Skip to main content

Advertisement

Log in

Role of Avian Seed Dispersers in Tree Recruitment in Woodland Pastures

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

The rewilding of abandoned agricultural lands opens up opportunities for the recovery of forest ecosystem extent. Frugivorous animals not only take part in the regeneration of unaltered forests, but leave a visible footprint in restoring areas in the form of the number and spatial distribution of new trees recruited from dispersed seeds. Nevertheless, their contribution is conditioned by how environmental factors affect both the patterns of seed dispersal and the fate of post-dispersal regeneration stages throughout the whole ecosystem. Here, we evaluated the role of avian seed dispersers in tree regeneration in woodland pastures resulting from anthropic deforestation. Using an integrative approach, considering the different tree regeneration stages, we dissected the ways in which forest loss conditioned the contribution of frugivores. Habitat structure influenced bird activity, mainly restricting seed dispersal to forested areas. Tree recruitment was severely reduced during early regeneration stages, but maintained the initial forest-biased spatial distribution. However, the presence of scrub in deforested areas, which protect against grazing at late regeneration stages, drastically increased the relevance of tree recruitment outside the forest. Frugivorous birds made a significant contribution to tree regeneration in the woodland pastures under study. The interplay between seed dispersal by birds and the protective role of scrub was fundamental in facilitating the recolonization of deforested areas. If we wish to encourage this natural reforestation, we will need to preserve populations of frugivorous birds while favoring landscape configurations that encourage seed dispersal outside the forest and species that promote tree establishment (like nurse scrubs).

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.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Balmford A, William B. 2005. Trends in state of nature and their implications for human well-being. Ecology Letters 8:1218–34.

    Article  PubMed  Google Scholar 

  • Bustamante-Sánchez MA, Armesto JJ. 2012. Seed limitations during early forest succession in a rural landscape on Chiloé Island, Chile: Implications for temperate forest restoration. Journal of Applied Ecology 49:1103–12.

    Article  Google Scholar 

  • Cardoso da Silva JMC, Uhl C, Murray G. 1996. Plant succession, landscapes management, and the ecology of frugivorous birds in abandoned Amazonian pastures. Conservation Biology 10:491–503.

    Article  Google Scholar 

  • Cavallero L, Raffaele E, Aizen MA. 2013. Birds as mediators of passive restoration during early post-fire recovery. Biological Conservation 158:342–50.

    Article  Google Scholar 

  • Chazdon RL. 2008. Beyond deforestation: Restoring forest and ecosystem services on degraded lands. Science 320:1458–60.

    Article  CAS  PubMed  Google Scholar 

  • Cramer VA, Hobbs RJ, Standish RJ. 2008. What’s new about all fields? Land abandonment and ecosystem assembly. Trends in Ecology and Evolution 23:104–12.

    Article  PubMed  Google Scholar 

  • Daily GC. 1997. Nature’s services. Societal dependence on natural ecosystems. Washington: Island Press.

    Google Scholar 

  • Darby HC. 1956. The clearing of the woodland in Europe. In: Thomas WL Jr, Ed. Man’s role in changing the face of the Earth. Chicago: University of Chicago Press. p 183–216.

    Google Scholar 

  • Duncan RS, Chapman CA. 2002. Limitations of animal seed dispersal for enhancing forest succession on degraded. In: Levey DJ, Silva WR, Galetti M, Eds. Seed dispersal and frugivory. Ecology, evolution and conservation. Wallingford: CAB International. p 437–50.

    Google Scholar 

  • Farwig N, Berens D. 2012. Imagine a world without seed dispersers: A review of threats, consequences and future directions. Basic and Applied Ecology 13:109–15.

    Article  Google Scholar 

  • García D, Chacoff NP. 2007. Scale-dependent effects of habitat fragmentation on hawthorn pollination, frugivory and seed predation. Conservation Biology 21:400–11.

    Article  PubMed  Google Scholar 

  • García D, Obeso JR. 2003. Facilitation by herbivore-mediated nurse plants in a threatened tree, Taxus baccata: Local effects and landscape level consistency. Ecography 26:739–50.

    Article  Google Scholar 

  • García D, Martínez I, Obeso JR. 2007. Seed transfer among bird-dispersed trees and its consequences for post-dispersal seed fate. Basic and Applied Ecology 8:533–43.

    Article  Google Scholar 

  • García D, Obeso JR, Martínez I. 2005a. Spatial concordance between seed rain and seedling establishment in bird-dispersed trees: Does the scale matter? Journal of Ecology 93:693–704.

    Article  Google Scholar 

  • García D, Rodríguez-Cabal M, Amico GC. 2009. Seed dispersal by a frugivorous marsupial shapes the spatial scale of a mistletoe population. Journal of Ecology 97:217–29.

    Article  Google Scholar 

  • García D, Zamora R, Amico GC. 2010. Birds as suppliers of seed dispersal in temperate ecosystems: Conservation guidelines from real-world landscapes. Conservation Biology 24:1070–9.

    Article  PubMed  Google Scholar 

  • García D, Martínez D, Herrera JM, Morales JM. 2013. Functional heterogeneity in a plant-frugivore assemblage enhances seed dispersal resilience to habitat loss. Ecography 36:197–208.

    Article  Google Scholar 

  • García D, Quevedo M, Obeso JR, Abajo A. 2005b. Fragmentation patterns and protection of montane forests in the Cantabrian range (NW Spain). Forest Ecology and Management 208:29–43.

    Article  Google Scholar 

  • Gómez-Aparicio L, Zamora R, Gómez JM, Hodar JA, Castro J, Baraza E. 2004. Applying plant facilitation to forest restoration: A meta-analysis of the use of nurse plants. Ecological Applications 14:1128–38.

    Article  Google Scholar 

  • González-Varo JP. 2010. Fragmentation, habitat composition and the dispersal/predation balance in interactions between the Mediterranean myrtle and avian frugivores. Ecography 33:185–97.

    Article  Google Scholar 

  • González-Varo JP, Nora S, Aparicio A. 2012. Bottlenecks for plant recruitment in woodland remnants: An ornithochorous shrub in a Mediterranean “relictual” landscape. Perspectives in Plant Ecology, Evolution and Systematics 14:111–22.

    Article  Google Scholar 

  • Grace JB. 2006. Structural equation modeling in natural systems. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Herrera JM, García D. 2010. Effects of forest fragmentation on dispersal and seedling establishment in ornithochorous trees. Conservation Biology 24:1089–98.

    Article  PubMed  Google Scholar 

  • Holl KD, Loik ME, Lin EHV, Samuels IA. 2000. Tropical montane forest restoration in Costa Rica: Overcoming barriers to dispersal and establishment. Restoration Ecology 8:339–49.

    Article  Google Scholar 

  • Hooper DU, Adair EC, Cardinales BJ, Byrnes JEK, Hungate BA, Matulich KL, González A, Duffy JE, Gamfeldt L, O’Connor MI. 2012. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–8.

    CAS  PubMed  Google Scholar 

  • Howe HF, Miriti MA. 2004. When seed dispersal matters. Bioscience 54:651–60.

    Article  Google Scholar 

  • Kapos V, Wandelli E, Camargo JL, Granade G. 1997. Edge-related changes in environment and plant responses due to forest fragmentation in central Amazonia. In: Laurence WF Jr, Bierregaard RO, Eds. Tropical forest remnants. Chicago: Chicago University Press. p 33–44.

    Google Scholar 

  • Keitt TH, Bjornstad ON, Nixon PM, Citron-Pousty S. 2002. Accounting for the spatial pattern when modeling organism-environment relationships. Ecography 25:616–25.

    Article  Google Scholar 

  • Kremen C. 2005. Managing ecosystem services: What do we need to know about their ecology. Ecology Letters 8:468–79.

    Article  PubMed  Google Scholar 

  • Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vázquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein AM, Regetz J, Ricketts TH. 2007. Pollination and other ecosystem services produced by mobile organisms: A conceptual framework for the effects of land-use change. Ecology Letters 10:299–314.

    Article  PubMed  Google Scholar 

  • Lundberg J, Moeberg F. 2003. Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6:87–98.

    Article  Google Scholar 

  • MacDonald D, Crabtree JR, Wiesinger G, Dax T, Stamou N, Fleury P, Gutierrez Lazpita J, Gibon A. 2000. Agricultural abandonment in mountain areas of Europe: Environmental consequences and policy response. Journal of Environmental Management 59:47–69.

    Article  Google Scholar 

  • Martínez D, García D. 2015. Disentangling habitat use by frugivorous birds: constant interactive effects of forest cover and fruit availability. Basic and Applied Ecology 16:460–8.

    Article  Google Scholar 

  • Martínez I, García D, Obeso JR. 2008. Differential seed dispersal patterns generated by a common assemblage of vertebrate frugivores in three fleshy-fruited trees. Ecoscience 15:189–99.

    Article  Google Scholar 

  • Nathan R, Muller-Landau HC. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15:278–85.

    Article  CAS  PubMed  Google Scholar 

  • Navarro LM, Pereira HM. 2012. Rewilding abandoned landscapes in Europe. Ecosystems 15:900–12.

    Article  Google Scholar 

  • Nyström M, Folke C. 2001. Spatial resilience of coral reefs. Ecosystems 4:406–17.

    Article  Google Scholar 

  • Padilla FM, Pugnaire FI. 2006. The role of nurse plants in the restoration of degraded environments. Frontiers in Ecology and the Environment 4:196–202.

    Article  Google Scholar 

  • Pejchar L, Pringle RM, Ranganathan J, Zook JR, Duran G, Oviedo F, Daily GC. 2008. Birds as agents of seed dispersal in a human-dominated landscape in southern Costa Rica. Conservation Biology 141:536–44.

    Article  Google Scholar 

  • Pereira HM, Navarro LM. 2015. Rewilding European landscapes. New York: Springer.

    Book  Google Scholar 

  • Rey P, Alcántara JM. 2014. Effects of habitat alteration on the effectiveness of plant-avian seed dispersal mutualisms: Consequences for plant regeneration. Perspectives in Plant Ecology, Evolution and Systematics 16:21–31.

    Article  Google Scholar 

  • Rivalan P, Frderiksen M, Loïs G, Julliard R. 2007. Contrasting responses of migration strategies in two European thrushes to climate change. Global Change Biology 13:275–87.

    Article  Google Scholar 

  • Rosseel Y. 2012. lavaan: An R package for structural equation modeling. Journal of Statistical Software 48:1–36.

    Article  Google Scholar 

  • Satorra A, Bentler PM. 1994. Corrections to test statistics and standard errors in covariance structure analyses. In: Von Eye A, Clogg CC, Eds. Latent variables analyses: Applications for developmental research. California: SAGE Publications. p 399–419.

    Google Scholar 

  • Schupp EW, Fuentes M. 1995. Spatial patterns of seed dispersal and the unification of plant population ecology. Écoscience 2:267–75.

    Article  Google Scholar 

  • Schupp EW, Jordano P, Gómez JM. 2010. Seed dispersal effectiveness revisited: A conceptual review. New Phytologist 188:333–53.

    Article  PubMed  Google Scholar 

  • SEO/BirdLife. 2013. Programas de seguimiento de avifauna de SEO/BirdLife en 2012. Spain: SEO/BirdLife.

    Google Scholar 

  • Smit C, Ruifrok JL, van Klink R, Olff H. 2015. Rewilding with large herbivores: The importance of grazing refuges for sapling establishment and wood-pasture formation. Biological Conservation 182:134–42.

    Article  Google Scholar 

  • Suárez-Esteban A, Delibes M, Fedriani JM. 2013. Unpaved road verges as hotspots of fleshy-fruited shrub recruitment and establishment. Biological Conservation 167:50–6.

    Article  Google Scholar 

  • Swanson ME, Franklin JF, Beschta RL, Crisafulli CM, DellaSala DA, Hutto RL, Lindenmayer DB, Swanson FJ. 2011. The forgotten stage of forest succession: early-successional ecosystems on forest sites. Frontiers in Ecology and the Environment 9:117–25.

    Article  Google Scholar 

  • Traveset A. 1998. Effect of seed passage through vertebrates’ guts on germination: A review. Perspectives in Plant Ecology, Evolution and Systematics 9:151–90.

    Article  Google Scholar 

  • Uriarte M, Bruna EM, Rubim P, Anciães M, Jonckheere I. 2010. Effects of forest fragmentation on the seedling recruitment of a tropical herb: assessing seed vs. safe-site limitation. Ecology 91:1317–28.

    Article  PubMed  Google Scholar 

  • Vera FWM. 2000. Grazing ecology and forest history. Wallingford: CABI Publishing.

    Book  Google Scholar 

  • Wenny DG. 2000. Seed dispersal, seed predation and seedling recruitment of a neotropical montane tree. Ecological Monographs 70:331–51.

    Article  Google Scholar 

  • Wunderle JM. 1997. The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. Forest Ecology and Management 99:223–35.

    Article  Google Scholar 

Download references

Acknowledgements

We thank C. Guardado, J. Rodríguez, R. Pérez, and D. O. Pastene for technical support and R. Lendrum for linguistic advice. We are also grateful to K. With and three anonymous reviewers who provided helpful suggestions to improve the manuscript. Field work was conducted with the permission of the Wildlife Service of Asturias. Funding was provided by the Spanish Government and the European Social Fund (FPI BES2009-25093 Grant to DM and CGL2008-01275, CGL2011-28430, and CGL2015-68963-C2-2-R Grants to DG).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel Martínez.

Additional information

Author Contribution

DM and DG contributed equally to the conception and the design of the study. DM performed the research and the analysis of the data, and wrote the manuscript. DG contributed substantially to the research and the writing.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Appendix A

Additional information on sampling methodologies (DOC 910 kb)

Online Appendix B

Spatial Simultaneous Autoregressive models (DOC 88 kb)

Online Appendix C

Direct, indirect and total effects estimated in Structural Equation Models (DOC 69 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martínez, D., García, D. Role of Avian Seed Dispersers in Tree Recruitment in Woodland Pastures. Ecosystems 20, 616–629 (2017). https://doi.org/10.1007/s10021-016-0043-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-016-0043-6

Keywords

Navigation