Analysis of the contribution of landscape attributes on the genetic diversity of Artibeus jamaicensis Leach, 1821

  • Elida María Leiva-González
  • Darío Navarrete-Gutiérrez
  • Lorena Ruiz-Montoya
  • Antonio Santos-Moreno
  • Cristian Kraker-Castañeda
  • Maricela García-Bautista
Original Paper


It is commonly assumed that bats, due to their flight capacity, are not affected by landscape attributes across small geographic extensions. However, recent studies with phyllostomids have found evidence of negative responses, such as decreasing genetic diversity with decreasing forest amount, specifically in areas dominated by agricultural land. The purpose of this study was to evaluate if landscape composition and configuration could be influencing the genetic diversity of a common frugivorous bat: Artibeus jamaicensis. We worked in an area characterized by the presence of extensive agricultural land, with a trend towards open spaces of high contrast with forests. Through mtDNA control region sequences, we inferred high levels of genetic diversity in the surveyed landscapes. In order to determine a possible relationship between genetic diversity and landscape attributes, we employed a multivariate exploratory analysis that allowed us to determine the independent contribution of each variable, in a hierarchical model. We found a negative relationship between genetic diversity and total forest edge, which is a variable that reflects the degree of fragmentation. This procedure can be implemented in population genetics, allowing the incorporation of spatially explicit variables.


Bats Fragstats Hierarchical partitioning mtDNA Spatially explicit 



We thank C. Lorenzo and J. Bolaños from the Colección Mastozoológica (ECOSUR-SCLC), for housing the tissue samples. We appreciate the support of the PNLM-CONANP authorities, staff and park rangers, especially O. Cervantes and A. León, as well as the support of G. Lalo Jacinto and the authorities of the Instituto Nacional de Antropología e Historia (INAH), for permission to work in the Chinkultic archeological site. We are grateful with G. Castellanos, B. Cruz and C. Lorenzo for the revision of early versions of this manuscript. The Instituto Politécnico Nacional (IPN) of Mexico provided support during fieldwork. Finally, we thank landowners and local authorities for permission to work in the area.


This project was partially funded by Idea Wild. E. M. Leiva-González received a scholarship (No. 597881) provided by the Consejo Nacional de Ciencia y Tecnología (CONACyT-Mexico).


  1. American Museum of Natural History [AMNH] (2018) Wing Punch and Hair Sampling Protocols. Available from:
  2. Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James PMA, Rosenberg MS, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575CrossRefGoogle Scholar
  3. Anthony ELP (1988) Age determination in bats: In: Kunz TH (ed). Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, DC, pp 47–58Google Scholar
  4. Arroyo-Rodríguez V, Rojas C, Saldaña-Vásquez RA, Stoner KE (2016) Landscape composition is more important than landscape configuration for phyllostomid bat assemblages in a fragmented biodiversity hotspot. Biol Conserv 198:84–92CrossRefGoogle Scholar
  5. Ávila-Cabadilla LD, Sánchez-Azofeifa GA, Stoner KE, Álvarez-Añorve MY, Quesada M, Portillo-Quintero CA (2012) Local and landscape factors determining occurrence of Phyllostomid bats in tropical secondary forests. PLoS One 7(4):e35228CrossRefGoogle Scholar
  6. Baguette M, Blanchet S, Legrand D, Stevens VM, Turlure C (2013) Individual dispersal, landscape connectivity and ecological networks. Biol Rev 88:310–326CrossRefGoogle Scholar
  7. Balkenhol N, Cushman SA, Storfer A, Waits LP (2016) Introduction to landscape genetics-concepts, methods, applications. In: Balkenhol N, Chushman SA, Storfer AT, Waits LP (eds) Landscape genetics: concepts, methods, applications. Wiley Blackwell, UK, pp 1–7Google Scholar
  8. Bennett AF, Saunders DA (2010) Habitat fragmentation and landscape change. In: Sodhi NS, Ehrlich PR (eds) Conservation biology for all. Oxford University Press, New York, pp 88–104CrossRefGoogle Scholar
  9. Bernard E, Fenton MB (2003) Bat mobility and roosts in a fragmented landscape in Central Amazonia, Brazil. Biotropica 35(2):262–277Google Scholar
  10. Bolívar-Cimé B, Laborde J, MacSwiney MC, Muñoz-Robles C, Tun-Garrido J (2013) Response of phytophagous bats to patch quality and landscape attributes in fragmented tropical semi-deciduous forest. Acta Chiropterol 15(2):399–409CrossRefGoogle Scholar
  11. Bolton PE, West AJ, Cardilini APA, Clark JA, Maute KL, Legge S, Brazill-Boast J, Griffith SC, Rollins LA (2016) Three molecular markers show no evidence of population genetic structure in the Gouldian finch (Erythrura gouldiae). PLoS One 11(12):e0167723CrossRefGoogle Scholar
  12. Burland TM, Worthington-Wilmer J (2001) Seeing in the dark: molecular approaches to the study of bat populations. Biol Rev 76:389–409CrossRefGoogle Scholar
  13. Carstens BC, Sullivan J, Davalos LM, Larsern PA, Pedersen SC (2004) Exploring population genetic structure in three species of Lesser Antillean bats. Mol Ecol 13:2557–2566CrossRefGoogle Scholar
  14. Chevan A, Sutherland M (1991) Hierarchical partitioning. Am Stat 45(2):90–96Google Scholar
  15. Comisión Nacional de Áreas Naturales Protegidas [CONANP] (2007) Programa de conservación y manejo del Parque Nacional Lagunas de Montebello. SEMARNAT, Mexico CityGoogle Scholar
  16. Corthals A, Martin A, Warsi OM, Woller-Skar M, Lancaster W, Russell A, Dávalos LA (2015) From the field to the lab: best practices for field preservation of bat specimens for molecular analysis. PLoS One 10(3):e0118994CrossRefGoogle Scholar
  17. Cushman SA, McGarigal K, Neel MC (2008) Parsimony in landscape metrics: strength, universality, and consistency. Ecol Indic 8:691–703CrossRefGoogle Scholar
  18. Davy CM, Martínez-Núñez F, Willis CKR, Good SV (2015) Spatial genetic structure among bat hibernacula along the leading edge of a rapidly spreading pathogen. Conserv Genet 16(5):1013–1024CrossRefGoogle Scholar
  19. De la Peña-Cuéllar E, Benítez-Malvido J, Ávila-Cabadilla LD, Martínez-Ramos M, Estrada A (2014) Structure and diversity of phyllostomid bats assemblages on riparian corridors in a human-dominated tropical landscape. Ecol Evol 5(4):903–913CrossRefGoogle Scholar
  20. Diniz-Filho JAF, Soares TN, Lima JS, Dobrovolski R, Lemes-Landeiro V, Telles MP, Rangel TF, Bini LM (2013) Mantel test in population genetics. Genetics Mol Biol 36(4):475–485CrossRefGoogle Scholar
  21. Diniz-Filho JAF, Telles MP, Bonatto SL, Eizirik E, de Freitas TRO, de Marco P, Santos FR, Sole-Cava A, Nascimiento-Soares T (2008) Mapping the evolutionary twilight zone: molecular markers, populations and geography. J Biogeogr 35:753–763CrossRefGoogle Scholar
  22. Dixo M, Metzger JP, Morgante JS, Zamudio KR (2009) Habitat fragmentation reduces diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol Conserv 142:1560–1569CrossRefGoogle Scholar
  23. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of population. Mol Ecol 11:2571–2581CrossRefGoogle Scholar
  24. Eastman JR (2012) IDRISI selva tutorial: manual versión 17. Clark Labs, Clark UniversityGoogle Scholar
  25. Ethier K, Fahrig L (2011) Positive effects of forest fragmentation, independent of forest amount, on bat abundance in eastern Ontario, Canada. Landsc Ecol 26:865–876CrossRefGoogle Scholar
  26. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinforma 1:47–50CrossRefGoogle Scholar
  27. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  28. Fahrig L (1999) Forest lost and fragmentation: which has the greater effect on persistence of forest-dwelling animals. In: Rochelle JA, Lehman LA, Wisniewski J (eds) Forest fragmentation: wildlife and management implication. Brill Press, Netherlands, pp 87–95Google Scholar
  29. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515CrossRefGoogle Scholar
  30. Fleming TH, Murray KL (2009) Population and genetic consequences of hurricanes for three species of West Indian phyllostomid bats. Biotropica 42(2):250–256CrossRefGoogle Scholar
  31. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  32. Frankham R, Ballou JD, Briscoe DA (2002) Genetic diversity. Introduction to conservation genetics. Cambridge University Press, New York, pp 45–71Google Scholar
  33. García-García JL, Santos-Moreno A (2014) Efectos de la estructura del paisaje y de la vegetación en la diversidad de murciélagos filostómidos (Chiroptera: Phyllostomidae) de Oaxaca, México. Rev Biol Trop 62(1):217–239CrossRefGoogle Scholar
  34. Gonçalves da Silva A, Gaona O, Medellín RA (2008) Diet and trophic structure in a community of fruit-eating bats in Lacandon forest, Mexico. J Mammal 89(1):43–49CrossRefGoogle Scholar
  35. Handley CO, Gardner AL, Wilson DE (1991) Movements. In: Handley CO, Wilson DE, Gardner AL (eds) Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Smithsonian Institution Press, Washington, DC, pp 89–130Google Scholar
  36. Heim O, Treitler JT, Tschapka M, Knörnschild M, Jung K (2015) The importance of landscape elements for bat activity and species richness in agricultural areas. PLoS One 10:e0134443CrossRefGoogle Scholar
  37. Höglund J (2009) Evolutionary conservation genetics. Oxford University Press, USA, pp 60–80Google Scholar
  38. Holderegger R, Wagner HH (2008) Landscape genetics. Bioscience 58:199–207CrossRefGoogle Scholar
  39. Jackson ND, Fahrig L (2016) Habitat amount, not habitat configuration, best predicts population genetic structure in fragmented landscapes. Landsc Ecol 31:951–968CrossRefGoogle Scholar
  40. Kraker-Castañeda C, Santos-Moreno A, Lorenzo C, Horváth A, MacSwiney MC, Navarrete-Gutiérrez D (2017) Responses of phyllostomid bats to forest cover in upland landscapes in Chiapas, southeast Mexico. Stud Neotropical Fauna Environ 52(2):112–121CrossRefGoogle Scholar
  41. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948 Available from: CrossRefGoogle Scholar
  42. Larsen PA, Hoofer SR, Bozeman MC, Pedersen SC, Genoways HH, Carleton JP, Pumo DE, Baker RJ (2007) Phylogenetics and phylogeography of the Artibeus jamaicensis complex based on cytochrome-b DNA sequences. J Mammal 88(3):712–727CrossRefGoogle Scholar
  43. Laurance WF (2014) Contemporary drivers of habitat fragmentation. In: Kettle CJ, Pin Koh L (eds). CAB International, p 20–27Google Scholar
  44. Librado P, Rozas J (2009) DnaSP v.5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452 Available from: CrossRefGoogle Scholar
  45. Lindenmayer DB, Fischer J (2006) Habitat fragmentation and landscape change: an ecological and conservation synthesis. Island Press, Washington DC, pp 15–25Google Scholar
  46. Llaven-Macías V, Ruiz-Montoya L, García-Bautista M, Lesher-Gordillo J, Machkour M’Rabet S (2017) Genetic diversity and structure of Artibeus jamaicensis (Chiroptera: Phyllostomidae) in Chiapas, Mexico. Acta Zool Mex 33(1):55–66Google Scholar
  47. Lu D, Weng Q (2007) A survey of image classification methods and techniques for improving classification performance. Int J Remote Sens 28(5):823–870CrossRefGoogle Scholar
  48. Mac Nally R (2000) Regression and model-building in conservation biology, biogeography and ecology: the distinction between -and reconciliation of- ‘predictive’ and ‘explanatory’ models. Biodivers Conserv 9:655–671CrossRefGoogle Scholar
  49. Mac Nally R (2002) Multiple regression and inference in ecology and conservation biology: further comments on identifying important predictor variables. Biodivers Conserv 11:1397–1401CrossRefGoogle Scholar
  50. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trend Ecol Evol 18(4):189–197CrossRefGoogle Scholar
  51. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2):209–220Google Scholar
  52. Martínez-Sánchez J (2005) Frugívoros voladores y la dispersión de semillas en el Parque Nacional Lagunas de Montebello, Chiapas, México. (Master’s thesis). El Colegio de la Frontera Sur (ECOSUR)Google Scholar
  53. McCulloch ES, Tello SJ, Whitehead A, Rolón-Mendoza CMJ, Maldonado-Rodríguez MCD, Stevens RD (2013) Fragmentation of Atlantic Forest has not affected gene flow of a widespread seed-dispersing bat. Mol Ecol 22:4619–4633CrossRefGoogle Scholar
  54. McGarigal K (2015) Fragstats help. Fragstats 4.2: Spatial pattern analysis program for categorical and continuous maps. University of MassachusettsGoogle Scholar
  55. McGarigal K, Ene E (2013) Fragstats 4.2 v4.2.1.603: spatial pattern analysis program for categorical and continuous maps. University of Massachusetts, Amherst Available from: Google Scholar
  56. McGarigal K, Marks BJ (1995) Fragstats. Spatial pattern analysis program for quantifying landscape structure. Version 2.0. USDA Forest Service General Technical ReportGoogle Scholar
  57. 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(1):95–102CrossRefGoogle Scholar
  58. 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, Switzerland, pp 63–103CrossRefGoogle Scholar
  59. Morrison DW (1978a) Foraging ecology and energetics of the frugivorous bat Artibeus jamaicensis. Ecology 59(4):716–723CrossRefGoogle Scholar
  60. Morrison DW (1978b) Influence of habitat on the foraging distances of the fruit bat, Artibeus jamaicensis. J Mammal 59(3):622–624CrossRefGoogle Scholar
  61. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  62. Nei M, Li W (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases (molecular evolution/mitochondrial DNA/nucleotide diversity). Proc Natl Acad Sci U S A 76(10):5269–5273CrossRefGoogle Scholar
  63. Norberg UM, Rayner MV (1987) Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc Lond Ser B Biol Sci 326(1179):335–427CrossRefGoogle Scholar
  64. Olea PP, Mateo-Tomás P, de Frutos A (2010) Estimating and modelling bias of the hierarchical partitioning public-domain software: implications in environmental management and conservation. PLoS One 5(7):e11698CrossRefGoogle Scholar
  65. Ortega J, Castro-Arellano I (2001) Artibeus jamaicensis. Mamm Species 662:1–9CrossRefGoogle Scholar
  66. Ortega J, Maldonado JE, Wilkinson GS, Arita HT, Fleischer RC (2003) Male dominance, paternity, and relatedness in the Jamaican fruit-eating bat (Artibeus jamaicensis). Mol Ecol 12:2409–2415CrossRefGoogle Scholar
  67. Pinto N, Keitt TH (2008) Scale-dependent responses to forest cover displayed by frugivore bats. Oikos 117:1725–1731CrossRefGoogle Scholar
  68. Pulido-Solís MT (2000) Haciendas de Chiapas. CONECULTA-Chiapas, Tuxtla GutiérrezGoogle Scholar
  69. Pumo DE, Goldin EZ, Elliot B (1988) Mitochondrial DNA polymorphism in three Antillean island populations of the fruit bat, Artibeus jamaicensis. Mol Biol 5(1):79–89Google Scholar
  70. Pumo DE, Kim I, Remsen J, Phillips CJ, Genoways HH (1996) Molecular systematics of the fruit bat, Artibeus jamaicensis: origin of an unusual island population. J Mammal 77(2):491–503CrossRefGoogle Scholar
  71. Ramírez-Marcial N, González-Espinosa M, Camacho-Cruz A, Ortiz-Aguilar D (2010) Forest restoration in Lagunas de Montebello National Park, Chiapas, Mexico. Ecol Restor 28(3):354–360CrossRefGoogle Scholar
  72. 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 14:925–934CrossRefGoogle Scholar
  73. Ripperger SP, Tschapka M, Kalko EKV, Rodriguez-Herrera B, Mayer F (2014) Resisting habitat fragmentation: high genetic connectivity among populations of the frugivorous bat Carollia castanea in an agricultural landscape. Agric Ecosyst Environ 185:9–15CrossRefGoogle Scholar
  74. Ruiz EA, Vargas-Miranda B, Zúñiga G (2013) Late-Pleistocene phylogeography and demographic history of two evolutionary linages of Artibeus jamaicensis (Chiroptera: Phyllostomidae) in Mexico. Acta Chiropterol 15(1):19–33CrossRefGoogle Scholar
  75. Ruz MH (1992) Savia india, floración ladina. Apuntes para una historia de las fincas comitecas (siglos XVIII y XIX). CONACULTA, Mexico cityGoogle Scholar
  76. Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5(1):18–32CrossRefGoogle Scholar
  77. Sikes RS, the Animal Care and Use Committee of the American Society of Mammalogists (2016) 2016 guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mammal 92(1):235–253CrossRefGoogle Scholar
  78. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedPubMedCentralGoogle Scholar
  79. Turner MG, Gardner RH, RV O’N (2001) Landscape ecology in theory and practice: pattern and process. Springer-Verlag, New YorkGoogle Scholar
  80. Vázquez-Domínguez E, Mendoza-Martínez A, Orozco-Lugo L, Cuarón AD (2013) High dispersal and generalist habits of the bat Artibeus jamaicensis on Cozumel Island, México: an assessment using molecular genetics. Acta Chiropterol 15(2):411–421CrossRefGoogle Scholar
  81. Verbyla DL (1995) Satellite remote sensing of natural resources. CRC Press, Boca RatonGoogle Scholar
  82. Walsh C, Mac Nally R (2013) hier.part: hierarchical partitioning. R Package, version 1.0–4. Available from:
  83. Wan QH, Wu H, Fujihara T, Fang SG (2004) Which genetic marker for which conservation genetics issue? Electrophoresis 25:2165–2176CrossRefGoogle Scholar
  84. Wang X, Blanchet FG, Koper N (2014) Measuring habitat fragmentation: an evaluation of landscape patter metrics. Methods Ecol Evol 5(7):634–646CrossRefGoogle Scholar
  85. Worthington-Wilmer JW, Barratt E (1996) A non-lethal method of tissue sampling for genetic studies of chiropteran. Bat Res News 37:1–3Google Scholar
  86. Wright S (1943) Isolation by distance. Genetics 28(2):114–138Google Scholar
  87. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214CrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2018

Authors and Affiliations

  1. 1.Departamento de Conservación de la BiodiversidadEl Colegio de la Frontera Sur (ECOSUR)San Cristóbal de Las CasasMexico
  2. 2.Escuela de BiologíaUniversidad de San Carlos de Guatemala (USAC)Guatemala CityGuatemala
  3. 3.Laboratorio de Análisis de Información Geográfica y EstadísticaEl Colegio de la Frontera Sur (ECOSUR)San Cristóbal de Las CasasMexico
  4. 4.Laboratorio de Ecología Animal, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR)Instituto Politécnico NacionalSanta Cruz XoxocotlánMexico
  5. 5.Unidad para el Conocimiento, Uso y Valoración de la Biodiversidad, Centro de Estudios Conservacionistas (CECON)Universidad de San Carlos de GuatemalaGuatemala CityGuatemala
  6. 6.Laboratorio de GenéticaEl Colegio de la Frontera Sur (ECOSUR)San Cristóbal de Las CasasMexico

Personalised recommendations