| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
What's this? |
Article |
Department of Biology, Central Connecticut State University, 332 Copernicus–1615 Stanley Street, New Britain, Connecticut 06050 USA
Received for publication May 18, 2006. Accepted for publication November 7, 2006.
ABSTRACT
Maintaining green leaves beyond the growing season has been hypothesized to benefit plants by supplying either a nutrient or a carbon source. Understanding such ecophysiological aspects of plants will help us to appreciate how a species functions in its environment and predict how it might be affected by future changes in that environment. The wintergreen fern species Dryopteris intermedia does not retranslocate nitrogen and phosphorus from old fronds in spring, but photosynthesis does take place in the old fronds during this season. To determine if carbon fixed in the old fronds is translocated to other parts of the plant, we labeled old fronds with 13C via photosynthetic uptake and examined old fronds, new fronds, fine roots, and rhizomes for 13C content 1 day and 1 month after labeling the old fronds. Vernally fixed carbon was translocated to the new fronds but not significantly to the below ground tissues. Old fronds in this species, therefore, serve as a carbon source for vernal growth of new fronds. This is the first study in which a fern was labeled with 13C to track vernally fixed carbon from old fronds to the rest of the plant in a wintergreen species. Future research should examine the precise timing of this carbon movement and examine other species for a similar or contrasting strategy.
Key Words: 13C • Aspleniaceae • Connecticut • photosynthesis • spring • stable isotopes • translocation
It has long been hypothesized that plant species keep green leaves beyond the growing season to serve as a location for storage of nutrients (Monk, 1966
; Moore, 1980
, 1984
) or as a site of photosynthesis and therefore as a carbon source (Bell and Bliss, 1977
; Moore, 1980
, 1984
; Chabot and Hicks, 1982
; Landhäusser et al., 1997
). An understanding of how plant species function in their environment helps us to appreciate their evolutionary adaptations to that environment. It will also help us to predict the impact of future changes to that environment on plant species, given changes in the global climate and more local habitat disruptions. Wintergreen species (those that develop a set of leaves in spring and keep them for 1 year until they are replaced with a new set) are of particular interest because they serve as an intermediate phenological strategy between deciduous species (those that keep green leaves only during the growing season) and evergreen species (those that keep green leaves for more than 1 calendar year) (Tessier, 2004
). Removal of old wintergreen leaves prior to the development of new leaves did not affect new growth in Dryopteris crassirhizoma Nakai (Tani and Kudo, 2005
) and Aristotelia chilensis (Mol.) Stuntz (Damascos et al., 2005
) but reduced and/or slowed new growth in Dryopteris intermedia (Muhl.) A. Gray (Van Buskirk and Edwards, 1995
) and Rhododendron laponicum (L.) Wahlenb. (Jonasson, 1995
). Growth reduction was hypothesized to be either a result of decreased carbon availability (Jonasson, 1995
) or a combination of reduced carbon and nutrient availability (Van Buskirk and Edwards, 1995
).
Species differ in vernal retranslocation of nutrients. Polystichum acrostichoides (Michx.) Schott retranslocates nitrogen and phosphorus from old fronds to the rest of the plant during spring (Minoletti and Boerner, 1993
) but D. intermedia (Tessier, 2001
) and D. crassirhizoma (Tani and Kudo, 2003
) do not. Therefore, maintenance of old leaves in wintergreen plants may serve as a nutrient benefit in some species but not all.
Wintergreen species tend to be shade tolerant (Decocq and Hermy, 2003
) and therefore slow at photosynthesis (Brach et al., 1993
; Landhäusser et al., 1997
), but they do extend their duration of photosynthesis by photosynthesizing in the spring (Kriebitzsch, 1992
; Minoletti and Boerner, 1993
; Landhäusser et al., 1997
; Tessier, 2001
; Prado and Damascos, 2001
). Therefore, it is likely that wintergreen species make use of old leaves for their ability to provide carbon and therefore energy to the plant during the early growing season when canopy tree leaves have not yet expanded.
While researchers performing leaf removal experiments have demonstrated a benefit of old leaves in some species, none has documented the mechanism by which intact old leaves enhance plant growth (Van Buskirk and Edwards, 1995
; Jonasson, 1995
). This study was designed to test whether or not vernal photosynthesis in intact old fronds results in carbon translocation and therefore an energetic benefit to the plant. We chose to study D. intermedia because old fronds in this species do not supply nutrients to the plant as they senesce, and it was therefore likely that the vernal growth benefit provided by the old fronds is an energetic one (Tessier, 2001
). We hypothesized that old fronds benefit the plant by moving vernally fixed carbon to new fronds and belowground structures prior to their own senescence. We therefore predicted that photosynthetic products labeled with 13C in the old fronds in early spring would be found in new fronds, fine roots, and rhizomes late in spring.
MATERIALS AND METHODS
Study species
Dryopteris intermedia is a shade-tolerant (Brach et al., 1993
), wintergreen fern species (Mahall and Bormann, 1978
). At the site for this study, old fronds senesce and new fronds emerge in May each year (J. Tessier, unpublished data). Dryopteris intermedia maintains intact vascular tissue through the winter and following spring in old fronds through a softened hinge at the base of the frond (Noodén and Wagner, 1997
). Old fronds therefore lie flat under snow and remain prostrate during spring and through senescence. As with all ferns, D. intermedia reproduces via spores but its gametophytes are unisexual, requiring adjacent gametophytes of different genders to reproduce sexually (Xiang et al., 2000
). Dryopteris intermedia is a common species in northern hardwood and mixed hardwood forests of the northeastern United States and Canada.
Study site
Algonquin State Forest of northwestern Connecticut, USA (42°00' N, 73°04' W) is a transitional forest between central and northern hardwoods plus stands of Tsuga canadensis (L.) Carrière and Pinus strobus L. Common canopy tree species include Carya cordiformis (Wangenh.) K. Koch, C. ovata (Miller) K. Koch, Fagus grandifolia Ehrh., Quercus rubra L., Betula alleghaniensis Britton, B. lenta L., Acer saccharum Marshall, and A. rubrum L. The mean January temperature is –3.5°C, the mean July temperature is 23.2°C, and the annual mean temperature is 10.1°C (NOAA, 2006
). The annual mean precipitation is 117.3 cm, and the annual mean snowfall is 125.2 cm (NOAA, 2006
). Soils are of the very rocky, Charlton-Chatfield complex (NRCS, 2006
).
Field and laboratory methods
We labeled old fronds of D. intermedia with 13C from 13CO2. On 10 April 2005 (a cloudless day), 12 plants with two or three old fronds were chosen for inclusion in this study. (The number of unexpanded new fronds was not evaluated at the start of the study.) This criterion was used to promote similarity in size and hopefully function among included plants. All plants included in the study were at least 3 m apart to minimize the chance of cross contamination with the tracer among plants. Half of these plants were randomly chosen to be labeled and half were left as control plants. Labeled plants had a plastic bag placed around their old fronds at 1000 hours and 13CO2 (Isotec, Miamisburg, Ohio, USA) was injected to fill the bag prior to sealing. Bags with 13CO2 were left in place for 3 h, and then they were punctured at the distal end to minimize exposure of the new fronds to the tracer. When the bags were empty of 13CO2 gas, they were fully removed.
On 11 April 2005, we randomly chose three plants from both the labeled and control groups and completely harvested them for above- and belowground material. This procedure was repeated on 11 May 2005. Harvested plants were cleaned of soils and other debris using distilled water and separated into old fronds, new fronds, fine roots, and rhizomes prior to drying at 60°C for 2 wk. Dried plants were ground in a Wiley Mill (Thomas Scientific, Swedesboro, New Jersey, USA) to pass through a 40-mesh screen and shipped to the UC Davis Stable Isotope Facility for analysis of 13C concentration.
Data analysis
Statistical procedures were carried out in SAS (SAS Institute, Inc., Cary, North Carolina, USA) version 8.0 at 
= 0.05. Residuals were assessed prior to analysis to ensure their conformity with the assumptions of analysis of variance (ANOVA). A 2 x 2 factorial ANOVA was conducted to compare 
13C concentration among time of harvest and treatment using PROC GLM. Both time of harvest and treatment were considered fixed effects. This procedure was repeated for each tissue type (i.e., old fronds, new fronds, fine roots, and rhizome). Tukey's honestly significant difference (HSD) test was used as a means comparison test. In the case of a significant interaction (new fronds), simple effects were isolated by examining least square means using PROC MIXED.
RESULTS
Within 1 day, labeled old fronds held a higher concentration of 13C than unlabeled old fronds (F0.05,1,1 = 6.61, P = 0.0189, Fig. 1). No other tissues had a significant difference in 13C concentration 1 day after labeling (new fronds: T = –0.04, P = 0.9726; fine roots: F0.05,1,1 = 1.82, P = 0.2310; rhizome: F0.05,1,1 = 1.56, P = 0.2829; Fig. 1). After 1 month, both old fronds and new fronds held more 13C in labeled plants than in unlabeled plants (old fronds: F0.05,1,1 = 6.61, P = 0.0189; new fronds: T = –4.06, P = 0.0048; Fig. 1). Labeled plants did not have a significant increase in 13C concentration in belowground structures compared to unlabeled plants after 1 month (fine roots: F0.05,1,1 = 1.82, P = 0.2310; rhizome: F0.05,1,1 = 1.56, P = 0.2829; Fig. 1).
|
The labeling procedure was successful based on the immediate uptake of 13C in the old fronds but not in the new fronds. The new fronds therefore were not contaminated with 13C during the labeling procedure. Only the target structure (the old fronds) received the label at the outset.
Movement of vernally fixed carbon from old fronds to new fronds indicates that the old fronds serve as a carbon source and therefore an energy source in D. intermedia (Fig. 1). There was a significant change in the 13C concentration of new fronds in labeled plants relative to unlabeled control plants. To our knowledge, this is the first documentation of translocation of vernally fixed carbon from old leaves to new leaves in a wintergreen species. Therefore, because D. intermedia does not retranslocate nutrients during spring, the benefit of keeping the old fronds through winter is to serve as an energy source for the newly expanding fronds. Old frond removal (Van Buskirk and Edwards, 1995
) therefore limits the supply of photosynthetic products during this critical time of growth and high light (Hutchison and Matt, 1977
); it is not known when the new fronds shift from being a carbon sink to becoming a carbon source.
The nonsignificant increasing trend in 13C concentration in the old fronds during spring (Fig. 1) indicates that the old fronds may use old carbon for respiration prior to using recently fixed carbon. Therefore, vernal photosynthesis may prolong the life of the old fronds themselves via an energy storage benefit for the old fronds, collectively elongating the time period (Moore, 1980
, 1984
; Chabot and Hicks, 1982
; Landhäusser et al., 1997
) and surface area of photosynthesis for the plant. Future work should seek to assess this possibility.
While there was a visible increase in the 13C concentration in belowground tissues (Fig. 1), this change was not statistically significant. Two possibilities could account for this pattern. First, the small sample size (N = 3) may have allowed too high an error to fully describe a pattern of movement of vernally fixed carbon from old fronds to fine roots and the rhizome. Future work should expand on this sample size to test this possibility. Second, the carbon that moved to the new fronds may have done so after first moving to the rhizome. Because belowground structures often serve as storage sites for carbohydrates in herbaceous plants (Mooney and Billings, 1960
; Risser and Cottam, 1968
), the large rhizome in D. intermedia may be a distribution point where carbon can move to the fine roots or to the new fronds once translocated from the old fronds. If this pattern is true, one would predict to see a peak in 13C concentration in the rhizome prior to the second harvest followed by a decline as carbon moved to the fine roots and to the new fronds. Carbon movement to the fine roots may be eclipsed by movement to the new fronds during this time of rapid expansion of the new fronds. Future work should include collections at critical periods of time in this process to test this hypothesis. Further, the old fronds may serve as an autumnal carbon source as well. Future work should examine this possibility.
Because of the variability in ecophysiology among fern and other wintergreen species of different life form, such as forbs, shrubs, and trees (Minoletti and Boerner, 1993
; Van Buskirk and Edwards, 1995
; Jonasson, 1995
; Tessier, 2001
; Tani and Kudo, 2003
, 2005
; Damascos et al., 2005
; Reudink et al., 2005
), future work should compare multiple species for the patterns of seasonal carbon uptake and translocation that they employ. Full elucidation of the adaptive value of the wintergreen leaf phenology will depend on a more complete documentation of ecophysiological patterns among these species. This study and future research will help to explain differences and similarities among species in their ecophysiological adaptations to their local environment. They will also help to make predictions regarding community composition and species range pending future changes in climate and local habitat quality.
In conclusion, old fronds of D. intermedia serve as a carbon source for the developing new fronds, but do not serve as a nutrient source for those new fronds. In future work, researchers should examine more specific temporal patterns of carbon acquisition and translocation and should examine additional species of wintergreen plants for their seasonal use and movements of carbon.
FOOTNOTES
1 The authors thank the Connecticut State University for the University Research Grant that supported this research, the Connecticut Department of Environmental Protection for permission to use Algonquin State Forest, G. Sobkiewicz and L. Tessier for field assistance, and J. Jarrett and two anonymous reviewers for constructive comments on the manuscript. 
2 Author for correspondence (e-mail: TessierJ{at}ccsu.edu
)
LITERATURE CITED
Bell K. L. Bliss L. C.. 1977. Overwinter phenology of plants in a polar semi-desert. Arctic 30: 118-121.[Web of Science]
Brach A. R. McNaughton S. J. Raynal D. J.. 1993. Photosynthetic adaptability of two fern species of a northern hardwood forest. American Fern Journal 83: 47-53.[CrossRef]
Chabot B. F. Hicks D. J.. 1982. The ecology of leaf life spans. Annual Review of Ecology and Systematics 13: 229-259.[CrossRef][Web of Science]
Damascos M. A. Prado C. H. B. A. Ladio A. A. Arribere M. A. Guevara S. R.. 2005. Consequences of the elimination of old leaves upon spring phenological events and the new leaves nutrient concentration in a wintergreen woody species in the southern hemisphere. Plant Ecology 181: 1-8.[CrossRef][Web of Science]
Decocq G. Hermy M.. 2003. Are there herbaceous dryads in temperate deciduous forests?. Acta Botanica Gallica 150: 373-382.[Web of Science]
Hutchison B. A. Matt S. R.. 1977. The distribution of solar radiation within a deciduous forest. Ecological Monographs 47: 185-207.[CrossRef][Web of Science]
Jonasson S.. 1995. Resource allocation in relation to leaf retention time of the wintergreen Rhododendron lapponicum. Ecology 76: 475-485.[CrossRef][Web of Science]
Kriebitzsch W.-U.. 1992. CO2 and H2O gas exchange of understorey plants in a submontane beech forest on limestone II. CO2 balances and net primary production. Flora 187: 135-158.[Web of Science]
Landhäusser S. M. Stadt K. J. Lieffers V. J.. 1997. Photosynthetic strategies of summergreen and evergreen understory herbs of the boreal mixedwood forest. Oecologia 112: 173-178.[CrossRef][Web of Science]
Mahall B. E. Bormann F. H.. 1978. A quantitative description of the vegetative phenology of herbs in a northern hardwood forest. Botanical Gazette 139: 467-481.[CrossRef]
Minoletti M. L. Boerner R. E. J.. 1993. Seasonal photosynthesis, nitrogen and phosphorus dynamics, and resorption in the wintergreen fern Polystichum acrostichoides (Michx.) Schott. Bulletin of the Torrey Botanical Club 120: 397-404.[CrossRef][Web of Science]
Monk C. D.. 1966. An ecological significance of evergreenness. Ecology 47: 504-505.[CrossRef][Web of Science]
Mooney H. A. Billings W. D.. 1960. The annual carbohydrate cycle of alpine plants as related to growth. American Journal of Botany 47: 594-598.[CrossRef][Web of Science]
Moore P.. 1980. The advantages of being evergreen. Nature 285: 535..[Medline]
Moore P. D.. 1984. Why be an evergreen?. Nature 312: 703..
NOAA.. 2006. National Oceanic and Atmospheric Administration. Website http://www.noaa.gov/ [Accessed 30 March 2006]..
Noodén L. D. Wagner W. H. Jr.. 1997. Photosynthetic capacity and leaf reorientation in two wintergreen ferns, Polysticum acrostichoides and Dryopteris intermedia. American Fern Journal 87: 143-149.[CrossRef][Web of Science]
NRCS.. 2006. Natural Resources Conservation Service. Website http://www.websoilsurvey.nrcs.usda.gov/ [Accessed 30 March 2006]..
Prado C. H. B. A. Damascos M. A.. 2001. Gas exchange and leaf specific mass of different foliar cohorts of the wintergreen shrub Aristotelia chilensis (Mol.) Stuntz (Eleocarpaceae) fifteen days before the flowering and the fall of the old cohort. Brazilian Archives of Biology and Technology 44: 277-282.[Web of Science]
Reudink M. W. Snyder J. P. Xu B. Cunkelman A. Balsamo R. A.. 2005. A comparison of physiological and morphological properties of deciduous and wintergreen ferns in southeastern Pennsylvania. American Fern Journal 95: 45-56.[CrossRef]
Risser P. G. Cottam G.. 1968. Carbohydrate cycles in the bulbs of some spring ephemerals. Bulletin of the Torrey Botanical Club 95: 359-369.[CrossRef][Web of Science]
Tani T. Kudo G.. 2003. Storage ability of overwintering leaves and rhizomes in a semi-evergreen fern, Dryopteris crassirhizoma (Dryopteridaceae). Ecological Research 18: 15-24.[CrossRef][Web of Science]
Tani T. Kudo G.. 2005. Overwintering leaves of a forest-floor fern, Dryopteris crassirhizoma (Dryopteridaceae): a small contribution to the resource storage and photosynthetic carbon gain. Annals of Botany 95: 263-270.
Tessier J. T.. 2001. Vernal photosynthesis and nutrient retranslocation in Dryopteris intermedia. American Fern Journal 91: 187-196.[CrossRef][Web of Science]
Tessier J. T.. 2004. Leaf longevity of Oxalis acetosella in the Catskill Mountains, New York, USA. American Journal of Botany 91: 1371-1377.
Van Buskirk J. Edwards J.. 1995. Contribution of wintergreen leaves to early spring growth in the wood fern Dryopteris intermedia. American Fern Journal 85: 54-57.[CrossRef]
Xiang L. Werth C. R. Emery S. N. McCauley D. E.. 2000. Population-specific gender-biased hybridization between Dryopteris intermedia and D. carthusiana: evidence from chloroplast DNA. American Journal of Botany 87: 1175-1180.
CiteULike Complore Connotea Del.icio.us Digg Facebook Reddit Technorati Twitter What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
