Abstract
Which functional traits allow a bat species to survive habitat disturbance? Empirical evidence regarding this question remains limited for many tropical regions despite their importance for conservation. Here, we used body mass, wing morphology, trophic level, and diet to identify which traits make phyllostomid bat species more vulnerable to human impacts in the Colombian Orinoco Llanos. Bats were sampled using mist nets in riparian forests, unflooded forests, flooded savannahs, and conventional rice crops on traditional farmlands with high-intensity agriculture and in private reserves with greater ecosystem protection. We tested the associations between species traits and landscape-structure variables (habitat cover and type, number of habitat patches, shortest distance to water) using RLQ and fourth-corner analyses, accounting for both spatial and phylogenetic autocorrelation. Trophic level and diet were the most important traits linked to disturbance sensitivity. Our results indicated that rice crop cover, savannah patches, and altered unflooded forest act as a filter, benefiting disturbance-adapted frugivorous genera in farmlands (e.g., Artibeus spp., Carollia spp., Platyrrhinus spp., Uroderma spp.). Conversely, animalivorous species were strongly associated with savannah cover and riparian forests within reserves (e.g., Lampronycteris brachyotis, Lophostoma brasiliense, Micronycteris minuta, Trachops cirrhosus). Encouraging the creation of more wildlife-friendly landscapes through payments for ecosystem services across the Colombian Llanos will ensure the long-term persistence of disturbance-sensitive species and sustain a complete set of ecological functions and ecosystem services that these bats provide.
Similar content being viewed by others
Data availability
Data on species functional traits: uploaded as online supporting information (Table S1).
Environmental descriptors of the study sites: uploaded as online supporting information (Table S2).
Bat species occupancy and abundance change: uploaded as online supporting information (Table S3).
References
Aldana A, Mitchley J (2013) Protected areas legislation and the conservation of the Colombian Orinoco Basin natural ecosystems. Nat Conserv 4:15–28. https://doi.org/10.3897/natureconservation.4.3682
Arroyo-Rodríguez V, Rojas C, Saldaña-Vázquez RA, Stoner KE (2016) Landscape composition is more important than landscape configuration for phyllostomid bat assemblages in a fragmented biodiversity hotspot. Biol Conserv 198:84–92. https://doi.org/10.1016/j.biocon.2016.03.026
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B: Stat Methodol 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bernard E, Fenton MB (2003) Bat mobility and roosts in a fragmented landscape in Central Amazonia. Brazil Biotropica 35:262–277. https://doi.org/10.1111/j.1744-7429.2003.tb00285.x
Bobrowiec PED, Farneda FZ, Nobre CC, Tavares VC (2022) Taxonomic and functional responses of bats to habitat flooding by an amazonian mega-dam. Biodivers Conserv 31:1359–1377. https://doi.org/10.1007/s10531-022-02396-8
Borghetti F, Barbosa E, Ribeiro L et al (2019) South American Savannas. In: Scogings PF, Sankaran M (eds) Savanna Woody Plants and large herbivores. John Wiley & Sons, pp 77–122
Braga J, ter Braak CJF, Thuiller W, Dray S (2018) Integrating spatial and phylogenetic information in the fourth-corner analysis to test trait–environment relationships. Ecology 99:2667–2674. https://doi.org/10.1002/ecy.2530
Buchadas A, Baumann M, Meyfroidt P, Kuemmerle T (2022) Uncovering major types of deforestation frontiers across the world’s tropical dry woodlands. Nat Sustain 5:619–627. https://doi.org/10.1038/s41893-022-00886-9
Cadotte MW, Tucker CM (2017) Should environmental filtering be abandoned? Trends Ecol Evol 32:429–437. https://doi.org/10.1016/j.tree.2017.03.004
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x
Carballo-Morales JD, Saldaña-Vázquez RA, Villalobos F (2021) Trophic guild and forest type explain phyllostomid bat abundance variation from human habitat disturbance. Glob Ecol Conserv 25:e01425. https://doi.org/10.1016/j.gecco.2020.e01425
Carvalho WD, Mustin K, Farneda FZ et al (2021) Taxonomic, functional and phylogenetic bat diversity decrease from more to less complex natural habitats in the Amazon. Oecologia 197:223–239. https://doi.org/10.1007/s00442-021-05009-3
Castillo-Figueroa D, Pérez-Torres J (2021) On the development of a trait-based approach for studying neotropical bats. Pap Avulsos Zool 61:e20216124. https://doi.org/10.11606/1807-0205/2021.61.24
Castro-Luna AA, Galindo-González J (2012) Enriching agroecosystems with fruit-producing tree species favors the abundance and richness of frugivorous and nectarivorous bats in Veracruz, Mexico. Mamm Biol 77:32–40. https://doi.org/10.1016/j.mambio.2011.06.009
Chambers CL, Cushman SA, Medina-Fitoria A et al (2016) Influences of scale on bat habitat relationships in a forested landscape in Nicaragua. Landsc Ecol 31:1299–1318. https://doi.org/10.1007/s10980-016-0343-4
Chichorro F, Juslén A, Cardoso P (2019) A review of the relation between species traits and extinction risk. Biol Conserv 237:220–229. https://doi.org/10.1016/j.biocon.2019.07.001
Cleary KA, Waits LP, Finegan B (2016) Agricultural intensification alters bat assemblage composition and abundance in a dynamic neotropical landscape. Biotropica 48:667–676. https://doi.org/10.1111/btp.12327
Colinvaux P (1980) Why big fierce animals are rare? An ecologist’s perspective. Penguin Books, London, UK
Colombo GT, Di Ponzio R, Benchimol M et al (2023) Functional diversity and trait filtering of insectivorous bats on forest islands created by an amazonian mega dam. Funct Ecol 37:99–111. https://doi.org/10.1111/1365-2435.14118
Crane M, Silva I, Grainger MJ, Gale GA (2022) Limitations and gaps in global bat wing morphology trait data. Mamm Rev 52:165–176. https://doi.org/10.1111/mam.12270
Cushman SA, McGarigal K, Neel MC (2008) Parsimony in landscape metrics: strength, universality, and consistency. Ecol Indic 8:691–703. https://doi.org/10.1016/j.ecolind.2007.12.002
Dávalos LM, Cirranello AL, Geisler JH, Simmons NB (2012) Understanding phylogenetic incongruence: lessons from phyllostomid bats. Biol Rev 87:991–1024. https://doi.org/10.1111/j.1469-185X.2012.00240.x
De Marco P, De Souza RA, Andrade AFA, Villén-Pérez S, Nóbrega CC, Campello LM, Caldas M (2023) The value of private properties for the conservation of biodiversity in the Brazilian Cerrado. Science 380:298–301. https://doi.org/10.1126/science.abq7768
R Development Core Team (2020) R: A language and environment for statistical computing
Díaz-B CA, Otálora-Ardila A, Valdés-Cardona MC et al (2023) Bat functional traits associated with environmental, landscape, and conservation variables in neotropical dry forests. Front for Glob Change. https://doi.org/10.3389/ffgc.2023.1082427. 6:
Dolédec S, Chessel D, ter Braak CJF, Champely S (1996) Matching species traits to environmental variables: a new three-table ordination method. Environ Ecol Stat 3:143–166. https://doi.org/10.1007/BF02427859
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20. https://doi.org/10.18637/jss.v022.i04
Dray S, Choler P, Dolédec S et al (2014) Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology 95:14–21. https://doi.org/10.1890/13-0196.1
Etter A (1997) Sabanas. In: Chaves ME, Arango N (eds) Informe Nacional Sobre El Estado De La Biodiversidad en Colombia. Tomo I: Diversidad Biológica. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, pp 76–95
Fahrig L, Baudry J, Brotons L et al (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112. https://doi.org/10.1111/j.1461-0248.2010.01559.x
Falcão F, Dodonov P, Caselli CB et al (2021) Landscape structure shapes activity levels and composition of aerial insectivorous bats at different spatial scales. Biodivers Conserv 30:2545–2564. https://doi.org/10.1007/s10531-021-02210-x
Farneda FZ, Rocha R, López-Baucells A et al (2015) Trait-related responses to habitat fragmentation in amazonian bats. J Appl Ecol 52:1381–1391. https://doi.org/10.1111/1365-2664.12490
Farneda FZ, Rocha R, López-Baucells A et al (2018) Functional recovery of amazonian bat assemblages following secondary forest succession. Biol Conserv 218:192–199. https://doi.org/10.1016/j.biocon.2017.12.036
Giannini NP, Kalko EKV (2004) Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105:209–220. https://doi.org/10.1111/j.0030-1299.2004.12690.x
Gonçalves F, Fischer E, Dirzo R (2017) Forest conversion to cattle ranching differentially affects taxonomic and functional groups of neotropical bats. Biol Conserv 210:343e348. https://doi.org/10.1016/j.biocon.2017.04.021
Gonçalves-Souza T, Chaves LS, Boldorini GX et al (2023) Bringing light onto the Raunkiæran shortfall: a comprehensive review of traits used in functional animal ecology. Ecol Evol 13:e10016. https://doi.org/10.1002/ece3.10016
Grace J, José JS, Meir P et al (2006) Productivity and carbon fluxes of tropical savannas. J Biogeogr 33:387–400. https://doi.org/10.1111/j.1365-2699.2005.01448.x
Green SJ, Brookson CB, Hardy NA, Crowder LB (2022) Trait-based approaches to global change ecology: moving from description to prediction. Proc R Soc B: Biol Sci 289:20220071. https://doi.org/10.1098/rspb.2022.0071
Hesselbarth MHK, Sciaini M, With KA et al (2019) Landscapemetrics: an open-source R tool to calculate landscape metrics. Ecography 42:1648–1657. https://doi.org/10.1111/ecog.04617
Hill MO, Smith AJE (1976) Principal component analysis of taxonomic data with multi-state discrete characters. Taxon 25:249–255. https://doi.org/10.2307/1219449
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613
IDEAM (2015) Atlas climatológico de Colombia. atlas.ideam.gov.co/visorAtlasClimatologico.html. Accessed 19 Apr 2023
Jeliazkov A, Mijatovic D, Chantepie S et al (2020) A global database for metacommunity ecology, integrating species, traits, environment and space. Sci Data 7:6. https://doi.org/10.1038/s41597-019-0344-7
Kalko EKV, Handley CO, Handley D (1996) Organization, diversity, and long-term dynamics of a neotropical bat community. In: Cody M, Smallwood J (eds) Long-term studies in Vertebrate Communities. pp 503–553
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Kleyer M, Dray S, Bello F et al (2012) Assessing species and community functional responses to environmental gradients: which multivariate methods? J Veg Sci 23:805–821. https://doi.org/10.1111/j.1654-1103.2012.01402.x
Klingbeil BT, Willig MR (2009) Guild-specific responses of bats to landscape composition and configuration in fragmented amazonian rainforest. J Appl Ecol 46:203–213. https://doi.org/10.1111/j.1365-2664.2008.01594.x
Kunz TH, Braun de Torrez E, Bauer D et al (2011) Ecosystem services provided by bats. Trans N Y Acad Sci 1223:1–38. https://doi.org/10.1111/j.1749-6632.2011.06004.x
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
López-Arévalo HF, Liévano-Latorre LF, Montenegro Díaz OL (2021) El Papel De las pequeñas reservas en la conservación de mamíferos en Colombia. Caldasia 43:354–365
Marinello MM, Bernard E (2014) Wing morphology of neotropical bats: a quantitative and qualitative analysis with implications for habitat use. Can J Zool 92:141–147. https://doi.org/10.1139/cjz-2013-0127
Marques JT, Ramos Pereira MJ, Marques TA et al (2013) Optimizing sampling design to deal with mist-net avoidance in amazonian birds and bats. PLoS ONE 8:1–8. https://doi.org/10.1371/journal.pone.0074505
Marroquin C, Gerth T, Muñoz-Garcia A (2023) The influence of roost type and diet on energy expenditure in bats. Diversity 15:655. https://doi.org/10.3390/d15050655
McKechnie AE, Wolf BO (2019) The physiology of heat tolerance in small endotherms. Physiology 34:302–313. https://doi.org/10.1152/physiol.00011.2019
Melo FPL, Arroyo-Rodríguez V, Fahrig L et al (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:462–468. https://doi.org/10.1016/j.tree.2013.01.001
Meyer CFJ, Struebig MJ, Willig MR (2016) Responses of tropical bats to habitat fragmentation, logging and deforestation. In: Voigt C, Kingston T (eds) Bats in the Anthropocene: conservation of bats in a changing world. Springer, pp 63–105
Morales-Martínez DM, Rodríguez-Posada ME, Fernández-Rodríguez C et al (2018) Spatial variation of bat diversity between three floodplain-savanna ecosystems of the Colombian Llanos. Therya 9:1–9. https://doi.org/10.12933/therya-18-537
Newbold T, Hudson LN, Hill SLL et al (2016) Global patterns of terrestrial assemblage turnover within and among land uses. Ecography 39:1151–1163. https://doi.org/10.1111/ecog.01932
Núñez SF, López-Baucells A, Rocha R et al (2019) Echolocation and stratum preference: key trait correlates of vulnerability of insectivorous bats to tropical forest fragmentation. Front Ecol Evol 7:373. https://doi.org/10.3389/fevo.2019.00373
Otálora-Ardila A, López-Arévalo HF (2021) Effect of the matrix-edge-forest interior gradient on the phyllostomid bats assemblage in sub-andean forest fragments. Caldasia 43:274–285. https://doi.org/10.15446/caldasia.v43n2.85071
Palacio FX, Callaghan CT, Cardoso P et al (2022) A protocol for reproducible functional diversity analyses. Ecography 2022:e06287. https://doi.org/10.1111/ecog.06287
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412
Pasquini L, Fitzsimons J, Cowell S, Brandon K, Wescott G (2011) The establishment of large private nature reserves by conservation NGOs: key factors for successful implementation. Oryx 45:373–380. https://doi.org/10.1017/S0030605310000876
Pereira HM, Daily GC (2006) Modeling biodiversity dynamics in countryside landscapes. Ecology 87:1877–1885. https://doi.org/10.1890/0012-9658(2006)87[1877:MBDICL]2.0.CO;2
Piraquive-Bermúdez D, Behling H (2022) Holocene paleoecology in the neotropical savannas of Northern South America (Llanos of the Orinoquia ecoregion, Colombia and Venezuela): what do we know and on what should we focus in the future? Front Ecol Evol 10. https://doi.org/10.3389/fevo.2022.824873
Ramírez-Mejía AF, Urbina‐Cardona JN, Sánchez F (2020) Functional diversity of phyllostomid bats in an urban–rural landscape: a scale‐dependent analysis. Biotropica 52:1168–1182. https://doi.org/10.1111/btp.12816
Rex K, Michener R, Kunz TH, Voigt CC (2011) Vertical stratification of neotropical leaf-nosed bats (Chiroptera: Phyllostomidae) revealed by stable carbon isotopes. J Trop Ecol 27:211–222. https://doi.org/10.1017/S0266467411000022
Rojas D, Warsi OM, Dávalos LM (2016) Bats (Chiroptera: Noctilionoidea) challenge a recent origin of extant neotropical diversity. Syst Biol 65:432–448. https://doi.org/10.1093/sysbio/syw011
Romero-Ruiz M, Etter A, Sarmiento A, Tansey K (2010) Spatial and temporal variability of fires in relation to ecosystems, land tenure and rainfall in savannas of Northern South America. Glob Change Biol 16:2013–2023. https://doi.org/10.1111/j.1365-2486.2009.02081.x
Romero-Ruiz MH, Flantua SGA, Tansey K, Berrio JC (2012) Landscape transformations in savannas of Northern South America: land use/cover changes since 1987 in the Llanos Orientales of Colombia. Appl Geogr 32:766–776. https://doi.org/10.1016/j.apgeog.2011.08.010
Semper-Pascual A, Bischof R, Milleret C et al (2022) Occupancy winners in tropical protected forests: a pantropical analysis. Proc R Soc B 289:20220457. https://doi.org/10.1098/rspb.2022.0457
Sikes RS (2016) Guidelines of the American Society of mammalogists for the use of wild mammals in research. J Mammal 97:663–688. https://doi.org/10.1093/jmammal/gyw078
Straube FC, Bianconi GV (2002) Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chirop Neotrop 8:150–152
Suárez-Castro AF, Ramírez-Chaves HE, Noguera-Urbano EA et al (2021) Vacíos de información espacial sobre la riqueza de mamíferos terrestres continentales de Colombia. Caldasia 43:247–260. https://doi.org/10.15446/caldasia.v43n2.85443
ter Braak CJF, Cormont A, Dray S (2012) Improved testing of species traits–environment relationships in the fourth-corner problem. Ecology 93:1525–1526. https://doi.org/10.1890/12-0126.1
ter Hofstede HM, Faure PA (2023) Predator–prey interactions between gleaning bats and katydids. Can J Zool 101:936–944. https://doi.org/10.1139/cjz-2023-0023
Velazco P, Lim BK (2014) A new species of broad-nosed bat Platyrrhinus Saussure, 1860 (Chiroptera: Phyllostomidae) from the Guianan Shield. Zootaxa 3796:175–193. https://doi.org/10.11646/zootaxa.3796.1.9
Villalobos-Chaves D, Santana SE (2022) Craniodental traits predict feeding performance and dietary hardness in a community of Neotropical free-tailed bats (Chiroptera: Molossidae). Funct Ecol 36:1690–1699. https://doi.org/10.1111/1365-2435.14063
Voss RS, Fleck DW, Strauss RE et al (2016) Roosting ecology of Amazonian bats: evidence for guild structure in hyperdiverse mammalian communities. Am Mus Novit 2016:1–43. https://doi.org/10.1206/3870.1
Weiss KCB, Ray CA (2019) Unifying functional trait approaches to understand the assemblage of ecological communities: synthesizing taxonomic divides. Ecography 42:2012–2020. https://doi.org/10.1111/ecog.04387
Williams BA, Watson JEM, Beyer HL et al (2022) Global drivers of change across tropical savannah ecosystems and insights into their management and conservation. Biol Conserv 276:109786. https://doi.org/10.1016/j.biocon.2022.109786
Wordley CFR, Sankaran M, Mudappa D, Altringham JD (2017) Bats in the Ghats: agricultural intensification reduces functional diversity and increases trait filtering in a biodiversity hotspot in India. Biol Conserv 210:48–55. https://doi.org/10.1016/j.biocon.2017.03.026
Zou W, Liang H, Wu P et al (2022) Correlated evolution of wing morphology and echolocation calls in bats. Front Ecol Evol 10. https://doi.org/10.3389/fevo.2022.1031548
Acknowledgements
We thank the Instituto Alexander von Humboldt, Grupo en Conservación y Manejo de Vida Silvestre, and Instituto de Ciencias Naturales at the Universidad Nacional de Colombia (Sede Bogotá) for support of equipment and field supplies. The following people helped with fieldwork: Jessica Blanco, Yuri Chantre, Andrés Julián Lozano, Jonatan Caro Montoya, Daniela Amórtegui, Sara Acosta Morales, Daniela Reyes, and María Fernanda Monguí. We thank Romeo Saldaña-Vásquez and one anonymous reviewer for insightful comments. We are grateful to Stéphane Dray for insights concerning the “fourthcorner” and “msr” R-functions, Hernán Serrano for the help with cartographic analysis, Camila Valdés-Cardona with the R package “landscapemetrics”, Mary Choperena with the ethical endorsement, Fundación Natura Colombia with the receipt and transfer of the grant, and to landowners of the private reserves and farmlands for logistic support.
Funding
AOA and FZF were supported by a post-doctoral fellowship (MinCiencias call No. 848 of 2019 and “Convocatoria de Estancias Posdoctorales en la Universidad Nacional de Colombia - Sede Medellín 2021”, respectively). Actually, FZF is a “Bolsista CAPES/BRASIL”. Project funding was provided by the “Neotropical Grassland Conservancy” and “The Rufford Foundation (Project 35308-1)” to AOA.
Author information
Authors and Affiliations
Contributions
A.O-A. and F.Z.F. designed research; F.Z.F. and A.O-A. performed the landscape/statistical analyses and F.Z.F. led the writing of the manuscript, supported mainly by A.O-A. and C.F.J.M.; A.O-A. and F.Z.F. collected data; A.O-A. and F.Z.F. carried out the field expeditions, funding acquisition and project administration. C.G-P. gave support from Instituto Alexander von Humboldt and H.F.L-A. and J.P. from Colombia National University as project supervisors. All authors contributed critically to the drafts, gave final approval for publication, and do not have any conflict of interest to declare.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Communicated by Daniel Hending.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Otálora-Ardila, A., Farneda, F.Z., Meyer, C.F.J. et al. Trait-mediated filtering predicts phyllostomid bat responses to habitat disturbance in the Orinoco Llanos. Biodivers Conserv 33, 1285–1302 (2024). https://doi.org/10.1007/s10531-024-02792-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-024-02792-2