Skip to main content

Advertisement

Log in

Landscape structure shapes carnivore-mediated seed dispersal kernels

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

Abstract

Context

Seed dispersal is recognized as having profound effects on the distribution, dynamics and structure of plant populations and communities. However, knowledge of how landscape structure shapes carnivore-mediated seed dispersal patterns is still scarce, thereby limiting our understanding of large-scale plant population processes.

Objectives

We aim to determine how the amount and spatial configuration of forest cover impacted the relative abundance of carnivorous mammals, and how these effects cascaded through the seed dispersal kernels they generated.

Methods

Camera traps activated by animal movement were used for carnivore sampling. Colour-coded seed mimics embedded in common figs were used to know the exact origin of the dispersed seed mimics later found in carnivore scats. We applied this procedure in two sites differing in landscape structure.

Results

We did not find between-site differences in the relative abundance of the principal carnivore species contributing to seed dispersal patterns, Martes foina. Mean dispersal distance and the probability of long dispersal events were higher in the site with spatially continuous and abundant forest cover, compared to the site with spatially aggregated and scarcer forest cover. Seed deposition closely matched the spatial patterning of forest cover in both study sites, suggesting behaviour-based mechanisms underpinning seed dispersal patterns generated by individual frugivore species.

Conclusions

Our results provide the first empirical evidence of the impact of landscape structure on carnivore-mediated seed dispersal kernels. They also indicate that seed dispersal kernels generated strongly depend on the effect that landscape structure exerts on carnivore populations, particularly on habitat-use preferences.

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

Similar content being viewed by others

References

  • Bateman PW, Fleming PA (2012) Big city life: carnivores in urban environments. J Zool 287:1–23

    Article  Google Scholar 

  • Bolker B (2011a) bbmle: Tools for general maximum likelihood estimation. R package, version 1.0.3. See http://cran.r-project.org/web/packages/bbmle/index.html

  • Bolker B (2011b) emdbook: Ecological models and data—book support. R package, version 1.0.3. See http://cran.r-project.org/web/packages/emdbook/index.html

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Carlo TA, Tewksbury JJ, Martínez del Rio C (2009) A new method to track seed dispersal and recruitment using 15N isotope enrichment. Ecology 90:3516–3525

    Article  PubMed  Google Scholar 

  • Chernick, LaBudde RA (2011) An introduction to bootstrap methods with applications to R. Wiley, Hoboken, p 240

    Google Scholar 

  • Dekker JA, Stein A, Heitkönig IMA (2001) A spatial analysis of a population of red fox (Vulpes vulpes) in the Dutch coastal dune area. J Zool 255:505–510

    Article  Google Scholar 

  • Delignette-Muller ML, Pouilot R, Denis JB, Dutang C (2011) fitdistrplus: Help to fit of a parametric distribution to non-censored or censored data. R package, version 1.0.3. See http://cran.r-project.org/web/packages/fitdistrplus/index.html

  • Dennis AJ, Westcott DA (2007) Estimating dispersal kernels produced by a diverse community of vertebrates. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CAB International, Wallingford, pp 201–228

    Chapter  Google Scholar 

  • Díaz-Ruiz F, Delibes-Mateos M, García-Moreno JL, López-Martín JM, Ferreira C, Ferreras P (2011) Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian Peninsula. Mammal Rev 43:59–70

    Article  Google Scholar 

  • Escribano-Ávila G, Calviño-Cancela M, Pías B, Virgós E, Valladares F, Escudero A (2014) Diverse guilds provide complementary dispersal services in a woodland expansion process after land abandonment. J Appl Ecol 51:1701–1711

    Article  Google Scholar 

  • Galantinho A, Mira A (2009) The influence of human, livestock, and ecological features on the occurrence of genet (Genetta genetta): a case study on Mediterranean farmland. Ecol Res 24:671–685

    Article  Google Scholar 

  • González-Varo JP, Arroyo JM, Jordano P (2014) Who dispersed the seeds? The use of DNA barcoding in frugivory and seed dispersal studies. Methods Ecol Evol 5:806–814

    Article  Google Scholar 

  • González-Varo JP, López-Vao JL, Guitián J (2013) Functional diversity among seed dispersal kernels generated by carnivorous mammals. J Anim Ecol 82:562–571

    Article  PubMed  Google Scholar 

  • Goslee S, Urban D (2015) Ecodist: Dissimilarity-based functions for ecological analysis. R package, version. 1.2.2. https://cran.r-project.org/web/packages/ecodist/ecodist.pdf

  • Guiomar N, Batista T, Fernandes JP, Souto-Cruz C (2009) Corine Land Cover nível 5. Contribuição para a Carta de uso do solo em Portugal Continental. AMDE Edt. Évora. 226 pp

  • Hargis CD, Bissonette JA, Turner DL (1999) The influence of forest fragmentation and landscape pattern on American martens. J Appl Ecol 36:157–172

    Article  Google Scholar 

  • Herrera JM, Doblas-Miranda E (2013) Land-cover change effects on trophic interactions: current knowledge and future challenges in research and conservation. Basic Appl Ecol 14:1–11

    Article  Google Scholar 

  • Herrera JM, García D (2010) Effects of forest fragmentation on seed dispersal and seedling establishment in ornithochorous trees. Conserv Biol 24:1089–1098

    Article  PubMed  Google Scholar 

  • Herrera CM (2003) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant–animal Interactions: an evolutionary approach. Blackwell Publishing, Oxford, pp 185–208

    Google Scholar 

  • Herrera JM, Morales JM, García D (2011) Differential effects of fruit availability and habitat cover for frugivore-mediated seed dispersal in a heterogeneous landscape. J Ecol 99:1100–1107

    Article  Google Scholar 

  • Higgins SI, Nathan R, Cain ML (2003) Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology 84:1945–1956

    Article  Google Scholar 

  • Jordano P, García C, Godoy JA, García-Castaño JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Nat Acad Sci USA 104:3278–3282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly MJ (2008) Design, evaluate, refine: camera trap studies for elusive species. Anim Conserv 11:182–184

    Article  Google Scholar 

  • Koike S, Masaki T, Nemoto Y, Kozakai C, Yamazaki K, Kasai S, Nakajima A, Kaji K (2011) Estimate of the seed shadow created by the Asiatic black bear Ursus thibetanus and its characteristics as a seed disperser in Japanese cool-temperate forest. Oikos 120:280–290

    Article  Google Scholar 

  • Lenz J, Fiedler W, Caprano T, Friedrichs W, Gaese BH, Wikelski M, Böhning-Gaese K (2011) Seed-dispersal distributions by trumpeter hornbills in fragmented landscapes. Proc R Soc Biol Sci B 278:2257–2264

    Article  Google Scholar 

  • Levine JM, Murrell DJ (2003) The community-level consequences of seed dispersal patterns. Ann Rev Ecol Evol Syst 34:549–574

    Article  Google Scholar 

  • López-Bao JV, González-Varo JP (2011) Frugivory and spatial patterns of seed dispersal by carnivorous mammals in anthropogenic landscapes: a multi-scale approach. PLoS One 6:e14569

    Article  PubMed  PubMed Central  Google Scholar 

  • MacKenzie DI, Kendall WL (2002) How should detection probability be incorporated into estimates of relative abundance? Ecology 83:2387–2393

    Article  Google Scholar 

  • Matías L, Zamora R, Mendoza I, Hódar JA (2010) Seed dispersal patterns by large frugivorous mammals in a degraded mosaic landscape. Rest Ecol 18:619–627

    Article  Google Scholar 

  • Morales JM, Carlo TA (2006) The effects of plant distribution and frugivore density on the scale and shape of dispersal kernels. Ecology 87:1489–1496

    Article  PubMed  Google Scholar 

  • Morales JM, García D, Martínez D, Rodríguez-Pérez J, Herrera JM (2013) Frugivore behavioural details matter for seed dispersal: a multi-species model for Cantabrian thrushes and trees. PLoS One 8:e65216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morales JM, Rivarola MD, Amico G, Carlo T (2012) Neighborhood effects on seed dispersal by frugivores: testing theory with a mistletoe-marsupial system in Patagonia. Ecology 93:741–748

    Article  PubMed  Google Scholar 

  • Nathan R (2006) Long distance dispersal of plants. Science 313:786–788

    Article  CAS  PubMed  Google Scholar 

  • Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285

    Article  PubMed  Google Scholar 

  • Pinto-Correia T, Ribeiro N, Sa-Sousa P (2011) Introducing the montado, the cork and holm oak agroforestry system of Southern Portugal. Agrofor Syst 82:99–104

    Article  Google Scholar 

  • Quantum GIS Development Team (2014) Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rodríguez-Pérez J, Wiegand T, Santamaría JL (2012) Frugivore behaviour determines plant distribution: a spatially-explicit analysis of a plant-disperser interaction. Ecography 35:113–123

    Article  Google Scholar 

  • Rosalino LM, Santos-Reis M (2009) Fruit consumption by carnivores in Mediterranean Europe. Mammal Rev 39:67–78

    Article  Google Scholar 

  • Russo SE, Augspurger CK (2004) Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol Lett 7:1058–1067

    Article  Google Scholar 

  • Santos MJ, Santos-Reis M (2010) Stone marten (Martes foina) habitat in a Mediterranean ecosystem: effects of scale, sex, and interspecific interactions. Eur J Wildlife Res 56:275–286

    Article  Google Scholar 

  • Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–386

    Article  Google Scholar 

  • Westcott DA, Bentrupperbäumer J, Bradford MG, McKeown A (2005) Incorporating patterns of disperser behaviour into models of seed dispersal and its effects on estimated dispersal curves. Oecologia 146:47–57

    Article  Google Scholar 

  • Zalewski A, Jedrzejewski W, Jedrzejewska B (2004) Mobility and home ranges use by pine martens (Martes martes) in a Polish primeval forest. Écoscience 11:113–122

    Google Scholar 

Download references

Acknowledgments

This work was supported by Integrated Program of IC&DT (1/SAESCTN/ALENT-07-0224 FEDER-001755). Ronnie Lendrum, greatly improved the quality of the English in the manuscript and two anonymous referees provided helpful comments which greatly improved a previous version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José M. Herrera.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 617 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Herrera, J.M., de Sá Teixeira, I., Rodríguez-Pérez, J. et al. Landscape structure shapes carnivore-mediated seed dispersal kernels. Landscape Ecol 31, 731–743 (2016). https://doi.org/10.1007/s10980-015-0283-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-015-0283-4

Keywords

Navigation