Hostname: page-component-848d4c4894-nmvwc Total loading time: 0 Render date: 2024-06-29T09:13:19.226Z Has data issue: false hasContentIssue false
  • English
  • Français

Bat diversity is driven by elevation and distance to the nearest watercourse in a terra firme forest in the northeastern Brazilian Amazon

Published online by Cambridge University Press:  09 December 2022

Marcelo Martins Ferreira ,
Bruna da Silva Xavier ,
Paulo Estefano Dineli Bobrowiec ,
Isaí Jorge de Castro ,
Renato Hilário Open the ORCID record for Renato Hilário [Opens in a new window] ,
Alan Cavalcanti da Cunha ,
Leidiane Leão Oliveira ,
José Júlio de Toledo  and
William Douglas Carvalho
Marcelo Martins Ferreira*
Affiliation:
Programa de Pós-Graduação em Biodiversidade Tropical, Universidade Federal do Amapá (UNIFAP), Macapá, Brazil Programa de Pós-Graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil
Bruna da Silva Xavier
Affiliation:
Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil
Paulo Estefano Dineli Bobrowiec
Affiliation:
Programa de Pós-Graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil
Isaí Jorge de Castro
Affiliation:
Laboratório de Mamíferos, Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá (IEPA), Macapá, Brazil
Renato Hilário
Affiliation:
Programa de Pós-Graduação em Biodiversidade Tropical, Universidade Federal do Amapá (UNIFAP), Macapá, Brazil
Alan Cavalcanti da Cunha
Affiliation:
Programa de Pós-Graduação em Biodiversidade Tropical, Universidade Federal do Amapá (UNIFAP), Macapá, Brazil
Leidiane Leão Oliveira
Affiliation:
Instituto de Ciências e Tecnologia das Águas – ICTA, Universidade Federal do Oeste do Pará, Santarém, Brazil
José Júlio de Toledo
Affiliation:
Programa de Pós-Graduação em Biodiversidade Tropical, Universidade Federal do Amapá (UNIFAP), Macapá, Brazil
William Douglas Carvalho
Affiliation:
Programa de Pós-Graduação em Biodiversidade Tropical, Universidade Federal do Amapá (UNIFAP), Macapá, Brazil Terrestrial Ecology Group (TEG-UAM), Department of Ecology, Faculty of Sciences, Autonomous University of Madrid, Madrid, Spain Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, Madrid, Spain
*
Author for correspondence: Marcelo Martins Ferreira, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Variations in environmental conditions along gradients play an important role in species distribution through environmental filtering of morphological and physiological traits; however, their effects on bat diversity remain poorly understood. Here, we investigate the effect of the distance to the nearest watercourse, terrain elevation, vegetation clutter, basal area and canopy height on taxonomic, functional and phylogenetic diversity and on the predominance of some functional traits (body mass, wing morphology and trophic level) of bat assemblages (phyllostomid and mormoopid bats) in a terra firme forest, in the northeastern Brazilian Amazon. We captured bats using mist nets in 15 permanent plots over a 25 km2 area of continuous forest. We captured 279 individuals belonging to 28 species with a total of 77.760 m2.h of sampling effort. Our results showed that bat richness increases as a function of distance to the nearest watercourse and that the assemblage also changes, with more diverse taxonomic and functional groups in areas further from the watercourse. Furthermore, elevation positively affects species richness, and the basal area of the forest positively influences the average body mass of bats. Taken together, our results demonstrate that subtle variations in the environmental conditions along a local scale gradient impact on the main dimensions of bat diversity in primary forests.

Keywords

Chiropteraenvironmental filterfunctional diversityphylogenetic diversityphyllostomid batstaxonomic diversitytopographyvegetation structure
Type
Research Article
Information
Journal of Tropical Ecology , Volume 39 , 2024 , e1
Check for updates
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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

Aguirre, LF, Lens, L and Matthysen, E (2003) Patterns of roost use by bats in a neotropical savanna: implications for conservation. Biological Conservation 111, 435–443.CrossRefGoogle Scholar
Andrade, TY, Thies, W, Rogeri, PK, Kalko, EKV and Mello, MAR (2013) Hierarchical fruit selection by Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae). Journal of Mammalogy 94, 1094–1101.CrossRefGoogle Scholar
Asner, GP, Knapp, DE, Broadbent, EN, Oliveira, PJC, Keller, M and Silva, JN (2005) Selective logging in the Brazilian Amazon. Science 310, 480–482.CrossRefGoogle ScholarPubMed
Atauri, JA and Lucio, JV (2001) The role of landscape structure in species richness distribution of birds, amphibians, reptiles and lepidopterans in Mediterranean landscapes. Landscape Ecology 16, 147–159.CrossRefGoogle Scholar
Baccaro, FB, Rocha, IF, del Aguila, BEG, Schietti, J, Emilio, T, Pinto, JLPV, Lima, AP and Magnusson, WE (2013) Changes in ground-dwelling ant functional diversity are correlated with water-table level in an Amazonian terra firme forest. Biotropica 45, 755–763.CrossRefGoogle Scholar
Barton, K (2018) MuMIn: Multi-Model Inference, Version 1.7.2/r75. Available at https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf Google Scholar
Bazzaz, FA (1975) Plant species diversity in old-field successional ecosystems in southern lllinois. Ecology 56, 485–488.CrossRefGoogle Scholar
Blanchet, S, Helmus, MR, Brosse, S and Grenouillet, G (2014) Regional vs local drivers of phylogenetic and species diversity in stream fish communities. Freshwater Biology 59, 450–462.CrossRefGoogle Scholar
Bobrowiec, PED, Rosa, LS, Gazarini, J and Haugaasen, T (2014) Phyllostomid bat assemblage structure in Amazonian flooded and unflooded forests. Biotropica 46, 312–321.CrossRefGoogle Scholar
Bobrowiec, PED and Tavares, VC (2017) Establishing baseline biodiversity data prior to hydroelectric dam construction to monitoring impacts to bats in the Brazilian Amazon. PLoS One 12, e0183036.CrossRefGoogle ScholarPubMed
Bogoni, JA, Carvalho-Rocha, V, Ferraz, KMPMB and Peres, CA (2021) Interacting elevational and latitudinal gradients determine bat diversity and distribution across the neotropics. Journal of Animal Ecology 90, 2729–2743.CrossRefGoogle ScholarPubMed
Brasil (2012) Código Florestal Brasileiro–LEI Nº 12.651. Presidência da República Casa Civil Subchefia para Assuntos Jurídicos, DF-Brasil.Google Scholar
Bueno, AS, Bruno, RS, Pimentel, TP, Sanaiotti, TM and Magnusson, WE (2012) The width of riparian habitats for understory birds in an Amazonian forest. Ecological Applications 22, 722–734.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (1998) Model Selection and Inference: A Practical Information-Theoretical Approach. New York: Springel-Verlag.CrossRefGoogle Scholar
Capaverde, UD, Pereira, LGA, Tavares, VC, Magnusson, WE, Baccaro, FB and Bobrowiec, PED (2018) Subtle changes in elevation shift bat-assemblage structure in Central Amazonia. Biotropica 50, 674–683.CrossRefGoogle Scholar
Carbone, MS, Czimczik, CI, Keenan, TF, Murakami, PF, Pederson, N, Schaberg, PG, Xu, X and Richardson, AD (2013) Age, allocation and availability of nonstructural carbon in mature red maple trees. New Phytologist 200, 1145–1155.CrossRefGoogle ScholarPubMed
Cardoso, P, Mammola, S, Rigal, F and Carvalho, J (2021) BAT: Biodiversity Assessment Tools. Available at https://cran.r-project.org/web/packages/BAT/BAT.pdf Google Scholar
Carvalho, WD, Gomes, LAC, Castro, IJD, Martins, AC, Esbérard, CEL and Mustin, K (2018) Beyond the Amazon forest: richness and abundance of bats in the understory of Savannahs, Campinaranas and Terra Firme forest. Acta Chiropterologica 20, 407–419.CrossRefGoogle Scholar
Carvalho, WD, Martins, MA, Esbérard, CEL and Palmeirim, JM (2019) Traits that allow bats of tropical lowland origin to conquer mountains: bat assemblages along elevational gradients in the South American Atlantic forest. Journal of Biogeography 46, 316–331.CrossRefGoogle Scholar
Carvalho, WD, Mustin, K, Farneda, FZ, Castro, IJ, Hilário, RR, Martins, ACM, Miguel, JD, Xavier, BS and Toledo, JJ (2021) Taxonomic, functional and phylogenetic bat diversity decrease from more to less complex natural habitats in the Amazon. Oecologia 197, 223–239.CrossRefGoogle ScholarPubMed
Carvalho, WD, Norris, D and Michalski, F (2016) Opportunistic predation of a common scale-backed Antbird (Willisornis poecilinotus) by a Goliath bird-eating spider (Theraphosa blondi) in the Eastern Brazilian Amazon. Studies on Neotropical Fauna and Environment 51, 239–241.CrossRefGoogle Scholar
Castilho, CV, Magnusson, WE, de Araújo, RNO, Luizao, RC, Luizao, FJ, Lima, AP and Higuchi, N (2006) Variation in aboveground tree live biomass in a central Amazonian forest: effects of soil and topography. Forest Ecology and Management 234, 85–96.CrossRefGoogle Scholar
Castilho, CV, Schietti, J, Freitas, MA, Araújo, MC, Coelho, F, Magnusson, WE and Costa, FRS (2014) Manual para Medição e Marcação de Árvores em grades e módulos RAPELD do PPBio. Manaus: Instituto Nacional de Pesquisas Amazônicas (INPA), 22 pp.Google Scholar
Castillo-Figueroa, D and Pérez-Torres, J (2021) On the development of a trait-based approach for studying Neotropical bats. Papéis Avulsos de Zoologia 61, e20216124.CrossRefGoogle Scholar
Chao, A, Chiu, C-H and Jost, L (2014a) Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers. Annual Review of Ecology, Evolution, and Systematics 45, 297–324.CrossRefGoogle Scholar
Chao, A, Chiu, C-H, Villéger, S, Sun, I-F, Thorn, S, Lin, Y-C, Chiang, J-M and Sherwin, WB (2019) An attribute-diversity approach to functional diversity, functional beta diversity, and related (dis) similarity measures. Ecological Monographs 89, e01343.CrossRefGoogle Scholar
Chao, A, Gotelli, NJ, Hsieh, TC, Sander, EL, Ma, KH, Colwell, RK and Ellison, AM (2014b) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84, 45–67.CrossRefGoogle Scholar
Chatterjee, S and Hadi, AS (2006) Regression Analysis by Example. (ed). New York: John Wiley and Sons.CrossRefGoogle Scholar
Chiu, C-H and Chao, A (2014) Distance-based functional diversity measures and their decomposition: a framework based on Hill numbers. PLoS One 9, e100014.CrossRefGoogle ScholarPubMed
Cintra, R and Naka, LN (2012) Spatial variation in bird community composition in relation to topographic gradient and forest heterogeneity in a Central Amazonian Rainforest. International Journal of Ecology 2012, 1–25.Google Scholar
Cisneros, LM, Burgio, KR, Dreiss, LM, Klingbeil, BT, Patterson, BD, Presley, SJ and Willig, MR (2014) Multiple dimensions of bat biodiversity along an extensive tropical elevational gradient. Journal of Animal Ecology 83, 1124–1136.CrossRefGoogle ScholarPubMed
Clark, DB, Olivas, PC, Oberbauer, SF, Clark, DA and Ryan, MG (2008) First direct landscape-scale measurement of tropical rain forest Leaf Area Index, a key driver of global primary productivity. Ecology Letters 11, 163–172.Google ScholarPubMed
Costa, FRC, Guillaumet, JL, Lima, AP and Pereira, OS (2008) Gradients within gradients: the mesoscale distribution patterns of palms in a Central Amazonian forest. Journal of Vegetation Science 20, 1–10.Google Scholar
Costa, FRC, Magnusson, WE and Luizao, RC (2005) Mesoscale distribution patterns of Amazonian understory herbs in relation to topography, soil and watersheds. Journal of Ecology 93, 863–878.CrossRefGoogle Scholar
Crane, M, Silva, I, Matthew, JG and George, AG (2022) Limitations and gaps in global bat wing morphology trait data. Mammal Review 52, 165–176.CrossRefGoogle Scholar
Dale, MR and Fortin, MJ (2014) Spatial Analysis: A Guide for Ecologists. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Daly, AJ, Baetens, JM and De Baets, B (2018) Ecological diversity: measuring the unmeasurable. Mathematics 6, 119.CrossRefGoogle Scholar
Delgado-Jaramillo, M, Aguiar, LMS, Machado, RB and Bernard, E (2020) Assessing the distribution of a species-rich group in a continental mega-diverse country: bats in Brazil. Diversity and Distributions 26, 632–643.CrossRefGoogle Scholar
Dias-Terceiro, RG, Kaefer, IL, de Fraga, R, de Araújo, MC, Simões, PI and Lima, AP (2015) A matter of scale: historical and environmental factors structure anuran assemblages from the Upper Madeira River, Amazonia. Biotropica 47, 259–266.CrossRefGoogle Scholar
Drucker, DP, Costa, FRC and Magnusson, WE (2008) How wide is the riparian zone of small streams in tropical forests? A test with terrestrial herbs. Journal of Tropical Ecology 24, 65–74.CrossRefGoogle Scholar
Esbérard, C and Daemon, C (1999) Um novo método para marcação de morcegos. Chiroptera Neotropical 5, 116–117.Google Scholar
Estrada-Villegas, S, McGill, BJ and Kalko, EKV (2012) Climate, habitat, and species interactions at different scales determine the structure of a Neotropical bat community. Ecology 93, 1183–1193.CrossRefGoogle ScholarPubMed
Ferreira, LV (2000) Effects of flooding duration on species richness, floristic composition and forest structure in river margin habitat in Amazonian blackwater floodplain forests: implications for future design of protected areas. Biodiversity & Conservation 9, 1–14.CrossRefGoogle Scholar
Fraga, R, Lima, AP and Magnusson, WE (2011) Mesoscale spatial ecology of a tropical snake assemblage: the width of riparian corridors in Central Amazonia. Herpetological Journal 21, 51–57.Google Scholar
Freitas, JR and Mantovani, W (2017) An overview of the applicability of functional diversity in biological conservation. Brazilian Journal of Biology 78, 517–524.CrossRefGoogle ScholarPubMed
Fukui, DAI, Murakami, M, Nakano, S and Aoi, T (2006) Effect of emergent aquatic insects on bat foraging in a riparian forest. Journal of Animal Ecology 75, 1252–1258.CrossRefGoogle Scholar
Giannini, NP and Kalko, EKV (2004) Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105, 209–220.CrossRefGoogle Scholar
Gorgens, EB, Nunes, MH, Jackson, T, Coomes, D, Keller, M, Reis, CR, Valbuena, R, Rosette, J, Almeida, DRA, Gimenez, B, Cantinho, R, Motta, AZ, Assis, M, Pereira, FRS, Spanner, G, Higuchi, N and Ometto, JP (2021) Resource availability and disturbance shape maximum tree height across the Amazon. Global Change Biology 27, 177–189.CrossRefGoogle ScholarPubMed
Graça, MB, Morais, JW, Franklin, E, Pequeno, PACL, Souza, JLP and Bueno, AS (2016) Combining taxonomic and functional approaches to unravel the spatial distribution of an Amazonian butterfly community. Environmental Entomology 45, 301–309.CrossRefGoogle ScholarPubMed
Grinnell, J (1917) Field tests of theories concerning distributional control. The American Naturalist 51, 115–128.CrossRefGoogle Scholar
Guilherme, DR, Souza, JLP, Franklin, E, Pequeno, PACL, Chagas, AC and Baccaro, FB (2019) Can environmental complexity predict functional trait composition of ground-dwelling ant assemblages? A test across the Amazon Basin. Acta Oecologica 99, 103434.CrossRefGoogle Scholar
Hagen, EM and Sabo, JL (2011) A landscape perspective on bat foraging ecology along rivers: does channel confinement and insect availability influence the response of bats to aquatic resources in riverine landscapes? Oecologia 166, 751–760.CrossRefGoogle ScholarPubMed
Hagen, EM and Sabo, JL (2014) Temporal variability in insectivorous bat activity along two desert streams with contrasting patterns of prey availability. Journal of Arid Environments 102, 104–112.CrossRefGoogle Scholar
Hansen, MC, Potapov, PV, Moore, R, Hancher, M, Turubanova, SA, Tyukavina, A, Thau, D, Stehman, SV, Goetz, SJ, Loveland, TR, Kommareddy, A, Egorov, A, Chini, L, Justice, CO and Townshend, JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342, 850–853.CrossRefGoogle ScholarPubMed
Hanspach, J, Fischer, J, Ikin, K, Stott, J and Law, BS (2012) Using trait-based filtering as a predictive framework for conservation: a case study of bats on farms in southeastern Australia. Journal of Applied Ecology 49, 842–850.CrossRefGoogle Scholar
Hill, MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54, 427–432.CrossRefGoogle Scholar
Holloway, GL and Barclay, RM (2000) Importance of prairie riparian zones to bats in southeastern Alberta. Ecoscience 7, 115–122.CrossRefGoogle Scholar
Hortal, J, Bello, F, Diniz-Filho, JAF, Lewinsohn, TM, Lobo, JM and Ladle, RJ (2015) Seven shortfalls that beset large-scale knowledge of biodiversity. Annual Review of Ecology, Evolution, and Systematics 46, 523–549.CrossRefGoogle Scholar
Hsieh, TC, Ma, KH and Chao, A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7, 1451–1456.CrossRefGoogle Scholar
ICMBio (2016) Plano de manejo da Floresta Nacional do Amapá. Volume I, dignostico. Macapá-Ap: Intituto Chico Mendes de Conservação da Biodiversidade (ICMBio)-Unidades de Conservação, 113 pp.Google Scholar
Kalko, EKV, Handley, CO and Handley, D (1996a) Chapter 16: Organization, diversity, and long-term dynamics of a Neotropical bat community. In Cody, ML and Smallwood, JA (eds), Long-Term Studies of Vertebrate Communities. Los Angeles: Academic Press, pp. 503–553.CrossRefGoogle Scholar
Kalko, EKV, Herre, EA and Handley, CO (1996b) Relation of fig fruit characteristics to fruit-eating bats in the new and old world tropics. Journal of Biogeography 23, 565–576.CrossRefGoogle Scholar
Kaufman, DM (1995) Diversity of new world mammals: universality of the latitudinal gradients of species and Bauplans. Journal of Mammalogy 76, 322–334.CrossRefGoogle Scholar
Keddy, PA (1992) Assembly and response rules: two goals for predictive community ecology. Journal of Vegetation Science 3, 157–164.CrossRefGoogle Scholar
Kinap, NM, Nagy-Reis, M, Bobrowiec, PED, Gordo, M and Spironello, WR (2021) Influence of topography gradient and seasonality on primate habitat use in Central Amazonia. Mammalian Biology 101, 1–9.CrossRefGoogle Scholar
Kinupp, VF and Magnusson, WE (2005) Spatial patterns in the understorey shrub genus Psychotria in central Amazonia: effects of distance and topography. Journal of Tropical Ecology 21, 363–374.CrossRefGoogle Scholar
Kraxner, F, Nordström, E-M, Havlík, P, Gusti, M, Mosnier, A, Frank, S, Valin, H, Fritz, S, Fuss, S, Kindermann, G, McCallum, I, Khabarov, N, Böttcher, M, See, L, Aoki, K, Schimid, E, Máthé, L and Obersteiner, M (2013) Global bioenergy scenarios–future forest development, land-use implications, and trade-offs. Biomass and Bioenergy 57, 86–96.CrossRefGoogle Scholar
Larjavaara, M and Muller-Landau, HC (2013) Measuring tree height: a quantitative comparison of two common field methods in a moist tropical forest. Methods in Ecology and Evolution 4, 793–801.CrossRefGoogle Scholar
Lavorel, S, Grigulis, K, McIntyre, S, Williams, NSG, Garden, D, Dorrough, J, Berman, S, Quétier, F, Thébault, A and Bonis, A (2008) Assessing functional diversity in the field–methodology matters! Functional Ecology 22, 134–147.Google Scholar
Lees, AC and Peres, CA (2008) Conservation value of remnant riparian forest corridors of varying quality for Amazonian birds and mammals. Conservation Biology 22, 439–449.CrossRefGoogle ScholarPubMed
Levin, SA (1992) The problem of pattern and scale in ecology: the Robert H. MacArthur award lecture. Ecology 73, 1943–1967.CrossRefGoogle Scholar
Li, D (2018a) hillR: taxonomic, functional, and phylogenetic diversity and similarity through Hill Numbers. Journal of Open Source Software 3, 1041.CrossRefGoogle Scholar
Li, D (2018b) Package ‘hillR’ versão 0.5.0. Available at https://cran.r-project.org/web/packages/hillR/hillR.pdf Google Scholar
Lim, BK and Engstrom, MD (2001) Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: implications for conservation. Biodiversity & Conservation 10, 613–657.CrossRefGoogle Scholar
Lindquist, EJ, D’Annunzio, R, Gerrand, A, MacDicken, K, Achard, F, Beuchle, R, Brink, A, Eva, HD, Mayaux, P, San-Miguel-Ayanz, J and Stibig, HJ (2012) Global Forest Land-Use Change 1990–2005. Rome: Food and Agriculture Organization of the United Nations (FAO), 59 pp.Google Scholar
López-Baucells, A, Rocha, R, Bobrowiec, P, Bernard, E, Palmerim, J and Meyer, CFJ (2016) Field Guide to the Bats of the Amazon. Manaus: Instituto Nacional de Pesquisas Amazônicas.Google Scholar
Magnusson, WE, Braga-Neto, R, Pezzini, F, Baccaro, F, Bergallo, H, Penha, J, Rodrigues, D, Verdade, LM, Lima, A, Albernaz, AL, Hero, JM, Lawson, B, Castilho, C, Drucker, D, Franklin, E, Mendonça, F, Costa, F, Galdino, G, Castley, G, Zuanon, J, do Vale, J, dos Santos, JLC, Luizão, R, Cintra, R, Barbosa, RI, Lisboa, A, Koblitz, RV, da Cunha, CN and Pontes, ARM (2013) Biodiversity and Integrated Environmental Monitoring (Biodiversidade e monitoramento ambiental integrado). Santo André: Áttema Editorial.Google Scholar
Magnusson, WE, Lima, AP, Luizão, R, Luizão, F, Costa, FRC, Castilho, CV and Kinupp, VF (2005) RAPELD: a modification of the Gentry method for biodiversity surveys in long-term ecological research sites. Biota Neotropica 5, 19–24.CrossRefGoogle Scholar
Marciente, R, Bobrowiec, PED and Magnusson, WE (2015) Ground-vegetation clutter affects Phyllostomid bat assemblage structure in lowland Amazonian forest. PLoS One 10, e0129560.CrossRefGoogle ScholarPubMed
Marinello, MM and Bernard, E (2014) Wing morphology of Neotropical bats: a quantitative and qualitative analysis with implications for habitat use. Canadian Journal of Zoology 92, 141–147.CrossRefGoogle Scholar
Marques, JT, Ramos Pereira, MJ and Palmeirim, JM (2012) Availability of food for frugivorous bats in lowland Amazonia: the influence of flooding and of river banks. Acta Chiropterologica 14, 183–194.CrossRefGoogle Scholar
McGill, BJ, Enquist, BJ, Weiher, E and Westoby, M (2006) Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21, 178–185.CrossRefGoogle ScholarPubMed
McNab, BK (1969) The economics of temperature regulation in neutropical bats. Comparative biochemistry and Physiology 31, 227–268.CrossRefGoogle ScholarPubMed
Menegassi, D (2021) Mineração em Terras Indígenas, regularização fundiária e mais, entenda as prioridades de Bolsonaro para 2021. Available at https://www.oeco.org.br/author/duda/ Google Scholar
Michalski, LJ, Norris, D, de Oliveira, TG and Michalski, F (2015) Ecological relationships of meso-scale distribution in 25 neotropical vertebrate species. PLoS One 10, e0126114.CrossRefGoogle ScholarPubMed
Minor, DM and Kobe, RK (2019) Fruit production is influenced by tree size and size-asymmetric crowding in a wet tropical forest. Ecology and Evolution 9, 1458–1472.CrossRefGoogle Scholar
Monteiro, LR and Nogueira, MR (2011) Evolutionary patterns and processes in the radiation of phyllostomid bats. BMC Evolutionary Biology 11, 1–23.CrossRefGoogle ScholarPubMed
Muller, J, Mehr, M, Bassler, C, Fenton, MB, Hothorn, T, Pretzsch, H, Klemmt, HJ and Brandl, R (2012) Aggregative response in bats: prey abundance versus habitat. Oecologia 169, 673–684.CrossRefGoogle ScholarPubMed
Norberg, UM and Rayner, JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London. B: Biological Sciences 316, 335–427.Google Scholar
Ober, HK and Hayes, JP (2008) Influence of vegetation on bat use of riparian areas at multiple spatial scales. Journal of Wildlife Management 72, 396–404.CrossRefGoogle Scholar
Oliveira, J, Almeida, SM, Florencio, FP, Pinho, JB, Oliveira, DMM, Ligeiro, R and Rodrigues, DJ (2019) Environmental structure affects taxonomic diversity but not functional structure of understory birds in the southwestern Brazilian Amazon. Acta Amazonica 49, 232–241.CrossRefGoogle Scholar
Oliveira, LL, Cunha, AC, Jesus, ES and Barreto, NJC (2010) Características Hidroclimáticas da Bacia do Rio Araguari (AP). In Cunha, AC, Souza, EB and Cunha, HFA (ed.), Tempo, clima e recursos hídricos: resultados do Projeto REMETAP no Estado do Amapá. Macapá: Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá (IEPA), pp. 83–88.Google Scholar
Oliveira, LL, Canani, LGC, Barreto, NJC and Cunha, AC (2020) Water ecosystem services in an undisturbed forest in the Amazon, Amapá, Brazil. Nature and Conservation 13, 45–54.CrossRefGoogle Scholar
Oliveira, LQ, Marciente, R, Magnusson, WE and Bobrowiec, PED (2015) Activity of the insectivorous bat Pteronotus parnellii relative to insect resources and vegetation structure. Journal of Mammalogy 96, 1036–1044.CrossRefGoogle Scholar
Pansonato, MP, Costa, FRC, Castilho, CV, Carvalho, FA and Zuquim, G (2012) Spatial scale or amplitude of predictors as determinants of the relative importance of environmental factors to plant community structure. Biotropica 45, 299–307.CrossRefGoogle Scholar
Parker, GG, Lowman, MD and Nadkarni, NM (1995) Forest canopies (Physiological Ecology). San Diego: Academic Press.Google Scholar
Patterson, BD, Pacheco, V, and Solari, S (1996) Distributions of bats along an elevational gradient in the Andes of south-eastern Peru. Journal of Zoology 240, 637–658.CrossRefGoogle Scholar
Peixoto, JMA, Nelson, BW and Wittmann, F (2009) Spatial and temporal dynamics of river channel migration and vegetation in central Amazonian white-water floodplains by remote-sensing techniques. Remote Sensing of Environment 113, 2258–2266.CrossRefGoogle Scholar
Pereira, LGA, Capavede, UD Jr, Tavares, CV, Magnusson, WE, Bobrowiec, PED and Baccaro, FB (2019) From a bat’s perspective, protected riparian areas should be wider than defined by Brazilian laws. Journal of Environmental Management 232, 37–44.CrossRefGoogle ScholarPubMed
Poff, NL (1997) Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. Journal of the North American Benthological Society 16, 391–409.CrossRefGoogle Scholar
Poulsen, BO (2002) Avian richness and abundance in temperate Danish forests: tree variables important to birds and their conservation. Biodiversity & Conservation 11, 1551–1566.CrossRefGoogle Scholar
Ramos Pereira, MJ, Marques, JT and Palmeirim, JM (2010) Ecological responses of frugivorous bats to seasonal fluctuation in fruit availability in Amazonian forests. Biotropica 42, 680–687.CrossRefGoogle Scholar
Ramos Pereira, MJ, Marques, JT, Santana, J, Santos, CD, Valsecchi, J, Queiroz, HL, Beja, P and Palmeirim, JM (2009) Structuring of Amazonian bat assemblages: the roles of flooding patterns and floodwater nutrient load. Journal of Animal Ecology 78, 1163–1171.CrossRefGoogle Scholar
R Development Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.r-project.org/ Google Scholar
Reis, NR, Fregonezi, MN, Peracchi, AL and Shibatta, OA (2013) Morcegos do Brasil: guia de campo. Rio de Janeiro: Technical Books Editora, 252 pp.Google Scholar
Reis, NR, Peracchi, AL, Batista, CB, de Lima, IP and Pereira, AD (2017) História Natural dos morcegos brasileiros: chave de identificação de espécies. Rio de Janeiro: Technical Books Editora, 416 pp.Google Scholar
Rex, K, Michener, R, Kunz, TH and Voigt, CC (2011) Vertical stratification of Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes. Journal of Tropical Ecology 27, 211–222.CrossRefGoogle Scholar
Rodrigues, LF, Cintra, R, Castilho, CV, Pereira, OS and Pimentel, TP (2014) Influences of forest structure and landscape features on spatial variation in species composition in a palm community in central Amazonia. Journal of Tropical Ecology 30, 565–578.CrossRefGoogle Scholar
Rojas-Ahumada, DP, Landeiro, VL and Menin, M (2012) Role of environmental and spatial processes in structuring anuran communities across a tropical rain forest. Austral Ecology 37, 865–873.CrossRefGoogle Scholar
Roswell, M, Dushoff, J and Winfree, R (2021) A conceptual guide to measuring species diversity. Oikos 130, 321–338.CrossRefGoogle Scholar
Salo, J, Kalliola, R, Häkkinen, I, Mäkinen, Y, Niemelä, P, Puhakka, M and Coley, PD (1986) River dynamics and the diversity of Amazon lowland forest. Nature 322, 254–258.CrossRefGoogle Scholar
Schietti, J, Emilio, T, Rennó, CD, Drucker, DP, Costa, FRC, Nogueira, A, Baccaro, FB, Figueiredo, F, Castilho, CV, Kinupp, V, Guillaumet, JT, Garcia, ARN, Lima, AP and Magnusson, WE (2014) Vertical distance from drainage drives floristic composition changes in an Amazonian rainforest. Plant Ecology & Diversity 7, 241–253.CrossRefGoogle Scholar
Schnitzler, HU and Kalko, EKV (1998) How echolocating bats search and find food. In Kunz, TH and Racey, PA (eds.), Bat Biology and Conservation. Washington (DC): Smithsonian Institution Press, pp. 183–196.Google Scholar
Schnitzler, HU, Moss, CF and Denzinger, A (2003) From spatial orientation to food acquisition in echolocating bats. Trends in Ecology & Evolution 18, 386–394.CrossRefGoogle Scholar
Serviço Florestal Brasileiro (2019) Plano Anual de Outorga Florestal 2020 – Serviço Florestal Brasileiro. Distrito Federal, Brasil: Ministério de Agricultura, Pecuária e Abastecimento, pp. 23–24.Google Scholar
Serviço Florestal Brasileiro (2020) Edital 01/2020 – Concorrência Pública – Concessão Florestal – Floresta Nacional do Amapá (AP). Distrito Federal, Brasil: Ministério de Agricultura, Pecuária e Abastecimento.Google Scholar
Shanahan, M and Compton, SG (2001) Vertical stratification of figs and fig-eaters in a Bornean lowland rain forest: how is the canopy different? In Plant Ecology (ed.), Tropical Forest Canopies: Ecology and Management. Proceedings of the European Science Foundation Conference. Springer: Oxford University, pp. 121–132.CrossRefGoogle Scholar
Silva, RMT (2012) Efeito da obstrução gerada pela densidade da vegetação do sub-bosque sobre morcegos frugívoros e animalívoros catadores (Chiroptera: Phyllostomidae) na Amazônia central, Brasil. Dissertação (Biologia (Ecologia)). Manaus: Instituto Nacional de Pesquisas da Amazônia, 51 pp.Google Scholar
Sleep, DJH and Brigham, RM (2003) An experimental test of clutter tolerance in bats. Journal of Mammalogy 84, 216–224.2.0.CO;2>CrossRefGoogle Scholar
Sobral, FL and Cianciaruso, MV (2016) Functional and phylogenetic structure of forest and savanna bird assemblages across spatial scales. Ecography 39, 533–541.CrossRefGoogle Scholar
Stevens, RD, Cox, SB, Strauss, RE and Willig, MR (2003) Patterns of functional diversity across an extensive environmental gradient: Vertebrate consumers, hidden treatments and latitudinal trends. Ecology Letters 6, 1099–1108.CrossRefGoogle Scholar
Stevens, RD, López-González, C and Presley, SJ (2007) Geographical ecology of Paraguayan bats: spatial integration and metacommunity structure of interacting assemblages. Journal of Animal Ecology 76, 1086–1093.CrossRefGoogle ScholarPubMed
Stevens, RD and Willig, MR (2000) Density compensation in new world bat communities. Oikos 89, 367–377.CrossRefGoogle Scholar
Stockwell, EF (2001) Morphology and flight manoeuvrability in New World leaf-nosed bats (Chiroptera: Phyllostomidae). Journal of Zoology 254, 505–514.CrossRefGoogle Scholar
Straube, FC and Bianconi, GV (2002) Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical 8(1–2), 150–152.Google Scholar
Tavares, AS, Morcatty, TQ, Zuanon, J and Magnusson, WE (2019) Influence of body size, topography, food availability and tree-fall gaps on space use by yellow-footed tortoises (Chelonoidis denticulatus) in Central Amazonia. PLoS One 14, e0211869.CrossRefGoogle ScholarPubMed
Tavares, VC, Nobre, CC, Palmuti, CF, Nogueira, EP, Gomes, JD, Marcos, MH, Silva, RF, Farias, SG and Bobrowiec, PED (2017) The bat fauna from southwestern Brazil and its affinities with the fauna of western Amazon. Acta Chiropterologica 19, 93–106.CrossRefGoogle Scholar
Tews, J, Brose, U, Grimm, V, Tielbörger, K, Wichmann, MC, Schwager, M and Jeltsch, F (2003) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31, 79–92.CrossRefGoogle Scholar
Toledo, JJ, Castilho, CV, Magnusson, WE and Nascimento, HEM (2017) Soil controls biomass and dynamics of an Amazonian forest through the shifting of species and traits. Brazilian Journal of Botany 40, 451–461.CrossRefGoogle Scholar
Tucker, CM, Cadotte, MW, Carvalho, SB, Davies, TJ, Ferrier, S, Fritz, SA, Grenyer, R, Helmus, MR, Jin, LS, Mooers, AO, Pavoine, S, Purschke, O, Redding, DW, Rosauer, DF, Winter, M and Mazel, F (2017) A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biological Reviews 92, 698–715.CrossRefGoogle ScholarPubMed
Upham, NS, Esselstyn, JA and Jetz, W (2019) Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biology 17, e3000494.CrossRefGoogle ScholarPubMed
Van Schaik, CP, Terborgh, JW and Wright, SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics 24, 353–377.CrossRefGoogle Scholar
Voigt, CC (2010) Insights into strata use of forest animals using the ‘canopy effect’. Biotropica 42, 634–637.CrossRefGoogle Scholar
Voigt, CC and Holderied, MW (2012) High manoeuvring costs force narrow-winged molossid bats to forage in open space. Journal of Comparative Physiology B 182, 415–424.CrossRefGoogle ScholarPubMed
Williams, SE, Marsh, H and Winter, J (2002) Spatial scale, species diversity, and habitat structure: small mammals in Australian tropical rain forest. Ecology 83, 1317–1329.CrossRefGoogle Scholar
Winter, Y and Von Helversen, O (1998) The energy cost of flight: do small bats fly more cheaply than birds? Journal of Comparative Physiology B 168, 105–111.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Ferreira et al. supplementary material

Ferreira et al. supplementary material 1

Download Ferreira et al. supplementary material(PDF)
PDF 33.1 KB
Supplementary material: PDF

Ferreira et al. supplementary material

Ferreira et al. supplementary material 2

Download Ferreira et al. supplementary material(PDF)
PDF 326.8 KB
Supplementary material: PDF

Ferreira et al. supplementary material

Ferreira et al. supplementary material 3

Download Ferreira et al. supplementary material(PDF)
PDF 840.7 KB