Skip to main content
Log in

High regeneration capacity helps tropical seeds to counter rodent predation

  • Plant-Animal interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Rapid germination of non-dormant seeds is one adaptation plants have evolved to counter seed predation by rodents. Some rodent species have evolved behaviors that prevent or slow the seed germination process through seed embryo removal or seed pruning; however, no plant species is known to have successfully escaped embryo removal or seed pruning by rodents. Here, we report that the non-dormant seeds of Pittosporopsis kerrii Craib in tropical rain forests in China have a high regeneration capacity to counter seed pruning by rodents. We found seed pruning, instead of embryo removal, was commonly used by rodents to increase food storage time by slowing down the seed germination process, but that P. kerrii seeds have a high regeneration capacity to escape seed predation by rodents: all pruned seeds, pruned roots and embryo-removed seeds by rodents or people retain the ability to develop into seedlings. Seeds of P. kerrii also have other capacities (i.e. rapid seed decomposition and indigestible dormant taproots) to escape predation by reducing the plant’s attractiveness to rodents. The association between seed pruning behavior in rodents and high regeneration capacity of pruned seeds or roots in P. kerrii seeds are likely novel adaptation strategies adopted by seeds and rodents, respectively.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Barnett RJ (1977) The effect of burial by squirrels on germination and survival of oak and hickory nuts. Am Mid Nat 98:319–330

    Article  Google Scholar 

  • Chang G, Xiao ZS, Zhang ZB (2009) Hoarding decisions by Edward’s long-tailed rats (Leopoldamys edwardsi) and South China field mice (Apodemus draco): the responses to seed size and germination schedule in acorns. Behav Process 82:7–11

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dalling JW, Harms KE (1999) Damage tolerance and cotyledonary resource use in the tropical tree Gustavia superba. Oikos 85:257–264

    Article  Google Scholar 

  • Elliott L (1978) Social behavior and foraging ecology of eastern chipmunk (Tamias striatus) in the Adirondack Mountains. Smithson Contrib Zool 265:1–107

    Article  Google Scholar 

  • Fox JF (1982) Adaptation of gray squirrel behavior to autumn germination by white oak acorns. Evolution 36:800–809

    Article  Google Scholar 

  • Grubb PJ, Metcalfe DJ, Grubb EAA, Jones GD (1998) Nitrogen-richness and protection of seeds in Australian tropical rainforest: a test of plant defence theory. Oikos 82:467–482

    Article  Google Scholar 

  • Hadj-Chikh LZ, Steele MA, Smallwood PD (1996) Caching decisions by grey squirrels: a test of the handling time and perishability hypotheses. Anim Behav 52:941–948

    Article  Google Scholar 

  • Hulme PE (1997) Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111:91–98

    Article  Google Scholar 

  • Jansen PA, Bongers F, Prins HHT (2006) Tropical rodents change rapidly germinating seeds into long-term food supplies. Oikos 113:449–458

    Article  Google Scholar 

  • Janzen DH (1969) Seed-eaters versus seed size, number, toxicity and dispersal. Evolution 23:1–27

    Article  Google Scholar 

  • Lan GY et al (2008) Establishment of Xishuangbanna tropical forest dynamics plot: species compositions and spatial distribution patterns. J Plant Ecol Sin 32:287–298

    Google Scholar 

  • Mack AL (1998) An advantage of large seed size: tolerating rather than succumbing to seed predators. Biotropica 30:604–608

    Article  Google Scholar 

  • McEuen AB, Steele MA (2005) Atypical acorns appear to allow seed escape after apical notching by squirrels. Am Mid Nat 154:450–458

    Article  Google Scholar 

  • Mendoza E, Dirzo R (2009) Seed tolerance to predation: evidence from the toxic seeds of the buckeye tree (Aesculus Californica; Sapindaceae). Am J Bot 96:1255–1261

    Article  PubMed  Google Scholar 

  • Rosenthal GA, Bell EA (1979) Naturally occurring, toxic nonprotein amino acids. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic, New York, pp 353–385

    Google Scholar 

  • Steele MA (2008) Evolutionary interactions between tree squirrels and trees: a review and synthesis. Curr Sci India 95:871–876

    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, Manierre S, Genna T, Contreras TA, Smallwood PD, Pereira ME (2006) The innate basis of food-hoarding decisions in grey squirrels: evidence for behavioural adaptations to the oaks. Anim Behav 71:155–160

    Article  Google Scholar 

  • Vallejo-Marin M, Dominguez CA, Dirzo R (2006) Simulated seed predation reveals a variety of germination responses of neotropical rain forest species. Am J Bot 93:369–376

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philos Trans R Soc Lond B 365:989–997

    Article  Google Scholar 

  • Vazquez-Yanes C, Orozco-Segovia A (1993) Patterns of seed longevity and germination in the tropical rainforest. Annu Rev Ecol Syst 24:69–87

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Xiao ZS, Harris MK, Zhang ZB (2007) Acorn defenses to herbivory from insects: implications for the joint evolution of resistance, tolerance and escape. For Ecol Manag 238:302–308

    Article  Google Scholar 

  • Xiao ZS, Gao X, Jiang MM, Zhang ZB (2009) Behavioral adaptation of Pallas’s squirrels to germination schedule and tannins in acorns. Behav Ecol 20:1050–1055

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zhang ZB (2003) Mutualism or cooperation among competitors promotes coexistence and competitive ability. Ecol Model 164:271–282

    Article  Google Scholar 

  • Zhang ZB, Wang FS (2001) Effect of rodents on seed dispersal and survival of wild apricot Prunus armeniaca. Acta Ecol Sin 21:839–845

    Google Scholar 

  • Zhang HM, Zhang ZB (2008) Endocarp thickness affects seed removal speed by small rodents in a warm-temperate broad-leafed deciduous forest, China. Acta Oecol 34:285–293

    Article  Google Scholar 

  • Zhang ZB, Xiao ZX, Li HJ (2005) Impact of small rodents on tree seeds in temperate and subtropical forests, China. In: Forget PM, Lambert J, Hulme PE, Vander Wall SB (eds) Seed fates: predation, dispersal and seedling establishment. CAB International, Wallingford, pp 269–282

    Chapter  Google Scholar 

Download references

Acknowledgments

This work was supported by the grant of National Natural Science Foundation (grant no. 30930016), the State Basic Research Program (grant no. 2007CB109102), and the CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences. We are grateful to the Xishuangbanna Station of Tropical Rainforest Ecosystem Studies for support in field work and for providing vegetation data of the study sites. We are thankful to Prof. Michael Steel, Wilkes University, and Prof. Stephen B. Vander Wall, University of Nevada, for providing valuable comments after reviewing an earlier version of this manuscript. Dr. Guangshun Jiang provided help in conducting statistical analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhibin Zhang.

Additional information

Communicated by Mark Chappell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cao, L., Xiao, Z., Wang, Z. et al. High regeneration capacity helps tropical seeds to counter rodent predation. Oecologia 166, 997–1007 (2011). https://doi.org/10.1007/s00442-011-1908-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-1908-1

Keywords

Navigation