Seed dispersal by fruit bats in Colombia generates ecosystem services

Abstract

When fruit bats forage, they serve an important ecological function, such as seed dispersal. Although several authors have approached the significance of bats in generating ecosystem services, there is a gap in understanding the importance of the seed dispersal by fruit bats for ecosystems and society. To fill this gap, we considered different components, such as ecosystem service drivers, functional ecosystem services, structural ecosystem services, and ecosystem services to humans. By taking two agroecosystems from the Colombian Andean region (mixed crops and extensive livestock) as the study cases, the following methodological approach was applied: (i) sampling of frugivorous bats (driver) present in the agroecosystems; (ii) identification of plants dispersed by bats (functional ecosystem services) in each agroecosystem; (iii) identification of the uses given to the plants spread (ecosystem services to humans). Finally, the plants spread by bats were considered drivers for soil fertility as well. In line of this, this research is the first in proposing a “causality chain approach” regarding the generation of ecosystem services by focusing on bat-dispersed plants. The research highlights that the diversity in frugivorous bats, the plants spread by bats, and the number of uses made of these plants were higher in mixed crops.

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References

  1. Ancillotto L, Ariano A, Nardone V, Budinski I, Rydell J, Russo D (2017) Effects of free-ranging cattle and landscape complexity on bat foraging: implications for bat conservation and livestock management. Agric Ecosyst Environ 241:54–61. https://doi.org/10.1016/j.agee.2017.03.001

    Article  Google Scholar 

  2. Ayivor JS, Ohemeng F, Tweneboah Lawson E, Waldman L, Leach M, Ntiamoa-Baidu Y (2017) Living with bats: the case of Ve Golokuati township in the Volta region of Ghana. J Environ Public Health 5938934:1–11. https://doi.org/10.1155/2017/5938934

    Article  Google Scholar 

  3. Bagstad KJ, Wiederholt R (2013) Tourism values for Mexican free-tailed bat viewing. Hum Dimens Wildl 18:307–311. https://doi.org/10.1080/10871209.2013.789573

    Article  Google Scholar 

  4. Barbaro L, Allan E, Ampoorter E, Castagneyrol B, Charbonnier Y, De Wandeler H et al (2019) Biotic predictors complement models of bat and bird responses to climate and tree diversity in European forests. Proc R Soc B 286:20182193. https://doi.org/10.1098/rspb.2018.2193

    Article  PubMed  Google Scholar 

  5. Baker HG, Baker I, Hodges SA (1998) Sugar compositions of nectars and fruits consumed by birds and bats in the tropics and subtropics. Biotropica 30:559–586. https://doi.org/10.1111/j.1744-7429.1998.tb00097.x

    Article  Google Scholar 

  6. Bedoya-Osorio C (2009) Dispersión de semillas por el conjunto de murciélagos frugívoros en dos sistemas productivos (Ganadería extensiva y Cultivos Mixtos) en el eje cafetero, Colombia. Trabajo de grado. Pregrado en Biología. Pontificia Universidad Javeriana. Facultad de Ciencias. Departamento de Biología

  7. Bloedel P (1955) Observations on the life histories of Panamá bats. J Mammal 36:232–235. https://doi.org/10.2307/1375881

    Article  Google Scholar 

  8. Bonaccorso FJ (1979) Foraging and reproductive ecology in a Panamanian bat community. Bull Fla State Mus Niol Sci 24:359–408 https://ufdc.ufl.edu/AA00024888/00001

    Google Scholar 

  9. Boyles JG, Cryan PM, McCracken GF, Kunz TH (2011) Economic importance of bats in agriculture. Science 332:41–42 https://science.sciencemag.org/content/332/6025/41

    Article  Google Scholar 

  10. Calle Z, Méndez LE (2009) Estructura y composición de la vegetación arbórea en el agropaisaje del río La Vieja. En: Valoración de la Biodiversidad en la Ecorregión del Eje Cafetero. CIEBREG. Pereira, Colombia, pp. 171–184

  11. Casanoves F, Pla L, Rienzo JA (2011) Valoración y análisis de la diversidad funcional y su relación con los Servicios Ecosistémicos. Centro Agronómico Tropical de Investigación y Enseñanza, CATIE. Serie Técnica, Informe Técnico No. 384. http://www.nucleodiversus.org/uploads/file/Casanoves%20et%20al%202011%20Serie%20Tecnica%20CATIE.pdf

  12. Chapin FS III, Matson PA, Mooney HA (2002) Principles of ecosystem ecology. Springer-Verlag, New York, New York

    Google Scholar 

  13. Cely-Gómez MA, 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 10:149–153 http://www.revistas-conacyt.unam.mx/therya/index.php/THERYA/article/view/682

    Article  Google Scholar 

  14. Chabert A, Sarthou JP (2020) Conservation agriculture as a promising trade-off between conventional and organic agriculture in bundling ecosystem services. Agric Ecosyst Environ 292:106815. https://doi.org/10.1016/j.agee.2019.106815

    CAS  Article  Google Scholar 

  15. Classen A, Peters MK, Ferger SW, Helbig-Bonitz M, Schmack JM, Maassen G, Schleuning M, Kalko EKV, Böhning-Gaese K, Steffan-Dewenter I (2014) Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields. Proc R Soc B 281:20133148. https://doi.org/10.1098/rspb.2013.3148

    Article  PubMed  Google Scholar 

  16. Cleveland CJ, Betke M, Federico P, Frank JD, Hallam TG, Horn J, López JD Jr, McCracken GF, Medellín RA, Moreno-Valdez A, Sansone CG, Westbrook JK, Kunz TH (2006) Economic value of the pest control service provided by Brazilian free-tailed bats in south-central Texas. Front Ecol Environ 4:238–243. https://doi.org/10.1890/1540-9295(2006)004[0238:EVOTPC]2.0.CO;2

    Article  Google Scholar 

  17. Cloutier D, Thomas DW (1992) Carollia perspicillata. Mamm Species 417:1–9 https://academic.oup.com/mspecies/article/doi/10.2307/3504157/2600673

    Google Scholar 

  18. Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Steege H, Morgan HD, Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardized and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380 https://www.uv.es/jgpausas/papers/Cornelissen%20et%20al%202003%20handbook.pdf

    Article  Google Scholar 

  19. Cortés-Delgado N, Pérez-Torres J (2011) Habitat edge context and the distribution of phyllostomid bats in the Andean forest and anthropogenic matrix in Central Andes of Colombia. Biol Conserv 20:987–999. https://doi.org/10.1007/s10531-011-0008-1

    Article  Google Scholar 

  20. Costa WF, Ribeiro M, Saraiva AM, Imperatriz-Fonseca VL, Giannini TC (2018) Bat diversity in Carajás National Forest (Eastern Amazon) and potential impacts on ecosystem services under climate change. Biol Conserv 218:200–210. https://doi.org/10.1016/j.biocon.2017.12.034

    Article  Google Scholar 

  21. CRQ, CVC, CARDER et al. (2018) Actualización POMCA rio La Vieja: Plan de ordenación y manejo de la cuenca hidrográfica 2018–2032. Retrieved from: https://crq.gov.co/index.php/2016-12-28-22-26-17/pomca

  22. Dale VH, Polasky S (2007) Measures of the effects of agricultural practices on ecosystem services. Ecol Econ 64:286–296. https://doi.org/10.1016/j.ecolecon.2007.05.009

    Article  Google Scholar 

  23. Davidai N, Westbrook JK, Lessard JP, Hallam TG, McCracken GF (2015) The importance of natural habitats to Brazilian free-tailed bats in intensive agricultural landscapes in the Winter Garden Region of Texas, United States. Biol Conserv 190:107–114. https://doi.org/10.1016/j.biocon.2015.05.015

    Article  Google Scholar 

  24. Denmead LH, Darras K, Clough Y, Diaz P, Grass I, Hoffmann MP, Nurdiansyah F, Fardiansah R, Tscharntke T (2017) The role of ants, birds and bats for ecosystem functions and yield in oil palm plantations. Ecology 98:1945–1956. https://doi.org/10.1002/ecy.1882

    Article  PubMed  Google Scholar 

  25. Díaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. https://doi.org/10.1016/S0169-5347(01)02283-2

    Article  Google Scholar 

  26. Díaz S, Lavorel S, Mcintyre V, Falczuk F, Casanoves DG et al (2006) Plant trait responses to grazing-a global synthesis. Glob Chang Biol 12:1–26. https://doi.org/10.1111/j.1365-2486.2006.01288.x

    Article  Google Scholar 

  27. Díaz S, Quétier F, Cáceres D, Trainor S, Pérez-Harguindeguy N, Bre-Harte M, Finegan B, Peña-Claros B, Poorter L (2011) Linking functional diversity and social actor strategies in a framework for interdisciplinary analysis of nature’s benefits to society. PNAS 108:895–902. https://doi.org/10.1073/pnas.1017993108

    Article  PubMed  Google Scholar 

  28. Dumont ER (2003) Bats and fruit: an ecomophological approach. In Bat ecology (eds. T. H. Kunz and M. B. Fenton), pp. 398–429. University of Chicago Press, Chicago, IL

  29. Enríquez-Acevedo T (2012) Aproximación económica y ecológica del aporte de las plantas dispersadas por murciélagos frugívoros al bienestar de los pobladores de dos sistemas productivos (cuenca del río la vieja). Trabajo de grado. Maestría en Ciencias Biológicas. Universidad Javeriana. Facultad de Ciencias. Departamento de Biología

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

    Article  Google Scholar 

  31. Estrada A, Coates-Estrada R (2001) Species composition and reproductive phenology of bats in a tropical landscape at Los Tuxtlas, México. J Trop Ecol 17:627–646

    Article  Google Scholar 

  32. Federico P, Hallam TG, McCracken GF, Purucker ST, Grant WE, Correa-Sandoval AN et al (2008) Brazilian free-tailed bats as insect pest regulators in transgenic and conventional cotton crops. Ecol Appl 18:826–837. https://doi.org/10.1890/07-0556.1

    Article  PubMed  Google Scholar 

  33. Fernández AB (1982) Murciélagos de Venezuela II: Phyllostomidae-Stenodermatinae. Rev Fac Agron 12:327–352

    Google Scholar 

  34. Fleming TH (1988) The short-tailed fruit bat. University of Chicago Press, Chicago

    Google Scholar 

  35. Galindo-González J (2005) ¿Regeneración de la selva? Los murciélagos expertos en el asunto. La Ciencia y el hombre 18:37–40

    Google Scholar 

  36. García QS, Rezende JL, Aguiar LM (2000) Seed dispersal by bats in a disturbed area of Southeastern Brazil. Rev Biol Trop 48: 125–128

  37. García-Morales RG, Chapa-Vargas L, Galindo-González J, Badano EI (2012) Seed dispersal among three different vegetation communities in the Huasteca region, Mexico, analyzed from bat feces. Acta Chiropt 14:357–367. https://doi.org/10.3161/150811012X661675

    Article  Google Scholar 

  38. García-Morales R, Moreno CE, Badano EI, Zuria I, Galindo-González J, Rojas-Martínez AE, Ávila-Gómez ES (2016) Deforestation impacts on bat functional diversity in tropical landscapes. PLoS One 11:e0166765. https://doi.org/10.1371/journal.pone.0166765

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Ghanem SJ, Voigt C (2012) Increasing awareness of ecosystem services provided by bats. In Advances in the study of behavior (Vol. 44, pp. 279-302). Academic Press

  40. Giannnini NP, Kalko EK (2004) Trophic structure in a large assemblage of phyllostomid bats in Panamá. Oikos 105:209–220. https://doi.org/10.1111/j.0030-1299.2004.12690.x

    Article  Google Scholar 

  41. Gómez-Junco GP (2008) Capacidad de germinación de semillas consumidas por murciélagos frugívoros y su calidad de dispersión en un bosque de cañada en un sistema de ganadería intensiva en el norte del Valle del Cauca (Colombia). Trabajo de grado. Pregrado en Biología. Pontificia Universidad Javeriana. Facultad de Ciencias. Departamento de Biología

  42. Gorchov DL, Cornejo F, Ascorra C, Jaramillo M (1993) The role of seed dispersal in the natural regeneration of rain forest after strip-cutting in the Peruvian Amazon. Vegetation 107–108:339–349

  43. Gorchov DL, Cornejo F, Ascorra CF (1995) Dietary overlap between frugivorous birds and bats in the Peruvian Amazon. Oikos. 74:235–250 https://www.jstor.org/stable/3545653

    Article  Google Scholar 

  44. Gras P, Tscharntke T, Maas B, Tjoa A, Hafsah A, Clough,Y (2016) How ants, birds and bats affect crop yield along shade gradients in tropical cacao agroforestry. J Appl Ecol 53: 953–963. https://doi.org/10.1111/1365-2664.12625

  45. Handley C, Leigh EG (1991) Diet and food supply. pp. 147-149. In: C.O Handley Jr., D.E. Wilson & A.L. Gardner. Demography and natural history of the common fruit bat Artibeus jamaicensis on Barro Colorado Island, Panamá. Smithsonian Institution Press, Washington, D.C.

  46. Heim O, Lorenz L, Kramer-Schadt S, Jung K, Voigt C, Eccard JA (2017) Landscape and scale-dependent spatial niches of bats foraging above intensively used arable fields. Ecol Process 6:24. https://doi.org/10.1186/s13717-017-0091-7

    Article  Google Scholar 

  47. Heithaus ER, Flemming TH, Opler P (1975) Foraging patterns and the resource utilization in seven species of bats in a seasonal tropical forest. Ecology. 56:841–854. https://doi.org/10.2307/1936295

    Article  Google Scholar 

  48. Hooper DU, Chapin S, Ewel J, Hector A, Inchausti P, Lavorel S et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–55. https://doi.org/10.1890/04-0922

    Article  Google Scholar 

  49. Horsley TW, Bicknell JE, Lim BK, Ammerman LK (2015) Seed dispersal by frugivorous bats in Central Guyana and a description of previously unknown plant-animal interactions. Acta Chiropt 17:331–336. https://doi.org/10.3161/15081109ACC2015.17.2.008

    Article  Google Scholar 

  50. Isaacs R, Tuell J, Fiedler A, Gardiner M, Landis D (2009) Maximizing arthropod-mediated ecosystem services in agricultural landscapes: the role of native plants. Front Ecol Environ 7:196–203. https://doi.org/10.1890/080035

    Article  Google Scholar 

  51. Kemp J, López-Baucells A, Rocha R, Wangensteen OS, Andriatafika Z, Nair A, Cabeza M (2019) Bats as potential suppressors of multiple agricultural pests: a case study from Madagascar. Agric Ecosyst Environ 269:88–96. https://doi.org/10.1016/j.agee.2018.09.027

    Article  Google Scholar 

  52. Kremen C (2005) Managing ecosystem services: what do we need to know about their ecology? Ecol Lett 8:468–479. https://doi.org/10.1111/j.1461-0248.2005.00751.x

    Article  PubMed  Google Scholar 

  53. Kunz TH, de Torrez EB, Bauer D, Lobova T, Fleming TH (2011) Ecosystem services provided by bats. Ann N Y Acad Sci 1223:1–38. https://doi.org/10.1111/j.1749-6632.2011.06004.x

    Article  PubMed  Google Scholar 

  54. Lacoeuilhe A, Machon N, Julien JF, Kerbiriou C (2018) The relative effects of local and landscape characteristics of hedgerows on bats. Diversity 10:72. https://doi.org/10.3390/d10030072

    Article  Google Scholar 

  55. Laurindo RS, Novaes RLM, Vizentin-Bugoni J, Gregorin R (2019) The effects of habitat loss on bat-fruit networks. Biodivers Conserv 28:589–601. https://doi.org/10.1007/s10531-018-1676-x

    Article  Google Scholar 

  56. Lobova T, Geiselman C, Mori S (2009) Seed dispersal by bats in the Neotropics. In: Memoirs of the New York Botanical Garden. New York Botanical Garden Press. The Bronx, New York

  57. López-Hoffman L, Diffendorfer J, Wiederholt R, Bagstad KJ, Thogmartin WE, McCracken G, Medellin RL, Russell A, Semmens DJ (2017) Operationalizing the telecoupling framework for migratory species using the spatial subsidies approach to examine ecosystem services provided by Mexican free-tailed bats. Ecol Soc 22(4) https://www.ecologyandsociety.org/vol22/iss4/art23/

  58. Maas B, Clough Y, Tscharntke T (2013) Bats and birds increase crop yield in tropical agroforestry landscapes. Ecol Lett 16:1480–1487. https://doi.org/10.1111/ele.12194

    Article  PubMed  Google Scholar 

  59. Maine J, Boyles JG (2015) Bats initiate vital agroecological interactions in corn. PNAS 112:12438–12443. https://doi.org/10.1073/pnas.1505413112

    CAS  Article  PubMed  Google Scholar 

  60. Medellin RA, Wiederholt R, Lopez-Hoffman L (2017) Conservation relevance of bat caves for biodiversity and ecosystem services. Biol Conserv 211:45–50. https://doi.org/10.1016/j.biocon.2017.01.012

    Article  Google Scholar 

  61. Méndez LE, Calle Z (2007) Árboles y arbustos de la cuenca media del río la Vieja, Guía de campo. CIPAV y CIEBREG. Cali, Colombia. 192 p

  62. Méndez LE, Calle Z (2010) Plantas de la Cuenca Media del Río La Vieja. Cali, Colombia. CIPAV y CIEBREG. 236 p

  63. Muscarella R, Fleming TH (2007) The role of frugivorous bats in tropical forest succession. Biol Rev 82:573–590. https://doi.org/10.1111/j.1469-185X.2007.00026.x

    Article  PubMed  Google Scholar 

  64. Olea-Wagner A, Lorenzo C, Naranjo E, Ortiz E, León-Paniagua L (2007) Diversidad de frutos que consumen tres especies de murciélagos (Chiroptera: Phyllostomidae) en la selva lacandona, Chiapas, México. Rev Mex Biodiv 78(1)

  65. Olimpi EM, Philpott SM (2018) Agroecological farming practices promote bats. Agric Ecosyst Environ 265:282–291. https://doi.org/10.1016/j.agee.2018.06.008

    Article  Google Scholar 

  66. Oliveira MT, Silva JL, Cruz-Neto O, Borges LA, Girão LC, Tabarelli M, Lopes AV (2020) Urban green areas retain just a small fraction of tree reproductive diversity of the Atlantic forest. Urban For Urban Greening 54:126779. https://doi.org/10.1016/j.ufug.2020.126779

    Article  Google Scholar 

  67. Ortegón-Martínez DA, 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). Actual Biol 29:215–228

    Google Scholar 

  68. Park KJ (2015) Mitigating the impacts of agriculture on biodiversity: bats and their potential role as bioindicators. Mamm Biol 80:191–204. https://doi.org/10.1016/j.mambio.2014.10.004

    Article  Google Scholar 

  69. Pattanayak S, Evan MD (1996) Valuing soil conservation benefits of agroforestry practices. Southeastern Center for Forest Economics Research, Research Triangle Park. NC. FPEI Working Paper No. 59. 21 p

  70. Pérez-Torres J, Sánchez C, Cortés N (2009) Murciélagos asociados a sistemas naturales y transformados en la Ecorregión del Eje Cafetero. En: Valoración de la Biodiversidad en la Ecorregión del Eje Cafetero. CIEBREG. Pereira, Colombia, pp. 157–167

  71. Perfecto I, Armbrecht I (2003) The coffee agroecosystems in the neotropics: combining ecological and economic goals. In: Tropical Agroecosystems (ed. Vandermeer, H.J). CRC Press, Boca Raton, USA, pp 159-194

  72. Pla L, Casanoves F, Di Rienzo J (2012) Quantifying functional biodiversity. Springer Science & Business Media

  73. Raudsepp-Hearne C, Peterson GD, Bennett EM (2010) Ecosystem service bundles for analyzing tradeoffs in diverse landscapes. PNAS 107:5242–5247. https://doi.org/10.1073/pnas.0907284107

    Article  PubMed  Google Scholar 

  74. Rivas-Rojas E (2005) Diversity bats of dry forest and cocoa plantation. Lyona J Ecol Application 8:29–39

    Google Scholar 

  75. Rodríguez JM, Camargo JC, Niño J, Pineda AM, Arias LM, Echeverry M A, Miranda CL, (eds). (2009) Valoración de la Biodiversidad en la Ecorregión del Eje Cafetero. CIEBREG. Pereira, Colombia. 238 p

  76. Rodríguez-San Pedro A, Chaperon P, Beltrán N, Allendes C, Ávila F (2018) Influence of agricultural management on bat activity and species richness in vineyards of Central Chile. J Mammal 99:1495–1502. https://doi.org/10.1093/jmammal/gyy121

    Article  Google Scholar 

  77. Saldaña-Vázquez RA, Ruiz-Sanchez E, Herrera-Alsina L, Schondube JE (2015) Digestive capacity predicts diet diversity in Neotropical frugivorous bats. J Anim Ecol 84:1396–1404. https://doi.org/10.1111/1365-2656.12383

    Article  PubMed  Google Scholar 

  78. Sánchez F (2017) Murciélagos de Villavicencio (Meta, Colombia): evaluación preliminar de su diversidad trófica y servicios ecosistémicos. Bol Cient Mus Hist 21:96–111

    Google Scholar 

  79. Santos-Barrera G, Urbina-Cardona J (2011) The role of the matrix–edge dynamics of amphibian conservation in tropical montane fragmented landscapes. Rev Mex Biodivers 82:679–687

    Google Scholar 

  80. Scanlon AT, Petit S, Tuiwawa M, Naikatini A (2014) High similarity between a bat-serviced plant assemblage and that used by humans. Biol Conserv 174:111–119. https://doi.org/10.1016/j.biocon.2014.03.023

    Article  Google Scholar 

  81. Sosa V, Hernández-Salazar E, Hernández-Conrique D, Castro-Luna A (2008) Murciélagos (Mammalia: Chiroptera). pp. 181-192. In: Manson, R., V. Hernández-Ortíz, S. Gallina & K. Mehltreter (Eds.). Agroecosistemas Cafetaleros de Veracruz: Biodiversidad, Manejo y Conservación. Instituto de Ecología A. C. (INECOL). México

  82. Starik N, Göttert T, Heitlinger E, Zeller U (2018) Bat community responses to structural habitat complexity resulting from management practices within different land use types—a case study from north-eastern Germany. Acta Chiropt 20:387–405. https://doi.org/10.3161/15081109ACC2018.20.2.010

    Article  Google Scholar 

  83. Suarez A (2012) Transición hacia la Multifuncionalidad agrícola en la cuenca Barbas: Procesos agrícolas multifuncionales en fincas de Colombia. Editorial Académica Española. 66 pp. ISBN: 978-659-02911-0

  84. Syafiq M, Atiqah ARN, Ghazali A, Asmah S, Yahya MS, Aziz N et al (2016) Responses of tropical fruit bats to monoculture and polyculture farming in oil palm smallholdings. Acta Oecol 74:11–18. https://doi.org/10.1016/j.actao.2016.06.005

    Article  Google Scholar 

  85. Taylor PJ, Grass I, Alberts AJ, Joubert E, Tscharntke T (2018) Economic value of bat predation services–a review and new estimates from macadamia orchards. Ecosyst Serv 30:372–381. https://doi.org/10.1016/j.ecoser.2017.11.015

    Article  Google Scholar 

  86. Triplett S, Luck GW, Spooner P (2012) The importance of managing the costs and benefits of bird activity for agricultural sustainability. Int J Agric Sustain 10:268–288. https://doi.org/10.1080/14735903.2012.700102

    Article  Google Scholar 

  87. Vanitharani J (2014) Sustainable management of forest through ecosystem services of bats. Int Res J Biol Environ Sci 1:1–18 https://www.scrutinyjournals.com/articles?articleid=78

    Google Scholar 

  88. Wainger LA, King DM, Mack RN, Price EW, Maslin T (2010) Can the concept of ecosystem services be practically applied to improve natural resource management decisions? Ecol Econ 69:978–987. https://doi.org/10.1016/j.ecolecon.2009.12.011

    Article  Google Scholar 

  89. Wanger TC, Darras K, Bumrungsri S, Tscharntke T, Klein AM (2014) Bat pest control contributes to food security in Thailand. Biol Conserv 171:220–223. https://doi.org/10.1016/j.biocon.2014.01.030

    Article  Google Scholar 

  90. Wiederholt R, Bagstad KJ, McCracken GF, Diffendorfer JE, Loomis JB, Semmens DJ et al (2017) Improving spatio-temporal benefit transfers for pest control by generalist predators in cotton in the southwestern US. Int J Biodivers Sci Ecosyst Serv Manag 13:27–39. https://doi.org/10.1080/21513732.2016.1240712

    Article  Google Scholar 

  91. Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst 42:1–22. https://doi.org/10.1146/annurev-ecolsys-102710-145042

    Article  Google Scholar 

  92. Zhang W, Ricketts TH, Kremen C, Carney K, Swinton SM (2007) Ecosystem services and dis-services to agriculture. Ecol Econ 64:253–260. https://doi.org/10.1016/j.ecolecon.2007.02.024

    Article  Google Scholar 

  93. Znajda SK (2000) Conservación de hábitat, diversidad de aves y agroecosistemas de café en Costa Rica. Presentado En: Coloquio Internacional “Desarrollo sustentable, participación comunitaria y conservación de la biodiversidad en México y América Latina”

  94. Zorita E (2003) Ponencia: Sistemas de producción ganaderos: situación actual y perspectivas. En: Libro blanco de la Agricultura y el desarrollo rural

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Acknowledgments

We want to thank Dr. Arias-Arévalo for her valuable suggestions. We thank the members of the Laboratory of Functional Ecology from the Universidad Javeriana. Also, we want to thank the peer reviewers for their valuable suggestions.

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Correspondence to Andres Suarez.

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This research was funded by CIEBREG and supported by the Laboratory of Functional Ecology from the Universidad Javeriana.

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C. Ruiz-Agudelo, J. Pérez-Tórres, and T. Enríquez-Acevedo: conceptualization, validation, methodology, writing–reviewing. A. Suarez: conceptualization, methodology, writing–original draft preparation. T. Enríquez-Acevedo: data curation, field research, and editing.

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Enríquez-Acevedo, T., Pérez-Torres, J., Ruiz-Agudelo, C. et al. Seed dispersal by fruit bats in Colombia generates ecosystem services. Agron. Sustain. Dev. 40, 45 (2020). https://doi.org/10.1007/s13593-020-00645-0

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Keywords

  • Functional diversity
  • Farms
  • Driver
  • Mixed crops
  • Livestock