Clements G R and Laurance W F. (2019). Land management strategies can increase oil palm plantation use by some terrestrial mammals in Colombia. Scientific Reports 9: 7812. https://doi.org/10.1038/s41598-019-44288-y

Pardo L E, Campbell M J, Edwards W, Clements GR and Laurance W F. (2018a). Terrestrial mammal responses to oil palm dominated landscapes in Colombia. PLoS ONE 13: e0197539. https://doi.org/10.1371/journal.pone.0197539

Pardo L E, de Oliveira Roque F, Campbell M, Younes N, Edwards W and Laurance W F. (2018b). Identifying critical limits in oil palm cover for the conservation of terrestrial mammals in Colombia. Biological Conservation 227: 65–73. https://doi.org/10.1016/j.biocon.2018.08.026

Pardo L E, Laurance W F, Clements G R and Edwards W. (2015). The impacts of oil palm agriculture on Colombia’s biodiversity: what we know and still need to know. Tropical Conservation Science 88: 828–845. https://doi.org/10.1177/194008291500800317

Park K J. (2014). Mitigating the impacts of agriculture on biodiversity: Bats and their potential role as bioindicators. Mammalian Biology 80: 191–204. https://doi.org/10.1016/j.mambio.2014.10.004

Payán E and Boron V. (2019). The future of wild mammals in oil palm landscapes in the neotropics. Frontiers in Forests and Global Change 2: 61. https://doi.org/10.3389/ffgc.2019.00061

Saldaña-Vásquez R A, Sosa V J, Hernández-Montero J R and López-Barrera F. (2010). Abundance responses of frugivorous bats (Stenodermatinae) to coffee cultivation and selective logging practices in mountainous central Veracruz, México. Biodiversity and Conservation 19: 2111–2124. https://doi.org/10.1007/s10531-010-9829-6

Syafiq M, Atiqah A R N, Ghazali A, Asmah S, Yahya M S, Aziz N, Puang C L and Azhar B. (2016). Responses of tropical fruit bats to monoculture and polyculture farming in oil palm smallholdings. Acta Oecologica 74: 11–18. https://doi.org/10.1016/j.actao.2016.06.005

Turner E and Foster W. (2009). The impact of forest conversion to oil palm on arthropod abundance and biomass in Sabah, Malaysia. Journal of Tropical Ecology 25(1): 23–30. https://doi.org/10.1017/S0266467408005658

Velazco P M. (2005). Morphological phylogeny of the bat genus Platyrrhinus saussure, 1860 (Chiroptera: Phyllostomidae) with the description of four new species. Zoology 1860: 1–54. https://doi.org/10.5962/bhl.title.2689

Yancey F D, Goetze J R and Jones C. (1998). Saccopteryx bilineata. Mammalian Species 581: 1–5. https://doi.org/10.2307/3504459