Skip to main content

Advertisement

Log in

Seed removal patterns of pioneer trees in an agricultural landscape

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

The seeds of most tropical plants are dispersed by animals, many of which also act as seed predators. Shifts in animal community composition, such as those driven by the clearing of native vegetation, are therefore likely to drive changes in plant recruitment. We used manipulative experiments excluding ants, small rodents, and birds to quantify the relative impacts of these granivores on animal-dispersed pioneer trees (ADPT) in fragments of savanna vegetation and adjacent soy plantations in Brazil’s Cerrado. We found that ants were the main consumers of ADPT seeds, that the rates of seed removal varied with seed size, and that removal rates were higher in savanna fragments than in soy plantations. However, we also found significant interactions between habitat type, seed species, and the type of seed predator being excluded. Our results underscore how challenging it can be to predict the influence of human disturbances on the interactions between plant and animal communities. Because ants, rodents, and birds are Cerrado’s the main seed dispersers and granivores, seedling recruitment in Cerrado landscape mosaics will depend on how these distinct but related processes are each influenced by species-specific patterns of seed size and seed abundance.

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

Similar content being viewed by others

References

  • Aguiar RWS, dos Santos SF, da Silva Morgado F, Ascencio SD, de Mendonça Lopes M, Viana KF (2015) Insecticidal and repellent activity of Siparuna guianensis Aubl. (Negramina) against Aedes aegypti and Culex quinquefasciatus. PLoS ONE 10:e0116765. doi:10.1371/journal.pone.0116765

    Article  PubMed  PubMed Central  Google Scholar 

  • Arroyo-Rodríguez V, Melo FPL, Martínez-Ramos Miguel, Bongers F, Chazdon RL, Meave JA, Norden N, Santos BA, Leal IR, Tabarelli M (2015) Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biol Rev. doi:10.1111/brv.12231

  • Bao F, Lima LB, Luz PB (2014) Caracterização morfológica do ramo, sementes e plântulas de Matayba guianensis Aubl. e produção de mudas em diferentes recipientes e substratos. Rev Árvore 38:63–71

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2015) Lme4: linear mixed-effect models using S4 classes. R package version 0.999375–39. http://CRAN.R-project.org/package=lme4. Accessed Oct 2015

  • Beckman NG (2013) The distribution of fruit and seed toxicity during development for eleven neotropical trees and vines in Central Panama. PLoS ONE 8:e66764. doi:10.1371/journal.pone.0066764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bello C, Galetti M, Pizo MA, Magnago LF S, Rocha MF, Lima RAF, Jordano P (2015) Defaunation affects carbon storage in tropical forests. Science 1:1–11. https://doi.org/10.1126/sciadv.1501105

  • Brandão CRF, Silva RR, Feitosa RM (2011) Cerrado ground-dwelling ants (Hymenoptera: Formicidae) as indicators of edge effects. Zoologia 28:379–387

    Article  Google Scholar 

  • Briani DC, Guimarães PR (2007) Seed predation and fruit damage of Solanum lycocarpum (Solanaceae) by rodents in the cerrado of central Brazil. Acta Oecol 31:8–12

    Article  Google Scholar 

  • Briones-Salas M, Sánchez-Cordero V, Sánchez-Rojas G (2006) Multi-species fruit and seed removal in a tropical deciduous forest in Mexico. Can J Bot 84:433–442

    Article  Google Scholar 

  • Bruna EM, Guimarães JF, Lopes CT, Duarte P, Gomes ACL, Belentani SCS, Vasconcelos HL (2010) Mammalia, Estação Ecológica do Panga, a Cerrado protected area in Minas Gerais state, Brazil. Check List 6:668–675

    Article  Google Scholar 

  • 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

  • Castellani ED, Damião Filho CF, Aguiar IB (2001) Caracterização morfológica de frutos e sementes de espécies arbóreas do gênero Xylopia (Annonaceae). Rev Bras Sementes 30:102–113

    Article  Google Scholar 

  • Christianini AV, Galetti M (2007) Spatial variation in post-dispersal seed removal in an Atlantic forest: effects of habitat, location and guilds of seed predators. Acta Oecol 32:328–336

    Article  Google Scholar 

  • Christianini AV, Oliveira PS (2010) Birds and ants provide complementary seed dispersal in a neotropical savanna. J Ecol 98:573–582

    Article  Google Scholar 

  • Cole RJ (2009) Postdispersal seed fate of tropical montane trees in an agricultural landscape, Southern Costa Rica. Biotropica 41:319–327. doi:10.1111/j.1744-7429.2009.00490.x

    Article  Google Scholar 

  • Côrtes MC, Uriarte M (2013) Integrating frugivory and animal movement: a review of the evidence and implications for scaling seed dispersal. Biol Rev Camb Philos Soc 88:255–272. doi:10.1111/j.1469-185X.2012.00250.x

    Article  PubMed  Google Scholar 

  • Costa AN, Vasconcelos HL, Vieira-Neto EHM, Bruna EM (2008) Do herbivores exert top-down effects in neotropical savannas? Estimates of biomass consumption by leaf-cutter ants. J Veg Sci 19:849–854

    Article  Google Scholar 

  • Costa AN, Vasconcelos HL, Bruna EM (2017) Biotic-drivers of plant early-recruitment success: selective herbivory by leaf-cutter ants as an ecological filter in neotropical savannas. J Ecol 105:132–141

    Article  Google Scholar 

  • Craig MT, Orrock JL, Brudvig LA (2011) Edge-mediated patterns of seed removal in experimentally connected and fragmented landscapes. Landsc Ecol 26:1373–1381

    Article  Google Scholar 

  • Cramer JM, Mesquita RCG, Williamson BG (2007) Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biol Conserv 137:415–423. https://doi.org/10.1016/j.biocon.2007.02.019

  • Cuevas-Reyes P, Gilberti L, González-Rodríguez A, Wilson Fernandes G (2013) Patterns of herbivory and fluctuating asymmetry in Solanum lycocarpum St. Hill (Solanaceae) along an urban gradient in Brazil. Ecol Indic 24:557–561

    Article  Google Scholar 

  • De Assis PA, Theodoro PNET, de Paula JE, Araújo AJ, Costa-Lotufo LV, Michel S, Grougnet R, Kritsanida M, Espindola LS (2014) Antifungal ether diglycosides from Matayba guianensis Aublet. Bioorg Med Chem Lett 24:1414–1416

    Article  PubMed  Google Scholar 

  • De Oliveira AP, Machado CG, Sigrist MR (2013) Matayba guianensis (Sapindaceae): frugivoria por aves em remanescente de Cerrado do Centro-Oeste brasileiro. SITIENTIBUS Série Ciências Biológicas 13:1–7. https://doi.org/10.13102/scb319

  • Dirzo R, Mendoza E, Ortiz P (2007) Size-related differential seed predation in a heavily defaunated neotropical rain forest. Biotropica 39:355–362

    Article  Google Scholar 

  • Donoso DS, Grez AA, Simonetti JA (2004) Effects of forest fragmentation on the granivory of differently sized seeds. Biol Conserv 115:63–70

    Article  Google Scholar 

  • Doust SJ, Erskine PD, Lamb D (2006) Direct seeding to restore rainforest species: microsite effects on the early establishment and growth of rainforest tree seedlings on degraded land in the wet tropics of Australia. For Ecol Manag 234:333–343. https://doi.org/10.1016/j.foreco.2006.07.014

  • Ferreira AV, Bruna EM, Vasconcelos HL (2011) Seed predators limit plant recruitment in neotropical savannas. Oikos 120:1013–1022

    Article  Google Scholar 

  • Fischer C, Türke M (2016) Seed preferences by rodents in the agri-environment and implications for biological weed control. Ecol Evol 6:5796–5807. https://doi.org/10.1002/ece3.2329

  • Françoso R, Brandão R, Nogueirac CC, Salmonaa YB, Machadoa RB, Collia GL (2015) Habitat loss and the effectiveness of protected areas in the Cerrado biodiversity hotspot. Nat Conserv 13:35–40. doi:10.1016/j.ncon.2015.04.001

    Article  Google Scholar 

  • Frizzo TLM, Vasconcelos HL (2013) The potential role of scattered trees for ant conservation in an agriculturally dominated neotropical landscape. Biotropica 45:644–651

    Article  Google Scholar 

  • Gallegos SC, Hensen I, Schleuning M (2014) Secondary dispersal by ants promotes forest regeneration after deforestation. J Ecol 102:659–666. https://doi.org/10.1111/1365-2745.12226

  • García D, Chacoff NP (2007) Scale-dependent effects of habitat fragmentation on hawthorn pollination, frugivory and seed predation. Conserv Biol 21:400–411

    Article  PubMed  Google Scholar 

  • Gonçalves VF, Silva AM, Baesse CQ, Melo C (2015) Frugivory and potential of birds as dispersers of Siparuna guianensis. Braz J Biol 75:300–304. doi:10.1590/1519-6984.11413

    Article  PubMed  Google Scholar 

  • Google Earth Pro (2016) https://www.google.com/earth/download/gep/agree.html. Accessed Dec 2016

  • Gustafson EJ, Parker GR (1994) Using an index of habitat patch proximity for landscape design. Landsc Urban Plan 29:117–130

    Article  Google Scholar 

  • Herrera JM, García D, Morales JM (2011) Matrix effects on plant-frugivore and plant-predator interactions in forest fragments. Landsc Ecol 26:125–135. https://doi.org/10.1007/s10980-010-9541-7

  • Iacona GD, Kirkman LK, Bruna EM (2010) Effects of resource availability on patterns of seedling recruitment in a fire maintained savanna. Oecologia 163:171–180

    Article  PubMed  Google Scholar 

  • Iacona GD, Kirkman LK, Bruna EM (2012) Experimental test for facilitation of seedling recruitment by the dominant bunchgrass in a fire-maintained savanna. PLoS ONE 7:e39108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelt DA, Meserve PL, Gutierrez JR (2004) Seed removal by small mammals, birds and ants in semi-arid Chile, and comparisons with other systems. J Biogeogr 31:931–942

    Article  Google Scholar 

  • Laurance WF, Ferreira LV, Rankin-de Mérona J, Laurance SG, Hutchings RG, Lovejoy TE (1998) Effects of forest fragmentation on recruitment patterns in Amazonian tree communities. Conserv Biol 12:460–464

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology, 2nd English edn. Elsevier Science BV, Amsterdam, The Netherlands

    Google Scholar 

  • Lombardi JA, Junior M (1993) Seed dispersal of Solanum lycocarpum St. Hil. (Solanaceae) by the maned wolf, Chrysocyon brachyurus Illiger(Mammalia, Canidae). Ciencia e cultura 45:126–127

    Google Scholar 

  • Lorenzi H (2009) Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil 3 ed. Instituto Plantarum de Estudos da Flora

  • Martinson HM, Fagan WF (2014) Trophic disruption: A meta-analysis of how habitat fragmentation affects resource consumption in terrestrial arthropod systems. Ecol Lett 17:1178–1189. https://doi.org/10.1111/ele.12305

  • Melo FPL, Dirzo R, Tabarelli M (2006) Biased seed rain in forest edges: evidence from the Brazilian Atlantic forest. Biol Conserv 132:50–60

    Article  Google Scholar 

  • Mercival RF, Lunardi V, Guimarães PR Jr, Galetti M (2008) Factors affecting seed predation of Eriotheca gracipiles (Bombacaceae) by parakeets in a Cerrado fragment. Acta Oecol Int J Ecol 33:240–245

    Article  Google Scholar 

  • Miranda-Melo AA, Martins FR, Santos FAM (2007) Estrutura populacional de Xylopia aromatica (Lam.) Mart. e de Roupala montana Aubl. em fragmentos de cerrado no Estado de São Paulo. Rev Bras Bot 30:501–507

    Article  Google Scholar 

  • Moles AT, Warton DI, Westoby M (2003) Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 84:3148–3161

    Article  Google Scholar 

  • Motzke I, Tscharntke T, Sodhi NS, Klein AM, Wanger TC (2013) Ant seed predation, pesticide applications and farmers’ income from tropical multi-cropping gardens. Agric For Entomol 15:245–254. doi:10.1111/afe.12011

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Myster RW (2004) Regeneration filters in post-agricultural fields of Puerto Rico and Ecuador. Plant Ecol 172:199–209

    Article  Google Scholar 

  • Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120

    Chapter  Google Scholar 

  • Ordóñez JL, Retana J (2004) Early reduction of post-fire recruitment of Pinus nigra by post-dispersal seed predation in different time-since-fire habitats. Ecography 27:449–458

    Article  Google Scholar 

  • Perez EM, Bulla L (2000) Dietary relationships among four granivorous doves in Venezuelan savannas. J Trop Ecol 16:865–882

    Article  Google Scholar 

  • Pinto LVA, da Silva EAA, Davide AC, Mendes V, Toorop PE, Hilhorst HWM (2007) Mechanism and control of Solanum lycocarpum seed germination. Ann Bot 100:1175–1187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pirk GI, Lopez de Casenave J (2010) Influence of seed size on feeding preference and diet composition of three sympatric harvester ants in the central Monte Desert, Argentina. Ecol Restor 25:439–445

    Article  Google Scholar 

  • Prevedello JA, Vieira MV (2010) Plantation rows as dispersal routes: a test with didelphid marsupials in the Atlantic Forest, Brazil. Biol Conserv 143:131–135. https://doi.org/10.1016/j.biocon.2009.09.016

  • Pufal G, Klein AM (2013) Post-dispersal seed predation of three grassland species in a plant diversity experiment. J Plant Ecol 6:468–479

    Article  Google Scholar 

  • R Core Team (2016). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rey PJ, Garrido JL, Alcántara JM, Ramírez JM, Aguilera A, García L, Manzaneda AJ, Fernández R (2002) Spatial variation in ant and rodent post-dispersal seeds of vertebrate-dispersed predation. Funct Ecol 16:773–781

    Article  Google Scholar 

  • Santos SWM, Silva-Mann R, Ferreira RA, Arrigoni-Blank MF, Fitzgerald AB, Melo JCP (2009) Morphology of fruits, flowers and seeds of pau-pombo (Tapirira guianensis Aublet—Anacardiaceae) in São Cristóvão, SE, Brazil. Sci For 37:47–54

    Google Scholar 

  • Silva LE, Reis RA, Moura EA, Amararal W, Sousa Jr, PT (2015) Plantas do Gênero Xylopia: Composição Química e Potencial Farmacológico. Revista Brasileira de Plantas Medicinais, 17:814–826. https://dx.doi.org/10.1590/1983-084X/14_076

  • Suazo AA, Craig DJ, Vanier CH, Abella SR (2013) Seed removal patterns in burned and unburned desert habitats: Implications for ecological restoration. J Arid Environ 88:165–174

    Article  Google Scholar 

  • Sunyer P, Muñoz A, Bonal R, Espelta JM (2013) The ecology of seed dispersal by small rodents: A role for predator and conspecific scents. Funct Ecol 27: 1313–1321. https://doi.org/10.1111/1365-2435.12143

  • Terborgh J (1992) Maintenance of diversity in tropical forests. Biotropica 24:283–292

    Article  Google Scholar 

  • Tewksbury JJ, Levey DJ, Haddad NM, Sargent S, Orrock JL, Weldon A, Danielson BJ, Brinkerhoff J, Damschen EI, Townsend P (2002) Corridors affect plants, animals, and their interactions in fragmented landscapes. Proc Nat Acad Sci USA 99:12923–12926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valentini CMA, Rodríguez-Ortíz CE, Coelho MFB (2010) Siparuna guianensis Aublet (negramina): Uma revisão. Rev Bras Plantas Med 12:96–104

    Article  Google Scholar 

  • Vander Wall SB, Longland WS (2004) Diplochory: are two seed dispersers better than one? Trends Ecol Evol 19:155–161. https://doi.org/10.1016/j.tree.2003.12.004

  • Vander Wall SB, Kuhn KM, Beck MJ (2005) Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806

    Article  Google Scholar 

  • Vasconcelos PB, Araujo GM, Bruna EM (2014) The role of roadsides in conserving Cerrado plant diversity. Biodivers Conserv 23:3035–3050

    Article  Google Scholar 

  • Viani RAG, Vidas NM, Pardib MM, Vásquez DCC, Gusson E, Brancalion PHS (2015) Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration plantations. Nat Conserv 13:41–46. doi:10.1016/j.ncon.2015.03.005

    Article  Google Scholar 

  • Vié J, Hilton-Taylor C, Stuart SN (2009) Wildlife in a changing world—an analysis of the 2008 IUCN red list of threatened species. IUCN, Gland, Switzerland, p 180

    Google Scholar 

Download references

Acknowledgements

We thank the anonymous reviewers for comments on the manuscript and for assistance in the field. E. M. B. and M. R. O. were supported by the CAPES Special Visiting Researcher Fellowship Program (Grant AUXPE-PVE-0205/2013). H. L. V. was supported by Grants from the Brazilian Council of Research and Scientific Development (CNPq Grants 403733/2012-0 and 302588/2015-9).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maya Rocha-Ortega.

Additional information

Communicated by Miguel Franco.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 305 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rocha-Ortega, M., Bartimachi, A., Neves, J. et al. Seed removal patterns of pioneer trees in an agricultural landscape. Plant Ecol 218, 737–748 (2017). https://doi.org/10.1007/s11258-017-0725-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-017-0725-y

Keywords

Navigation