La depredación de semillas nativas y no-nativas varía en plantaciones de pino del noroeste de la Patagonia

Genevieve M. Conley; Luciana M. Motta; Sebastián Ballari

doi:10.25260/EA.22.32.3.0.1876

Authors

Genevieve M. Conley School of Earth and Sustainability, College of the Environment, Forestry and Natural Sciences, Northern Arizona University. Flagstaff, Arizona, Estados Unidos
Luciana M. Motta Parque Nacional Nahuel Huapi (CENAC-APN). Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). San Carlos de Bariloche, Río Negro, Argentina. Grupo de Ecología de Invasiones, INIBIOMA - CONICET, Universidad Nacional del Comahue. San Carlos de Bariloche, Río Negro, Argentina
Sebastián Ballari Parque Nacional Nahuel Huapi (CENAC-APN). Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). San Carlos de Bariloche, Río Negro, Argentina

DOI:

https://doi.org/10.25260/EA.22.32.3.0.1876

Keywords:

patagonian forest, protected area, invasive alien species, seed dispersion, plant-animal interaction, restoration

Abstract

Human disturbances can cause functional alterations in ecosystems, affecting key interactions such as those between plants and animals. For example, post-seed dispersal predation determines plant establishment in many terrestrial ecosystems and can have positive or negative effects on plant community composition, which can, then, influence ecosystem structure and functionality. However, seed predation can be altered in modified environments, with consequences on the establishment and dispersal of native and non-native plants. The objective of this study was to evaluate the post-dispersal predation of native and non-native seeds at different spatial scales in modified environments: pine plantations, clearcut areas and native forests in Isla Victoria, northwestern Patagonia (Argentina). We used a cafeteria-type experiment offering native and non-native seed species in each habitat and measured the vegetation cover around each seed offering area to assess the effect of microsite characteristics. After evaluating predation in the three environments, we only found that there is a greater preference for predation of native seeds in pine forest plantations. On the other hand, we identified that vegetation cover at ground level (strongly correlated with the type of environment) keeps a positive relationship with seed predation. This study shows that seed predation of native and non-native plants could be driven in part by microsite characteristics (greater plant cover = greater seed predation), perhaps through generating refuge (safe site) for the main seed predators of these forests (i.e., rodents). Forest conservation, management and restoration strategies must consider the short- and long-term dynamics of a post-intervention restoration site with the aim of creating an environment conducive to native forest regeneration.

References

Arroyo‐Correa, B., L. A. Burkle, and C. Emer. 2020. Alien plants and flower visitors disrupt the seasonal dynamics of mutualistic networks. J Ecol 108:1475-1486. https://doi.org/10.1111/1365-2745.13332.

Ballari, S. A., B. D. Hendrix, M. Sample, and M. A. Núñez. 2019. Management of invasive Pinaceae is imperiled by the lack of invasive ungulate control: successful restoration requires multiple-species management. Mammal Res 64:535-542. https://doi.org/10.1007/s13364-019-00439-0.

Bates, D., M. Mächler, B. Bolker, and S. Walker. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1-48. https://doi.org/10.18637/jss.v067.i01.

Brockerhoff, E. G., L. Barbaro, B. Castagneyrol, D. I. Forrester, B. Gardiner, et al. 2017. Forest biodiversity, ecosystem functioning and the provision of ecosystem services. Biodivers Conserv 26:3005-3035. https://doi.org/10.1007/s10531-017-1453-2.

Caccia, F. D., E. J. Chaneton, and T. Kitzberger. 2006. Trophic and non‐trophic pathways mediate apparent competition through post‐dispersal seed predation in a Patagonian mixed forest. Oikos 113:469-480. https://doi.org/10.1111/j.2006.0030-1299.14390.x.

Chiuffo, M. C., J. Moyano, M. A. Rodríguez-Cabal, and M. A. Núñez. 2018. Seed predation of non-native species along a precipitation gradient. Plant Ecol 219:1307-1314. https://doi.org/10.1007/s11258-018-0880-9.

Connolly, B., D. Pearson, and R. Mack R. 2014. Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95:1759-1769. https://doi.org/10.1890/13-1774.1.

Fedriani, J. M. 2005. Do frugivorous mice choose where or what to feed on? J Mammal 86:576-586. https://doi.org/10.1644/1545-1542.

Fedriani, J. M., and A. J. Manzaneda. 2005. Pre-and postdispersal seed predation by rodents: balance of food and safety. Behav Ecol 16:1018-1024. https://doi.org/10.1644/1545-1542(2005)86[576:DFMCWO]2.0.CO;2.

García, D., and N. P. Chacoff. 2007. Scale‐dependent effects of habitat fragmentation on hawthorn pollination, frugivory, and seed predation. Conservation Biol 21:400-411. https://doi.org/10.1111/j.1523-1739.2006.00593.x.

Jacob, J., and J. S. Brown. 2000. Microhabitat use, giving‐up densities and temporal activity as short‐and long‐term anti‐predator behaviors in common voles. Oikos 91:131-138. https://doi.org/10.1034/j.1600-0706.2000.910112.x.

Kollmann, J., and M. Buschor. 2003. Edges effects on seed predation by rodents in deciduous forests of northern Switzerland. Plant Ecol 164:249-261. https://doi.org/10.1023/A:1021225728493.

Lantschner, M. V., V. Rusch, and J. P. Hayes. 2011. Influences of pine plantations on small mammal assemblages of the Patagonian forest-steppe ecotone. Mammalia 75:249-255. https://doi.org/10.1515/mamm.2011.031.

Lichti, N. I., M. A. Steele, and R. K. Swihart. 2017. Seed fate and decision‐making processes in scatter‐hoarding rodents. Biol Rev 92:474-504. https://doi.org/10.1111/brv.12240.

Manson, R. H., and E. W Stiles. 1998. Links between microhabitat preferences and seed predation by small mammals in old fields. Oikos 82:37-50. https://doi.org/10.2307/3546915.

Markl, J. S., M. Schleuning, P. M. Forget, P. Jordano, J. E. Lambert, et al. 2012. Meta‐analysis of the effects of human disturbance on seed dispersal by animals. Conserv Biol 26:1072-1081. https://doi.org/10.1111/j.1523-1739.2012.01927.x.

Maron, J. L., D. E. Pearson, T. Potter, and Y. K. Ortega. 2012. Seed size and provenance mediate the joint effects of disturbance and seed predation on community assembly. J Ecol 100:1492-1500. https://doi.org/10.1111/j.1365-2745.2012.02027.x.

Meiss, H., L. Le Lagadec, N. Munier-Jolain, R. Waldhardt, and S. Petit. 2010. Weed seed predation increases with vegetation cover in perennial forage crops. Agric Ecosyst Environ 138:10-16. https://doi.org/10.1016/j.agee.2010.03.009.

Miguel, M. F., P. Jordano, S. Tabeni, and C. M. Campos. 2018. Context‐dependency and anthropogenic effects on individual plant-frugivore networks. Oikos 127:1045-1059. https://doi.org/10.1111/oik.04978.

Morales, J. M., M. D. Rivarola, G. Amico, and T. A. Carlo. 2012. Neighborhood effects on seed dispersal by frugivores: testing theory with a mistletoe-marsupial system in Patagonia. Ecology 93:741-748. https://doi.org/10.1890/11-0935.1.

Motta, L., A. Vitali, G. C. Amico, D. García, and M. A. Rodríguez-Cabal. 2021. Post-dispersal seed predation in Patagonia temperate forest depends on habitat patchiness and seed species. Plant Ecol 222:819-827. https://doi.org/10.1007/s11258-021-01145-1.

Moyano, J., M. C. Chiuffo, M. A. Núñez, and M. A. Rodríguez-Cabal. 2019. Seed predation does not explain pine invasion success. Oecologia 189:981-991. https://doi.org/10.1007/s00442-019-04354-8.

Núñez, M. A., D. Simberloff, and M. A. Relva. 2008. Seed predation as a barrier to alien conifer invasions. Biol Invasions 10:1389-1398. https://doi.org/10.1007/s10530-007-9214-x.

Parker, J. D., and M. E. Hay. 2005. Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959-967. https://doi.org/10.1111/j.1461-0248.2005.00799.x.

Parrotta J., J. W. Turnbull, and N. Jones. 1997. Catalyzing native forest regeneration on degraded forest lands. For Ecol Manag 99:1-7. https://doi.org/10.1016/S0378-1127(97)00190-4.

Pearson, D. E., J. L. Hierro, M. Chiuffo, and D. Villarreal. 2014. Rodent seed predation as a biotic filter influencing exotic plant abundance and distribution. Biol Invasions 16:1185-1196. https://doi.org/10.1007/s10530-013-0573-1.

Pereira Marinho, F., G. G. Mazzochini, A. P. Manhães, W. W. Weisser, and G. Ganade. 2016. Effects of past and present land use on vegetation cover and regeneration in a tropical dryland forest. J Arid Environ 132:26-33. https://doi.org/10.1016/j.jaridenv.2016.04.006.

R Development Core Team. 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL: r-project-org.

Redford, K. H., and J. F. Eisenberg. 1992. Mammals of the Neotropics. Vol. 2. The Southern Cone: Chile, Argentina, Uruguay, Paraguay. University of Chicago Press. Chicago, USA. Pp. 430.

Relva, M. A., M. A. Núñez, and D. Simberloff. 2010. Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown. Biol Invasions 12:303-311. https://doi.org/10.1007/s10530-009-9623-0.

Sample, M., C. E. Aslan, N. Policelli, R. L. Sanford, E. Nielsen, et al. 2019. Increase in nonnative understorey vegetation cover after nonnative conifer removal and passive restoration. Austral Ecol 44:1384-1397. https://doi.org/10.1111/aec.12812.

Sanguinetti, J., and T. Kitzberger. 2010. Factors controlling seed predation by rodents and non-native Sus scrofa in Araucaria araucana forests: potential effects on seedling establishment. Biol Invasions 12:689-706. https://doi.org/10.1007/s10530-009-9474-8.

Sarabi, V. 2019. Factors that influence the level of weed seed predation: A review. Weed Biol Manag 19:61-74. https://doi.org/10.1111/wbm.12186.

Simberloff, D., M. A. Relva, and M. Núñez. 2003. Introduced species and management of a Nothofagus/Austrocedrus forest. Environ Manage 31:0263-0275. https://doi.org/10.1007/s00267-002-2794-4.

Sunyer, P., A. Muñoz, R. Bonal, and J. M. Espelta. 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.

Torres, A., P. A. E. Alarcón, M. A. Rodríguez-Cabal, and M. A. Núñez. 2018. Secondary invasions hinder the recovery of native communities after the removal of nonnative pines along a precipitation gradient in Patagonia. Forests 9:394. https://doi.org/10.3390/f9070394.