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11-2010
Disappearing Plants: Why They Hide and How They Return
Jennifer R. Gremer
Anna Sala University of Montana - Missoula, [email protected]
Elizabeth E. Crone
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Recommended Citation Gremer, Jennifer R.; Sala, Anna; and Crone, Elizabeth E., "Disappearing Plants: Why They Hide and How They Return" (2010). Biological Sciences Faculty Publications. 319. https://scholarworks.umt.edu/biosci_pubs/319
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Ecology, 91(11), 2010, pp. 3407-3413 ? 2010 by the Ecological Society of America
return Disappearing plants: why theyhide and how they
Jennifer R. Gremer,1,3 Anna Sala,1 and Elizabeth E. Crone2
1Division of Biological Sciences, University ofMontana, Missoula, Montana 59812 USA 2 Wildlife Biology Program, College of Forestry and Conservation, University ofMontana, Missoula, Montana 59812 USA
Abstract. Prolonged dormancy is a life-historystage in which mature plants fail to resprout for one or more growing seasons and instead remain alive belowground. Prolonged dormancy is relativelycommon, but the proximate causes and consequences of this intriguing strategyhave remained elusive. In this studywe testedwhether stored resources are associated with remaining belowground, and investigated the resource costs of remaining belowground during the growing season. We measured stored resources at the beginning and end of the growing season in Astragalus scaphoides, an herbaceous perennial in southwestMontana, USA. At the beginning of the growing season, dormant plants had lower concentrations of stored mobile carbon (nonstructural carbohydrates, NSC) than did emergent plants. Surprisingly, during the growing season, dormant plants gained as much NSC as photosynthetically active plants, an increasemost likelydue to remobilization of structural carbon. Thus, low levels of storedNSC were associated with remaining belowground, and remobilization of structuralcarbon may allow for dormant plants to emerge in later seasons. The dynamics ofNSC in relation to dormancy highlights the ability of plants to change their own resource status somewhat independently of resource assimilation, as well as the importance of considering stored resources in understanding plant responses to the environment.
Key words: Astragalus scaphoides; carbon metabolism; life history; nonstructural carbohydrates; prolonged dormancy; stored resources; vegetative dormancy.
Introduction consequences of prolonged dormancy in a long-lived
native perennial, Astragalus scaphoides. Prolonged dormancy is a relatively common stage in known as herbaceous perennial plants in which mature plants Prolonged dormancy (also "vegetative see Lesica and Steele 1994, Shefferson remain belowground during one or more entire growing dormancy"; is differentfrom other, more extensively studied seasons instead of emerging to grow and acquire 2009) of The metabolic costs of resources (Lesica and Steele 1994). Interestingly,pro types plant dormancy. mature longed dormancy occurs in many unrelated species, maintaining plant parts belowground during are than costs of seed suggesting that it is a strategy that has evolved many prolonged dormancy likelyhigher in contrast to seasonal times (Lesica and Steele 1994). Prolonged dormancy has dormancy. Further, dormancy, where all individuals been most frequentlyobserved in theOrchid family,but go dormant, prolonged dormancy often involves a fractionof individuals in it has been reported in over 10 plant families and 52 only any given The lack of and species of plants (Lesica and Steele 1994, Shefferson year. photosynthesis reproduction by individuals have 2009). Despite the fact that it is relativelycommon, the undergoing prolonged dormancy could fitness the causes and consequences for this behavior remain large negative impacts. However, prevalence or even unclear. Why do some plants forego the opportunity of this strategy suggests either neutral positive to grow and reproduce, while others resume seasonal effects.For instance, prolonged dormancy may allow or activity?Here we investigate the proximate causes and individuals to avoid large resource demands risks (e.g., biotic or abiotic stress) associated with growing received 9 October revised 8 March 2010; Manuscript 2009; aboveground tissues (Shefferson2009). To date, little is accepted 10 March 2010. Corresponding Editor: N. Underwood. known about what causes certain individuals to remain 3 E-mail: [email protected] belowground while others are able to grow and
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reproduce aboveground, or about the costs and benefits belowground during otherwise favorable conditions? of doing so. If prolonged dormancy is associated with stored Two leading hypotheses have been proposed to resources, we expect that dormant plants will be explain prolonged dormancy: (1) it occurs in response lacking in one or more stored resources at the to external cues, such as herbivory or drought (Morrow beginning of the growing season. If prolonged dor and Olfelt 2003, Shefferson et al. 2003, 2005?, Miller et mancy is similar to other types of dormancy, such as al. 2004, Lesica and Crone 2007), and (2) plants remain winter dormancy, we expect dormant plants to deplete belowground because they lack resources to build leaves stored resources over the growing season. However, if (Shefferson et al. 2005a, Shefferson et al. 2006). If prolonged dormancy differs fundamentally from other prolonged dormancy occurs in response to some critical types of dormancy, dormant plants may be able to limiting resource, then plants must gain this resource conserve or acquire stored resources during the while dormant so they can emerge in later years. growing season. However, plants typically lose stored resources during Methods the non-growing season due to metabolic demands and lack of photosynthesis (Wyka 1999). Prolonged dor Study species could incur a similar or even resource mancy greater Astragalus scaphoides (Fabaceae) is an iteroparous cost. Plants that are dormant the summermiss a during legume with a long, narrow taproot, found on south season of carbon and gain through photosynthesis, facing slopes in high-elevation sagebrush steppe com lose even more carbon to in summer likely respiration munities (Lesica 1995). It has an estimated life span of than inwinter due to soil higher temperatures (Amthor 21 years (Ehrlen and Lehtila 2002), and does not If would be a life 2000). so, prolonged dormancy costly reproduce vegetatively (Lesica 1995). On average, 20% because need stored resources to stage plants remaining of the individuals in our population are dormant in any survive another as well as to initiate seasonal winter, given year (Crone and Lesica 2004) and dormancy and Such resource costs could growth reproduction. events typically last one year. Dormancy is weakly have on future significant impacts performance and, correlated (0.2 < r< 0.3) with warm, dryweather in the on fitness. It is that metabolism ultimately, possible spring (J.Gremer, unpublishedanalyses). However, even differ during prolonged dormancy may fundamentally in years of high dormancy, only a portion of individuals from winter and or that dormancy during drought, remain dormant while the rest emerge as vegetative or individuals that remain dormant the during growing reproductive plants. Plants flower approximately in season resources may gain through belowground pro alternate years (Lesica 1995, Crone et al. 2005), and cesses. no one To date, has tested these alternatives by this strategyis driven by fluctuations in stored resources of stored resources in directlymeasuring the dynamics rather than changes in climate (Crone et al. 2005, 2009). dormant plants. Plants that do not flowermay produce leaves and be causes We investigated the and consequences of vegetative, or remain dormant during the growing prolonged dormancy by measuring stored resources of season. at a plants different life history stages in long-lived If plants emerge aboveground, they initiategrowth in perennial wildflower, Astragalus scaphoides. We em April, and biomass senesces back to perennating roots in phasized stored resources not only because they are a early July.Mature dormant plants can be located by component of one of the leading hypotheses for dried flowering stalks that persist aboveground for 2-3 prolonged dormancy but also because they reflect years. Evidence of previous flowering events can be seen current as well as condition integrate past performance on root crowns, because the flowering stalks leave scars as resource to such capture and allocation various life that are apparent even after several years. history functions (Chap?n et al. 1990, Crone et al. Harvests 2009). Stored resources are critical for numerous plant functions, including plant growth following winter Sampling took place during 2006-2008 at Sheep dormancy, reproduction, recovery from herbivory, Corral Ridge, located in Beaverhead County in south and survival (Mooney and Hays 1973, Ho and Rees western Montana, USA (45?06'55" N, 113?02'58" W). 1976, Chap?n et al. 1990, Boyce and Volenec 1992, The climate is semiarid;mean annual precipitation is 250 Zimmerman and Whigham 1992,Van der Heyden and mm, with peak rainfall inMay (Crone and Lesica 2006). Stock 1996, Kobe 1997,Wyka 1999). Furthermore, The 10 upper cm of taproot (closest to the soil surface) stored resources play critical roles in signaling path from randomly selected dormant, vegetative, and = ways that control plant growth and development reproductive plants (n between 5 and 7 plants per life (Halford and Paul 2003, Rolland et al. 2006, Lee et stage) were destructively harvested in earlyMay each al. 2007). Here, we asked: (1) Are stored resources year, as soon as the three stages could be clearly associated with the entry into prolonged dormancy? (2) distinguished. In 2007 and 2008 roots were also What are the resource consequences of remaining harvested at the end of the growing season in July,after
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aboveground biomass of emergent plants had senesced. to analyze concentrations (Miller and Kotuby While we could not control for the age of dormant Amacher 1996). Because did not appear to have any plants, we harvested only reproductivelymature indi major role (see Results, below) samples from 2008 were viduals (as evidenced on root crown, see Study species, not sent for analysis. above). Because it is not possible to sample thesenarrow Since A. scaphoides has long narrow taproots (
This content downloaded from 150.131.192.151 on Wed, 30 Oct 2013 18:29:29 PM All use subject to JSTOR Terms and Conditions NOTES Vol. ^ Ecology, 91,NoTll^^^^^J = among life stages (ANOVA; for stage: F2?6 1.933, = = = X 0.17; for time Fh27 2.616, 0.12; for time stage = = ^2,26 2.374, P 0.12). Increases inNSC were driven by sucrose concentrations, the main transport sugar in = plants (Fig. 2B, average gain 6.9%, 95% CI [4.13 9.66]). At the end of the season, NSC concentrations did = not differamong lifestages (ANOVA; stageF2?5 2.54, = 0.10).
Nitrogen and phosphorus Dormant plants were not depleted in either or at the beginning of the season, and they did not gain mineral nutrients during the growing season. Dormant plants had higher content than both reproductiveand vegetativeplants at thebeginning of the season (Fig. IB, = ANOVA; stageF2A6 7.72, < 0.001). However, they did not gain during the season (95% CI [-0.301, 0.300]) while reproductive and vegetative plants did (reproductive 95% CI [0.27, 0.82], vegetative 95% CI [0.43, 0.98]). These patterns were not affected by year = = (ANOVA; year FU6 0.005, 0.94). There were no differences in content among life stages at the season 1.5H-1-1 beginning of the (ANOVA; stage F2^= 1.011, April May July 50 Fig. 1. Concentration of stored dynamics nonstructural Total C carbohydrates (NSC) and nitrogen (N) concentrations over all NSC life stages (emergent, reproductive, dormant, and vegetative) for Astragalus scaphoides, an herbaceous perennial in southwest Montana, USA. Data are means ? SE, averaged over 2006 2008. (A) Dynamics of NSC. Dormant plants began the season with low NSC concentrations and increased concentrations over the growing season. (B) Nitrogen dynamics. Dormant plants had higher concentrations at the beginning of the season but did not gain through the season.
photosynthetic carbon gain by reproductive and vege tative from to NSC plants early emergence May; 12? concentrations in in were not emergent plants April mGlucose different from those of or significantly reproductive Sucrose in hsd, = 0.84 and P = vegetative plants May (Tukey's c Starch 0.18, respectively). However, they were significantly o higher than those of dormant plants inMay (Tukey's = hsd, 0.001). Over the season, NSC concentrations in c 4? growing O creased for all life stages (reproductive, vegetative, and O dormant) (Fig. 1A). Dormant plants gained an average 8.0% (95% CI [5.48-10.52]), an increase that was greater than vegetative and reproductive plants, although differenceswere not statistically significant (vegetative = = Fig. 2. in nonstructural 0.08, reproductive 0.42). The increaseof NSC in (A) Change carbohydrate (NSC) concentrations in relation to total carbon concentrations for dormant was not associated with an increase in plants dormant plants. Data are averages of 2007 and 2008 seasons total carbon concentration (Fig. 2A), which did not and are means and SE. Total carbon concentrations remained constant as the of carbon as soluble significantly change over the season for any life stages relatively proportion sugars (NSC) increased. (B) NSC dynamics fraction for dormant (dormant, 95% CI [-0.92-2.73]; vegetative, 95% CI by plants. Data are^ averages of 2007 and 2008 seasons. Sucrose, 95% CI There [-3.91-0.95]; reproductive, [-1.65-2.94]). the major transport sugar throughout plants, is the only were no differences in total carbon concentrations fraction that significantly increased.
This content downloaded from 150.131.192.151 on Wed, 30 Oct 2013 18:29:29 PM All use subject to JSTOR Terms and Conditions November2010 3411 ^^^^H ^^^^H = 0.37), and plants did not significantlygain over the We suspect that plants may enter dormancy because = = growing season (ANOVA; stageFU55 1.364, 0.25). they lack key resources that they gain through remobi No significantdifferences were detected among stages at lization. An alternative would be that plants gain the end of the growing season for either or ( resources from symbionts. In mycotrophic species such = ANOVA; stageF2,34= 1.923, 0.18, year ?^34= 1.99, as orchids, plants may gain resources frommycorrhizal = = = 0.17; ANOVA; stage F2,?S 0.016, 0.98). partners or other symbiontswhile they remain below ground (Gill 1989, Shefferson et al. 20056, 2007). A. Discussion scaphoides does not have strong associations with Our results indicate that stored nonstructural carbo mycorrhizal or rhizobial partners (E. Crone, H. Addy, hydrates are associated with prolonged dormancy of and M. Rillig, unpublisheddata), so it is not likely to be mature plants. Although plants that remain dormant gaining C from belowground symbionts.However, the during the growing season do not have lower stored potential for resource transfer in other species increases mineral resources (N and P) relative to plants that the plausibility of the idea that plants gain resources emerge aboveground, theydo have lower nonstructural during prolonged dormancy. In mycorrhizal species, carbohydrates (NSC). Further, dormant plants do not soluble C may be transferredeither to mycorrhizae or gain or lose or while belowground. Surprisingly, from them (Gill 1989,Lesica and Steele 1994,Lesica and despite being entirely belowground, dormant plants Crone 20?7, Shefferson 2009). Orchids have particular increase NSC concentrations during the growing season, mycorrhizal associations thatusually result in a net gain and end with concentrations comparable to plants that of C for the plant, even while dormant (Gill 1989, had emerged. Our results are consistent with the Shefferson et al. 20056, 2007, Shefferson2009). Howev hypothesis that plants enter prolonged dormancy due er, species with arbuscular mycorrhizal (AM) associa to a lack of stored resources (Shefferson et al. 2005??, tions (such as Sil?ne spaldingii, see Lesica and Crone 2006) . In this case, dormant plants may remain 2007), typicallyallocate C tomycorrhizae in return for belowground because they simply lack sufficientmobile mineral nutrients. Such allocation could lead to low carbon (C) to construct leaves. Alternatively, low sugar NSC and dormancy, if low NSC causes prolonged concentrations may interruptdevelopmental pathways dormancy. Alternatively, ifmineral nutrients, rather for aboveground growth. Recent work with model thanNSC, limitemergence forAM plants, theymay be systems amenable to laboratory and greenhouse study able to gain those resources through mycorrhizal has highlighted the pivotal role of C compounds in symbionts while dormant. The resource dynamics signaling pathways for growth and development (Half associated with dormancy for species with these ord and Paul 2003, Rolland et al. 2006, Lee et al. 2007). symbiotic relationships deserve additional research. Thus, the shortage ofNSC indormant plantsmay reflect Our results strongly point to a causal link between a shortage of the raw material to build tissue, or an NSC and prolonged dormancy. However, ?s with any interruption in signaling pathways that allow plants to observational study, the link between NSC and dor emerge aboveground. mancy could be due to a spurious correlationwith other In the past the hypothesis that plants entered driving factors. For example, both NSC and the prolonged dormancy due to low resource stores seemed tendency to remain dormant could be associated with puzzling. If a plant lacks the resources to emerge plant age; however, dormancy inA. scaphoides declines = aboveground, how would it gain those necessary very weakly with age (r ?0.048), whereas younger resources bymerely stayingbelowground? In Astragalus plants tend to have higher NSC concentrations (J. R. scaphoides total C concentrations remained constant, Gremer, unpublished data). Alternatively, local low while the proportion of available C increased. We resource availability around sampled plants could speculate that dormant plants remobilized cell-wall reduce NSC and also stimulate dormancy. However, compounds (e.g., hemicelluloses) into available forms, dormancy in A. scaphoides is not strongly associated as suggested by Hoch (2007). In other systems, C with environmental resource availability. We attempted starvation in tissues has been demonstrated to stimulate to alter plant performance by adding supplemental the degradation of cell-wall compounds (Lee et al. water over three years (Crone and Lesica 2006) and 2007) .Dormant plants begin the season with lowNSC supplemental and in 2007 (E. E. Crone unpublished values, do not photosynthesize, and likely incurmeta data); neither affected the probability of prolonged bolic costs during the summer due to higher tempera dormancy (J. R. Gremer, unpublished analysis). As a tures.These conditions are likely to lead toC starvation, thirdpossibility, Morrow and Olfelt (2003) showed that which could then triggercell-wall degradation, and the Solidago missouriensis plants were most likely to be subsequent release of sugars from cell-wall materials. dormant afteryears of high herbivory, and it isplausible Further research in this area could provide more insight thatherbivory would also affectNSC stores.At our field ~ into the role of C metabolism, and not just assimilation, site 1% of plants are defoliated in any given year (J.R. in the life-historystrategies of wild plants in the field. Gremer, personal observation) and other consumers are
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rare, but ?20% of plants go dormant in any given year. that include manipulation of carbon stores, is necessary Therefore, we doubt thatherbivory alone is the primary to fully understand the relationship between stored C cause of prolonged dormancy in this species. Finally, we and dormancy. Itmay be that individual variation inC no reason to that some some have suspect individual plants gain, allocation, and metabolism can explain why are inherentlymore likely to remain dormant than plants go dormant while others do not. Because the others;most bouts of dormancy last only one year in this availability of mobile carbon compounds depends on our species (Lesica 1995), and most plants in 25-year environmental effectson C acquisition (e.g., drought or once monitoring studyhave gone dormant at least (E. E. herbivory) as well as on internal C metabolism and Crone and J. R. Gremer, unpublished data). Further subsequent effects on developmental pathways, our we with visible flower more, harvested dormant plants results can reconcile the two leading hypotheses for stalks from that these ing previous years, indicating prolonged dormancy because carbon resources below had flowered in the recent our plants past. Overall, groundmay be under both external and internalcontrol. results do not to be confounded appear by specific To our knowledge, we document for the first time that environmental factors or stored plant age. However, carbon metabolism may be associated with lifehistory carbon resources reflect the effect of integrated plant strategies in a long-lived perennial plant in the wild. over NSC after performance time, including depletion Because these strategieshave important implications for et al. and combined to flowering (Crone 2009) responses population dynamics, our resultsmay open exciting lines environmental factors et al. 1999, (Chapin 1990,Wyka of research spanning from plant molecular biology to Crone et al. Our results that low NSC 2009). suggest population ecology and evolution. reflectsthis integratedeffect rather than the effectof any single external environmental factor. Further research is Acknowledgments needed to the link between environmental investigate The authors thank E. Miller, E. Lahr, and K. Hopping for factors, NSC stores, and prolonged dormancy. their assistance in field and laboratory work. We also thank two reviewers for careful and valuable comments on the Overall, we did not detect a large cost of dormancy in anonymous manuscript. This research was supported by the National terms of stored resources; we suspect dormant plants Science Foundation (NSF DEB 05-15756 to E. E. Crone and A. remobilize existing resources. However, this remobiliza Sala, NSF DEB 02-40963 to E. E. Crone) and the University of tion of structural carbon could a cost. carry long-term Montana (J. Schmautz Fellowship to J. R. Gremer). Studies that have investigated the demographic costs Literature and benefits of prolonged dormancy have sometimes, Cited but not always, reported long-term costs. For some Amthor, J. S. 2000. The McCree-deWit-Pennirfg de Vries species, prolonged dormancy decreased survival proba Thornley respiration paradigms: 30 years later. Annals of 86:1-20. bility compared to plants that did not remain below Botany Boyce, P. J., and J. J. Volenec. 1992. Taproot carbohydrate ground (Hutchings 1987, Shefferson et al. 2003; but see concentrations and stress tolerance of contrasting alfalfa in Shefferson et al. Shefferson counterexamples [2005a], genotypes. Crop Science 32:757-761. [2006], and Lesica and Crone [2007]). Similarly, Shef Chap?n, F. S., III, E. Schultze, and H. A. Mooney. 1990. The ferson et al. (2003) found that dormant Cypripedium ecology and economics of storage in plants. Annual Review of and 21:423-447. calceolus plants were less likely to reproduce in the year Ecology Systematics Crone, E. E., and P. Lesica. 2004. Causes of synchronous following dormancy, while Lesica and Crone (2007) flowering in Astragalus scaphoides, an iteroparous perennial showed dormant Silene were more than spaldingii likely plant. Ecology 85:1944-1954. vegetative or floweringplants to reproduce the following Crone, E. E., and P. Lesica. 2006. Pollen and water limitation in a year. It may be that, in some cases, remobilization of Astragalus scaphoides, plant that flowers in alternate years. Oecologia 150:40-49. resources during dormancy carries a long-term cost in Crone, E. E., E. Miller, and A. Sala. 2009. How do plants know terms of future survival or reproduction, even if this when other plants are flowering? Resource depletion, pollen remobilization is better than death. Alternatively, limitation and mast-seeding in a perennial wildflower. prolonged dormancy may have differentmetabolic Ecology Letters 12:1119-1126. consequences in differentplant species. Crone, E. E., L. Polansky, and P. Lesica. 2005. Empirical models of resource and mast Our results suggest that C storagemay help explain pollen limitation, acquisition, a wildflower. American Naturalist some individuals for one or seeding by bee-pollinated why disappear belowground 166:396-408. more years, and the mechanism for their return. provide Ehrlen, J., and K. Lehtila. 2002. How perennial are perennial are Low levels of mobile C associated with remaining plants? Oikos 98:308-322. belowground, while remobilization of structural C Gill, D. E. 1989. Fruiting failure, pollinator inefficiency, and in orchids. in D. during dormancy could be a mechanism that allows speciation Pages 458-481 Otte and J. A. Endler, editors. Speciation and its consequences. Sinauer plants to come back up again. This suggests that Associates, Sunderland, Massachusetts, USA. not be under prolonged dormancy may exclusively Haiford, N. G., and M. J. Paul. 2003. Carbon metabolite environmental control but it is also under strong sensing and signalling. Plant Biotechnology Journal 1:381 internal control. Further work, such as experiments 398.
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