Abstract
Recent studies have demonstrated the higher likelihood of regeneration in forest gaps compared with the understory for the dominant species in pine-oak mixed forest. Here, we tested whether rodent seed predation or dispersal was beneficial for gap regeneration. We tracked the seed predation and dispersal of Quercus aliena var. acuteserrata and Pinus armandii using coded plastic tags in the forest understory close to gaps. Our results demonstrated that the proportions of initial buried seeds of both species were significantly more abundant in the forest understory compared with gaps. After seed caching, however, significantly lower proportions of the seeds of both species survived in the forest understory compared with gaps during the 30-day observation period. The final survival proportions of the seeds cached in the forest understory were lower than those cached in the gaps the next spring, which indicated that small rodents rarely retrieved scatter-hoarded seeds from forest gaps. Our findings suggest that rodent seed predation patterns contribute to the regeneration of the dominant species in gaps compared with the understory in a pine-oak mixed forest. In the study area, reforestation usually involves planting seedlings but direct sowing in forest gaps may be an alternative means of accelerating forest recovery and successional processes.
Similar content being viewed by others
References
Abe H, Matsuki R, Ueno S, Nashimoto M, Hasegawa M (2006) Dispersal of Camellia japonica seeds by Apodemus speciosus revealed by maternity analysis of plants and behavioral observation of animal vectors. Ecol Res 21:732–740
Bélisle M, Desrochers A (2002) Gap-crossing decisions by forest birds: an empirical basis for parameterizing spatially-explicit, individual-based models. Landscape Ecol 17:219–231
Birkedal M, Fischer A, Karlsson M, Löf M, Madsen P (2009) Rodent impact on establishment of direct-seeded Fagus sylvatica, Quercus robur and Quercus petraea on forest land. Scand J For Res 24:298–307
Briggs JS, Vander Wall SB, Jenkins SH (2009) Forest rodents provide directed dispersal of Jeffery pine seeds. Ecology 90:675–687
Caccia FD, Chaneton EJ, Kitzberger T (2006) Trophic and non-trophic pathways mediate apparent competition through post-dispersal seed predation in a Patagonian mixed forest. Oikos 113:469–480
Chang G, Jin TZ, Pei JF, Chen XN, Zhang B, Shi ZJ (2012a) Seed dispersal of three sympatric oak species by forest rodents in the Qinling Mountains, Central China. Plant Ecol 213:1633–1642
Chang G, Wang KF, Wang Z (2012b) Effect of forest rodents on predation and dispersal of Pinus armandii seeds in Qinling Mountains. Acta Ecol Sin 32(10):3177–3181, in Chinese, English abstract
Crawley MJ (1992) Seed predators and plant population dynamics. In: Fenner M (ed) Seeds: The Ecology of Regeneration in Plant Communities. CAB International, Wallingford, pp 157–191
Duncan RS, Chapman CA (1999) Seed dispersal and potential forest succession in abandoned agriculture in tropical Africa. Ecol Appl 9:998–1008
Forget PM, Vander Wall SB (2001) Scatter-hoarding rodents and marsupials: convergent evolution on diverging continents. Trends Ecol Evol 16(2):65–67
Gómez JM (2003) Spatial patterns in long-distance dispersal of Quercus ilex acorns in a heterogeneous landscape. Ecography 26:573–584
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
Hoshizaki K, Suzuki W, Sasaki S (1997) Impacts of secondary seed dispersal and herbivory on seedling survival in Aesculus turbinata. J Veg Sci 8:735–742
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–218
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
Iida S (1996) Quantitative analysis of acorn transportation by rodents using magnetic locator. Vegetatio 124:39–43
Iida S (2006) Dispersal patterns of Quercus serrata acorns by wood mice in and around canopy gaps in a temperate forest. For Ecol Manag 227:71–78
Jansen PA, Forget PM (2001) Scatter-hoarding rodents and tree regeneration. In: Bongers F, Charles-Dominique P, Forget PM, Théry M (eds) Dynamics and plant–animal interactions in a neotropical rainforest. Nouragues: Kluwer Academic Publisher, Dordrecht, The Netherlands, pp 275–288
Jansen PA, Bartholomeus M, Bongers F, Elzinga JA, Ouden J, Van Wieren SE (2002) The role of seed size in dispersal by a scatterhoarding rodent. In: Levey D, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford, pp 209–225
Jansen PA, Hemerik L, Bongers F (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecol Monogr 74:369–389
Janzen DH (1970) Herbivores and the number of tree species in tropical forest. Am Nat 104:501–528
Lan GY, Lei RD, An F, Zhao YH, Chen W (2006) Spatial distribution pattern, its scale, and gap characteristics of Pinus armandii population in Qinling Mountains. Chin J Ecol 25(6):652–656, in Chinese, English abstract
Li HJ, Zhang ZB (2003) Effect of rodents on acorn dispersal and survival of the Liaodong oak (Quercus liaotungensis Koidz.). For Ecol Manag 176:387–396
Lima SL (1998) Stress and decision making under the risk of predation: recent development from behavioral, reproductive, and ecological perspectives. Adv Study Behav 27:215–290
Liu CQ, Liu GL, Shen Z, Yi XF (2013) Effects of disperser abundance, seed type, and interspecific seed availability on dispersal distance. Acta Theriol 58:267–278
Lu JQ, Zhang ZB (2004) Effects of habitat and season on removal and hoarding of seeds of wild apricot (Prunus armeniaca) by small rodents. Acta Oecol 26:247–254
Manson RH, Stiles EW (1998) Links between microhabitat preferences and seed predation by small mammals in old fields. Oikos 82:37–50
Mohr K, Vibe-Petersen S, Jeppesen LL, Bildsøe M, Leirs H (2003) Foraging of multimammate mice, Mastomys natalensis, under different predation pressure: cover, patch-dependent decisions and density-dependent GUDs. Oikos 100:459–468
Muňoz A, Bonal R (2011) Linking seed dispersal to cache protection strategies. J Ecol 99:1016–1025
Pérez-Ramos IM, Marañón T (2008) Factors affecting post-dispersal seed predation in two coexisting oak species microhabitat, burial and exclusion of large herbivores. For Ecol Manag 255:3506–3514
Price MV, Jenkins SH (1986) Rodents as seeds consumers and dispersers. In: Murray DR (ed) Seed Dispersal. Academic Press, Sydney, Australia, pp 191–235
Price MV, Waser NM, McDonald S (2000) Seed caching by heteromyid rodents from two communities: implications for coexistence. J Mammal 81:97–106
Russell SK, Schupp EW (1998) Effects of microhabitat patchiness on patterns of seed dispersal and seed predation of Cercocarpus ledifolius (Rosaceae). Oikos 81:424–443
Scheper J, Smit C (2011) The role of rodents in the seed fate of a thorny shrub in an ancient wood pasture. Acta Oecol 37:133–139
Smit C, Verwijmeren M (2011) Tree-shrub associations in grazed woodlands: first rodents, then cattle? Plant Ecol 212:483–493
Smit C, Gusberti M, Müller-Schärer H (2006) Safe for saplings; safe for seeds? For Ecol Manag 237:471–477
Sone K, Hiroi S, Nagahama D, Ohkubo C, Nakano E, Murao S, Hata K (2002) Hoarding of acorns by granivorous mice and its role in the population processes of Pasania edulis (Makino) Makino. Ecol Res 17:553–564
Stapanian MA, Smith CC (1978) A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts. Ecology 59:884–896
Theimer TC (2001) Seed scatterhoarding by white-tailed rats: consequences for seedling recruitment by an Australian rain forest tree. J Trop Ecol 17:177–189
van Ginkel HAL, Kuijper DPJ, Churski M, Zub K, Szafrańska P, Smit C (2013) Safe for saplings not safe for seeds: Quercus robur recruitment in relation to coarse woody debris in Białowieża Primeval Forest, Poland. For Ecol Manag 304:73–79
Vander Wall SB (1990) Food Hoarding in Animals. University of Chicago Press, Chicago
Vander Wall SB, Jenkins SH (2003) Reciprocal pilferage and the evolution of food-hoarding behavior. Behav Ecol 14:656–667
Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464
Wenny DG (1999) Two-stage dispersal of Guarea glabraand G. Kunthiana (Meliaceae) in Monteverde, Costa Rica. J Trop Ecol 15:481–496
Wenny DG, Levy DJ (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proc Natl Acad Sci U S A 95:6204–6207
Wilkinson EB, Branch LC, Miller DL (2013) Functional habitat connectivity for beach mice depends on perceived predation risk. Landscape Ecol 28:547–558
Xiao XG, Xiong GM, Xie ZQ (2002) The regeneration of tree species in the mixed evergreen-deciduous broad-leaved forests in the Shennongjia Mountains, Hubei province. Acta Ecol Sin 22(11):2001–2005, in Chinese, English abstract
Xiao ZS, Zhang ZB, Wang YS (2005a) Effects of seed size on dispersal distance in five rodent-dispersed fagaceous species. Acta Oecol 18:221–229
Xiao ZS, Zhang ZB, Wang YS (2005b) The effects of seed abundance on seed predation and dispersal by rodents in Castanopsis fargesii (Fagaceae). Plant Ecol 177:249–257
Xiao ZS, Jansen PA, Zhang ZB (2006) Using seed-tagging methods for assessing post-dispersal seed fate in rodent-dispersed trees. For Ecol Manag 223:18–23
Yi XF, Zhang ZB (2008) Seed predation and dispersal of glabrous filbert (Corylus heterophylla ) and pilose filbert (Corylus mandshurica) by small mammals in a temperate forest, northeast China. Plant Ecol 196:135–142
Yu F, Wang DX, Shi XX, Yi XF, Li G (2013a) Seed dispersal by small rodents favours oak over pine regeneration in the pine-oak forests of the Qinling Mountains, China. Scand J For Res 28:540–549
Yu F, Wang DX, Shi XX, Yi XF, Huang QP, Hu YN (2013b) Effects of environmental factors on tree seedling regeneration in a pine-oak mixed forest in the Qinling Mountains, China. J Mt Sci 10:845–853
Zhang ZB, Wang FS (2001) Effect of rodents on seed dispersal and survival of wild apricot (Prunus armeniaca). Acta Ecol Sin 21:839–845
Acknowledgments
The authors thank two anonymous reviewers for valuable comments on the manuscript and Dr. Duncan E. Jackson for improving the English language content of the manuscript. We also thank Qinling National Forest Ecosystem Research Station at Huoditang, Ningshaan County, Shaanxi Province, for much support to our field investigation. Funds were provided by the Special Research Program for Public–Welfare Forestry of the State Forestry Administration of China (No. 20100400206), National Natural Science Funds (No. 31070570), and CFERN & GENE Award Funds on Ecological Paper. The experiments complied with the current laws of our country.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Dries Kuijper
Fei Yu and Xiaoxiao Shi contributed equally to this work
Rights and permissions
About this article
Cite this article
Yu, F., Shi, X., Wang, D. et al. Seed predation patterns favor the regeneration of dominant species in forest gaps compared with the understory in an oak-pine mixed forest. Acta Theriol 59, 495–502 (2014). https://doi.org/10.1007/s13364-014-0192-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13364-014-0192-y