Frequency-dependent selection by tree squirrels: adaptive escape of nondormant white oaks

Xiao, Zhishu; Gao, Xu; Steele, Michael; Zhang, Zhibin

doi:10.1093/beheco/arp169

Cited by 51 publications

(67 citation statements)

References 32 publications

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“…It is notable that the improved mutualism is likely caused by adaptation of both plants (high regeneration capacity) and rodents (root pruning). Seeds of P. kerrii were observed to germinate very rapidly after seed fall, often within 1 week, which seems to be a common strategy adopted by many tree species in tropical forests Vazquez-Yanes and Orozco-Segovia 1993;Xiao et al 2009Xiao et al , 2010. However, instead of developing into seedlings, the germinated seeds of P. kerrii first developed into indigestible taproots and then decomposed within 2-3 months.…”

Section: Discussionmentioning

confidence: 99%

“…Germinated seeds can escape seed predation by rodents when their energy reserves in cotyledons or endosperms are converted into indigestible taproots or seedlings (Barnett 1977;Fox 1982;Hadj-Chikh et al 1996;Jansen et al 2006;Steele et al 2001Steele et al , 2006Xiao et al 2010). Thus, early seed germination of non-dormant seeds is likely an evolutionary adaptation to escape seed predation by rodents (Chang et al 2009;Hadj-Chikh et al 1996).…”

Section: Introductionmentioning

confidence: 99%

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High regeneration capacity helps tropical seeds to counter rodent predation

et al. 2011

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

High regeneration capacity helps tropical seeds to counter rodent predation

et al. 2011

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“…However, we noticed that chipmunks preferred to select non-germinated acorns for caching in the acorn addition experiments. This discrepancy could be explained by the frequency-dependent effect that non-germinated acorns outnumber the germinating ones (Xiao et al 2010).…”

Section: Discussionmentioning

confidence: 99%

“…Embryo excision of white oak species by several species of Sciurus has been well documented in North America (Fox 1982;Steele et al 2001aSteele et al , b 2006Steele 2008), whereas no other rodent species are found to excise the embryo of white oak acorns, although many of them are sensitive to germination schedules. Xiao et al (2009Xiao et al ( , 2010 recently reported the behavior of embryo excision by Pallas's squirrel (Callosciurus erythraeus) and Père David's Rock squirrel (Sciurotamias davidianus) in Asia, implying a convergent evolution tactic to counter acorn germination among squirrel species across different continents. Although there are few studies that document re-visitation of scatter hoards (Vander Wall and Joyner 1998), Siberian chipmunks were found to prune radicles of some cached acorns for more than once in our study, displaying a deliberate behavior of cache management.…”

Section: Discussionmentioning

confidence: 99%

Repeated radicle pruning of Quercus mongolica acorns as a cache management tactic of Siberian chipmunks

Yang

2011

acta ethol

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Many rodents hoard seeds as a means of ensuring food availability during scarcity. Siberian chipmunks (Tamias sibiricus) feed on acorns of white oak Quercus mongolica and hoard them for future use. Such caches may deteriorate due to the early germination of the acorns in autumn, which can be inhibited by radicle pruning or embryo excision. Siberian chipmunks are found to frequently prune the radicles of germinated acorns of Q. mongolica; however, whether this behavior is a kind of cache management tactic remains unclear. Here, we performed semi-natural enclosure and field experiments to test the role of radicle pruning in cache management of T. sibiricus. We found that T. sibiricus preferred non-germinated acorns and tended to prune radicles of germinating acorns when scatter-hoarding them, but did not perform the behavior of embryo excision by squirrels. Both semi-natural enclosure and field experiments showed that T. sibiricus not only pruned radicles repeatedly but removed radicles varied in length from acorns, which significantly postponed acorn germination and radicle growth. These observations suggest that radicle pruning would be an evolutionary tactic for cache management of Siberian chipmunks.

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“…On the forest floor, when rains occur daily (end of summer, beginning of autumn), mild acorn hydration and dehydration might concentrate germination within a short time period. As a consequence, seedlings might be well established before the beginning of the dry season, preventing acorn depredation by rodents and insect larvae (Xiao et al 2009). However, during the dry season, even entire seedlings (5 months old) can be consumed by gophers when there is an overall shortage of food (personal observations).…”

Section: Seed Water Content and Germinationmentioning

confidence: 99%

Effect of hydropriming and acclimation treatments on Quercus rugosa acorns and seedlings

et al. 2011

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To facilitate restoration of the lava field forests surrounding Mexico City, we developed methods to improve the germination and field seedling performance of Quercus rugosa using hydropriming (regulated hydration of seeds in water), and we used special watering regimes to improve seedling acclimation. The size, dry mass, fresh mass and water content of seeds were measured, and curves were generated to evaluate acorn hydration and dehydration. The effects of stratification (5°C), heat shock (50°C) and scarification on germination were tested. All treated seeds and controls were germinated in control chambers at 21°C. One hydropriming cycle (PC) consisted of two hydration days followed by two dehydration days; treatments of 1, 2 and 3 PCs were tested. Seedlings from 1PC to 2PC were acclimated in a shade house under high and low watering regimes (400 and 200 mL week -1 , respectively). In the shade house and field, the effects of hydropriming and watering treatments were evaluated by measuring length, basal diameter, crown cover, number of leaves and branches and leaf area of seedlings. Dry and fresh mass were used to calculate acorn water content. Dehydration and hydration curves displayed hysteresis. Acorns exhibited physiological dormancy, which could be overcome by stratification or by 1 month of storage. 1PC led to increased germination rates and final germination. In both the shade house and field, 1PC showed a positive effect on all seedling growth parameters except branch number. Field survival was not affected. Generally, 1PC favoured efficient seed germination, seedling vigour and homogenous plant production.

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Frequency-dependent selection by tree squirrels: adaptive escape of nondormant white oaks

Cited by 51 publications

References 32 publications

High regeneration capacity helps tropical seeds to counter rodent predation

High regeneration capacity helps tropical seeds to counter rodent predation

Repeated radicle pruning of Quercus mongolica acorns as a cache management tactic of Siberian chipmunks

Effect of hydropriming and acclimation treatments on Quercus rugosa acorns and seedlings

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