Leaf litter hides post-dispersed seeds from invasive alien removers in a sclerophyll forest in central Chile

  • Luis Cáceres-Polgrossi 1. Departamento de Silvicultura y Conservación de la Naturaleza, Facultad de Ciencias Forestales y de la Conservación de la Naturaleza, Universidad de Chile, Chile. Santa Rosa 11315, La Pintana, Santiago, Chile. 2. Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Facultad de Ciencias Agronómicas, Universidad de Chile, Chile. Santa Rosa 11315, La Pintana, Santiago, Chile. http://orcid.org/0000-0001-9350-9815
  • Alvaro Promis Departamento de Silvicultura y Conservación de la Naturaleza, Facultad de Ciencias Forestales y de la Conservación de la Naturaleza, Universidad de Chile, Chile. Santa Rosa 11315, La Pintana, Santiago, Chile. http://orcid.org/0000-0002-1596-4940
  • Alvaro G. Gutiérrez Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Facultad de Ciencias Agronómicas, Universidad de Chile, Chile. Santa Rosa 11315, La Pintana, Santiago, Chile. http://orcid.org/0000-0001-8928-3198

Abstract

Aim of the study: Seed removal may be a determining filter for regeneration. Factors such as leaf litter, tree cover and seed density affect seed removal. This aims to assess three aspects involving on post dispersal seed removal of four woody species (Lithraea caustica, Maytenus boaria, Quillaja saponaria and Retanilla ephedra) of a sclerophyll forest.

Study area: Andean Mediterranean sclerophyll forest of Quillaja saponaria and Lithraea caustica located in the Río de Los Cipreses National Reserve, Chile.

Materials and methods: Seven experimental plots were set up, in which seeds were offered in an experiment with variations in leaf litter, tree cover and seed density. Generalized Linear Mixed Models (GLMM) were used for the statistical analysis. Camera traps were installed to identify the seed removers.

Main results: Q. saponaria seeds were more removed than the seeds of the other species (0.84, observed mean). Whereas that M. boaria and R. ephedra did not show significant differences on the removal of their seeds (0.77 and 0.67 respectively), both were more removed than L. caustica (0.59). The removal of M. boaria, Q. saponaria and R. ephedra seeds was lower in the presence of leaf litter. No factor influenced the removal of L. caustica seeds. Seed removers were identified as invasive alien species such as Rattus sp. and Oryctolagus cuniculus and native species such as Lycalopex culpaeus.

Research highlights: Three woody species of this forest suffer severe seed removal by invasive alien fauna with major implications for the resilience of these forests. The coverage of leaf litter is key to hide away the seeds, increasing survival and could promote germination.

Keywords: invasive alien fauna; Mediterranean forest; sclerophyll forest; seed removal factors.

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References

Alcántara J, Rey P, Sánchez-Lafuente A, Valera F, 2000. Early effects of rodent postdispersal seed predation on the outcome of the plant-seed disperser interaction. Oikos 88(1): 362- 370. https://doi.org/10.1034/j.1600-0706.2000.880215.x

Allendorf FW, Lundquist LL, 2003. Introduction: Population Biology, Evolution, and Control of Invasive Species. Conserv Bio 17(1): 24-30. https://doi.org/10.1046/j.1523-1739.2003.02365.x

Armesto JJ, Aravena JC, Villagrán C, Pérez C, Parker G, 1995. Bosques templados de la cordillera de la costa. In: Ecología de los Bosques Nativos de Chile; Armesto J, Villagrán C, Arroyo MK (eds). pp: 109 - 213. Editorial Universitaria, Santiago, Chile.

Armesto J, Arroyo M, Hinojosa L, 2007. The mediterranean environment of Central Chile. In: The physical geography of South America; Veblen T, Young K, Orme A (eds). pp: 184-199. Oxford University Press, New York, USA. https://doi.org/10.1093/oso/9780195313413.003.0019

Armesto J, Rozzi R, Smith-Ramírez C, Arroyo M, 1998. Conservation Targets in South American Temperate Forests. Science 282(5392): 1271-1272. https://doi.org/10.1126/science.282.5392.1271

Aronson J, Del Pozo A, Ovalle C, Avendaño J, Lavín A, Etienne M, 1998. Land use changes and conflicts in central Chile. In: Landscape Degradation and Biodiversity in Mediterranean Type Ecosystems; Rundel P, Montenegro G, Jaksic F (eds). pp: 155-168. Springer-Verlag, New York, USA. https://doi.org/10.1007/978-3-662-03543-6_9

Arroyo M, Uslar P, 1993. Breeding systems in a temperate mediterranean-type climate montane sclerophyllous forest in central Chile. Bot J Linn Soc 111(1): 83-102. https://doi.org/10.1006/bojl.1993.1008

Arroyo M, Armesto J, Squeo F, Gutiérrez J, 1993. Global change: The flora and vegetation of Chile. In: Earth-System Responses to Global Change: Contrasts between North and South America; Mooney H, Fuentes E, Kronberg B (eds). pp: 239-264. Academic Press, California, USA.

Baldini A, Pancel L, 2002. Agentes de daño en el bosque nativo. Editorial Universitaria, Santiago, Chile. 408 pp.

Barceló M., Simonetti JA, 2020. Rattus rattus, a potential threat to the endangered tree Gomortega keule in the Maulino forest of Chile. New Zeal J Bot, 1-6. https://doi.org/10.1080/0028825X.2020.1799041

Bates D, Maechler M, Bolker B, Walker S, 2015. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67(1): 1-48. https://doi.org/10.18637/jss.v067.i01

Bustamante R., Simonetti JA, Mella J, 1992. Are foxes legitimate and efficient seed dispersers? A field test. Acta Oecol 13(2): 203-208.

Bustamante R, 1995. Depredación de semillas en bosques templados de Chile. In: Ecología de los Bosques Nativos de Chile; Armesto J, Villagrán C, Arroyo M (eds). pp: 265-278. Editorial Universitaria, Santiago, Chile.

Bustamante R., Vásquez R, 1995. Granivoría en Cryptocarya alba (Mol.) Looser (Lauraceae): los efectos del tipo de hábitat y la densidad de semillas. Rev Chil Hist Nat 68(1): 117-122.

Camus P, Castro S, Jaksic F, 2008. El conejo europeo en Chile: Historia de una invasión biológica. Historia 41(2): 305-339. https://doi.org/10.4067/S0717-71942008000200001

Castro S, Silva S, Meserve P, Gutiérrez J, Contreras L, Jaksic F, 1994. Frugivoría y dispersión de semillas de pimiento (Schinus molle) por el zorro culpeo (Pseudalopex culpaeus) en el Parque Nacional Fray Jorge (IV Región, Chile). Rev Chil Hist Nat 67(1): 169-176.

Castro S, Bozinovic F, Jaksic F, 2008, Ecological efficiency and legitimacy in seed dispersal of an endemic shrub (Lithraea caustica) by the European rabbit (Oryctolagus cuniculus) in central Chile. J Arid Environ 72(7): 1164-1173. https://doi.org/10.1016/j.jaridenv.2007.12.012

Cintra R, 1997. Leaf litter effects on seed and seedling predation of the palm Astrocaryum murumuru and the legume tree Dipteryx micrantha in Amazonian forest. J Trop Ecol 13(5): 709-725. https://doi.org/10.1017/S0266467400010889

Connell J, 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forests. In: Dynamics of population. Centre for Agriculture Publishing and Documentation; den Boer P, Gradwell G (eds). pp: 298-312. UHR Books, Maine, USA.

Cowling R, Rundel P, Lamont B, Arroyo M, Arianoutsou M, 1996. Plant diversity in mediterranean-climate regions. Trends in Ecol Evol 11(9): 352-360. https://doi.org/10.1016/0169-5347(96)10044-6

Dalling J, 2002. Ecología de semillas. In: Ecología y conservación de Bosques Neotropicales; Guariguata M, Kattan G (eds). pp: 345-375. Libro Universitario Regional, Cartago, Costa Rica.

Dellafiore C, Muñoz S, Gallego J, 2006. Rabbits (Oryctolagus cuniculus) as dispersers of Retama monosperma (L.) Bois seeds in a coastal dune system. Ecoscience 13(1): 5-10. https://doi.org/10.2980/1195-6860(2006)13[5:ROCADO]2.0.CO;2

Dellafiore C, Gallego J, Muñoz S, 2010. The rabbit (Oryctolagus cuniculus) as a seed disperser in a coastal dune system. Plant Ecol 206(2): 251-261. https://doi.org/10.1007/s11258-009-9639-7

Del Pozo A, Fuentes E, Hajek E, Molina J, 1989. Zonación microclimática por efecto de los manchones de arbustos en el matorral de Chile central. Rev Chil Hist Nat 62(1): 85-94.

Díaz I, Papic C, Armesto J, 1999. An assessment of post-dispersal seed predation in temperate rain forest fragments in Chiloe Island, Chile. Oikos 87(2): 223-238. https://doi.org/10.2307/3546738

Dudenhöffer J H, Pufal G, Roscher C, & Klein AM, 2016. Plant density can increase invertebrate postdispersal seed predation in an experimental grassland community. Ecol Evol 6(11): 3796-3807. https://doi.org/10.1002/ece3.2039

Elizalde R, 1970. La sobrevivencia de Chile. El Escudo, Impresores-Editores Ltda., Servicio Agrícola y Ganadero, Ministerio de Agricultura, Santiago, Chile. 492 pp.

European Environment Agency, 2012. The impacts of invasive alien species in Europe. Technical report nro.16/2012. Work document for international use.

Fernández A, Sáiz F, 2007. The european rabbit (Oryctolagus cuniculus L.) as seed disperser of the invasive opium poppy (Papaver somniferum L.) in Robinson Crusoe Island, Chile. Mastozoo Neotro 14(1): 19-27

Forget P, 1992. Seed removal and seed fate in Gustavia superba (Lecythidaceae). Biotropica 24(3): 408-414. https://doi.org/10.2307/2388611

Forget P, 1993. Post-dispersal predation and scatterhoarding of Dipteryx panamensis (Papilionaceae) seeds by rodents in Panama. Oecologia 94(2): 255-261. https://doi.org/10.1007/BF00341325

Fox J, Weisberg S, 2019. An {R} Companion to Applied Regression, Third Edition. Thousand Oaks CA: Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/

Fuentes ER, Hoffmann AJ, Poiani A, Alliende MC, 1986. Vegetation change in large clearings: Patterns in the Chilean matorral. Oecologia 68, 358-366. https://doi.org/10.1007/BF01036739

Fuentes ER, Jaksic F, Simonetti JA, 1983. European rabbits versus native rodents in Central Chile: effects on shrub seedlings. Oecologia 58(3): 411-414. https://doi.org/10.1007/BF00385244

Fuentes ER, Muñoz M, 1995. The human role in changing landscapes in central Chile: Implications for intercontinental comparisons. In: Ecology and Biogeography of Mediterranean Ecosystems in Chile, California, and Australia; Arroyo MTK, Zedler PH, Fox MD (eds). pp: 401-407. Springer-Verlag, New York, USA. https://doi.org/10.1007/978-1-4612-2490-7_17

Gálvez-Bravo L, 2017. Conejo - Oryctolagus cuniculus. En: Enciclopedia Virtual de los Vertebrados Españoles. Salvador, A., Barja, I. (Eds.). Museo Nacional de Ciencias Naturales, Madrid. 35 pp.

García D, Obeso J, Martínez I, 2005. Rodent seed predation promotes differential recruitment among bird-dispersed trees in temperate secondary forests. Oecologia 144(3): 435-446. https://doi.org/10.1007/s00442-005-0103-7

González-Varo J, Fedriani J, López-Bao J, Guitián J, Suárez-Esteban A, 2015. Frugivoría y dispersión de semillas por mamíferos carnívoros: rasgos funcionales. Ecosistemas 24(3): 43-50. https://doi.org/10.7818/ECOS.2015.24-3.07

Gutiérrez J, Holmgren M, Manrique R, Squeo F, 2007. Reduced herbivore pressure under rainy ENSO conditions could facilitate dryland reforestation. J Arid Environ 68(2): 322-330. https://doi.org/10.1016/j.jaridenv.2006.05.011

Grubb P, 1977. The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol Rev 52(1): 107-145. https://doi.org/10.1111/j.1469-185X.1977.tb01347.x

Harper J, 1977. Population biology of plants. Academic Press, London, UK. 892 pp.

Haught J, Myster R, 2008. Effects of Species, Density, Season and Prairie-type on Post-dispersal Seed Removal in Oklahoma. Am Midl Nat 159(2): 482-488. https://doi.org/10.1674/0003-0031(2008)159[482:EOSDSA]2.0.CO;2

Herrera C, Jordano P, Lopez-Soria L, Amat J, 1994. Recruitment of a mast-fruiting, bird ispersed tree: Bridging frugivore activity and seedling establishment. Ecol Monogr 64(3): 315-344. https://doi.org/10.2307/2937165

Hobbs R, Richardson M, Davis W, 1995. Mediterranean-type ecosystems. Opportunities and constrains for studying the function of biodiversity. In: Mediterranean-type ecosystems. The function of biodiversity; Davis G, Richardson D. (eds). pp: 1-42. Springer-Verlag, California, USA. https://doi.org/10.1007/978-3-642-78881-9_1

Hulme P, Hunt M, 1999. Rodent post-dispersal seed predation in deciduous woodland: predator response to absolute and relative abundance of prey. J Anim Ecol 68(2): 417-428. https://doi.org/10.1046/j.1365-2656.1999.00294.x

Jaksic F, 2001. Spatiotemporal variation patterns of plants and animals in San Carlos de Apoquindo, central Chile. Rev Chil Hist Nat 74(2): 477-502. https://doi.org/10.4067/S0716-078X2001000200021

Janzen D, 1970. Herbivores and the number of tree species in tropical forest. Am Nat 104(940): 501-528. https://doi.org/10.1086/282687

Jaña R, 2012. Animal seed dispersal and its consequences for plant recruitment. Doctoral thesis. University of Canterbury, Christchurch, New Zeland.

Jiménez H, Armesto J, 1992. Importance of the soil seed bank of disturbed sites in Chilean matorral in early secondary succession. Journal of Vegetation Science 3(5): 579-586. https://doi.org/10.2307/3235824

Lenth RV, 2016. Least-Squares Means: The R Package lsmeans. J Stat Softw 69(1): 1-33. https://doi.org/10.18637/jss.v069.i01

León-Lobos P, Arroyo M, 1994. Germinación de semilla de Lithraea caustica (Mol.) H. et A. (Anacardiacea) dispersadas por Pseudalopex sp. (Canidae) en el bosque esclerófilo de Chile central. Rev Chil Hist Nat 67(1): 59-64.

Lobo N, Green D, Millar J, 2013. Effects of seed quality and abundance on the foraging behavior of deer mice. J Mammal 94(6): 1449-1459. https://doi.org/10.1644/12-MAMM-A-295.1

Lowe S, Browne M, Boudjelas S, De Poorter M, 2000. 100 of the World's Worst Invasive Alien Species A selection from the Global Invasive Species Specialist Group (ISSG) a specialist group of the species survival commission (SSC) of the World Conservation Union (IUCN). Auckland, New Zealand. 12 pp.

Luebert F, Pliscoff P, 2017. Sinopsis Bioclimática y Vegetacional de Chile. Segunda Edición. Editorial Universitaria, Santiago, Chile. 381 pp.

Marino P, Westeman P, Pinkert C, van der Werf W, 2005. Influence of seed density and aggregation on post dispersal weed seed predation in cereal fields. Agr Ecosyst Environ 106(1): 17- 25. https://doi.org/10.1016/j.agee.2004.07.001

Martin G, Twigg L, Zampichelli L, 2007. Seasonal changes in the diet of the European rabbit (Oryctolagus cuniculus) from three different Mediterranean habitats in south-western Australia. Wildlife Res 34(1): 25-42. https://doi.org/10.1071/WR06044

Medan D, Aagesen L, 1995. Comparative flower and fruit structure in Colletieae (Rhamnaceae). Bot Jahrb Syst 117(4): 531-564.

Medan D, Arce ME, 1999. Reproductive biology of the Andean-disjunct genus Retanilla (Rhamnaceae). Plant Syst Evol 218(3-4): 281-298 https://doi.org/10.1007/BF01089232

Meyer JY, Butaud JF, 2009. The impacts of rats on the endangered native flora of French Polynesia (Pacific Islands): drivers of plant extinction or coup de grâce species? Biol Invasions 11(7):1569-1585. https://doi.org/10.1007/s10530-008-9407-y

Montenegro G, Avila G, Aljaro E, Osorio R, Gómez M, 1989. Chile. In: Plant Pheno-morphological Studies in Mediterranean Type Ecosystems. G Orshan (ed). pp: 347-387. Springer Netherlands, Dordrecht, Netherlands. https://doi.org/10.1007/978-94-009-3107-7_5

Morales N, Becerra P, Arellano E, Gilabert B, 2015. Effect of large and small herbivores on seed and seedling survival of Beilschmiedia miersii in central Chile. Bosque 36(1): 127-132. https://doi.org/10.4067/S0717-92002015000100014

Morales-Paredes C, Valdivia C, Sade S, 2015. Frugivory by native (Lycalopex spp.) and allochthonous (Canis lupus familiaris) canids reduces the seed germination of litre (Lithrea caustica) in central Chile. Bosque 36(3): 481-486. https://doi.org/10.4067/S0717-92002015000300014

Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J, 2000. Biodiversity hotspots for conservation priorities. Nature 403(6772): 853-858. https://doi.org/10.1038/35002501

Myster R, 2003. Effects of species, density, patch-type, and season on post-dispersal seed predation in a Puerto Rican Pasture. Biotropica 35(4): 542- 546. https://doi.org/10.1111/j.1744-7429.2003.tb00610.x

Myster R, Pickett S, 1993. Effects of litter, distance, density and vegetation patch type on postdispersal tree seed predation in old fields. Oikos 66(3): 381-388. https://doi.org/10.2307/3544932

Naveh Z, Wittaker R, 1979. Structural and floristic diversity of shrublands and woodlands in Northern Israel and other Mediterranean areas. Vegetatio 41(3): 171-190. https://doi.org/10.1007/BF00052445

Newton AC, Cantarello E, 2015. Restoration of forest resilience: An achievable goal? New Forest 46(5-6): 645-668. https://doi.org/10.1007/s11056-015-9489-1

Pakeman R., Digneffe G, Small J, 2002. Ecological correlates of endozoochory by herbivores. Funct Ecol 16(3): 296-304. https://doi.org/10.1046/j.1365-2435.2002.00625.x

Radvanyi A, 1970. Small mammals and regeneration of white spruce forests in western Alberta. Ecology 51(6): 1102-1105. https://doi.org/10.2307/1933641

R Core Team, 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Reed A, Kaufman G, Kaufman D, 2004. Effect of plant litter on seed predation in three prairie types. Am Midl Nat 155(2): 278-285. https://doi.org/10.1674/0003-0031(2006)155[278:EOPLOS]2.0.CO;2

Reid S, Armesto J, 2011. Interaction dynamics of avian frugivores and plants in Chilean Mediterranean shrubland. J Arid Environ 75(3): 221-230. https://doi.org/10.1016/j.jaridenv.2010.10.002

Root-Bernstein M., Svenning J-C, 2017. Restoring connectivity between fragmented woodlands in Chile with a reintroduced mobile link species. Perspect Ecol Conser 15(4): 292-299. https://doi.org/10.1016/j.pecon.2017.09.001

Rundel P, 1998. Landscape disturbance in mediterranean-type ecosystems: An overview. In: Landscape Disturbance and Biodiversity in Mediterranean-Type Ecosystems; Rundel P, Montenegro G, Jaksic M (eds). pp: 3-22. Springer-Verlag, California, USA. https://doi.org/10.1007/978-3-662-03543-6_1

Salazar A, Baldi G, Hirota M, Syktus J, McAlpine C, 2015. Land use and land cover change impacts on the regional climate of non-Amazonian South America: A review. Global Planet Change 128: 103-119 https://doi.org/10.1016/j.gloplacha.2015.02.009

Scanes C, 2018. Invasive Species. In: Animal and human society; Scanes C, Toukhsati S (eds). pp: 413-426. Academic Press, London, UK. https://doi.org/10.1016/B978-0-12-805247-1.00024-1

Schulz J, Cayuela L, Echeverría C, Salas J, Rey M, 2010. Monitoring land cover change of the dryland forest landscape of Central Chile (1975-2008). Appl Geogr 30(3): 436-447. https://doi.org/10.1016/j.apgeog.2009.12.003

Schulz J, Cayuela L, Rey-Benayas J, Schroder B, 2011. Factors influencing vegetation cover change in Mediterranean Central Chile (1975-2008). Appl Veg Sci 14(4): 571-582. https://doi.org/10.1111/j.1654-109X.2011.01135.x

Schupp E, 1988. Factors affecting post-dispersal seed survival in a tropical forest. Oecología 76(4): 525-530. https://doi.org/10.1007/BF00397864

Shaw M, 1968. Factors affecting the regeneration of sessile oak (Quercus petraea) in North Wales. II. Acorn losses and germination under field conditions. J Ecol 56(3): 647-666. https://doi.org/10.2307/2258097

Simonetti JA, 1983a. Effect of goats upon native rodents and European rabbits in the Chilean matorral. Rev Chil Hist Nat 56(1): 27-30.

Simonetti JA, 1983b. Occurrence of the black rat (Rattus rattus) in central Chile. Mammalia 47(1): 131-132.

Uribe J, Cabrera R, de la Fuente A, Paneque M, 2012. Atlas Bioclimático de Chile. Departamento de Ciencias Ambientales y Recursos Naturales Renovables, Universidad de Chile, Santiago, Chile. 232 pp.

Velazco SJE, Blum CT, Hoffmann PM, 2018. Germination and seedlings development of the threatened species Quillaja brasiliensis. CERNE, 24(2), 90-97. https://doi.org/10.1590/01047760201824022530

Yu F, Shi X, Wei K, & Wang D, 2015. Leaf litter affects the survival and predation rates for large and smallPinusseeds in the Qinling Mountains, China. Isr J Ecol Evol 61(3-4): 162-168. https://doi.org/10.1080/15659801.2016.1176689

Westfall P, Tobias R, Rom D, Wolfinger R, Hochberg Y, 1999. Multiple Comparisons and Multiple Tests Using the SAS System. Cary, NC: SAS Institute Inc.

Willson M, 1988. Spatial heterogeneity of post-dispersal survivorship of Queensland rainforest seeds. Aust J Ecol 13(2): 137-146. https://doi.org/10.1111/j.1442-9993.1988.tb00963.x

Published
2021-02-03
How to Cite
Cáceres-PolgrossiL., PromisA., & GutiérrezA. G. (2021). Leaf litter hides post-dispersed seeds from invasive alien removers in a sclerophyll forest in central Chile. Forest Systems, 29(3), e022. https://doi.org/10.5424/fs/2020293-16845
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Research Articles