Abstract
Seed dispersal and predation are paramount for tropical plant diversity. When encountered by scatter-hoarding frugivores, seeds can be either eaten, dispersed or ignored. But even after dispersal, seed caches are still subjected to predation. Many factors are known to influence these dynamics; however, how frequently hoarders use certain patches has seldom been related to cache predation rates. We used the interaction between agoutis (Dasyprocta leporina), a scatter-hoarding rodent, and Joannesia princeps, a tropical tree, as a model to investigate how the number of visits by hoarders in certain areas influences cache predation and seed fate. Camera-traps were used for 30 days in twenty different locations in Tijuca National Park to assess number of visits by agoutis. Thereafter, we placed seed piles on the same areas and determined their fate using the spool-and-line method to track seeds for over one hundred days. We found a non-linear relationship between how often an area is used by hoarders and the final proportion of dispersed seeds. At areas with a low number of visits, proportion of dispersed seeds was low due to low removal. As frequency of visits by hoarders increased, seed removal and the number of dispersal events increased but so did cache predation. Thus, in areas intensively used by hoarders, high cache predation resulted in a low number of dispersed seeds that remained alive in caches. As a result, dispersal was maximized in areas with intermediate use by scatter-hoarders, where there was a balance between primary seed dispersal and cache predation.
Similar content being viewed by others
Data Availability
Data and code used in this study are archived at GitHub Repository (https://github.com/Pedro-Mittelman/Seed_Fate_and_Agouti_Space_Use).
References
Aliyu B, Thia JA, Moltchanova E, Forget P-M, Chapman HM (2018) Forest disturbance and seasonal food availability influence a conditional seed dispersal mutualism. Biotropica. https://doi.org/10.1111/btp.12570
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. https://doi.org/10.1126/science.1123412
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv Prepr arXiv14065823
Bogdziewicz M, Crone EE, Zwolak R (2019) Do benefits of seed dispersal and caching by scatterhoarders outweigh the costs of predation? An example with oaks and yellow-necked mice. J Ecol. https://doi.org/10.1111/1365-2745.13307
Bolker B, Ben BM (2017) Package ‘bbmle.’ Tools Gen Maximum Likelihood Estim 641:
Cao L, Wang Z, Yan C, Chen J, Guo C, Zhang Z (2016) Differential foraging preferences on seed size by rodents result in higher dispersal success of medium-sized seeds. Ecology 97:3070–3078. https://doi.org/10.1002/ecy.1555
Cao L, Wang B, Yan C, Wang Z, Zhang H, Geng Y, Chen J, Zhang Z (2018) Risk of cache pilferage determines hoarding behavior of rodents and seed fate. Behav Ecol 29:984–991. https://doi.org/10.1093/beheco/ary040
Chaves M, Davide A (1996) Caracterização morfológica de frutos, sementes e plântulas de Joannesia princeps Vell.-Euphorbiaceae.pdf. Rev Bras Sementes 18:208–213
Cid B, Figueira L (2014) Short-term success in the reintroduction of the red- humped agouti Dasyprocta leporina, an important seed disperser, in a Brazilian Atlantic Forest reserve. Trop Conserv Sci 7:796–810. https://doi.org/10.1177/194008291400700415
Dittel JW, Vander Wall SB (2018) Effects of rodent abundance and richness on cache pilfering. Integr Zool 13:331–338. https://doi.org/10.1111/1749-4877.12317
Donatti CI, Guimarães PR, Galetti M (2009) Seed dispersal and predation in the endemic Atlantic rainforest palm Astrocaryum aculeatissimum across a gradient of seed disperser abundance. Ecol Res 24:1187–1195. https://doi.org/10.1007/s11284-009-0601-x
Elwood EC, Lichti NI, Fitzsimmons SF, Dalgleish HJ (2018) Scatterhoarders drive long- and short-term population dynamics of a nut-producing tree, while pre-dispersal seed predators and herbivores have little effect. J Ecol 106:1191–1203. https://doi.org/10.1111/1365-2745.12902
Emmons L, Reid F (2016) Dasyprocta leporina. The IUCN Red List of Threatened Species 2016
Forget P-M, Wenny D (2005) How to elucidate seed fate? A review of methods used to study seed removal and secondary seed dispersal. In: Forget P-M, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate Predation, Dispersal and Seedling Establishment. CABI Publishing, Wallingford, UK, pp 379–393
Forget P-M, Hammond DS, Milleron T, Thomas R (2002) 16 Seasonality of Fruiting and Food Hoarding by Rodents in Neotropical Forests: Consequences for Seed Dispersal and Seedling Recruitment. Seed Dispersal Frugivory Ecol Evol Conserv 241
Galetti M, Donatti CI, Steffler C, Genini J, Bovendorp RS, Fleury M (2010) The role of seed mass on the caching decision by agoutis, Dasyprocta leporina (Rodentia: Agoutidae). Zool 27:472–476. https://doi.org/10.1590/S1984-46702010000300022
Gómez JM, Schupp EW, Jordano P (2018) Synzoochory: the ecological and evolutionary relevance of a dual interaction. Biol Rev. https://doi.org/10.1111/brv.12481
Harrison RD, Tan S, Plotkin JB, Slik F, Detto M, Brenes T, Itoh A, Davies SJ (2013) Consequences of defaunation for a tropical tree community. Ecol Lett 16:687–694. https://doi.org/10.1111/ele.12102
Hartig F (2017) DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R Packag version 01:5
Howe HF, Miriti MN (2004) When Seed Dispersal Matters. Bioscience 54:651–660. https://doi.org/10.1641/0006-3568(2004)054[0651:WSDM]2.0.CO;2
Hulme PE (1994) Post-Dispersal Seed Predation in Grassland: Its Magnitude and Sources of Variation. J Ecol 82:645. https://doi.org/10.2307/2261271
Hulme PE (1998) Post-dispersal seed predation: consequences for plant demography and evolution. Perspect Plant Ecol Evol Syst 1:32–46. https://doi.org/10.1078/1433-8319-00050
Hulme PE (2002) Seed-eaters: Seed Dispersal, Destruction and Demography. In: Seed dispersal and frugivory: Ecology, evolution, and conservation. Woodhead Publishing, p 257
Jansen PA, Bongers F, Hemerik L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecol Monogr 74:569–589. https://doi.org/10.1890/03-4042
Jansen PA, Hirsch BT, Emsens W-J, Zamora-Gutierrez V, Wikelski M, Kays R (2012) Thieving rodents as substitute dispersers of megafaunal seeds. Proc Natl Acad Sci U S A 109:12610–12615. https://doi.org/10.1073/pnas.1205184109
Jansen PA, Visser MD, Joseph Wright S, Rutten G, Muller-Landau HC (2014) Negative density dependence of seed dispersal and seedling recruitment in a Neotropical palm. Ecol Lett 17:1111–1120. https://doi.org/10.1111/ele.12317
Kenup CF, Sepulvida R, Kreischer C, Fernandez FAS (2018) Walking on their own legs: Unassisted population growth of the agouti Dasyprocta leporina, reintroduced to restore seed dispersal in an Atlantic Forest reserve. Oryx 52:571–578. https://doi.org/10.1017/S0030605316001149
Klinger R, Rejmánek M (2010) A strong conditional mutualism limits and enhances seed dispersal and germination of a tropical palm. Oecologia 162:951–963. https://doi.org/10.1007/s00442-009-1542-3
Li H, Zhang Z (2007) Effects of mast seeding and rodent abundance on seed predation and dispersal by rodents in Prunus armeniaca (Rosaceae). For Ecol Manage 242:511–517. https://doi.org/10.1016/j.foreco.2007.01.063
Lichti NI, Steele MA, Swihart RK (2017) Seed fate and decision-making processes in scatter-hoarding rodents. Biol Rev 92:474–504. https://doi.org/10.1111/brv.12240
Longland WS, Jenkins SH, Vander Wall SB, Veech JA, Pyare S (2001) Seedling recruitment in Oryzopsis hymenoides: are desert granivores mutualists or predators? Ecology 82:3131–3148
Marzluff JM, Knick ST, Millspaugh JJ (2001) High-tech behavioral ecology: modeling the distribution of animal activities to better understand wildlife space use and resource selection. In: Radio tracking and animal populations. Elsevier, pp 309–326
Mittelman P, Kreischer C, Pires AS, Fernandez FAS (2020) Agouti reintroduction recovers seed dispersal of a large-seeded tropical tree. Biotropica 52:766–774. https://doi.org/10.1111/btp.12788
Moore JE, Swihart RK (2008) Factors affecting the relationship between seed removal and seed mortality. Can J Zool 806:378–385. https://doi.org/10.1139/Z08-011
Muñoz A, Bonal R (2011) Linking seed dispersal to cache protection strategies. J Ecol 99:1016–1025. https://doi.org/10.1111/j.1365-2745.2011.01818.x
O’Brien TG (2011) Abundance, Density and Relative Abundance: A Conceptual Framework. Camera Traps in Animal Ecology. Springer, Tokyo, pp 71–96
Paradis E, Schliep K (2018) APE 5.0 an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528
R Core Team (2020) R: A Language and Environment for Statistical Computing
Rejmánek M, Klinger R (2009) The numerical and functional responses of a granivorous rodent and the fate of Neotropical tree seeds. Ecology 90:1549–1563
Rong K, Yang H, Ma J, Zong C, Cai T (2013) Food availability and animal space use both determine cache density of Eurasian red squirrels. PLoS ONE 8:e80632
Sawaya GM, Goldberg AS, Steele MA, Dalgleish HJ (2018) Environmental variation shifts the relationship between trees and scatterhoarders along the continuum from mutualism to antagonism. Integr Zool 13:319–330. https://doi.org/10.1111/1749-4877.12311
Silva KVKA, Kenuup CF, Kreischer C, Fernandez FAS, Pires AS (2018) Who let the dogs out? Occurrence, population size and daily activity of domestic dogs in an urban Atlantic Forest reserve. Perspect Ecol Conserv 16:228–233. https://doi.org/10.1016/j.pecon.2018.09.001
Smythe N (1978) The natural history of the Central American agouti (Dasyprocta punctata). Smithson Contrib to Zool. https://doi.org/10.5479/si.00810282.257
Sollmann R, Mohamed A, Samejima H, Wilting A (2013) Risky business or simple solution – Relative abundance indices from camera-trapping. Biol Conserv 159:405–412. https://doi.org/10.1016/j.biocon.2012.12.025
Theimer TC (2006) Rodent scatterhoarders as conditional mutualists. In: Forget P-M, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed fate. pp 283–296
Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philos Trans R Soc B Biol Sci 365:989–997. https://doi.org/10.1098/rstb.2009.0205
Xiao Z, Zhang Z, 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. J Ecol 101:1256–1264. https://doi.org/10.1111/1365-2745.12113
Zwolak R, Crone EE (2012) Quantifying the outcome of plant-granivore interactions. Oikos 121:20–27. https://doi.org/10.1111/j.1600-0706.2011.19849.x
Acknowledgements
We are thankful to all TNP staff and REFAUNA team for help with field work. We thank Mauro Galetti, Pedro Jordano and two anonymous reviewers for their critical comments on the manuscript.
Funding
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação Grupo Boticário de Proteção à Natureza gave financial support for this research. FASF and ASP received CNPq fellowships and PM received a CAPES scholarship.
Author information
Authors and Affiliations
Contributions
AP, FASF and PM conceived the ideas; AP, FASF and PM designed the methodology; PM collected and analysed the data. PM led the writing manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Elizabeth Pringle.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mittelman, P., Pires, A.S. & Fernandez, F.A.S. The intermediate dispersal hypothesis: seed dispersal is maximized in areas with intermediate usage by hoarders. Plant Ecol 222, 221–231 (2021). https://doi.org/10.1007/s11258-020-01100-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-020-01100-6