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Tree density-dependence effects on seed dispersal of a large-seeded tropical tree

Published online by Cambridge University Press:  13 April 2023

Fernanda Cristina Souza ,
Arleu Barbosa Viana-Junior ,
Pedro Uchoa Mittelman  and
Fernando Cesar Cascelli de Azevedo Open the ORCID record for Fernando Cesar Cascelli de Azevedo [Opens in a new window]
Fernanda Cristina Souza
Affiliation:
Programa de Pós-Graduação em Ecologia, Conservação e Manejo da Vida Silvestre, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil Departamento de Ecologia e Conservação, Instituto de Ciências Naturais, Universidade Federal de Lavras, Lavras, Minas Gerais, Brazil
Arleu Barbosa Viana-Junior
Affiliation:
Programa de Pós-graduação em Biodiversidade e Evolução, Laboratório de Ecologia de Invertebrados, Coordenação de Zoologia, Museu Paraense Emílio Goeldi, Belém, Pará, Brazil
Pedro Uchoa Mittelman
Affiliation:
Wildlife Sciences, University of Goettingen, Goettingen, Germany
Fernando Cesar Cascelli de Azevedo*
Affiliation:
Departamento de Ciências Naturais, Universidade Federal de São João del Rei, São João del Rei, Brazil Instituto Pró-Carnívoros, Atibaia, São Paulo, Brazil
*
Author for correspondence: Fernando Cesar Cascelli de Azevedo, Email: fazevedo@ufsj.edu.br
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Abstract

One of the biggest issues in plant ecology is determining the interaction outcome between seeds and scatter-hoarding rodents because the latter has a dual role as dispersers and predators of seeds. Density-dependence contexts involving resource abundance largely influence the outcome of this interaction. Here, we investigated how the variation in the density of a large-seeded tropical tree (Joannesia princeps Vell) affects its probability of seed removal, consumption, dispersal, and burial by a neotropical rodent (Dasyprocta azarae Lichtenstein). We tested whether the elevated resource availability in high tree density areas would cause scatter hoarder’s satiation by decreasing seed removal and consumption (predator satiation hypothesis) or increasing seed dispersal and burial (predator dispersal hypothesis). We tracked the fate of 461 seeds in 14 plots with distinct J. princeps abundances inside a large Atlantic Forest fragment. We used spool-and-line tracking and camera trappings to determine seed fate and identify interacting animals. Agouti was the only species removing J. princeps seeds. Tree density benefitted J. princeps by increasing seed dispersal through buried seed but not affecting seed removal and consumption. This result shows how density-dependent contexts, such as tree density, may alter seed fate in seed–rodent interactions supporting future studies aiming to reestablishing seed dispersal functions in Atlantic Forest fragments.

Keywords

Mutualismpredator dispersal hypothesisseed predationseed burialtropical forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 39 , 2024 , e17
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Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Bogdziewicz, M, Crone, EE and Zwolak, R (2020) Do benefits of seed dispersal and caching by scatterhoarders outweigh the costs of predation? An example with oaks and yellow-necked mice. Journal of Ecology 108, 1009–1018.CrossRefGoogle Scholar
Carvalho, PER (2005) Boleira: Taxonomia e nomenclatura. In Vencato, MF (eds), Circular Técnica. Paraná, Brasil: Embrapa Florestas, pp. 1–9.Google Scholar
Catzeflis, F, Patton, J, Percequillo, A and Weksler, M (2016) Dasyprocta azarae. The IUCN Red List of Threatened Species 2016: e. T6278A22198654. https://www.iucnredlist.org/species/6278/22198654 (accessed 1 June 2022).Google Scholar
Cid, B, Figueira, L, Mello, TAF, Pires, AS and Fernandez, FAS (2014) Short-Term success in the reintroduction of the red-humped agouti Dasyprocta leporina, an important seed disperser, in a Brazilian Atlantic Forest Reserve. Tropical Conservation Science 7, 796–810.CrossRefGoogle Scholar
Comita, LS, Queenborough, SA, Murphy, SJ, Eck, JL, Xu, K, Krishnadas, M, Beckman, N and Zhu, Y (2014) Testing predictions of the Janzen–Connell hypothesis: a meta-analysis of experimental evidence for distance-and density-dependent seed and seedling survival. Journal of Ecology 102, 845–856.CrossRefGoogle ScholarPubMed
Donatti, CI, Guimarães, PR and Galetti, M (2009) Seed dispersal and predation in the endemic Atlantic rainforest palm Astrocaryum aculeatissimum across a gradient of seed disperser abundance. Ecological Research 24, 1187–1195.CrossRefGoogle Scholar
Forget, PM and Wenny, D (2005) How to elucidate seed fate? A review of methods used to study seed removal and secondary seed dispersal. In Forget, PM, Lambert, JE, Hulme, PE and Vander Wall, SB (eds), Seed Fate: Predation, Dispersal and Seedling Establishment. Wallingford: CABI Publishing, pp. 379–393.CrossRefGoogle Scholar
Galetti, M, Brocardo, CR, Begotti, RA, Hortenci, L, Rocha-Mendes, F, Bernardo, CSS, Bueno, RS, Nobre, R, Bovendorp, RS, Marques, RM, Meirelles, F, Gobbo, SK, Beca, G, Schmaedecke, G and Siqueira, T (2017) Defaunation and Biomass collapse of mammals in the largest atlantic forest remnant. Animal Conservation 20, 270–281.CrossRefGoogle Scholar
Gomez, JM, Schupp, EW and Jordano, P (2019) Synzoochory: the ecological and evolutionary relevance of a dual interaction. Biological Reviews 94, 874–890 CrossRefGoogle ScholarPubMed
Guimarães, PR, Galetti, M and Jordano, P (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE 3, 1–3.CrossRefGoogle ScholarPubMed
Haugaasen, JMT, Haugaasen, T, Peres, CA, Gribel, R and Wegge, P (2010) Seed dispersal of the Brazil nut tree (Bertholletia excelsa) by scatter-hoarding rodents in a central Amazonian forest. Journal of Tropical Ecology 26, 251–262.CrossRefGoogle Scholar
Hirsch, BT, Kays, R, Pereira, VE and Jansen, PA (2012) Directed seed dispersal towards areas with low conspecific tree density by a scatter-hoarding rodent. Ecology Letters 15, 1423–1429.CrossRefGoogle ScholarPubMed
Jansen, PA and Forget, PM (2001) Scatter hoarding and tree regeneration. In Borges, F, Charles-Dominique, P, Forget, PM and Théry, M (eds), Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest. Dordrecht: Kluwer Academic Publishers, pp. 275–288.CrossRefGoogle Scholar
Jansen, PA, Bongers, F and Hemerik, L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecological Monographs 74, 569–589.CrossRefGoogle Scholar
Jansen, PA, Hirsch, BT, Emsens, WJ, Zamora-Gutierrez, V, Wikelski, M and Kays, R (2012) Thieving rodents as substitute dispersers of megafaunal seeds. Proceedings of the National Academy of Sciences of the United States of America 109, 12610–12615.CrossRefGoogle ScholarPubMed
Jansen, PA, Visser, MD, Wright, JS, Rutten, G and Muller-Landau, HC (2014) Negative density dependence of seed dispersal and seedling recruitment in a Neotropical palm. Ecology Letters 17, 1111–1120.CrossRefGoogle Scholar
Jones, FA and Comita, LS (2010) Density-dependent pre-dispersal seed predation and fruit set in a tropical tree. Oikos 119, 1841–1847.CrossRefGoogle Scholar
Kelly, D and Sork, VL (2002) Mast seeding in perennial plants: Why, how, where? Annual Review of Ecology and Systematics 33, 427–447.CrossRefGoogle Scholar
Kuprewicz, EK (2015) Scatter hoarding of seeds confers survival advantages and disadvantages to large-seeded tropical plants at different life stages. PLoS One 10, 1–16 CrossRefGoogle ScholarPubMed
Li, H and Zhang, Z (2007) Effects of mast seeding and rodent abundance on seed predation and dispersal by rodents in Prunus armeniaca (Rosaceae). Forest Ecology and Management 242, 511–517.CrossRefGoogle Scholar
Lichti, NI, Steele, MA and Swihart, RK (2017) Seed fate and decision-making processes in scatter-hoarding rodents. Biological reviews of the Cambridge Philosophical Society 92, 474–504.CrossRefGoogle ScholarPubMed
Lopes, WP, Silva, AF, Souza, AL and Meira Neto, JAA (2002) Estrutura fitossocióloga de um trecho de vegetação arbórea no Parque Estadual do Rio Doce - Minas Gerais, Brasil. Acta Botanica Brasilica 16, 443–456.CrossRefGoogle Scholar
Lorenzi, H (1998) Árvores brasileiras: Manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Brasil: Plantarum, Nova Odessa.Google Scholar
Mittelman, P, Kreischer, C, Pires, AS and Fernandez, FAS (2020) Agouti reintroduction recovers seed dispersal of a large-seeded tropical tree. Biotropica 52, 766–774.CrossRefGoogle Scholar
Mittelman, P, Dracxler, CM, Santos-Coutinho, PRO and Pires, AS (2021a) Sowing forests: a synthesis of seed dispersal and predation by agoutis and their influence on plant communities. Biological Reviews 96, 2425–2445.CrossRefGoogle ScholarPubMed
Mittelman, P, Pires, AS and Fernandez, FAS (2021b) The intermediate dispersal hypothesis: seed dispersal is maximized in areas with intermediate usage by hoarders. Plant Ecology 222, 221–231.CrossRefGoogle Scholar
Moore, CM and Dittel, JW (2020) On mutualism, models, and masting: The effects of seed-dispersing animals on the plants they disperse. Journal of Ecology 108, 1775–1783.CrossRefGoogle Scholar
Moore, JE, McEuen, AB, Swihart, RK, Contreras, TA and Steele, MA (2007) Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests. Ecology 88, 2529–2540.CrossRefGoogle ScholarPubMed
Oliveira, BR, Carvalho-Ribeiro, SM and Maia-Barbosa, PM (2020) A multiscale analysis of land use dynamics in the buffer zone of Rio Doce State Park, Minas Gerais, Brazil. Journal of Environmental Planning and Management 63, 935–957.CrossRefGoogle Scholar
R Core Team (2022) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Ribeiro, MC, Metzger, JP, Martensen, AC, Ponzoni, F and Hirota, M (2009) Brazilian Atlantic Forest: how much is left and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142, 1141–1153.CrossRefGoogle Scholar
Silvertown, JW (1980) The evolutionary ecology of mast seeding in trees. Biological Journal of the Linnean Society 14, 235–250.CrossRefGoogle Scholar
Silvius, KM and Fragoso, JMV (2003) Red-rumped agouti (Dasyprocta leporina) home range use in an Amazonian forest: implications for the aggregated distribution of forest trees. Biotropica 35, 74–83.Google Scholar
Smythe, N (1978) The natural history of the Central American agouti (Dasyprocta punctata). Smithsonian Contributions to Zoology, 257, 1–52 CrossRefGoogle Scholar
Stallings, JR, Fonseca, GAB, Pinto, LPS, Aguiar, LMS and Sábato, EL (1990) Mamíferos do Parque Florestal Estadual do Rio Doce, Minas Gerais, Brasil. Revista Brasileira de Zoologia 7, 663–677.CrossRefGoogle Scholar
Vander Wall, SB (2002) Masting in animal-dispersed pines facilitates seed dispersal. Ecology 83, 3508–3516.CrossRefGoogle Scholar
Vieira, EM, Ribeiro, JF and Iob, G (2011) Seed predation of Araucaria angustifolia (Araucariaceae) by small rodents in two areas with contrasting seed densities in the Brazilian Araucaria forest. Journal of Natural History 45, 843–854.CrossRefGoogle Scholar
Visser, MD, Muller-Landau, HC, Wright, SJ, Rutten, G and Jansen, PA (2011). Tri-trophic interactions affect density dependence of seed fate in a tropical forest palm. Ecology Letters 14, 1093–1100.CrossRefGoogle Scholar
Wang, B (2020) Seed density affects post-dispersal seed predation: evidence from a seed removal experiment of 62 species. Integrative Zoology 15, 135–143.CrossRefGoogle ScholarPubMed
Xiao, Z and Huang, X (2020) How seed defense and seed abundance predict dispersal and survival patterns in Camellia. Integrative Zoology 15, 103–114.CrossRefGoogle ScholarPubMed
Xiao, Z, Zhang, Z and Krebs, CJ (2013) Long-term seed survival and dispersal dynamics in a rodent-dispersed tree: testing the predator satiation hypothesis and the predator dispersal hypothesis. Journal of Ecology 101, 1256–1264.CrossRefGoogle Scholar
Zwolak, R, Bogdziewicz, M, Wróbel, A and Crone, EE (2016) Advantages of masting in European beech: timing of granivore satiation and benefits of seed caching support the predator dispersal hypothesis. Oecologia 180, 749–758.CrossRefGoogle ScholarPubMed
Zwolak, R and Crone, EE (2012) Quantifying the outcome of plant-granivore interactions. Oikos 121, 20–27.CrossRefGoogle Scholar
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