Abstract
Seed predation and seed dispersal are key factors that determine plant recruitment. In this study, we compared the role of small (<200 g) and ‘large’ mammals as predators of Araucaria angustifolia (Araucariaceae) seeds in the Brazilian Araucaria Forest. We also investigated the effect of deposition site, namely open grassland, forest edge or forest interior (>50 m from the edge) on seed-removal rates. We conducted field experiments on seed removal in July 2003 and 2004. We compared the habitat types using two exclusion treatments: semi-permeable exclosure (exclusive access of small rodents) and an open control (access of all mammal groups). We considered proportion of seeds removed after 15 days to investigate the effect of year, habitat type, and exclusion treatment on seed removal by using three-factor permutational ANOVA. We also evaluated seed fate and seed consumers by using spool-and-line devices attached to seeds and camera trapping. The results showed that seed removal differed significantly between years and among habitat types, but not between exclusion treatments. Removal rates were higher in 2004 than in 2003 and also were significantly lower in the open field when compared with both forested types (edge or interior) in both years. There was also a significant interaction between ‘year’ and ‘habitat’ which was driven by an increase in 2004 removal rates in the open field compared to the previous year. Our combination of manipulative experiments, camera-trapping survey, and spool-and-line seed tracking demonstrated that small rodents are responsible for the majority of seed removal of A. angustifolia in the study area. The low removal rates in open habitats indicate that they could serve as safe sites for A. angustifolia seeds. The results also suggested a potential role of small rodents as seed dispersers (about 4% of removed seeds were not consumed). The knowledge of how fragmentation affects pattern of seed predation and establishment of A. angustifolia through changes in abundance of different-sized mammals is essential for the conservation of the Brazilian Araucaria Forest and its most characteristic species.
Similar content being viewed by others
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46
Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand
Anderson MJ, ter Braak CJF (2003) Permutation tests for multi-factorial analysis of variance. J Stat Comp Simul 73:85–113
Andresen E, Levey DJ (2004) Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:45–54
Anjos L (1991) O ciclo anual de Cyanocorax caeruleus em Floresta de Araucária (Passeriformes: Corvidae). Ararajuba 2:19–23
Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps and pathogens. Ecology 65:1705–1712
Backes A (1999) Condicionamento climático e distribuição geográfica de Araucaria angustifolia (Bert.) O. Ktze no Brasil—II. Pesq Bot 49:31–51
Backes A (2001) Determinação da idade e regeneração natural de uma população de Araucaria angustifolia (Bertol.) Kuntze em um povoamento florestal localizado no município de Caxias do Sul, RS, Brasil. Iheringhia Ser Bot 56:115–130
Baldissera R, Ganade G (2005) Predação de sementes ao longo de uma borda de Floresta Ombrófila Mista e pastagem. Acta Bot Bras 19:161–165
Beck H (2006) A review of peccary-palm interactions and their ecological ramifications across the Neotropics. J Mammal 87:519–530
Bordignon M, Monteiro-Filho ELA (2000) O serelepe Sciurus ingrami (Sciuridae: Rodentia) como dispersor do Pinheiro do Paraná (Araucaria angustifolia) (Araucariaceae: Pinophyta). Arq Ciên Vet Zool 3:139–144
Brewer SW (2001) Predation and dispersal of large and small seeds of a tropical palm. Oikos 92:245–255
Brewer SW, Rejmánek M (1999) Small rodents as significant dispersers of tree seeds in a neotropical forest. J Veg Sci 10:165–174
Briani DC, Vieira EM, Vieira MV (2001) Nests and nesting sites of Brazilian forest rodents (Nectomys squamipes and Oryzomys intermedius) as revealed by a spool-and-line device. Acta Theriol 46:331–334
Burkey TV (1993) Edge effects in seed and egg predation at two neotropical rain forest sites. Biol Conserv 66:139–143
Cerqueira R, Gentile R, Fernandez FAS, D’Andrea PS (1993) A five-year population study of an assemblage of small mammals in southeastern Brazil. Mammalia 57:507–517
Cerveira J (2005) Mamíferos silvestres de médio e grande porte no planalto meridional: suas relações com a fragmentação da paisagem e a presença do gado. Dissertation, Universidade Federal do Rio Grande do Sul, Brazil
Chapman CA, Chapman LJ (1995) Survival without dispersers: seedling recruitment under parents. Conserv Biol 9:675–678
Cordeiro NJ, Howe HF (2001) Low recruitment of trees dispersed by animals in African forest fragments. Conserv Biol 15:1733–1741
Cullen L, Bodmer RE, Valladares-Pádua C (2000) Effects of hunting in habitat fragments of the Atlantic forest, Brazil. Biol Conserv 95:49–56
Dalby PL (1975) Biology of pampa rodents in the Balcarce Area, Argentina. Pub Mus Michigan State Univ 5:149–272
Dalmagro AD, Vieira EM (2005) Patterns of habitat utilization of small rodents in an area of Araucaria forest in Southern Brazil. Aust Ecol 30:353–362
DeMattia EA, Curran LM, Rathcke BJ (2004) Effects of small rodents and large mammals on neotropical seeds. Ecology 85:2161–2170
DeMattia EA, Rathcke BJ, Curran LM, Aguilar R, Vargas O (2006) Effects of small rodent and large mammal exclusion on seedling recruitment in Costa Rica. Biotropica 38:196–202
Díaz I, Papic C, Armesto JJ (1999) An assessment of post-dispersal seed predation in temperate rain forest fragments in Chiloé Island, Chile. Oikos 87:228–238
Donoso DS, Grez AA, Simonetti JA (2003) Effects of forest fragmentation on the granivory of differently sized seeds. Biol Conserv 115:63–70
Duarte LS, Dillenburg LR (2000) Ecophysiological responses of Araucaria angustifolia (Araucariaceae) seedlings to different irradiance levels. Aust J Bot 48:531–537
Duarte LS, Dillenburg LR, Rosa LMG (2002) Assessing the role of light availability in the regeneration of Araucaria angustifolia (Araucariaceae). Aust J Bot 50:741–751
Edwards GR, Crawley MJ (1999) Rodent seed predation and seedling recruitment in mesic grassland. Oecologia 118:288–296
Erb J, Boyce MS, Stenseth NC (2001) Population dynamics of large and small mammals. Oikos 92:3–12
Fagan WE, Cantrell RS, Cosner C (1999) How habitat edges change species interactions. Am Nat 153:165–182
Ferreira AG, Handro W (1979) Aspects of seed germination in Araucaria angustifolia. Rev Bras Bot 2:7–13
Fleury M, Galetti M (2006) Forest fragment size and microhabitat effects on palm seed predation. Biol Conserv 131:1–13
Forget P-M (1990) Seed-dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. J Trop Ecol 6:459–468
Forget P-M (1993) Post-dispersal predation and scatterhoarding of Dipteryx panamensis (Papilionaceae) seeds by rodents in Panama. Oecologia 94:255–261
Forget P-M (1994) Recruitment pattern of Vouacapoua americana (Caesalpiniaceae), a rodent-dispersed tree species in French Guiana. Biotropica 26:408–419
Forget P-M (1997) Effect of microhabitat on seed fate and seedling performance in two rodent-dispersed tree species in rain forest in French Guiana. J Ecol 85:693–703
Forget P-M, Milleron T, Feer F (1998) Patterns in post-dispersal seed removal by neotropical rodents and seed fate in relation with seed size. In: Newberry DM, Prins HHT, Brown ND (eds) Dynamics of tropical communities. Blackwell Science, Oxford
Forget P-M, Kitajima K, Foster RB (1999) Pre and post-dispersal seed predation in Tachigali versicolor (Caesalpiniaceae): effects of timing of fruiting and variation among trees. J Trop Ecol 15:61–81
Fragoso JMV, Silvius KM, Correa JA (2003) Long-distance seed dispersal by tapirs increases seed survival and aggregates tropical trees. Ecology 84:1998–2006
Galetti M, Donatti CI, Pires AS, Guimarães PR Jr, Jordano P (2006) Seed survival and dispersal of an endemic Atlantic forest palm: the combined effects of defaunation and forest fragmentation. Bot J Linn Soc 151:141–149
Guerra MP, Silveira V, Reis MS, Schneider L (2002) Exploração, manejo e conservação da araucária (Araucaria angustifolia). In: Simões LL, Lino CF (eds) Sustentável Mata Atlântica: a exploração de seus recursos florestais. Senac, São Paulo, Brazil
Guglielme I, Ganade G (2006) Predação de sementes afetando a distribuição de indivíduos de Araucaria angustifolia ao longo de uma borda de floresta com campo. Neot Biol Conserv 1:62–71
Guimarães PR Jr, Lopes PFM, Lyra ML, Muriel AP (2005) Fleshy pulp enhances the location of Syagrus romanzoffiana (Arecaceae) fruits by seed-dispersing rodents in an atlantic forest in southeastern Brazil. J Trop Ecol 21:109–112
Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Plant Ecol Evol Syst 1:46–60
Inoue MT, Galvão F, Torres DV (1979) Estudo ecofisiológico sobre Araucaria angustifolia (Bert.) O. Ktze.: fotossíntese em dependência da luz no estágio juvenil. Rev Florest 10:5–9
Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 101:501–528
Janzen DH (1971) Seed predation by animals. Ann Rev Ecol Syst 2:465–492
Jansen PA, Bongers F, Hemerik L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodents. Ecol Monogr 74:569–589
Kelt DA, Meserve PL, Forister ML, Nabors LK, Gutiérrez JR (2004) Seed predation by birds and small mammals in semiarid Chile. Oikos 104:133–141
Kindel EAI (1996) Padrões de dispersão e disposição espacial de Araucaria angustifolia (Bert.) O. Ktze. e suas relações com aves e pequenos mamíferos na Estação Ecológica de Aracuri, Esmeralda, RS. Dissertation, Universidade Federal do Rio Grande do Sul, Brazil
Klein RM (1960) O aspecto dinâmico do pinheiro brasileiro. Sellowia 12:17–44
Kollmann J, Buschor M (2002) Edge effects on seed predation by rodents in deciduous forests of northern Switzerland. Plant Ecol 164:249–261
Köppen W (1948) Climatologia. Fondo Cultura Econômica, Mexico City
Lamberts AVDH (2003) Predação e sobrevivência de sementes de Araucaria angustifolia (Bert.) Kuntze em matas nativas e plantação de Pinus eliotti na Floresta Nacional de São Francisco de Paula, RS. Dissertation, Universidade Estadual de Campinas, Brazil
Laurance WF, Bierregard RO Jr (1997) Tropical forest remnants: ecology, management, and conservation of fragmented communities. The University of Chicago Press, Chicago
Lidicker WZ Jr (1999) Responses of mammals to habitat edges: an overview. Land Ecol 14:333–343
Lott RH, Harrington GN, Irvine AK, McIntyre S (1995) Density-dependent seed predation and plant dispersion of the tropical palm Normambya normambyi. Biotropica 27:87–95
Magnusson WE, Sanaiotti TM (1987) Dispersal of Miconia Seeds by the rat Bolomys Lasiurus. J Trop Ecol 3:277–278
Mähler JKF Jr, Schneider M (2003) Ungulados. In: Fontana CS, Bencke GA, Reis RE (eds) Livro vermelho da fauna ameaçada de extinção no Rio Grande do Sul. Edipucrs. Porto Alegre, Brazil
Mantovani A, Morellato PC, dos Reis MS (2004) Fenologia reprodutiva e produção de sementes em Araucaria angustifolia (Bert.) O. Kuntze. Rev Bras Bot 27:787–796
Mattos JR (1994) O pinheiro brasileiro. Artes Gráficas Princesa, São Paulo, Brasil
Murcia C (1995) Edge effects in fragmented forest: implications for conservation. TREE 10:58–62
O’Connell MA (1989) Population dynamics of neotropical small mammals in seasonal habitats. J Mammal 70:532–548
Oliveira JM, Pillar VD (2004) Vegetation dynamics on mosaics of campos and Araucaria forest between 1974 and 1999 in southern Brazil. Commun Ecol 5:197–202
Ostfeld RS, Manson RH, Canham CD (1997) Effects of rodents on survival of tree seeds and seedlings invading old fields. Ecology 78:1531–1542
Paise G, Vieira EM (2005) Produção de frutos e distribuição espacial de angiospermas com frutos zoocóricos em uma Floresta Ombrófila Mista no Rio Grande do Sul, Brasil. Rev Bras Bot 28:615–625
Paise G, Vieira EM (2006) Daily activity of a neotropical rodent (Oxymycterus nasutus): seasonal changes and influence of environmental factors. J Mammal 87:733–739
Pardini R (2004) Effects of forest fragmentation on small mammals in an Atlantic Forest landscape. Biodiv Conserv 13:2567–2586
Pedó E (2005) Assembléia de pequenos mamíferos não-voadores em áreas de ecótono campo-floresta com Araucária na região dos Campos de Cima da Serra, RS. Dissertation, Universidade Federal do Rio Grande do Sul, Brazil
Pimentel DS, Tabarelli M (2004) Seed dispersal of the palm Attalea oleifera in a remnant of the Brazilian Atlantic Forest. Biotropica 36:74–84
Primack RB, Rodrigues E (2001) Biologia da Conservação. Midiograf, Londrina, Brazil
Redford KH (1992) The empty forest. Bioscience 42:412–422
Reitz PR, Klein RM, Reis A (1988) Projeto madeira do Rio Grande do Sul. Superintendência do Desenvolvimento da Região Sul/Herbário Barbosa Rodrigues/Secretaria da Agricultura e Abastecimento, Itajaí, Brazil
Sánchez-Cordero V, Martínez-Gallardo R (1998) Postdispersal fruit and seed removal by forest-dwelling rodents in a lowland rainforest in Mexico. J Trop Ecol 14:139–151
Schupp EW (1988) Factors affecting post-dispersal seed survival in a tropical forest. Oecologia 76:525–530
Schupp EW, Howe HF, Augspurger CK, Levey DJ (1989) Arrival and survival in tropical treefalls gaps. Ecology 70:562–564
Sick H (1984) Ornitologia brasileira: uma introdução. Universidade de Brasília, Brasília
Silman MR, Terborgh J, Kiltie RA (2003) Population regulation of a dominant rain forest tree by a major seed predator. Ecology 84:431–438
Soares RV (1980) Considerações sobre a regeneração natural de Araucaria angustifolia. In: IUFRO Meeting on forestry problems of the genus Araucaria, 1. Forestry problems of the genus Araucaria. FUPEF, Curitiba, Brazil
Solórzano-Filho JA (2001) Demografia, fenologia e ecologia da dispersão de sementes de Araucaria angustifolia em uma população relictual em Campos do Jordão, SP. Dissertation, Universidade de São Paulo, Brazil
Stevens SM, Husband TP (1998) The influence of edge on small mammals: evidence from Brazilian Atlantic forest fragments. Biol Conserv 85:1–8
Terborgh J, Losos E, Riley PM, Bolanos-Riley M (1993) Predation by vertebrates and invertebrates on the seeds of five canopy tree species of an Amazonian forest. Vegetatio 107/108:375–386
Vander Wall SB (2002) Masting in animal-dispersed pines facilitates seed dispersal. Ecology 83:3508–3516
Vieira EM, Pizo MA, Izar P (2003) Fruit and seed exploitation by small rodents of the Brazilian Atlantic forest. Mammalia 67:533–539
Vieira EM, Iob G, Becker RG (2004) Mammals of the Araucaria forest. In: Dutra TL (ed) Geological and biological aspects from a transect between the eastern part of southern Brazilian plateau and the coastal plain of Rio Grande do Sul, Brazil: from the subtropical rainforest with Araucaria angustifolia to coastal peat bogs. Unisinos, São Leopoldo, Brazil
Vieira EM, Paise G, Machado PHD (2006) Feeding of small rodents on seeds and fruits: a comparative analysis of three rodent species of the Araucaria forest, southern Brazil. Acta Theriol 51:311–318
Wang BC, Smith TB (2002) Closing the seed dispersal loop. TREE 17:379–385
Willson MF, Whelan CJ (1990) Variation in postdispersal survival of vertebrate-dispersed seeds: effects of density, habitat, location, season and species. Oikos 57:191–198
Wolff JO (1996) Population fluctuations of mast-eating rodents are correlated with production of acorns. J Mammal 77:850–856
Wright SJ, Zeballos H, Dominguez I, Gallardo MM, Moreno MC, Ibanez R (2000) Poachers alter mammal abundance, seed dispersal, and seed predation in a neotropical forest. Conserv Biol 14:227–239
Zanini L, Ganade G (2005) Restoration of Araucaria forest: the role of perches, pioneer vegetation, and soil fertility. Rest Ecol 13:507–514
Acknowledgments
We are grateful to R. Mello and B. Blochtein for the authorization and support to our fieldwork in the Pró-Mata and to two anonymous reviewers for helpful suggestions on earlier drafts of this article. We thank T. P. Wilberger, G. J. Hauschid, C. Azambuja, and M. Sayão for their help in the fieldwork. We are also grateful to the entire Pró-Mata staff, especially to Cleonir, for their hospitality and help. This study was supported by the Fundação O Boticário de Proteção a Natureza (process number: 0567/20022) and UNISINOS. While conducting this research work EMV received a personal research grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (306347/2004-0).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Iob, G., Vieira, E.M. Seed predation of Araucaria angustifolia (Araucariaceae) in the Brazilian Araucaria Forest: influence of deposition site and comparative role of small and ‘large’ mammals. Plant Ecol 198, 185–196 (2008). https://doi.org/10.1007/s11258-007-9394-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-007-9394-6