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Effectiveness of rodents as local seed dispersers of Holm oaks

Oecologia volume 155, pages 529–537 (2008)Cite this article

Abstract

In this study we assessed the effectiveness of rodents as dispersers of Quercus ilex in a patchy landscape in southeastern Spain. We experimentally followed the fates of 3,200 marked and weighed acorns from dispersal through the time of seedling emergence over three years. Rodents handled about 99% of acorns, and dispersed 67% and cached 7.4% of the dispersed acorns. Most caches were recovered and consumed, and only 1.3% of the original experimental acorns were found alive in caches the following spring. Dispersal distances were short (mean = 356.2 cm, median = 157 cm) and strongly right-skewed. Heavier acorns were dispersed further and were more likely to be cached and survive than lighter acorns. All caches were in litter or soil, and each contained a single acorn. Rodents moved acorns nonrandomly, mostly to oaks and pines. Most surviving acorns were either in oaks, a poor microhabitat for oak recruitment, or shrubs, a suitable microhabitat for oak recruitment. Our results suggest that rodents, by burying a relatively high proportion of acorns singly in shrubs and pines, act as moderately effective dispersers of Q. ilex. Nonetheless, this dispersal comes at a very heavy cost.

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References

  • Alcantara JM, Rey PJ, Sánchez-Lafuente AM, Valera F (2000) Early effects of rodent post-dispersal seed predation on the outcome of the plant–seed disperser interaction. Oikos 88:362–370

    Article  Google Scholar 

  • Bates D (2005) Fitting linear mixed models in R. R News 5:27–30

    Google Scholar 

  • Bonfil C (1998) The effect of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceae). Am J Bot 85:79–87

    Article  Google Scholar 

  • Cheng J, Xiao Z, Zhang Z (2005) Seed consumption and caching on seeds of three sympatric tree species by four sympatric rodent species in a subtropical forest, China. For Ecol Manage 216:331–341

    Article  Google Scholar 

  • Darley-Hill S, Johnson WC (1981) Acorn dispersal by the blue jay (Cyanocitta cristata). Oecologia 50:231–232

    Article  Google Scholar 

  • Espelta JM, Riba M, Retana J (1995) Patterns of seedling recruitment in west Mediterranean coppiced holm-oak (Quercus ilex L.) forests as influenced by canopy development. J Veg Sci 6:465–472

    Article  Google Scholar 

  • Fedriani JM, Manzaneda A (2005) Pre- and post-dispersal seed predation by rodents: balance of food and safety. Behav Ecol 16:1018–1024

    Article  Google Scholar 

  • Forget PM, Lambert JR, Hulme PE, Vander Wall SB (2005) Seed fate: predation, dispersal and seedling establishment. CABI Publishing, Wallingford, UK

  • Giannoni SM, Dacar M, Taraborelli P, Borghi CE (2001) Seed hoarding by rodents of the Monte Desert, Argentina. Austral Ecol 26:259–263

    Google Scholar 

  • Gómez JM (2003) Spatial patterns in long-distance dispersal of Quercus ilex acorns by jays in a heterogeneous landscape. Ecography 26:573–584

    Article  Google Scholar 

  • Gómez JM (2004a) Importance of microhabitat and acorn burial on Quercus ilex early recruitment: non-additive effects on multiple demographic processes. Plant Ecol 192:287–297

    Google Scholar 

  • Gómez JM (2004b) Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58:71–80

    PubMed  Google Scholar 

  • Gómez JM, García D, Zamora R (2003) Impact of vertebrate acorn- and seedling-predators on a Mediterrean Quercus pyrenaica forest. For Ecol Manage 180:125–134

    Article  Google Scholar 

  • Gómez-Aparicio L, Zamora R, Gómez JM, Hódar JA, Castro J, Baraza E (2004) Applying plant facilitation to forest restoration: a meta-analysis of the use of shrubs as nurse plants. Ecol Appl 14:1128–1138

    Article  Google Scholar 

  • Gómez-Aparicio L, Gómez JM, Zamora R, Boettinger JL (2005a) Canopy versus soil effects of shrubs facilitating tree seedlings in Mediterranean montane ecosystems. J Veg Sci 16:191–198

    Article  Google Scholar 

  • Gómez-Aparicio L, Valladares F, Zamora R, Quero JL (2005b) Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales. Ecography 28:757–768

    Article  Google Scholar 

  • Hollander JL, Vander Wall SB (2004) Effectiveness of six species of rodents as dispersers of single leaf pinon pine (Pinus monophylla). Oecologia 138:57–65

    Article  PubMed  Google Scholar 

  • Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228

    Article  Google Scholar 

  • Hulme PE (2002) Seed-eaters: seed dispersal, destruction and demography. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, UK, pp 257–273

  • Ibáñez I, Schupp EW (2001) Positive and negative interactions between environmental conditions affecting Cercocarpus ledifolius seedling survival. Oecologia 129:543–550

    Google Scholar 

  • Iida S (1996) Quantitative analysis of acorn transportation by rodents using magnetic locator. Vegetatio 124:39–43

    Article  Google Scholar 

  • Iida S (2004) Indirect negative influence of dwarf bamboo on survival of Quercus acorns by hoarding behavior of wood mice. For Ecol Manage 202:257–263

    Article  Google Scholar 

  • Iida S (2006) Dispersal patterns of Quercus serrata acorns by wood mice in and around canopy gaps in a temperate forest. For Ecol Manage 227:71–78

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jensen TS (1985) Seed-seed predator interactions of European beech, Fagus sylvatica and forest rodents, Clethrionomys glareolus and Apodemus flavicollis. Oikos 44:149–156

    Article  Google Scholar 

  • Jensen TS, Nielsen OF (1986) Rodents as seed dispersers in a heath-oak wood succession. Oecologia 70:214–221

    Article  Google Scholar 

  • Li HJ, Zhang ZB (2003) Effect of rodents on acorn dispersal and survival of Liaondong oak (Quercus liatungensis Koidz.). For Ecol Manage 176:387–396

    Article  Google Scholar 

  • Li HJ, Zhang ZB (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

    Article  Google Scholar 

  • Mendoza E, Dirzo R (2007) Seed-size variation determines interspecific differential seed predation by mammals in a neotropical rain forest. Oikos 116:1841–1852

    Google Scholar 

  • Miriti MN (2006) Ontogenetic shift from facilitation to competition in a desert shrub. J Ecol 94:973–979

    Article  Google Scholar 

  • Muñoz A, Bonal R (2007) Rodents change acorn dispersal behaviour in response to ungulate presence. Oikos 116:1631–1638

    Article  Google Scholar 

  • Pons JM, Pausas J (2007a) Acorn dispersal estimated by radio-tracking. Oecologia 153:903–911

    Article  PubMed  Google Scholar 

  • Pons JM, Pausas J (2007b) Rodent acorn selection in a Mediterranean oak landscape. Ecol Res 22:535–541

    Article  Google Scholar 

  • Puerta-Piñero C, Gómez JM, Zamora R (2006) Species-specific effects on topsoil development affect Quercus ilex seedling performance. Acta Oecol 29:65–71

    Article  Google Scholar 

  • Puerta-Piñero C, Gómez JM, Valladares F (2007) Irradiance and oak seedling survival and growth in a heterogeneous environment. For Ecol Manage 242:462–469

    Article  Google Scholar 

  • Pulido FJ (2002) Biología reproductiva y conservación: el caso de la regeneración de bosques templados y subtropicales de robles (Quercus spp.). Rev Chil Hist Nat 75:5–15

    Article  Google Scholar 

  • Pulido FJ, Díaz M (2005) Regeneration of a Mediterranean oak: a whole-cycle approach. EcoScience 12:92–102

    Article  Google Scholar 

  • Purves DW, Zavala MA, Ogle K, Prieto F, Rey Benayas JM (2007) Environmental heterogeneity, bird-mediated directed dispersal, and oak woodland dynamics in Mediterranean Spain. Ecol Monogr 77:77–98

    Article  Google Scholar 

  • Retana J, Espelta JM, Gracia M, Riba M (1999) Seedling recruitment. In: Rodá F, Retana J, Gracia CA, Bellot J (eds) Ecology of Mediterranean evergreen oak forests. Springer, Berlin, pp 89–103

  • Rey P, Alcántara JM (2000) Recruitment dynamics of a fleshy-fruited plant (Olea europaea): connecting patterns of seed dispersal to seedling establishment. J Ecol 88:622–633

    Article  Google Scholar 

  • Rey P, Garrido JL, Alcántara JM, Ramírez JM, Aguilera A, García L, Manzaneda AJ, Fernández R (2002) Spatial variation in ant and rodent post-dispersal predation of vertebrate-dispersed seeds. Funct Ecol 16:773–781

    Article  Google Scholar 

  • Roth JK, Vander Wall SB (2005) Primary and secondary seed dispersal of bush chinquapin (Fagaceae) by scatterhoarding rodents. Ecology 86:2428–2439

    Article  Google Scholar 

  • Santos T, Tellería JL (1997) Vertebrate predation on Holm oaks, Quercus ilex, acorns in a fragmented habitat: effects on seedling recruitment. For Ecol Manage 98:181–187

    Article  Google Scholar 

  • SAS Institute Inc. (2005) SAS/STAT Software: changes and enhancements through release 6.12. SAS Institute Inc., Cary, NC

  • Schupp EW (1990) Annual variation in seedfall, post-dispersal predation and recruitment of a neotropical tree. Ecology 71:504–515

    Article  Google Scholar 

  • Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107/108:15–29

    Google Scholar 

  • Schupp EW (2007) The suitability of a site for seed dispersal is context-dependent. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CABI International, Wallingford, UK, pp 445–462

  • Schupp EW, Fuentes M (1995) Spatial patterns of seed dispersal and the unification of plant population ecology. Écoscience 2:267–275

    Google Scholar 

  • Seiwa K (2000) Effects of seed size and emergence time on tree seedling establishment: importance of developmental constraints. Oecologia 123:208–215

    Article  Google Scholar 

  • Seiwa K, Watanabe A, Irie K, Kannu H, Saitoh T, Akasaka S (2002a) Impact of site-induced mouse caching and transport behaviour on regeneration in Castanea crenata. J Veg Sci 13:517–526

    Article  Google Scholar 

  • Seiwa K, Watanabe A, Saitoh T, Kannu H, Akasaka S (2002b) Effects of burying depth and seed size on seedling establishment of Japanese chestnuts, Castanea crenata. For Ecol Manage 164:149–156

    Article  Google Scholar 

  • Sork VL (1984) Examination of seed dispersal and survival on red oak, Quercus rubra (Fagaceae), using metal-tagged acorns. Ecology 65:1020–1022

    Article  Google Scholar 

  • Stapanian MA, Smith CC (1978) A model for seed scatter-hoarding: coevolution of fox squirrels and black walnuts. Ecology 59:884–898

    Article  Google Scholar 

  • Stapanian MA, Smith CC (1984) Density-dependent survival of scatterhoarded nuts: an experimental approach. Ecology 65:1387–1396

    Article  Google Scholar 

  • Takahashi K, Sato K, Washitani I (2006) The role of the wood mouse in Quercus serrata acorn dispersal in abandoned cut-over land. For Ecol Manage 229:120–127

    Article  Google Scholar 

  • Tomita M, Hirabuki Y, Seiwa K (2002) Post-dispersal changes in the spatial distribution of Fagus crenata seeds. Ecology 83:1560–1565

    Article  Google Scholar 

  • Traveset A, Gulias J, Nieras N, Mus M (2003) Transition probabilities from pollination to establishment in a rare dioecious species (Rhamnus ludovici-salvatoris) in two habitats. J Ecol 91:427–437

    Article  Google Scholar 

  • Tripathi RS, Khan ML (1990) Effects of seed weight and microsite characteristics on germination and seedling fitness in two species of Quercus in a subtropical wet hill forest. Oikos 57:289–296

    Article  Google Scholar 

  • Tyler CM, Kuhn B, Davis FW (2006) Demography and recruitment limitations of three oak species in California. Q Rev Biol 81:127–152

    Article  PubMed  Google Scholar 

  • Vander Wall SB (1990) Food hoarding in animals. The University of Chicago Press, Chicago, IL

  • Vander Wall SB (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117

    Article  Google Scholar 

  • Vander Wall SB (2002) Secondary dispersal of Jeffrey pine seeds by rodent scatter-hoarding: the roles of pilfering, reaching and a variable environment. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, UK, pp 193–208

  • Vander Wall SB, Longland WS (2004) Diplochory: are two seed dispersers better than one? Trends Ecol Evol 19:155–161

    Article  PubMed  Google Scholar 

  • Vander Wall SB, Kuhn KM, Beck MJ (2005) Seed removal, seed predation, and secondary dispersal. Ecology 86:801–806

    Article  Google Scholar 

  • Wenny DG (2001) Advantages of seed dispersal: a re-evaluation of directed dispersal. Evol Ecol Res 3:51–74

    Google Scholar 

  • Xiao Z, Zhang Z, Wang Y (2004) Dispersal and germination of big and small nuts of Quercus serrata in a subtropical broad-leaved evergreen forest. For Ecol Manage 195:141–150

    Article  Google Scholar 

  • Xiao Z, Jansen PA, Zhang Z (2006a) Using seed-tagging methods for assessing post-dispersal seed fate in rodent-dispersed trees. For Ecol Manage 223:18–23

    Article  Google Scholar 

  • Xiao Z, Wang Y, Harris M, Zhang Z (2006b) Spatial and temporal variation of seed predation and removal of sympatric large-seeded species in relation to innate seed traits in a subtropical forest, Southwest China. For Ecol Manage 222:46–54

    Article  Google Scholar 

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Acknowledgments

Janis Boettinger, Manuel López de las Huertas, Rocío Márquez, Ángel Navarra and Joaquín Sánchez provided important help in the field. Financial support was provided by the Spanish Ministry of Science and Education grant REN2003-07048, a doctoral fellowship AP2003-2444 and the Andalucía grant RNM220. Red de Jardínes Botánicos de Andalucía (Junta de Andalucía) and the headquarters of the Sierra Nevada National Park gave constant support and facilities for fieldwork.

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Authors and Affiliations

  1. Dpto de Ecología, Universidad de Granada, Granada, Spain

    José M. Gómez & Carolina Puerta-Piñero

  2. Department of Wildland Resources and the Ecology Center, Utah State University, Logan, UT, 84322, USA

    Eugene W. Schupp

Authors
  1. José M. Gómez
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  2. Carolina Puerta-Piñero
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  3. Eugene W. Schupp
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Correspondence to José M. Gómez.

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Communicated by Diethart Matthies.

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Gómez, J.M., Puerta-Piñero, C. & Schupp, E.W. Effectiveness of rodents as local seed dispersers of Holm oaks. Oecologia 155, 529–537 (2008). https://doi.org/10.1007/s00442-007-0928-3

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  • DOI: https://doi.org/10.1007/s00442-007-0928-3

Keywords

  • Acorn dispersal
  • Apodemus sylvaticus
  • Disperser effectiveness
  • Quercus ilex
  • Sciurus vulgaris