Abstract
The maintenance, restoration, and improvement of habitat structure are critical for biodiversity conservation. Under this context, studies assessing habitat connectivity become essential, especially those focused on anthropized regions holding high species richness. We calculated the habitat connectivity of four species of insectivorous bats with different dispersal capacity and habitat preferences in a highly anthropized region in central Mexico, Idionycteris phyllotis and Myotis thysanodes, with a high dispersal capacity and forest-dependency, and Eptesicus fuscus with a low dispersal capacity, and Tadarida brasiliensis with a high dispersal capacity, as the more tolerant bat species to anthropogenic disturbance. We developed niche-based species distribution models to identify suitable habitat patches for each species. We then assessed habitat connectivity and the importance of suitable habitat patches for maintaining connectivity using a graph theory approach. Our results showed that forest dependency was most important than dispersal capacity for connectivity. We also found that the Iztaccíhuatl-Popocatépetl mountain, a National Park comprising 4.2% of natural vegetation in the study area, was the most critical patch for maintaining connectivity for most of the study species. Our study demonstrates the importance of conserving the remnants of natural vegetation for maintaining habitat connectivity within a fragmented landscape and demonstrates the importance of conserving protected areas as well as other remnants of vegetation for the maintenance of habitat connectivity within a fragmented landscape.
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References
Aldridge H, Rautenbach I (1987) Morphology, echolocation and resource partitioning in insectivorous bats. J Anim Ecol 763:778. https://doi.org/10.2307/4947
Amorim FJ, Beja P, Rebelo H (2018) Following the water? Landscape-scale temporal changes in bat spatial distribution about Mediterranean summer drought. Ecol Evol 811:5801–5814. https://doi.org/10.1002/ece3.4119
Anderson R, Lew D, Peterson A (2003) Evaluating predictive models of species’ distributions: criteria for selecting optimal models. Ecol Model 162:3211–232. https://doi.org/10.1016/S0304-3800(02)00349-6
Arumoogum N, Schoeman MC, Ramdhani S (2019) The relative influence of abiotic and biotic factors on suitable habitat of Old World fruit bats under current and future climate scenarios. Mamm Biol 981:188–200. https://doi.org/10.1016/j.mambio.2019.09.006
Avila-Flores R, Fenton M (2005) Use of spatial features by foraging insectivorous bats in a large urban landscape. J Mammal 866:1193–1204. https://doi.org/10.1644/04-MAMM-A-085R1.1
Ayram C, Mendoza ME, Etter A, Salicrup DRP (2017) Anthropogenic impact on habitat connectivity: A multidimensional human footprint index evaluated in a highly biodiverse landscape of Mexico. Ecol Indic 72:895–909. https://doi.org/10.1016/j.ecolind.2016.09.007
Barnhart PR, Gillam EH (2014) The impact of sampling method on maximum entropy species distribution modeling for bats. Acta Chiropt 161:241–248. https://doi.org/10.3161/150811014X683435
Best TL, Geluso KN (2003) Summer foraging range of Mexican free-tailed bats (Tadarida brasiliensis mexicana) from Carlsbad Cavern, New Mexico. Southwest Nat 48:590–596. https://doi.org/10.1894/0038-4909(2003)048%3c0590:SFROMF%3e2.0.CO;2
Bogdanowicz W, Fenton MB, Daleszczyk K (1999) The relationships between echolocation calls, morphology and diet in insectivorous bats. J Zool 2473:381–393. https://doi.org/10.1111/j.1469-7998.1999.tb01001.x
Boyles G, Cryan P, McCracken G, Kunz T (2011) Economic importance of bats in agriculture. Science 332:602541–42. https://doi.org/10.1126/science.1201366
Boria R, Olson L, Goodman S, Anderson R (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Model 275:73–77. https://doi.org/10.1016/j.ecolmodel.2013.12.012
Briers R (2002) Incorporating connectivity into reserve selection procedures. Biol Conserv 103:177–83. https://doi.org/10.1016/S0006-3207(01)00123-9
Bunkley JP, McClure CJ, Kleist NJ, Francis CD, Barber JR (2015) Anthropogenic noise alters bat activity levels and echolocation calls. Glob Ecol Conserv 3:62–71. https://doi.org/10.1111/j.1469-7998.1999.tb01001.x
Burles DW, Brigham RM, Ring RA, Reimchen TE (2009) Influence of weather on two insectivorous bats in a temperate Pacific Northwest rainforest. Can J Zool 872:132–138. https://doi.org/10.1139/Z08-146
Cobos ME, Peterson AT, Barve N, Osorio-Olvera L (2019) kuenm: an R package for detailed development of ecological niche models using Maxent. PeerJ 7:e6281. https://doi.org/10.7717/peerj.6281
Collevatti RG, Vitorino LC, Vieira TB, Oprea M, Telles MP (2020) Landscape changes decrease genetic diversity in the Pallas’ long-tongued bat. Perspect Ecol Conserv 183:169–177. https://doi.org/10.1016/j.pecon.2020.06.006
Comisión Nacional de Áreas Naturales Protegidas (CONANP) – Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT) (2012) Manual de Organización específica de la Dirección General del Centro y Eje Noevolcánico pp 52 p
Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) (1998) 'Curvas de nivel para la República Mexicana'. Escala 1:250000. Extraído del Modelo Digital del Terreno. Instituto Nacional de Estadística, Geografía e Informática (INEGI). México. http://www.conabio.gob.mx/informacion/gis/. Accessed 04 November 2020
CONAPO (2010) Delimitación de las zonas metropolitanas de México. http://www.conapo.gob.mx/en/CONAPO/ Zonas_metropolitanas_2010. Accessed 04 November 2020
CONANP (2017) Areas Naturales Protegidas Federales de la República Mexicana, Comisión Nacional de Áreas Protegidas, México
Cornejo-Latorre C, Rojas-Martínez A, Aguilar-López M, Juárez-Castillo L (2011) Abundancia estacional de los murciélagos herbívoros y disponibilidad de los recursos quiropterófilos en dos tipos de vegetación de la Reserva de la Biosfera Barranca de Metztitlán, Hidalgo, México. Therya 2:2169–182. https://doi.org/10.12933/therya-11-38
de Sousa ML, Awade M, Jaffé R, Costa WF, Trevelin LC, Borges RC, Giannini TC (2021) Combining connectivity and species distribution modeling to define conservation and restoration priorities for multiple species: a case study in the Eastern Amazon. Biol Conserv 257:109–148. https://doi.org/10.1016/j.biocon.2021.109148
Dormann C, McPherson J, Araújo M, Bivand R, Bolliger J, Carl G, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 305:609–628. https://doi.org/10.1111/j.2007.0906-7590.05171.x
Erickson JL, West SD (2002) The influence of regional climate and nightly weather conditions on activity patterns of insectivorous bats. Acta Chiropt 41:17–24. https://doi.org/10.3161/001.004.0103
Evelyn M, Stiles D, Young R (2004) Conservation of bats in suburban landscapes: roost selection by Myotis yumanensis in a residential area in California. Biol Conserv 115:3463–473. https://doi.org/10.1016/S0006-3207(03)00163-0
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 341:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Fenton MB, Griffin DR (1997) High-altitude pursuit of insects by echolocating bats. J Mammal 781:247–250. https://doi.org/10.2307/1382658
Ferrusquía-Villafranca I (2007) Ensayo sobre la caracterización y significación biológica. In: Luna I, Morrone JJ, Espinoza D (eds) Biodiversidad de la Faja Volcánica Transmexicana, 1st edn. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, Universidad Nacional Autónoma de México, México, pp 7–23
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 3712:4302–4315. https://doi.org/10.1002/joc.5086
Findley JS, Studier EH, Wilson DE (1972) Morphologic properties of bat wings. J Mammal 533:429–444. https://doi.org/10.2307/1379035
Fischer J, Lindenmayer D (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. https://doi.org/10.1111/j.1466-8238.2007.00287.x
Flores-Abreu I, Trejo-Salazar R, Sánchez-Reyes L, Good S, Magallón S, García-Mendoza A, Eguiarte L (2019) Tempo and mode in coevolution of Agave sensu lato (Agavoideae, Asparagaceae) and its bat pollinators, Glossophaginae (Phyllostomidae). Mol Phylogenet Evol 133:176–188. https://doi.org/10.1016/j.ympev.2019.01.004
Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Helkowski JH (2005) Global consequences of land use. Science 3095734:570–574. https://doi.org/10.1126/science.1111772
Fuller T, Munguía M, Mayfield M, Sánchez-Cordero V, Sarkar S (2006) Incorporating connectivity into conservation planning: a multi-criteria case study from central Mexico. Biol Conserv 1332:131–142. https://doi.org/10.1016/j.biocon.2006.04.040
Gámez N, Escalante T, Rodríguez G, Linaje M, Morrone JJ (2012) Caracterización biogeográfica de la Faja Volcánica Transmexicana y análisis de los patrones de distribución de su mastofauna. Rev Mex Biodivers 831:258–272. http://ref.scielo.org/xqqnz4
GBIF.org (2020a) GBIF Occurrence Download. https://doi.org/10.15468/dl.24tapu. Accessed 5 Nov 2020
GBIF.org (2020b) GBIF Occurrence Download. https://doi.org/10.15468/dl.dujmmc. Accessed 5 Nov 2020
GBIF.org (2020c) GBIF Occurrence Download. https://doi.org/10.15468/dl.nfmzgn. Accessed 5 Nov 2022
GBIF.org (2020d) GBIF Occurrence Download. https://doi.org/10.15468/dl.a4mrhr. Accessed 5 Nov 2020
Gebhardt S, Wehrmann T, Ruiz MAM, Maeda P, Bishop J, Schramm M, Schmidt M (2014) MAD-MEX: Automatic wall-to-wall land cover monitoring for the Mexican REDD-MRV program using all Landsat data. Remote Sens 65:3923–3943. https://doi.org/10.3390/rs6053923
Gehrt SD, Chelsvig JE (2004) Species-specific patterns of bat activity in an urban landscape. Ecol Appl 142:625–635. https://doi.org/10.1890/03-5013
Geiser F, Brigham RM (2000) Torpor, thermal biology, and energetics in Australian long-eared bats (Nyctophilus). J Comp Physiol B 1702:153–162. https://doi.org/10.1007/s003600050270
Godínez-Gómez O, Correa-Ayram C (2020) Makurhini: Analyzing landscape connectivity. Zenodo
González-Fernández A, Manjarrez J, García-Vázquez U, D’Addario M, Sunny A (2018) Present and future ecological niche modeling of garter snake species from the Trans-Mexican Volcanic Belt. PeerJ 6:e-4618. https://doi.org/10.7717/peerj.4618
Guisan A, Zimmermann N (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186. https://doi.org/10.1016/S0304-3800(00)00354-9
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:9993–1009. https://doi.org/10.1111/j.1461-0248.2005.00792.x
Hanski I (1998) Home ranges and habitat use in the declining flying squirrel Pteromys volans in managed forests. Wildlife Biol 4:133–46. https://doi.org/10.2981/wlb.1998.013
Heller N, Zavaleta E (2009) Biodiversity management in the face of climate change: a review of 22 years of recommendations. Biol Conserv 142:114–32. https://doi.org/10.1016/j.biocon.2008.10.006
Hernández-Montero J, Rojas-Soto O, Saldaña-Vázquez R (2011) Consumo y dispersión de semillas de Solanum schlechtendalianum (Solanaceae) por el murciélago frugívoro Sturnira ludovici (Phyllostomidae). Chiropt Neotrop 17:21017–1021
Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodiv Conserv 131:207–251. https://doi.org/10.1023/B:BIOC.0000004319.91643.9e
Hope PR, Jones G (2012) Warming up for dinner: torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry. J Comp Physiol B 1824:569–578. https://doi.org/10.1007/s00360-011-0631-x
Huang JCC, Rustiati EL, Nusalawo M, Kingston T (2019) Echolocation and roosting ecology determine sensitivity of forest-dependent bats to coffee agriculture. Biotropica 515:757–768. https://doi.org/10.1111/btp.12694
INEGI (2015) Censos y Conteos de Población y Vivienda. https://www.inegi.org.mx/programas/intercensal/2015/#Publicaciones. Accessed 20 November 2020
Jaberg C, Guisan A (2001) Modelling the distribution of bats in relation to landscape structure in a temperate mountain environment. J Appl Ecol 1169:1181. https://www.jstor.org/stable/827290
Jantzen MK, Fenton MB (2013) The depth of edge influence among insectivorous bats at forest–field interfaces. Can J Zool 915:287–292. https://doi.org/10.1139/cjz-2012-0282
Jiménez-Valverde A, Lobo J (2007) Threshold criteria for conversion of probability of species presence to either–or presence–absence. Acta Oecol 31:3361–369. https://doi.org/10.1016/j.actao.2007.02.001
Komar E, Dechmann DK, Fasel NJ, Zegarek M, Ruczyński I (2020) Food restriction delays seasonal sexual maturation but does not increase torpor use in male bats. J Exp Biol 2238:jeb214825. https://doi.org/10.1242/jeb.214825
Li H, Wilkins KT (2015) Selection of building roosts by Mexican free-tailed bats (Tadarida brasiliensis) in an urban area. Acta Chiropt 172:321–330. https://doi.org/10.3161/15081109ACC2015.17.2.007
Limpens HJGA, Kapteyn K (1991) Bats, their behaviour and linear landscape elements. Myotis 29:39–48
Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:4778–789. https://doi.org/10.1111/jbi.12058
Luo J, Siemers BM, Koselj K (2015) How anthropogenic noise affects foraging. Glob Change Biol 219:3278–3289. https://doi.org/10.1111/gcb.12997
Menzel MA, Carter TC, Jablonowski LR, Mitchell BL, Menzel JM, Chapman BR (2001) Home range size and habitat use of big brown bats (Eptesicus fuscus) in a maternity colony located on a rural-urban interface in the southeast. J Elisha Mitchell Sci Soc 36–45. https://www.jstor.org/stable/24335366.
Milne D, Burwell C, Pavey C (2016) Dietary composition of insectivorous bats of the Top End of Australia. Aust Mammal 38:2213–220. https://doi.org/10.1071/AM15044
Miner K, Brown P, Berry B, Brown-Buescher C, Kisner A, Remington S, Underwood L (1996) Habitat use by Myotis evotis and M. thysanodes in a southern California pine-oak woodland. Bat Res News 37:141
Minor E, Urban D (2008) A graph-theory framework for evaluating landscape connectivity and conservation planning. Conserv Biol 22:2297–307. https://doi.org/10.1111/j.1523-1739.2007.00871.x
Morris AD, Miller DA, Kalcounis-Rueppell MC (2010) Use of forest edges by bats in a managed pine forest landscape. J Wildl Manag 741:26–34. https://doi.org/10.2193/2008-471
Morzillo A, Ferrari J, Liu J (2011) An integration of habitat evaluation, individual based modeling, and graph theory for a potential black bear population recovery in southeastern Texas, USA. Landsc Ecol 26:69–81. https://doi.org/10.1007/s10980-010-9536-4
Nabe-Nielsen J, Sibly RM, Forchhammer MC, Forbes VE, Topping CJ (2010) The effects of landscape modifications on the long-term persistence of animal populations. PloS one 51:e8932. https://doi.org/10.1371/journal.pone.0008932
Neuweiler G (1984) Foraging, echolocation and audition in bats. Sci Nat 71:9446–455. https://doi.org/10.1007/BF00455897
O’Brien D, Manseau M, Fall A, Fortin M (2006) Testing the importance of spatial configuration of winter habitat for woodland caribou: an application of graph theory. Biol Conserv 130:170–83. https://doi.org/10.1016/j.biocon.2005.12.014
O’farrell MJ, Studier EH (1970) Fall metabolism in relation to ambient temperatures in three species of Myotis. Comp Biochem Physiol 353:697–703
Olson DM et al (2001) Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 5111:933–938. https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2
Osorio-Olvera L, Lira-Noriega A, Soberón J, Townsend Peterson A, Falconi M, Contreras-Díaz RG, Martínez-Meyer E, Barve V, Barve N (2020) Ntbox: an R package with graphical user interface for modeling and evaluating multidimensional ecological niches. Methods Ecol Evol 1110:1199–1206. https://doi.org/10.1111/2041-210X.13452
Pascual-Hortal L, Saura S (2006) Comparison and development of new graph-based landscape connectivity indices: towards the priorization of habitat patches and corridors for conservation. Landsc Ecol 217:959–967. https://doi.org/10.1007/s10980-006-0013-z
Pascual-Hortal L, Saura S (2008) Integrating landscape connectivity in broad-scale forest planning through a new graph-based habitat availability methodology: application to capercaillie (Tetrao urogallus) in Catalonia (NE Spain). Eur J for Res 1271:23–31. https://doi.org/10.1007/s10342-006-0165-z
Peterson A, Vieglais D (2001) Predicting species invasions using ecological niche modeling: new approaches from bioinformatics attack a pressing problem: A new approach to ecological niche modeling, based on new tools drawn from biodiversity informatics, is applied to the challenge of predicting potential species’ invasions. BioScience 51:5363–371. https://doi.org/10.1641/0006-3568(2001)051[0363:PSIUEN]2.0.CO;2
Peterson A, Papeş M, Soberón J (2008) Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecol Model 213:163–72. https://doi.org/10.1016/j.ecolmodel.2007.11.008
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 1903–4:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pereira M, Segurado P, Neves N (2011) Using spatial network structure in landscape management and planning: a case study with pond turtles. Landsc Urban Plan 100(1–2):67–76. https://doi.org/10.1016/j.landurbplan.2010.11.009
Razgour O, Hanmer J, Jones G (2011) Using multi-scale modelling to predict habitat suitability for species of conservation concern: the grey long-eared bat as a case study. Biol Conserv 144:122922–2930. https://doi.org/10.1016/j.biocon.2011.08.010
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (Version 4. 0. 3) URL https://www.R-project.org/
Richard Y, Armstrong D (2010) The importance of integrating landscape ecology in habitat models: isolation-driven occurrence of north island robins in a fragmented landscape. Landsc Ecol 25:1363–1374. https://doi.org/10.1007/s10980-010-9488-8
Ripperger SP, Tschapka M, Kalko EK, Rodriguez-Herrera B, Mayer F (2013) Life in a mosaic landscape: anthropogenic habitat fragmentation affects genetic population structure in a frugivorous bat species. Conserv Genet 145:925–934. https://doi.org/10.1007/s10592-012-0434-y
Sarukhán J (2017) Capital natural de México: síntesis (actualizada a 2017): evaluación del conocimiento y tendencias de cambio, perspectivas de sustentabilidad, capacidad humanas e institucionales. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad.
Saura S, Pascual-Hortal L (2007) A new habitat availability index to integrate connectivity in landscape conservation planning: comparison with existing indices and application to a case study. Landsc 832–3:91–103. https://doi.org/10.1016/j.landurbplan.2007.03.005
Saura S, Rubio L (2010) A common currency for the different ways in which patches and links can contribute to habitat availability and connectivity in the landscape. ECOGEG 333:523–537. https://doi.org/10.1111/j.1600-0587.2009.05760.x
Saura S, Torné J (2009) Conefor Sensinode 2.2: a software package for quantifying the importance of habitat patches for landscape connectivity. Environ Model Softw 241:135–139. https://doi.org/10.1016/j.envsoft.2008.05.005
Saura S, Torné J (2012) Conefor 2.6 User Manual. Universidad Politécnica de Madrid, España
Schimpp SA, Li H, Kalcounis-Rueppell MC (2018) Determining species specific nightly bat activity in sites with varying urban intensity. Urban Ecosyst 213:541–550. https://doi.org/10.1007/s11252-018-0737-y
Schnitzler HU, Kalko EK (2001) Echolocation by insect-eating bats: we define four distinct functional groups of bats and find differences in signal structure that correlate with the typical echolocation tasks faced by each group. J Biosci 517:557–569. https://doi.org/10.1641/0006-3568(2001)051[0557:EBIEB]2.0.CO;2
Semarnat. 2016. Informe de la Situación del Medio Ambiente en México. Compendio de Estadísticas Ambientales. Indicadores Clave, de Desempeño Ambiental y de Crecimiento Verde. Edición 2015. Semarnat. México
Smeraldo S, Bosso L, Salinas-Ramos V, Ancillotto L, Sánchez-Cordero V, Gazaryan S, Russo D (2021) Generalists yet different: Distributional responses to climate change may vary in opportunistic bat species sharing similar ecological traits. Mamm Rev 51:4571–584. https://doi.org/10.1111/mam.12247
Soberón J, Peterson AT (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas. https://doi.org/10.17161/bi.v2i0.4
SolveskY BG, Chambers CL (2009) Roosts of Allen’s lappet-browed bat in northern Arizona. J Wildl Manag 735:677–682. https://doi.org/10.2193/2008-333
Soberón J, Osorio-Olvera L, Peterson T (2017) Diferencias conceptuales entre modelación de nichos y modelación de áreas de distribución. Rev Mex Biodivers 88:2437–441. https://doi.org/10.1016/j.rmb.2017.03.011
Sunny A, Monroy-Vilchis O, Zarco-González M, Mendoza-Martínez G, Martínez-Gómez D (2015) Genetic diversity and genetic structure of an endemic Mexican Dusky Rattlesnake (Crotalus triseriatus) in a highly modified agricultural landscape: implications for conservation. Genetica 143:705–716
Teixeira TS, Weber MM, Dias D, Lorini ML, Esberard CEL, Novaes RL, Cerqueira R, Vale MM (2014) Combining environmental suitability and habitat connectivity to map rare or Data Deficient species in the Tropics. J Nat Conserv 22:384–390. https://doi.org/10.1016/j.jnc.2014.04.001
Tournant P, Afonso E, Roué S, Giraudoux P, Foltête JC (2013) Evaluating the effect of habitat connectivity on the distribution of lesser horseshoe bat maternity roosts using landscape graphs. Biol Conserv 164:39–49. https://doi.org/10.1016/j.biocon.2013.04.013
Urban D, Keitt T (2001) Landscape connectivity: a graph-theoretic perspective. Ecology 825:1205–1218. https://doi.org/10.1890/0012-9658(2001)082[1205:LCAGTP]2.0.CO;2
Urban L, Minor E, Treml E, Schick R (2009) Graph models of habitat mosaics. Ecol Lett 12:3260–273. https://doi.org/10.1111/j.1461-0248.2008.01271.x
Velázquez A, Romero F, Rangel-Cordero H, Heil G (2003) Effects of habitat fragmentation on the mammalian assemblage at the Iztaccíhuatl and Popocatépetl Volcanoes, Mexico. In: Heil GW, Bobbink R, Trigo Boix N (eds) Ecology and Man in Mexico’s Central Volcanoes Area. Springer, Dordrecht 103–123 https://doi.org/10.1007/978-94-007-0969-0_5
Vidal-Zepeda R (1990) Precipitación: Clima, Hoja IV.4.6, scale 1:4000000. Atlas Nacional de México. Instituto de Geografía, Universidad Nacional Autónoma de México, México
Warren D, Wright A, Seifert S, Shaffer H (2014) Incorporating model complexity and spatial sampling bias into ecological niche models of climate change risks faced by 90 C alifornia vertebrate species of concern. Divers Distrib 20:3334–343. https://doi.org/10.1111/ddi.12160
Weber MM, Grelle C (2012) Does environmental suitability explain the relative abundance of the tailed tailless bat, Anoura caudifer. Nat Conserv 10:221–227. https://doi.org/10.4322/natcon.2012.035
Zanette L, Doyle P, Trémont SM (2000) Food shortage in small fragments: evidence from an area-sensitive passerine. Ecology 816:1654–1666. https://doi.org/10.1890/0012-9658(2000)081[1654:FSISFE]2.0.CO;2
Acknowledgements
The authors thank the support (infrastructure and administration team) given by the Centro Tlaxcala de Biología de la Conducta (CTBC-Uatx) and the grant award to EVR by the Consejo Nacional de Ciencia y Tecnología (CONACyT) (grant number 823321) for the doctoral studies. This work was supported by the project “Proyecto apoyado por el Fondo Sectorial de Investigación Secretaría de Relaciones Exteriores (SRE)-Consejo Nacional de Ciencia y Tecnología (CONACyT) (No. 286794) dentro del proyecto Análisis de la conectividad funcional entre los parques nacionales La Malinche e Iztaccíhuatl-Popocatépetl e identificación de áreas prioritarias para la conservación”. Angela thanks CONACyT for her postdoctoral research grant for the project: “Colecciones IBUNAM en movimiento: descubrir, estudiar y conservar la biodiversidad en el Antropoceno”.
Funding
This work was supported by project “Proyecto apoyado por el Fondo Sectorial de Investigación Secretaría de Relaciones Exteriores (SRE)-Consejo Nacional de Ciencia y Tecnología (CONACyT) (No. 286794) dentro del proyecto Análisis de la conectividad funcional entre los parques nacionales La Malinche e Iztaccíhuatl-Popocatépetl e identificación de áreas prioritarias para la conservación”.
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JAB and EVR conceived the idea. EVR gathered data and performed the models. ACR assessed and reviewed the models. All authors contributed to the writing of the final version of the manuscript.
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Vázquez-Rueda, E., Cuervo-Robayo, A.P. & Ayala-Berdon, J. Forest dependency could be more important than dispersal capacity for habitat connectivity of four species of insectivorous bats inhabiting a highly anthropized region in central Mexico. Mamm Res 68, 561–573 (2023). https://doi.org/10.1007/s13364-023-00707-0
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DOI: https://doi.org/10.1007/s13364-023-00707-0