Abstract
Anthropogenic landscape changes resulting in habitat degradation, loss and fragmentation might decrease connectivity and effective sizes of wild populations, threatening local biodiversity. Assumed large distributions of both species and habitats have probably discouraged studies correlating altered landscapes’ structure and composition to patterns of genetic diversity in the Neotropics. Yet, considering the increasingly high rates of deforestation and habitat conversion in Amazonia, investigating local and regional-scale effects of habitat conversion on Amazonian mammals is of paramount importance. Here, we use widespread, non-threatened, phyllostomid bats to understand how current forest dynamics are influencing genetic diversity patterns and functional connectivity of eastern Amazonian volant mammals. Four frugivorous species, Carollia perspicillata, Rhinophylla pumilio, Dermanura gnoma and Artibeus obscurus, were sampled across a heterogeneously fragmented region. Twelve more or less isolated rainforest remnants surrounded by urban areas, pastures, crops, secondary forests and other land uses comprise the studied landscapes, and are compared using a landscape genetics approach applied to mitochondrial DNA loci. Here, we report species-specific consequences of habitat fragmentation. Although the overall levels of genetic diversity were high, our data show that (i) population structure is heterogeneous across the altered landscapes; (ii) landscapes with higher habitat availability harbour populations with higher genetic diversity; and (iii) the populations assessed might be demographically declining.
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References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
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
Barquez R, Perez S, Miller B, Diaz M (2015) Carollia perspicillata. In: IUCN Red List of Threatened Species 2015: e.T3905A22133716. https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T3905A22133716.en
Benitez-Lopez A, Santini L, Schipper AM et al (2019) Intact but empty forests? Patterns of hunting-induced mammal defaunation in the tropics. PLoS Biol 17:e3000247. https://doi.org/10.1371/journal.pbio.3000247
Carvalho FMV, De Marco P, Ferreira LG (2009) The Cerrado into-pieces: habitat fragmentation as a function of landscape use in the savannas of central Brazil. Biol Conserv 142:1392–1403. https://doi.org/10.1016/j.biocon.2009.01.031
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
Cleary KA, Waits LP, Finegan B (2017) Comparative landscape genetics of two frugivorous bats in a biological corridor undergoing agricultural intensification. Mol Ecol 26:4603–4617. https://doi.org/10.1111/mec.14230
Cloutier D, Thomas DW (1992) Carollia perspicillata. Mamm Species 417:1–9. https://doi.org/10.2307/3504157
Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205:19–31. https://doi.org/10.1016/j.mbs.2006.09.015
Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinf 9:539. https://doi.org/10.1186/1471-2105-9-539
Costa WF, Ribeiro M, Saraiva AM, Imperatriz-Fonseca VL, Giannini TC (2018) Bat diversity in Carajás National Forest (Eastern Amazon) and potential impacts on ecosystem services under climate change. Biol Conserv 218:200–210. https://doi.org/10.1016/j.biocon.2017.12.034
Coutinho AC, Almeida C, Venturieri A, Esquerdo JCDM, Silva M (2013) Uso e cobertura da terra nas áreas desflorestadas da Amazônia Legal: TerraClass 2008. Embrapa Informática Agropecuária-Livro científico (ALICE), Brasília
Cushman SA, Shirk A, Landguth EL (2012) Separating the effects of habitat area, fragmentation and matrix resistance on genetic differentiation in complex landscapes. Landsc Ecol 27:369–380. https://doi.org/10.1007/s10980-011-9693-0
da Silva J, Cardoso M, Rylands AB (2005) The fate of the Amazonian areas of endemism. Conserv Biol 19:689–694. https://doi.org/10.1111/j.1523-1739.2005.00705.x
de Almeida AS, Stone TA, ICG V, Davidson EA (2010) Nonfrontier deforestation in the eastern Amazon. Earth Interact 14:1–15. https://doi.org/10.1175/2009EI290.1
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192. https://doi.org/10.1093/molbev/msi103
Farneda FZ, Rocha R, López-Baucells A, Groenenberg M, Silva I, Palmeirim JM, Bobrowiec PED, Meyer CFJ (2015) Trait-related responses to habitat fragmentation in Amazonian bats. J Appl Ecol 52:1381–1391. https://doi.org/10.1111/1365-2664.12490
Fearnside PM (2015) Environment: deforestation soars in the Amazon. Nature 521:423. https://doi.org/10.1038/521423b
Ferreira WAS, Borges BdN, Rodrigues-Antunes S, Andrade AFG, Aguiar GFS, Silva-Junior JS, Marques-Aguiar SA, Harada ML (2014) Phylogeography of the dark fruit-eating bat Artibeus obscurus in the Brazilian Amazon. J Hered 105:48–59. https://doi.org/10.1093/jhered/est066
Flather CH, Hayward GD, Beissinger SR, Stephens PA (2011) Minimum viable populations: is there a ‘magic number’ for conservation practitioners? Trends Ecol Evol 26:307–316. https://doi.org/10.1016/j.tree.2011.03.001
Haynes MA, Lee TE Jr (2004) Artibeus obscurus. Mamm Species 752:1–5. https://doi.org/10.1644/752
Henry M, Kalko EKV (2007) Foraging strategy and breeding constraints of Rhinophylla pumilio (Phyllostomidae) in the Amazon lowlands. J Mammal 88:81–93. https://doi.org/10.1644/06-MAMM-A-001R1.1
Hernández-Palma A, Stouffer PC (2018) Matrix and area effects on the nutritional condition of understory birds in Amazonian rainforest fragments. Perspect Ecol Conserv 16:139–145. https://doi.org/10.1016/j.pecon.2018.06.003
Ho SYW, Shapiro B (2011) Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour 11:423–434. https://doi.org/10.1111/j.1755-0998.2011.02988.x
Hua P, Zhang L, Guo T, Flanders J, Zhang S (2013) Dispersal, mating events and fine-scale genetic structure in the lesser flat-headed bats. PLoS One 8:e54428. https://doi.org/10.1371/journal.pone.0054428
Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064. https://doi.org/10.1139/Z07-095
Klingbeil B, Willig M (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.1365-2664.2007.0
Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191. https://doi.org/10.1111/j.1365-294X.2010.04808.x
Legendre P, Fortin M, Borcard D (2015) Should the Mantel test be used in spatial analysis? Methods Ecol Evol 6:1239–1247. https://doi.org/10.1111/2041-210X.12425
Leiva-González EM, Navarrete-Gutiérrez D, Ruiz-Montoya L, Santos-Moreno A, Kraker-Castañeda C, García-Bautista M (2019) Analysis of the contribution of landscape attributes on the genetic diversity of Artibeus jamaicensis Leach, 1821. Mammal Res 64:223–233. https://doi.org/10.1007/s13364-018-0403-z
Lino A, Fonseca C, Rojas D, Fischer E, Ramos Pereira MJ (2019) A meta-analysis of the effects of habitat loss and fragmentation on genetic diversity in mammals. Mamm Biol 94:69–76. https://doi.org/10.1016/j.mambio.2018.09.006
McGarigal K, Cushman SA, Neel MC, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. Univ Massachusettes, Amherst
Mello MAR, 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
Metzger JP, Martensen AC, Dixo M, Bernacci LC, Ribeiro MC, Teixeira AMG, Pardini R (2009) Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol Conserv 142:1166–1177. https://doi.org/10.1016/j.biocon.2009.01.033
Meyer CFJ, Kalko EKV, Kerth G (2009) Small-scale fragmentation effects on local genetic diversity in two phyllostomid bats with different dispersal abilities in Panama. Biotropica 41:95–102. https://doi.org/10.1111/j.1744-7429.2008.00443.x
Meyer CFJ, Struebig MJ, Willig MR (2016) Responses of tropical bats to habitat fragmentation, logging, and deforestation. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: conservation of bats in a changing world. Springer International Publishing, Cham, pp 63–103
Miguet P, Jackson HB, Jackson ND, Martin AE, Fahrig L (2016) What determines the spatial extent of landscape effects on species? Landsc Ecol 31:1177–1194. https://doi.org/10.1007/s10980-015-0314-1
Monteiro WP, Veiga JC, Silva AR, Carvalho CS, Lanes ÉCM, Rico Y, Jaffé R (2019) Everything you always wanted to know about gene flow in tropical landscapes (but were afraid to ask). PeerJ 7:e6446. https://doi.org/10.7717/peerj.6446
Nabholz B, Glemin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals: the longevity hypothesis. Mol Biol Evol 25:120–130. https://doi.org/10.1093/molbev/msm248
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Simpson GL, Solymos P, Henry MH, Stevens MHH, Wagner H (2015) Vegan: community ecology package. R Package Ver 2.3–2. https://CRAN.R-project.org/package=vegan. Accessed 18 Apr 2020
Pavan AC, Martins F, Santos FR, Ditchfield A, Redondo RAF (2011) Patterns of diversification in two species of short-tailed bats (Carollia Gray, 1838): the effects of historical fragmentation of Brazilian rainforests. Biol J Linn Soc 102:527–539. https://doi.org/10.1111/j.1095-8312.2010.01601.x
PRODES (2018) Monitoramento da Floresta Amazônica Brasileira por Satélite. Brasília
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Redondo RAF, Brina LPS, Silva RF, Ditchfield AD, Santos FR (2008) Molecular systematics of the genus Artibeus (Chiroptera: Phyllostomidae). Mol Phylogenet Evol 49:44–58. https://doi.org/10.1016/j.ympev.2008.07.001
Ribeiro BR, Sales LP, Loyola R (2018) Strategies for mammal conservation under climate change in the Amazon. Biodivers Conserv 27:1943–1959. https://doi.org/10.1007/s10531-018-1518-x
Rinehart JB, Kunz TH (2006) Rhinophylla pumilio. Mamm Species 791:1–5. https://doi.org/10.1644/791.1
Ripperger SP, Tschapka M, Kalko EKV, 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 14:925–934. https://doi.org/10.1007/s10592-012-0434-y
Ripperger SP, Heymann EW, Tschapka M, Kalko EKV (2014a) Fruit characteristics associated with fruit preferences in frugivorous bats and saddle-back tamarins in Peru. Ecotropica 20:53–63
Ripperger SP, Tschapka M, Kalko EKV, Rodríguez-Herrera B, Mayer F (2014b) Resisting habitat fragmentation: high genetic connectivity among populations of the frugivorous bat Carollia castanea in an agricultural landscape. Agric Ecosyst Environ 185:9–15. https://doi.org/10.1016/j.agee.2013.12.006
Ripple WJ, Wolf C, Galetti M et al (2017) World scientists’ warning to humanity: a second notice. Bioscience 70:1–9. https://doi.org/10.1093/biosci/bix125/4605229
Rocha R, López-Baucells A, Farneda FZ, Groenenberg M, Bobrowiec PED, Cabeza M, Palmeirim JM, Meyer CFJ (2017) Consequences of a large-scale fragmentation experiment for Neotropical bats: disentangling the relative importance of local and landscape-scale effects. Landsc Ecol 32:31–45. https://doi.org/10.1007/s10980-016-0425-3
Rocha R, Ovaskainen O, López-Baucells A, Farneda FZ, Sampaio EM, Bobrowiec PED, Cabeza M, Palmeirim JM, Meyer CFJ (2018) Secondary forest regeneration benefits old-growth specialist bats in a fragmented tropical landscape. Sci Rep 8:3819. https://doi.org/10.1038/s41598-018-21999-2
Sampaio E, Lim B, Peters S (2016) Artibeus obscurus. In: IUCN Red List Threatened Species 2016: e.T2137A21998064. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T2137A21998064.en
Sikes RS, Gannon WL (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253. https://doi.org/10.1644/10-MAMM-F-355.1
Silva SM, Ruedas LA, Hasnah Santos L, Silva-Junior JS, Aleixo A (2019) Illuminating the obscured phylogenetic radiation of South American Sylvilagus Gray, 1867 (Lagomorpha: Leporidae). J Mammal 100:31–44. https://doi.org/10.1093/jmammal/gyy186
Solari S (2015a) Rhinophylla pumilio. In: IUCN Red List of Threatened Species 2015: e.T19593A22000844. https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T19593A22000844.en
Solari S (2015b) Dermanura gnoma. In: IUCN Red List of Threatened Species 2015: e.T2129A97207684. https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T2129A21997242.en
Teske PR, Golla TR, Sandoval-Castillo J, Emami-Khoyi A, van der Lingen CD, von der Heyden S, Chiazzari B, Jansen van Vuuren B, Beheregaray LB (2018) Mitochondrial DNA is unsuitable to test for isolation by distance. Sci Rep 8:8448. https://doi.org/10.1038/s41598-018-25138-9
Traill LW, Bradshaw CJA, Brook BW (2007) Minimum viable population size: a meta-analysis of 30 years of published estimates. Biol Conserv 139:159–166. https://doi.org/10.1016/j.biocon.2007.06.011
Trevelin LC, Silveira M, Port-Carvalho M, Homem DH, Cruz-Neto AP (2013) Use of space by frugivorous bats (Chiroptera: Phyllostomidae) in a restored Atlantic forest fragment in Brazil. For Ecol Manag 291:136–143. https://doi.org/10.1016/j.foreco.2012.11.013
Trevelin LC, Novaes RLM, Colas-Rosas PF, Benathar TCM, Peres CA (2017) Enhancing sampling design in mist-net bat surveys by accounting for sample size optimization. PLoS One 12:1–16. https://doi.org/10.1371/journal.pone.0174067
Acknowledgements
We thank the staff of the Laboratory of Molecular Biology of Museu Paraense Emílio Goeldi (MPEG) and MPEG for laboratory support through resources from the FINEP grant “Parque analítico do MPEG: Análise das transformações da Amazônia e seus reflexos na sociobiodiversidade e na paisagem” (grant no. 0118003100). We also acknowledge Bat Conservation International for funding laboratory procedures. Fieldwork was financed by the project “Programa Institutos Nacionais de Ciência e Tecnologia - Uso da Terra e Biodiversidade na Amazônia” (grant no. 384368/2009-3). We appreciate the comments and suggestions of the editor and anonymous reviewers who helped to improve this manuscript. SMS was funded by a Programa Nacional de Pós-Doutorado/Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (PNPD/CAPES) fellowship at Programa de Pós-Graduação em Zoologia/MPEG – Federal University of Pará and a Pós-Doutorado Júnior/Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) fellowship (no. 150657/2017-0) at MPEG. LCT was awarded a PhD studentship by CAPES.
Funding
Bat Conservation International; Programa Institutos Nacionais de Ciência e Tecnologia - Uso da Terra e Biodiversidade na Amazonia (grant no. 384368/2009-3); Programa Nacional de Pós-Doutorado/Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; Conselho Nacional de Desenvolvimento Científico e Tecnológico; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.
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Silva, S.M., Ferreira, G., Pamplona, H. et al. Effects of landscape heterogeneity on population genetic structure and demography of Amazonian phyllostomid bats. Mamm Res 66, 217–225 (2021). https://doi.org/10.1007/s13364-020-00546-3
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DOI: https://doi.org/10.1007/s13364-020-00546-3