Skip to main content
Log in

Landscape drivers of connectivity for a forest rodent in a coffee agroecosystem

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

The majority of remaining tropical forests exist as fragments embedded in a matrix of agricultural production. Understanding the effects of these agricultural landscapes on species dispersal is crucial in the development of successful conservation planning.

Objective

The objective of this study was to examine the influence of five landscape features within a coffee agroecosystem (i.e., slope, elevation, streams, riparian effect, and tree cover) on Heteromys desmarestianus goldmani gene flow. We expected that landscape variables linked to more intense agricultural management (e.g., low tree cover, riparian effect) would reduce gene flow in H. d. goldmani.

Methods

This study was conducted in a 4 km × 2 km area within the coffee growing region of Soconusco in Chiapas, Mexico. We used 12 microsatellite markers to calculate individual-based estimates of gene flow as a measure of dispersal. We used resistance surface modelling, using ResistanceGA (Peterman in Methods Ecol Evol 9:1638–1647, 2018) to identify if any of the landscape features analyzed explained the patterns of gene flow.

Results

Our results showed patterns of population structure and weak isolation-by-distance, as found previously for H. d. goldmani by Otero Jiménez et al. (Conserv Genet 19:495–499, 2018). Slope and tree cover were the two landscape features that could best explain gene flow patterns. More specifically, intermediate slopes and tree cover represent the lowest resistance to gene flow for H. d. goldmani and, thus, have a role in promoting gene flow in this species.

Conclusion

This study highlights the potential of integrating molecular and landscape data to explore population connectivity of elusive species, such as terrestrial small mammals. Our study adds to the growing body of literature in landscape genetics by demonstrating that a rodent species shows population structure at a small scale resulting from landscape factors linked to agricultural management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Blois JL, McGuire JL, Hadly EA (2010) Small mammal diversity loss in response to late-Pleistocene climatic change. Nature 465(7299):771–774

    CAS  PubMed  Google Scholar 

  • Bohdal T, Navrátil J, Sedláček F (2016) Small terrestrial mammals living along streams acting as natural landscape barriers. Ekologia (Bratislava) 35(2):191–204

    Google Scholar 

  • Bolstad P (2016). GIS fundamentals. A first text on Geographic Information Systems (5th edition)

  • Brown JH, Heske EJ (1990) Control of a desert-grassland transition by a keystone rodent guild. Science 250(4988):1705–1707

    CAS  PubMed  Google Scholar 

  • Carver S (2010) Resistance of mammal assemblage structure to dryland salinity in a fragmented landscape. J R Soc West Aust 93:119–128

    Google Scholar 

  • Caudill SA, Rice RA (2016) Do bird friendly® coffee criteria benefit mammals? Assessment of mammal diversity in Chiapas, Mexico. PLoS ONE 11(11):e0165662–e0165662

    PubMed  PubMed Central  Google Scholar 

  • Clarke RT, Rothery P, Raybould AF (2002) Confidence limits for regression relationships between distance matrices: estimating gene flow with distance. J Agric Biol Environ Stat 7(3):361

    Google Scholar 

  • Davidson AD, Lightfoot DC (2006) Keystone rodent interactions: prairie dogs and kangaroo rats structure the biotic composition of a desertified grassland. Ecography 29(5):755–765

    Google Scholar 

  • DeMattia EA, Curran LM, Rathcke BJ (2004) Effects of small rodents and large mammals on Neotropical seeds. Ecology 85(8):2161–2170

    Google Scholar 

  • Dickman CR (1999) Rodent-ecosystem relationships: a review. Ecologically-based management of rodent pests. ACIAR Monograph 59:113–133

    Google Scholar 

  • ESRI (2015) ARCGIS. Environmental Systems Research Incorporated, Redlands

    Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Google Scholar 

  • Fischer C, Thies C, Tscharntke T (2011) Small mammals in agricultural landscapes: opposing responses to farming practices and landscape complexity. Biol Cons 144(3):1130–1136

    Google Scholar 

  • Fleming TH (1974) The population ecology of two species of Costa Rican Heteromyid rodents. Ecology 55(3):493–510

    Google Scholar 

  • Fleming TH (1983) Heteromys desmarestianus. In: Janzen DH (ed) Costa Rican natural history. University of Chicago Press, Chicago, pp 474–475

    Google Scholar 

  • Flores-Manzanero A, Luna-Bárcenas MA, Dyer RJ, Vázquez-Domínguez E (2018) Functional connectivity and home range inferred at a microgeographic landscape genetics scale in a desert-dwelling rodent. Ecol Evol 9(1):ece3.4762

    Google Scholar 

  • Guillot G (2008) Inference of structure in subdivided populations at low levels of genetic differentiation–the correlated allele frequencies model revisited. Bioinformatics 24(19):2222–2228

    CAS  PubMed  Google Scholar 

  • Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1(2):e1500052

    PubMed  PubMed Central  Google Scholar 

  • Hooke RL, Martín-Duque JF, Pedraza J (2012) Land transformation by humans: a review. GSA Today 22:4–10

    Google Scholar 

  • Iverson AL (2015) Biological control, biodiversity, and multifunctionality in coffee agroecosystems. (Unpublished PhD Dissertation) University of Michigan, Ann Arbor, Michigan, USA. https://hdl.handle.net/2027.42/113309

  • Jenson SK, Domingue JO (1988) Extracting topographic structure from digital elevation data for geographic information system analysis. Photogramm Eng Remote Sens 54(11):1593–1600

    Google Scholar 

  • Keeley ATH, Beier P, Gagnon JW (2016) Estimating landscape resistance from habitat suitability: effects of data source and nonlinearities. Landsc Ecol 31(9):2151–2162

    Google Scholar 

  • Klinger R (2007) Catastrophes, disturbances and density-dependence: population dynamics of the spiny pocket mouse (Heteromys desmarestianus) in a neotropical lowland forest. J Trop Ecol 23(05):507–518

    Google Scholar 

  • Lomolino MV, Perault DR (2001) Island biogeography and landscape ecology of mammals inhabiting fragmented, temperate rain forests. Glob Ecol Biogeogr 10(2):113–132

    Google Scholar 

  • Lynch M, Ritland K (1999a) Estimation of pairwise relatedness with molecular markers. Genetics 152(4):1753–1766

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martensen AC, Ribeiro MC, Banks-Leite C, Prado PI, Metzger JP (2012) Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance. Conserv Biol 26(6):1100–1111

    PubMed  Google Scholar 

  • Martínez-Gallardo R, Sánchez-Cordero V (1993) Dietary value of fruits and seeds to spiny pocket mice, Heteromys desmarestianus (Heteromyidae). J Mammal 74(2):436–442

    Google Scholar 

  • Moguel P, Toledo VM (1999) Biodiversity conservation in traditional coffee systems of Mexico. Conserv Biol 13(1):11–21

    Google Scholar 

  • Munshi-South J, Zolnik CP, Harris SE (2016) Population genomics of the Anthropocene: urbanization is negatively associated with genome-wide variation in white-footed mouse populations. Evol Appl 9(4):546–564

    PubMed  PubMed Central  Google Scholar 

  • Otero Jiménez B, Vandermeer JH, Tucker PK (2018) Effect of coffee agriculture management on the population structure of a forest dwelling rodent (Heteromys desmarestianus goldmani). Conserv Genet 19(2):495–499

    PubMed  Google Scholar 

  • Oyler-McCance SJ, Fedy BC, Landguth EL (2013) Sample design effects in landscape genetics. Conserv Genet 14(2):275–285

    Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28(19):2537–2539

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perfecto I, Vandermeer J (2002) Quality of agroecological matrix in a tropical montane landscape: ants in coffee plantations in southern Mexico. Conserv Biol 16(1):174–182

    Google Scholar 

  • Perfecto I, Vandermeer J (2008) Biodiversity conservation in tropical agroecosystems. Ann N Y Acad Sci 1134(1):173–200

    PubMed  Google Scholar 

  • Perfecto I, Vandermeer J, Wright A (2010) Nature's matrix: linking agriculture, conservation and food sovereignty. Routledge, London

    Google Scholar 

  • Peterman W (2018) ResistanceGA: an R package for the optimization of resistance surfaces using genetic algorithms. Methods Ecol Evol 9:1638–1647

    Google Scholar 

  • Peterman WE, Connette GM, Semlitsch RD, Eggert LS (2014) Ecological resistance surfaces predict fine-scale genetic differentiation in a terrestrial woodland salamander. Mol Ecol 23(10):2402–2413

    PubMed  Google Scholar 

  • Popescu VD, Hunter ML (2011) Clear-cutting affects habitat connectivity for a forest amphibian by decreasing permeability to juvenile movements. Ecol Appl 21(4):1283–1295

    PubMed  Google Scholar 

  • Rogers DS, González MW (2010) Phylogenetic relationships among spiny pocket mice (Heteromys) inferred from mitochondrial and nuclear sequence data. J Mammal 91(4):914–930

    Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13(1):58–62

    Google Scholar 

  • Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106

    Google Scholar 

  • Russo I-RM, Sole CL, Barbato M, von Bramann U, Bruford MW (2016) Landscape determinants of fine-scale genetic structure of a small rodent in a heterogeneous landscape (Hluhluwe-iMfolozi Park, South Africa). Sci Rep 6(1):29168–29168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santos-Filho M, Peres CA, da Silva DJ, Sanaiotti TM (2012) Habitat patch and matrix effects on small-mammal persistence in Amazonian forest fragments. Biodivers Conserv 21(4):1127–1147

    Google Scholar 

  • Savidge IR (1973) A stream as a barrier to homing in Peromyscus leucopus. J Mammal 54(4):982–984

    Google Scholar 

  • van Etten J (2017) R package gdistance: distances and routes on geographical grid. J Stat Softw 76(13):1–21

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538

    Google Scholar 

  • Van Strien MJ, Keller D, Holderegger R (2012) A new analytical approach to landscape genetic modelling: least-cost transect analysis and linear mixed models. Mol Ecol 21(16):4010–4023

    Google Scholar 

  • Wolff JO (1999) Behavioral model systems. In: Barrett GW, Peles JD (eds) Landscape ecology of small mammals. Springer-Verlag, New York, pp 11–40

    Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15(4):323–354

    CAS  PubMed  Google Scholar 

  • Zeller KA, McGarigal K, Whiteley AR (2012) Estimating landscape resistance to movement: review. Landsc Ecol 27(6):777–797

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Consuelo Lorenzo and El Colegio de la Frontera Sur-San Cristobal in Chiapas, Mexico for their help in sample collection. Thanks to Dr. Carlos J. Anderson for his valuable comments on the manuscript and support with statistical analysis and Dr. M. Raquel Marchan Rivadeneira for assistance with genetic analysis. We thank the managers, farmers and owners of Finca Irlanda and Finca Hamburgo in Chiapas, Mexico for allowing us to conduct this study and for their support with fieldwork. This work received financial support from the University of Michigan Center for Latin America and Caribbean Studies Tinker Field Research Grant and the University of Michigan Rackham Graduate School. Beatriz Otero Jiménez was supported in part by University of Michigan Genetics Training Program (T32-GM07544).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Beatriz Otero Jiménez.

Additional information

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.

Supplementary file1 (DOCX 880 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Otero Jiménez, B., Li, K. & Tucker, P.K. Landscape drivers of connectivity for a forest rodent in a coffee agroecosystem. Landscape Ecol 35, 1249–1261 (2020). https://doi.org/10.1007/s10980-020-00999-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-020-00999-6

Keywords

Navigation