Skip to main content
SpringerLink
Log in

Microhabitat affects acorn removal in three sympatric and endangered Neotropical oak species

  • Original Article
  • Published:
Ecological Research

Abstract

Acorn removal and predation are processes that can influence forest dynamics and the ecological niche segregation of sympatric oak species. Different factors affect these processes, including differences in acorn germination rate and exposure to predators and/or dispersers. This study evaluated acorn removal and predation patterns in three threatened tropical cloud forest oak species (Quercus germana, Quercus sartorii and Quercus cortesii). Acorns were placed in two accessibility treatments (open to all potential acorn consumers vs. accessible to mice only) and in two types of microhabitat (covered by trunks, shrubs and herbaceous plants vs. uncovered). In addition, acorn germination rate was evaluated in a greenhouse. After 130 days, 76.67 ± 2.45 % of the seeds had been removed and the two accessibility treatments did not differ significantly. Mice were therefore shown as important predators and/or dispersers of acorns. Removal was greater in the covered (93.33 ± 2.04 %) compared to the uncovered (60.00 ± 4.01 %; P < 0.05) microhabitat. Acorn removal and germination were highest for Q. germana (82.00 ± 3.86 %, 91.67 ± 4.41 %, respectively), followed by Q. sartorii (79.00 ± 4.09 %; 50.00 ± 7.64 %) and Q. cortesii (69.00 ± 4.64 %; 13.33 ± 4.41 %); the same trend was recorded in the acorn germination rate (P < 0.05). Our findings suggest that uncovered sites with partial shade might function as regeneration microhabitats where less acorn removal and higher germination occur. The implications of differential acorn trait preferences by rodents for the coexistence of these oak species are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Birkedal M, Fischer A, Karlsson M, Lof M, Madsen P (2009) Rodent impact on establishment of direct-seeded Fagus sylvatica, Quercus robur and Quercus petraea on forest land. Scan J For Res 24:298–307

    Article  Google Scholar 

  • Bonal R, Espelta JM, Vogler AP (2011) Complex selection on life-history traits and the maintenance of variation in exaggerated rostrum length in acorn weevils. Oecologia 167:1053–1061

    Article  PubMed  Google Scholar 

  • Chang G, Jin T, Pei J, Chen X, Zhang B, Shi Z (2012) Seed dispersal of three sympatric oak species by forest rodents in the Qinling Mountains, Central China. Plant Ecol 213:1633–1642

    Article  Google Scholar 

  • García D, Bañuelos MJ, Houle G (2002) Differential effects of acorn burial and litter cover on Quercus rubra recruitment at the limit of its range in eastern North America. Can J Botany 80:1115–1120

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Gómez JM, Puerta-Piñero C, Schupp EW (2008) Effectiveness of rodents as local seed dispersers of Holm oaks. Oecologia 155:529–537

    Article  PubMed  Google Scholar 

  • González-Espinosa M, Meave J, Lorea-Hernández FG, Ibarra-Manríquez G, Newton AC (2011) The red list of Mexican cloud forest trees. Fauna and Flora International, Cambridge

    Google Scholar 

  • González-Rodríguez V, Villar R (2012) Post-dispersal seed removal in four Mediterranean oaks: species and microhabitat selection differ depending on large herbivore activity. Ecol Res 27:587–594

    Article  Google Scholar 

  • Gribko LS, Jones WE (1995) Test of the float method of assessing northern red oak acorn condition. Tree Plant Notes 46:143–147

    Google Scholar 

  • Guzmán-Guzmán J, Williams-Linera G (2006) Edge effect on acorn removal and oak seedling survival in Mexican lower montane forest fragments. New For 31:487–495

    Article  Google Scholar 

  • Kalcounis-Ruppell MC, Millar JS (2002) Partitioning of space, food, and time by syntropic Peromyscus boylii and P. californicus. J Mammal 83:614–625

    Article  Google Scholar 

  • Kellner KF, Riegel JK, Swihart RK (2014) Effects of silvicultural disturbance on acorn infestation and removal. New For 45:265–281

    Article  Google Scholar 

  • Lei JJ, Shen Z, Yi X (2012) Pericarp thickness and seed size determine acorn dispersal of five rodent-dispersed oak species. Acta Theriol Sin 32:83–89

    Article  Google Scholar 

  • Lombardo JA, McCarthy BC (2009) Seed germination and seedling vigor of weevil-damaged acorns of red oak. Can J For Res 39:1600–1605

    Article  Google Scholar 

  • López-Barrera F, Manson RH, González-Espinosa M, Newton AC (2007) Effects of varying forest edge permeability on seed dispersal in a neotropical montane forest. Landscape Ecol 22:189–203

    Article  Google Scholar 

  • López-Barrera F, Newton A (2005) Edge type effect on germination of oak tree species in the Highlands of Chiapas, Mexico. For Ecol Manag 217:67–79

    Article  Google Scholar 

  • López-Barrera F, Newton A, Manson R (2005) Edge effects in a tropical montane forest mosaic: experimental tests of post-dispersal acorn removal. Ecol Res 20:31–40

    Article  Google Scholar 

  • Muñiz-Castro MA, Williams-Linera G, Benítez-Malvido J (2015) Restoring montane cloud forest: establishment of three Fagaceae species in the old fields of central Veracruz, Mexico. Rest Ecol 23:26–33

    Article  Google Scholar 

  • Perea R, González R, San Miguel A, Gil L (2011a) Moonlight and shelter cause differential seed selection and removal by rodents. Anim Behav 82:717–723

    Article  Google Scholar 

  • Perea R, San Miguel A, Gil L (2011b) Acorn dispersal by rodents: the importance of re-dispersal and distance to shelter. Basic Appl Ecol 12:432–439

    Article  Google Scholar 

  • Perea R, López D, San Miguel A, Gil L (2012a) Incorporating insect infestation into rodent seed dispersal: better if the larva is still inside. Oecologia 170:723–733

    Article  PubMed  Google Scholar 

  • Perea R, San Miguel A, Martınez-Jauregui M, Valbuena-Carabana M, Gil L (2012b) Effects of seed quality and seed location on the removal of acorns and beechnuts. Eur J For Res 131:623–631

    Article  Google Scholar 

  • Pérez-Ramos IM, Urbieta IR, Marañón T, Zavala MA, Kobe RK (2008) Seed removal in two coexisting oak species: ecological consequences of seed size, plant cover and seed-drop timing. Oikos 117:1386–1396

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ramírez-Bamonde ES, Sánchez-Velásquez LR, Andrade-Torres A (2005) Seedling survival and growth of three species of mountain cloud forest in Mexico, under different canopy treatments. New Forest 30:95–101

    Article  Google Scholar 

  • Ramos-Palacios CR, Badano EI (2014) The relevance of burial to evade acorn predation in an oak forest affected by habitat loss and land use changes. Bot Sci 92:299–308

    Article  Google Scholar 

  • Schnurr JL, Ostfeld RS, Canham CD (2002) Direct and indirect effects of masting on rodent populations and tree seed survival. Oikos 96:402–410

    Article  Google Scholar 

  • Smallwood PD, Steele MA, Faeth SH (2002) The ultimate basis of the caching preferences of rodents, and the oak-dispersal syndrome: tannins, insects, and seed germination. Am Zool 41:840–851

    Google Scholar 

  • Steele MA, Knowles T, Bridle K, Simms EL (1993) Tannins and partial consumption of acorns: implications for dispersal of oaks by seed predators. Am Midl Nat 130:229–238

    Article  Google Scholar 

  • Steele MA, Turner G, Smallwood PD, Wolff JO, Radillo J (2001) Cache management by small mammals: experimental evidence for the significance of acorn-embryo excision. J Mammal 82:35–42

    Article  Google Scholar 

  • Steele MA, Rompré G, Stratford JA, Zhang H, Suchocki M, Marino S (2015) Scatterhoarding rodents favor higher predation risks for cache sites: the potential for predators to influence the seed dispersal process. Integr Zool 10:257–266

    Article  PubMed  Google Scholar 

  • Sunyer P, Muñoz A, Bonal R, Espelta JM (2013) The ecology of seed dispersal by small rodents: a role for predator and conspecific scents. Funct Ecol 27:1313–1321

    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 Manag 229:120–127

    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 

  • Valencia S (2004) Diversidad del género Quercus (Fagaceae) en México. Bol Soc Bot Mex 75:33–53

    Google Scholar 

  • Valencia S, Gual-Díaz (2014) La familia Fagaceae en el Bosque Mesófilo de Montaña de México. Bot Sci 92:193–204

    Article  Google Scholar 

  • Wang B, Chen J (2008) Tannin concentration enhances seed caching by scatter-hoarding rodents: an experiment using artificial ‘seeds’. Acta Oecol 34:379–385

    Article  Google Scholar 

  • Wang B, Chen J, Corlett RT (2014) Factors influencing repeated seed movements by scatter-hoarding rodents in an alpine forest. Sci Rep. doi:10.1038/srep04786

    Google Scholar 

  • Wang W, Ma K, Liu C (1999) Removal and predation of Quercus liaotungensis acorns by animals. Ecol Res 14:225–232

    Article  Google Scholar 

  • Williams-Linera G, Pérez-García I, Tolome J (1996) El bosque mesófilo de montaña y un gradiente altitudinal en el centro de Veracruz, México. La Ciencia y el Hombre 23:149–161

    Google Scholar 

  • Williams-Linera G, Toledo-Garibaldi M, Gallardo-Hernández C (2013) How heterogeneous are the cloud forest communities in the mountains of central Veracruz, Mexico? Plant Ecol 214:685–701

    Article  Google Scholar 

  • Wilms J, Kappelle M (2006) Frugivorous Birds, habitat preference and seed dispersal in a fragmented costa rica montane oak forest landscape. In: Kappelle M (ed) Ecology and conservation of neotropical montane oak forests. Springer, Berlin, pp 309–324

    Chapter  Google Scholar 

  • Xiao Z, Chang G, Zhang Z (2008) Testing the high-tannin hypothesis with scatter-hoarding rodents: experimental and field evidence. Anim Behav 75:1235–1241

    Article  Google Scholar 

  • Xiao Z, Gao X, Steele M, Zhang Z (2010) Frequency-dependent selection by tree squirrels: adaptive escape of nondormant white oaks. Behav Ecol 21:169–175

    Article  Google Scholar 

  • Xiao Z, Zhang Z (2012) Behavioural responses to acorn germination by tree squirrels in an old forest where white oaks have long been extirpated. Anim Behav 83:945–951

    Article  Google Scholar 

  • Xiao Z, Zhang Z, Wang Y (2005) Effects of seed size on dispersal distance in five rodent-dispersed fagaceous species. Acta Oecol 28:221–229

    Article  Google Scholar 

  • Yang Y, Yi X (2012) Partial acorn consumption by small rodents: implication for regeneration of white oak, Quercus mongolica. Plant Ecol 213:197–205

    Article  Google Scholar 

  • Yi X, Wang Z (2015) Context-dependent seed dispersal determines acorn survival of sympatric oak species. Plant Ecol 216:123–132

    Article  Google Scholar 

  • Yi X, Yang Y, Curtis R, Bartlow AW, Agosta SJ, Steele M (2012) Alternative strategies of seed predator escape by early-germinating oaks in Asia and North America. Ecol Evol 2:487–492

    Article  PubMed  PubMed Central  Google Scholar 

  • Yi X, Zhang M, Bartlow AW, Dong Z (2014) Incorporating cache management behavior into seed dispersal: the effect of pericarp removal on acorn germination. PLoS One. doi:10.1371/journal.pone.0092544

    Google Scholar 

  • Yu F, Shi X, Wang D, Yi X, Fan D, Guo T, Lou Y (2015) Effects of insect infestation on Quercus aliena var. acuteserrata acorn dispersal in the Qinling Mountains, China. New For 46:51–61

    Article  Google Scholar 

  • Zhang H, Chen Y, Zhang Z (2008) Differences of dispersal fitness of large and small acorns of Liaodong oak (Quercus liaotungensis) before and after seed caching by small rodents in a warm temperate forest, China. For Ecol Manag 255:1243–1250

    Article  Google Scholar 

Download references

Acknowledgments

We thank Milton Hugo Díaz, Carlos Gustavo Iglesias and all of his team for the facilities provided for collection of seeds and permission to establish an experiment within the TMCF sanctuary of the Francisco Javier Clavijero botanic garden. We also thank Rosario Landgrave for her assistance with statistical analysis. Funding was provided by INECOL (20030.11084). We are also grateful to all of the people who collaborated in some stage of the study and in the revision of previous versions of the manuscript.

Author information

Authors and Affiliations

  1. Red de Ecología Funcional, Instituto de Ecología, A.C. (INECOL), Carretera Antigua a Coatepec No. 351, El Haya, C.P. 91070, Xalapa, Veracruz, Mexico

    María de los Ángeles García-Hernández, Fabiola López-Barrera & Víctor Manuel Vásquez-Reyes

Authors
  1. María de los Ángeles García-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabiola López-Barrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Víctor Manuel Vásquez-Reyes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabiola López-Barrera.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-Hernández, M.Á., López-Barrera, F. & Vásquez-Reyes, V.M. Microhabitat affects acorn removal in three sympatric and endangered Neotropical oak species. Ecol Res 31, 343–351 (2016). https://doi.org/10.1007/s11284-016-1342-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-016-1342-2

Keywords

Search

Navigation