Abstract
Ecuador is experiencing a rapid conversion of its natural habitats, especially in its Andean–Amazon piedmont forests, a conversion that in turn threatens the country’s biodiversity. Frugivorous bats (Phyllostomidae) are not only an example of a taxa affected by habitat loss but may also play a role in overturning habitat loss and degradation. As important seed dispersers, bats are key to many ecological processes such as forest regeneration and succession. To understand Phyllostomidae diversity and trophic structure of Ecuador’s piedmont forests, as well as the potential role of bats in forest recovery through seed dispersal, we sampled bats at both agroforestry (chagras) sites and patches of secondary forest in the buffer zone of the Colonso Chalupas Biological Reserve, Napo Province (750–900 m asl.). For 4 months, we used mist nets and seed traps to sample bats and the seeds they carried. In total, these efforts yielded 224 bats belonging to 33 species. We captured 224 bats belonging to 33 species of which 114 individuals from 24 species transported seeds. We captured more species but fewer individuals of bats in forests (17) than in chagras (15). The bats carried 15,685 seeds of 41 different morpho-seeds belonging to twelve plant genera, with Piper, Cecropia, and Solanum being those with the highest number of seeds. The main disperser we found was Carollia brevicauda, both in the forest (index value = 1.4) and in chagras (2.2). Bat-plant networks were more symmetric in forests (− 1.63) compared to chagras (− 9.28) and showed higher degrees of specialization in chagras. Our results show the great diversity of bats and the seeds they carry and highlight how this traditional agricultural system allows for connectivity between forest patches by providing food niches for seed dispersers. Therefore, we argue both bats and chagras must be considered in forest restoration programs.
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Data availability
The datasets we generated and analyzed during the current study are available from the corresponding author on reasonable request.
References
Anderson PJ, Putz F (2002) Harvesting and conservation: are both possible for the palm, Iriartea deltoidea? For Ecol Manage 170:271–283. https://doi.org/10.1016/S0378-1127(01)00753-8
Andrade TY, Thies W, Rogeri PK, Kalko EKV, Mello MAR (2013) Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae). J Mammal 94:1094–1101. https://doi.org/10.1644/12-MAMM-A-244.1
Arguero A, Jiménez-Robles O, Sánchez-Karste F, Baile A, De la Cadena G, Barboza K (2012) Observaciones Sobre Dispersión de Semillas por Murciélagos en la Alta Amazonía del Sur de Ecuador. In: Tirira DG and Burneo SF (ed) Investigación y Conservación sobre Murciélagos en el Ecuador. PUCE, FMC, AEM, Quito, pp 37–46
Armenteras D, Rodríguez N (2014) Dinámicas y causas de deforestación en bosques de Latino América: Una Revisión Desde 1990. Colombia Forestal 17:233–245. https://doi.org/10.14483/udistrital.jour.colomb.for.2014.2.a07
Bonaccorso FJ, Gush TJ (1987) Feeding behaviour and foraging strategies of captive phyllostomid fruit bats: an experimental study. J Anim Ecol 56:907. https://doi.org/10.2307/4956
Bracamonte JC (2018) Protocolo de muestreo para la estimación de la diversidad de murciélagos con redes de niebla en estudios de ecología. Ecología Austral 28:446–454. https://doi.org/10.25260/EA.18.28.2.0.272
Burneo SF, Tirira DG (2014) Murciélagos del Ecuador: un análisis de sus patrones de riqueza, distribución y aspectos de conservación. Therya 5:197–228. https://doi.org/10.12933/therya-14-184
Capparelli MV, Moulatlet GM, Abessa DM, Lucas-Solis O, Rosero B, Galarza E, Tuba D, Carpintero N, Ochoa-Herrera V, Cipriani-Avila I (2020) An integrative approach to identify the impacts of multiple metal contamination sources on the eastern Andean foothills of the Ecuadorian Amazonia. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.136088
Casallas-Pabón D, Calvo-Roa N, Rojas-Robles R (2017) Murciélagos dispersores de semillas en gradientes sucesionales de la Orinoquía (San Martín, Meta, Colombia). Acta Biológica Colombiana 22:348–358. https://doi.org/10.15446/abc.v22n3.63561
Castaño JH, Carranza JA, 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
Castro-Luna AA, Galindo-González J (2012) Seed dispersal by phyllostomid bats in two contrasting vegetation types in a Mesoamerican reserve. Acta Chiropterologica 14:133–142. https://doi.org/10.3161/150811012X654349
Cornejo F, Janovec J (2010) Seeds of Amazonian plants. Princeton University Press, New Jersey
da Silva AG, Gaona O, Medellín RA (2008) Diet and trophic structure in a community of fruit-eating bats in Lacandon Forest, México. J Mammal 89:43–49. https://doi.org/10.1644/06-MAMM-A-300.1
Dormann CF, Strauss R (2013) A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol 5:90–98. https://doi.org/10.1111/2041-210X.12139
Dormann F, Fruend J, Bernd G (2019) Package ‘bipartite.’ CRAN - R Project. https://github.com/biometry/bipartite. Accessed 2020
Estrada A, Coates-Estrada R (2002) Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, Mexico. Biol Cons 103:237–245. https://doi.org/10.1016/S0006-3207(01)00135-5
Etter A, Mcalpine C, Phinn S, Pullar D, Possingham H (2006) Characterizing a tropical deforestation wave: a dynamic spatial analysis of a deforestation hotspot in the Colombian Amazon. Glob Change Biol 12:1409–1420. https://doi.org/10.1111/j.1365-2486.2006.01168.x
Fleming TH (1986) Opportunism versus specialization: the evolution of feeding strategies in frugivorous bats. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal, 1st edn. Dr W. Junk Publishers, Dordrecht, pp 105–118
Galindo-Gonzalez J, Guevara S, Sosa VJ (2000) Bat- and bird-generated seed rains at isolated trees in pastures in a tropical rainforest. Conserv Biol 14:1693–1703. https://doi.org/10.1111/j.1523-1739.2000.99072.x
Galindo-González J, Vázquez-Domínguez G, Saldaña-Vázquez RA, Hernández-Montero JR (2009) A more efficient technique to collect seeds dispersed by bats. J Trop Ecol 25:205–209. https://doi.org/10.1017/S0266467409005859
Ghanem SJ, Voigt CC (2013) Defaunation of tropical forests reduces habitat quality for seed-dispersing bats in Western Amazonia: an unexpected connection via mineral licks. Anim Conserv 17:44–51. https://doi.org/10.1111/acv.12055
Gorchov DL, Cornejo F, Ascorra CF, Jaramillo M (1995) Dietary overlap between Frugivorous birds and bats in the Peruvian Amazon. Oikos 74:235. https://doi.org/10.2307/3545653
Guevara J, Mogollón H, Cerón C, Josse C (2013) Sistema de Clasificación de los Ecosistemas del Ecuador Continental. Ministerio del Ambiente del Ecuador
Guisande C (2019) Package ‘EcoIndR’. CRAN - R Project. https://cran.r-project.org/web/packages/EcoIndR/EcoIndR.pdf. Accessed 2021
Guisande C, Heine J, González-Dacosta J, García-Roselló E (2014) RWizard Software. University of Vigo, Vigo, Spain
Guisande C, Heine J, García-Roselló E, González-Dacosta J, Vilas LG, Perez-Schofield BJ (2017) DER: An algorithm for comparing species diversity between assemblages. Ecol Ind 81:41–46. https://doi.org/10.1016/j.ecolind.2017.05.049
Hernández-Montero JR, Saldana-Vazquez RA, Galindo-González J, Sosa VJ (2015) Bat-fruit interactions are more specialized in shaded-coffee plantations than in tropical mountain cloud forest fragments. PLoS ONE. https://doi.org/10.1371/journal.pone.0126084
Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am Nat 129:657–677. https://doi.org/10.1086/284665
Jose S (2009) Agroforestry for ecosystem services and environmental benefits: an overview. Adv Agroforestry. https://doi.org/10.1007/s10457-009-9229-7
Laurance SGW (2004) Landscape connectivity and biological corridors. In: Schroth G, da Fonseca GAB, Harvey CA, Gascon C, Vasconcelos HL, Izac A (eds) Agroforestry and biodiversity conservation in tropical landscapes. Island Press, Washington, DC, pp 50–63
Lewis SL, Edwards DP, Galbraith D (2015) Increasing human dominance of tropical forests. Science 349:827–832. https://doi.org/10.1126/science.aaa9932
Lindner A, Morawetz W (2006) Seed dispersal by Frugivorous bats on landslides in a montane rain forest in Southern Ecuador. Chiroptera Neotropical 12(1):232–237
Lobova TA, Geiselman CK, Mori SA (2009) Seed dispersal by bats in the Neotropics. New York Botanical Garden Press, New York
Loos J, Abson DJ, Chappell MJ, Hanspach J, Mikulcak F, Tichit M, Fischer J (2014) Putting meaning back into “sustainable intensification.” Front Ecol Environ 12:356–361. https://doi.org/10.1890/130157
López-Baucells A (2018) Field guide to the bats of the Amazon. Pelagic Publishing, Exeter, UK. https://pelagicpublishing.com/products/field-guide-to-the-bats-of-the-amazon-9781784271657-adria-baucells
Luzuriaga-Quichimbo CX, Barco MHD, Blanco-Salas J, Cerón-Martínez CE, Ruiz-Téllez T (2019) Plant biodiversity knowledge varies by gender in sustainable Amazonian agricultural systems called chacras. Sustainability 11:4211. https://doi.org/10.3390/su11154211
Magurran A (2004) Measuring biological diversity. Blackwell Publishing, Oxford
Medellin RA, Gaona O (1999) Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, Mexico. Biotropica 31:478–485. https://doi.org/10.1111/j.1744-7429.1999.tb00390.x
Mello MA, Schittini GM, Selig P, Bergallo HG (2004) Seasonal variation in the diet of the bat Carollia perspicillata (Chiroptera: Phyllostomidae) in an Atlantic Forest area in southeastern Brazil. Mammalia 68:49–55. https://doi.org/10.1515/mamm.2004.006
Mello MAR, Marquitti FMD, Guimarães PR, Kalko EKV, Jordano P, Aguiar MAMD (2011a) The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. PLoS ONE. https://doi.org/10.1371/journal.pone.0017395
Mello MAR, Marquitti FMD, Guimarães PR, Kalko EKV, Jordano P, Aguiar MAMD (2011b) The modularity of seed dispersal: differences in structure and robustness between bat– and bird–fruit networks. Oecologia 167:131–140. https://doi.org/10.1007/s00442-011-1984-2
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 Chiropterologica 14:357. https://doi.org/10.3161/150811012X661675
Muchhala N, Serrano D (2015) The complexity of background clutter affects nectar bat use of flower odor and shape cues. PLoS ONE. https://doi.org/10.1371/journal.pone.0136657
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
Muschler RB (2016) Agroforestry: essential for sustainable and climate-smart land use? In: Pancel L, Köhl M (eds) Tropical forestry handbook, 2nd edn. Springer, Berlin, pp 2013–2116
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GABD, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Olimpi EM, Philpott SM (2018) Agroecological farming practices promote bats. Agr Ecosyst Environ 265:282–291. https://doi.org/10.1016/j.agee.2018.06.008
Ordóñez L, Valle D, Veintimilla D (2012) Fauna de la parte alta del Bosque Protector Colonso Fundación Bosques Para La Conservación y Ministerio Del Ambiente. Quito. https://doi.org/10.13140/RG.2.2.25838.00325
Parolin P (2002) Life history and environment of Cecropia latiloba in Amazonian floodplains. Rev Biol Trop 50:531–545
Parolin LC, Bianconi GV, Mikich SB (2016) Consistency in fruit preferences across the geographical range of the frugivorous bats Artibeus, Carollia and Sturnira (Chiroptera). Iheringia Série Zoologia. https://doi.org/10.1590/1678-4766e2016010
Pedrozo AR, Gomes LAC, Uieda W (2018) Feeding behavior and activity period of three Neotropical bat species (Chiroptera: Phyllostomidae) on Musa paradisiaca inflorescences (Zingiberales: Musaceae). Iheringia Série Zoologia. https://doi.org/10.1590/1678-4766e2018022
Peñuela MC, Schwarz A, Monteros-Altamirano Á, Zurita-Benavides MG, Cayapa R, Romero N (2016) Guía de la Agrobiodiversidad: Tres comunidades kichwa: Atacapi, Alto Tena y Pumayacu. Universidad Regional Amazónica Ikiam, Tena. http://repositorio.ikiam.edu.ec:8080/jspui/handle/RD_IKIAM/140
Renninger HJ, Phillips N, Salvucci GD (2009) Wet- vs. dry-season transpiration in an Amazonian rain forest palm Iriartea deltoidea. Biotropica 42:470–478. https://doi.org/10.1111/j.1744-7429.2009.00612.x
Ricaurte LF, Jokela J, Siqueira A, Núñez-Avellaneda M, Marin C, Velázquez-Valencia A, Wantzen KM (2012) Wetland habitat diversity in the Amazonian Piedmont of Colombia. Wetlands 32:1189–1202. https://doi.org/10.1007/s13157-012-0348-y
Rinehart JB, Kunz TH (2006) Rhinophylla Pumilio. Mamm Species 791:1–5. https://doi.org/10.1644/791.1
Rodríguez C, Castillo M (2005) Análisis de los Sistemas de Producción en el Territorio de Seis Comunidades Kichwas Asentadas en la Zona Noroccidental del Parque Nacional Yasuní, Río Napo, Orellana – Ecuador. Informe Técnico. Wildlife Conservation Society (WCS), Quito. ftp://ftp.puce.edu.ec/Facultades/CienciasHumanas/Ecoturismo/ArticulosTurismo/Art%EDculos%20cient%EDficos/Estudios%20de%20caso/Kichwa_Parque%20Nacional%20Yasuni/An%E1lisis%20Sistemas%20Producci%F3n%20Territorio%20Comunidades%20Kichwas.pdf
Rojas D, Vale Á, Ferrero V, Navarro L (2011) When did plants become important to leaf-nosed bats? Diversification of feeding habits in the family Phyllostomidae. Mol Ecol 20:2217–2228. https://doi.org/10.1111/j.1365-294X.2011.05082.x
Saldaña-Vázquez RA (2014) Intrinsic and extrinsic factors affecting dietary specialization in Neotropical frugivorous bats. Mammal Rev 44:215–224. https://doi.org/10.1111/mam.12024
Sánchez MS, Giannini NP (2018) Trophic structure of frugivorous bats in the Neotropics: emergent patterns in evolutionary history. Mammal Rev 48:90–107. https://doi.org/10.1111/mam.12116
Sánchez-Villacis HG, Quintana YG, López GG, Crespo YA, Rios-Obregon J, Guerrero-Rubio JP (2017) Efecto del grado de antropización en la estructura, en tres sitios fragmentados bosque siempreverde piemontano. Revista Cubana de Ciencias Forestales: CFORES 5: 172–180. ISSN-e 2310–3469. https://rc.upr.edu.cu/jspui/handle/DICT/2686
Sarmento R, Alves-Costa CP, Ayub A, Mello MA (2014) Partitioning of seed dispersal services between birds and bats in a fragment of the Brazilian Atlantic Forest. Zoologia (curitiba) 31:245–255. https://doi.org/10.1590/S1984-46702014000300006
Schöngart J, Wittmann F, Worbes M, Piedade MT, Krambeck HJ, Junk WJ (2007) Management criteria for Ficus insipida Willd. (Moraceae) in Amazonian white-water floodplain forests defined by tree-ring analysis. Ann for Sci 64:657–664. https://doi.org/10.1051/forest:2007044
Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Frugivory and seed dispersal: ecological and evolutionary aspects. Vegetatio 107:15–29
Sodhi NS, Ehrlich P (2010) Conservation biology for all. Oxford Univ. Press, Oxford
Soriano PJ (2000) Functional structure of bat communities in Tropical Rainforests and Andean cloud forests. Ecotropicos 13:1–20
Thies W, Kalko EK (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 104:362–376. https://doi.org/10.1111/j.0030-1299.2004.12747.x
Tirira DG (2017) Guía de campo de los mamíferos del Ecuador. Editorial Murciélago Blanco, Quito
Tirira DG, Brito J, Burneo D, Moreno P, Pinto M (2020) Mamíferos del Ecuador: Lista Actualizada de Especies. Asociación Ecuatoriana de Mastozoología. http://aem.mamiferosdelecuador.com. Accessed 2021
Torres B, Maza OJ, Aguirre P, Hinojosa L, Günter S (2015) The Contribution of Traditional Agroforestry to Climate Change Adaptation in the Ecuadorian Amazon: The Chakra System. In: Leal Filo W (ed) Handbook of Climate Change Adaptation, 1st edn. Springer, Berlin, Heidelberg, pp 1973–1994. https://doi.org/10.1007/978-3-642-38670-1_102
Tostes LD, Carim MD, Gonçalves JF, Torres AM, Guimarães JR (2018) Spatial distribution pattern and diameter structure of Protium Burm. f. in Iratapuru river sustainable development reserve, Amapá, Brazil. Acta Scientiarum Biol Sci. https://doi.org/10.4025/actascibiolsci.v40i1.35854
van der Hoek Y (2018) The potential of protected areas to halt deforestation in Ecuador. Environ Conserv 44:124–130. https://doi.org/10.1017/S037689291700011X
Vera VRR, Cota-Sánchez JH, Grijalva Olmedo JE (2019) Biodiversity, dynamics, and impact of chakras on the Ecuadorian Amazon. J Plant Ecol 12:34–44. https://doi.org/10.1093/jpe/rtx060
Vleut I, Galindo-González J, Boer WFD, Levy-Tacher SI, Vazquez LB (2015) Niche differentiation and its relationship with food abundance and vegetation complexity in four Frugivorous bat species in Southern Mexico. Biotropica 47:606–615. https://doi.org/10.1111/btp.12238
Zurita Benavides MG, Schwarz A, Monteros Altamirano A & Peñuela Mora MC (2021) Transiciones alimentarias: Uso de la tierra, plantas y dietas entre los kichwas de Tena, Napo. In: Rebaï N, Bilhaut AG, de Suremain CE, Katz E & Paredes M (ed) Patrimonios Alimentarios en América Latina. Recursos locales, actores y globalización. IFEA/IRD, pp 59–82. ISBN: 978–612–4358–08–1
Acknowledgements
We are grateful to the owners of chagras in the buffer zone Libio Grefa, Lulu Grefa, Fermin Grefa, Klever Grefa y Norma Shiguango. We also thank John White for the English review and especially to Dr. Brock Fenton, Yntze van der Hoek, and an anonymous reviewer for the insightful comments that improved this manuscript. Captures and collections were done with the authorization of the Ministry of the Environment with research permit No. 20-19-IC-FAU/FLO-DPAN/MA.
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MH, NMR, MCP: Study conception and design; MH, NMR: Acquisition of data; MH, MCP: Analysis and interpretation of data: MCP, MH: Drafting of manuscript.
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Hinojosa, M., Méndez-Romero, N. & Peñuela, M.C. Diet and trophic structure of frugivorous bats (Phyllostomidae) in forests and chagras of the Andean–Amazon piedmont, Ecuador. Mamm Biol 101, 481–495 (2021). https://doi.org/10.1007/s42991-021-00144-z
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DOI: https://doi.org/10.1007/s42991-021-00144-z