Abstract
Seed dispersal by scatter hoarders is widely assumed to involve directed dispersal, in which microhabitats selected for caching also benefit seedling establishment and growth. However, in many systems, this may not be true if animal-favored cache sites do not match the safe sites for plants, or if cache sites benefit the plant in one life stage and not another. Here, we investigated whether cache sites selected by rodents are favorable for seedling establishment and growth of shade-intolerant wild apricot (Prunus armeniaca Linn.) in northern China. We tracked tagged seeds and compared the germination and growth of seedlings from rodent-cached seeds with that of naturally established seedlings in a secondary forest and shrubland stand. Rodents preferred to cache seeds under shrubs with medium canopy cover (31–60 %) in litter substrate in the secondary forest, and under shrubs with high canopy cover (>60 %) in soil or litter substrate in the shrubland stand, neither of which conveyed an advantage for seedling establishment. Although fewer caches were made along shrub edges, or under low canopy cover (≤30 %) in the secondary forest, or along shrub edges, open areas of grass, or under low canopy cover in the shrubland stand, these cache sites consistently contributed to higher survival rates. The microhabitats of grass, soil, or low canopy cover significantly promoted the emergence, survival, and growth of naturally established seedlings. Our results are best explained by the conflicting demands of rodents for caching seeds in more secure sites and P. armeniaca’s high-light requirements for seedling recruitment. We argue that the relationship between favored cache sites for seed hoarders and safe sites for plants will often not match but may still allow a reasonable rate of establishment and regeneration.
Similar content being viewed by others
References
Briggs JS, Vander Wall SB, Jenkins SH (2009) Forest rodents provide directed dispersal of Jeffrey pine seeds. Ecology 90:675–687
Carlo TA, Campos-Arceiz A, Steele MA, Xiong W (2011) Frugivory and seed dispersal: integrating patterns, mechanisms and consequences of a key animal-plant interaction. Integr Zool 6:165–167
Chimera CG, Drake DR (2011) Could poor seed dispersal contribute to predation by introduced rodents in a Hawaiian dry forest? Biol Invasions 13:1029–1042
Donohue K (1997) Seed dispersal in Cakile edentula var. lacustris: decoupling the fitness effects of density and distance from the home site. Oecologia 110:520–527
Garcia D, Banuelos MJ, Houle G (2002) Differential effects of acorn burial and litter cover on Quercus rubra at the limit of its range in eastern North America. Can J Bot 80:1115–1120
Green AK, Ward D, Griffiths ME (2009) Directed dispersal of mistletoe (Plicosepalus acaciae) by yellow-vented Bulbuls (Pycnonotus xanthopygos). J Ornithol 150:167–173
Hoshizaki K, Suzuki W, Nakashizuka T (1999) Evaluation of secondary dispersal in a large-seeded tree Aesculus turbinate: a test of directed dispersal. Plant Ecol 144:167–176
Howe HF, Miriti MN (2004) When seed dispersal matters. Bioscience 54:651–660
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228
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
Kitajima K (1994) Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419–428
Klinger R, Rejmánek M (2010) A strong conditional mutualism limits and enhances seed dispersal and germination of a tropical palm. Oecologia 162:951–963
Li H, Zhang Z (2003) Effect of rodents on acorn dispersal and survival of the Liaodong oak (Quercus liaotungensis Koidz.). For Ecol Manage 176:387–396
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
Lu J, Zhang Z (2004) Effects of microhabitat and season on removal and hoarding of seeds of wild apricot (Prunus armeniaca) by small rodents. Acta Oecol 26:247–254
Lu J, Li H, Zhang Z (2005) Seed rain of wild apricot and predation by small rodents. Chin J Zool 24:528–532 (in Chinese with English abstract)
McAlpine KG, Jesson LK (2008) Linking seed dispersal, germination and seedling recruitment in the invasive species Beberis darwinii (Darwin’s barberry). Plant Ecol 197:119–129
Muñoz A, Bonal R (2011) Linking seed dispersal to cache protection strategies. J Ecol 99:1016–1025
Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285
Pearson KM, Theimer TC (2004) Seed-caching responses to substrate and rock cover by two Peromyscus species: implications for pinyon pine establishment. Oecologia 141:76–83
Rey PJ, 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
Schupp EW (2007) The suitability of a site for seed dispersal is context-dependent. In: Dennis AJ, Schupp EW, Green RJ, Westcott DW (eds) Seed dispersal: theory and its application in a changing world. CAB International, Wallingford, pp 445–462
Spiegel O, Nathan R (2010) Incorporating density dependence into the directed-dispersal hypothesis. Ecology 91:1538–1548
Spiegel O, Nathan R (2012) Empirical evaluation of directed dispersal and density-dependent effects across successive recruitment phases. J Ecol 100:392–404
SPSS Inc (2008) SPSS for Windows. Version 16.0. SPSS, Chicago, IL
Vander Wall SB (1990) Food hoarding in animals. University of Chicago Press, Chicago
Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Phil Trans R Soc B 365:989–997
Vander Wall SB, Jenkins SH (2003) Reciprocal pilferage and the evolution of food-hoarding behavior. Behav Ecol 14:656–667
Visser MD, Muller-Landau HC, Wright SJ, Rutten G, Jansen PA (2011) Tri-trophic interactions affect density dependence of seed fate in a tropical forest palm. Ecol Lett 14:1093–1100
Wenny DG (2001) Advantages of seed dispersal: a reevaluation of directed dispersal. Evol Ecol Res 3:51–57
Wenny DG, Levey DJ (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proc Natl Acad Sci USA 95:6204–6207
Xiao Z, Jansen P, Zhang Z (2006) Using seed-tagging methods for assessing post-dispersal seed fate in rodent-dispersed trees. For Ecol Manage 223:18–23
Zhang H (2007) Interactions between rodents and forest seeds in the Donglingshan Mountain, northwestern Beijing. PhD dissertation, Institute of Zoology, Chinese Academy of Science, Beijing, China
Zhang Z, Wang F (2001) Effect of rodents on seed dispersal and survival of wild apricot (Prunus armeniaca). Acta Ecol Sinica 21:839–845
Zhang H, Zhang Z (2008) Endocarp thickness affects seed removal speed by small rodents in a warm-temperate broad-leafed deciduous forest, China. Acta Oecol 34:285–293
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 Manage 255:1243–1250
Acknowledgments
We thank F. Wang, C. Yi, Y. Li, and X. Shang for assistance with field work. M. A. Steele acknowledges the support of a Bullard Fellowship from Harvard Forest during preparation of the manuscript. This work was partially supported by the National Natural Science Foundation of China (31172102, 30800120, 30930016), the CCNU Project (CCNU11A02010), and the State Basic Research Program of China (2007BC109102).
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
See Table 1.
Rights and permissions
About this article
Cite this article
Zhang, H., Luo, Y., Steele, M.A. et al. Rodent-favored cache sites do not favor seedling establishment of shade-intolerant wild apricot (Prunus armeniaca Linn.) in northern China. Plant Ecol 214, 531–543 (2013). https://doi.org/10.1007/s11258-013-0187-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-013-0187-9