Biological Invasions

, Volume 20, Issue 11, pp 3055–3068 | Cite as

Combined impacts of multiple non-native mammals on two life stages of a critically endangered Neotropical tree

  • Francisco V. DénesEmail author
  • José L. Tella
  • Viviane Zulian
  • Nêmora P. Prestes
  • Jaime Martínez
  • Fernando Hiraldo
Original Paper


Despite of the widespread co-occurrence of multiple invaders, little is known on their combined ecological impacts and on their effects on different life stages of native species. We assessed the joint impacts of four non-native mammals (cattle, horse, European hare Lepus europaeus, and wild boar Sus scrofa) on seed surplus and seedling abundance of the Paraná pine (Araucaria angustifolia), a critically-endangered species of the Atlantic Forest. We found that its seeds constitute an autumn food resource for a native community richer than previously thought, with 70 bird and mammal species as confirmed or potential seed consumers, of which 40 were not previously recognized as such. We also recorded the number of uneaten seeds and seedlings at the middle-end of autumn under 520 female Paraná pine trees across the species’ distribution and identified signs of the species consuming seeds from each tree through direct observations combined with camera trapping. Most of the sampled trees (98%) were visited by at least one seed consumer species, and over 60% were visited by at least one non-native mammal. Seed surplus strongly declined in the presence of cattle, horses and wild boars, their impacts being additive, whereas the number of seedlings declined in the presence of European hares. Our results emphasize the importance of Paraná pine seeds for native fauna and the additive impact of invaders in a species-rich ecosystem. Seed predation by non-native species reduces the potential regeneration of Paraná pine forests, and may severely reduce food supply for its native consumers.


Araucaria angustifolia Exotic species Invasion ecology Invasive species Keystone species Life stages Seed predation 



We thank G. Ferraz and managers and staff of Estação Ecológica de Aracuri-Esmeralda, Floresta Nacional de São Francisco de Paula and Centro de Pesquisas e Conservação da Natureza Pró-Mata (PUC-RS). We are grateful to James Russell, and an anonymous reviewer for their helpful comments and suggestions. We also thank Andrew Crosby for the English review. Funds were provided by Fundación Repsol. F.V.D. was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (206107/2014-5). N.P. and J.M. thank the Fundação Grupo Boticário de Proteção à Natureza for financial support of long-term work on parrots in southern Brazil.

Data accessibility

The dataset with seed and seedling counts and covariates for all observations, and the analysis R code file are uploaded as online supporting information.

Author’s contributions

FH, FVD and JLT designed the work; FH, FVD, JLT, VZ, NM and JM conducted field work; FVD and JLT analysed the data; FVD led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Supplementary material

10530_2018_1758_MOESM1_ESM.docx (3.8 mb)
Supplementary material 1 (DOCX 3868 kb)
10530_2018_1758_MOESM2_ESM.csv (24 kb)
Appendix S2 CSV dataset with seed and seedling counts and covariates used in modeling analysis (CSV 23 kb)
10530_2018_1758_MOESM3_ESM.docx (20 kb)
Supplementary material 3 (DOCX 20 kb)


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Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Conservation BiologyEstación Biológica de Doñana, CSICSevilleSpain
  2. 2.Departamento de EcologiaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  3. 3.Instituto de Ciências BiológicasUniversidade de Passo FundoPasso FundoBrazil
  4. 4.Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada

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