Abstract
Plant population and community dynamics may be altered by increasing atmospheric CO2 concentrations {[CO2]} through intraspecific variation in the responses of vegetative and reproductive growth. Although these responses may be regulated by age at flowering, little is known about the direct effects of age at flowering on growth responses to elevated [CO2]. In this study, we examined the interactive effects of elevated [CO2] and age at flowering on absolute and relative allocation to vegetative and reproductive growth in the determinate, short-day species Xanthium strumarium L. (common cocklebur). Six cohorts were planted at 5-day intervals in chambers maintained at either 365 or 730 µmol mol-1 CO2, with an 18-h photoperiod and a non-limiting nutrient supply. All plants were simultaneously induced to flower by switching the photoperiod to 12 h for 2 days, then switching back to an 18-h photoperiod for the remainder of the experiment. All plants were harvested 15 days after the onset of flowering. Total plant biomass increased 11–41% with increasing [CO2] and 45% from the youngest to the oldest cohort. Vegetative growth responses to elevated [CO2] significantly increased with increasing age at flowering, associated with increasing sink relative to source capacity. In contrast, total fruit mass decreased 32% from the youngest to the oldest cohort and was not significantly affected by CO2 supply. Relative biomass allocation to fruit decreased 47% from the youngest to the oldest cohort, reflecting decreased numbers of fruit, and 6–28% with increasing [CO2], reflecting decreased mean mass per mature fruit. Our findings suggest that elevated [CO2] may increase vegetative growth in Xanthium without increasing reproductive biomass, and that age at flowering may influence these responses through effects on source:sink balance. Further, changes in the allometric relationship between vegetative and reproductive growth associated with growth in elevated [CO2] suggest that long-term population and community-level responses to elevated [CO2] may differ substantially from predictions based on vegetative responses.
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References
Andalo C, Godelle B, LeFranc M, Mousseau M, Till-Bottraud I (1996) Elevated CO2 decreases seed germination in Arabidopsis thaliana. Global Change Biol 2:129–135
Anten NPR, Hirose T (1998) Biomass allocation and light partitioning among dominant and subordinate individuals in Xanthium canadense stands. Ann Bot 82:665–673
Atkin OK, Schortemeyer M, McFarlane N, Evans JR (1999) The response of fast- and slow-growing Acacia species to elevated atmospheric CO2: an analysis of the underlying components of relative growth rate. Oecologia 120:544–554
Bazzaz FA, Ackerly DD, Woodward FI, Rochefort L (1992) CO2 enrichment and dependence of reproduction on density in an annual plant and a simulation of its population dynamics. J Ecol 80:643–651
Bazzaz FA, Miao SL, Wayne PM (1993) CO2 induced growth enhancements of co-occurring tree species decline at different rates. Oecologia 96:478–482
Billings WD, Billings SM (1983) Growth and reproduction in four populations of Saxifraga flagellaris, a rare arctic-alpine plant species, in controlled environments. Bull Ecol Soc Am 64:58
Bruhn D, Leverenz JW, Saxe H (2000) Effects of tree size and temperature on relative growth rate and its components of Fagus sylvatica seedlings exposed to two partial pressures of atmospheric [CO2]. New Phytol 146:415–425
Centritto M, Lee HS, Jarvis PG (1999) Increased growth in elevated CO2: an early, short-term response? Global Change Biol 5:623–633
Clauss MJ, Aarssen LW (1994) Phenotypic plasticity of size-fecundity relationships in Arabidopsis thaliana. J Ecol 82:447–455
Coleman JS, McConnaughay KDM, Ackerly DD (1994) Interpreting phenotypic variation in plants. Trends Ecol Evol 9:187–191
Conroy J, Hocking P (1993) Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations. Physiol Plant 89:570–576
Cure JD, Acock B (1986) Crop responses to carbon dioxide doubling: a literature survey. Agric For Meteor 38:127–145
Curtis PS, Snow AA, Miller AS (1994) Genotype-specific effects of elevated CO2 on fecundity in wild radish Raphanus raphanistrum. Oecologia 97:101–105
Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form and physiology. Oecologia 113:299–313
Edwards GR, Clark H, Newton PCD (2001) The effects of elevated CO2 on seed production and seedling recruitment in a sheep-grazed pasture. Oecologia 127:383–394
Ellis RH, Craufurd PQ, Summerfield RJ, Roberts EH (1995) Linear relations between carbon dioxide concentration and rate of development toward flowering in sorghum, cowpea and soybean. Ann Bot 75:193–198
Farnsworth EJ, Bazzaz FA (1995) Inter- and intra-generic differences in growth, reproduction, and fitness of nine herbaceous annual species grown in elevated CO2 environments. Oecologia 104:454–466
Fischer M, Matthies D, Schmid B (1997) Responses of rare calcareous grassland plants to elevated CO2: a field experiment with Gentianella germanica and Gentiana cruciata. J Ecol 85:681–693
Garbutt K, Bazzaz FA (1984) The effects of elevated CO2 on plants. III. Flower, fruit and seed production and abortion. New Phytol 98:433–446
Gebauer RLE, Reynolds JF, Strain BR (1996) Allometric relations and growth in Pinus taeda: the effect of elevated CO2 and changing N availability. New Phytol 134:85–93
Geber MA (1990) The cost of meristem limitation in Polygonum arenastrum: negative genetic correlations between fecundity and growth. Evolution 44:799–819
Grünzweig JM, Körner C (2000) Growth and reproductive responses to elevated CO2 in wild cereals of the northern Negev of Israel. Global Change Biol 6:631–638
Harper JL (1977) Population biology of plants. Academic Press, San Diego, Calif.
Hicklenton PR, Jolliffe PA (1980) Carbon dioxide and flowering in Pharbitis nil Choisy. Plant Physiol 66:13–17
Hikosaka K, Sudoh S, Hirose T (1999) Light acquisition and use of individuals competing in a dense stand of an annual herb Xanthium canadense. Oecologia 118:388–396
Huxman TE, Hamerlynck EP, Jordan DS, Salsman KL, Smith SD (1998) Effects of parental CO2 environment on seed quality and subsequent seed performance in Bromus rubens. Oecologia 114:202–208
Huxman TE, Hamerlynck EP, Smith SD (1999) Reproductive allocation and seed production in Bromus madritensis ssp. rubens at elevated atmospheric CO2. Funct Ecol 13:769–777
Jackson RB, Sala OE, Field CB, Mooney HA (1994) CO2 alters water use, carbon gain, and yield for the dominant species in a natural grassland. Oecologia 98:257–262
LaDeau SL, Clark JS (2001) Rising CO2 levels and the fecundity of forest trees. Science 292:95–98
Lewis JD, Strain BR (1996) The role of mycorrhizas in the response of Pinus taeda seedlings to elevated CO2. New Phytol 133:431–443
Lewis JD, Wang XZ, Griffin KL, Tissue DT (2002) Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations. Plant Cell Environ 25:359–368
Lindman HR (1991) Analysis of variance in experimental design. Springer, Berlin Heidelberg New York
Lindroth RL, Roth S, Nordheim EV (2001) Genotypic variation in response of quaking aspen (Populus tremuloides) to atmospheric CO2 enrichment. Oecologia 126:371–379
Loehle C (1995) Anomalous responses of plants to CO2 enrichment. Oikos 73:181–187
Lüscher A, Hendry GR, Nösberger J (1998) Long-term responsiveness to free air CO2 enrichment of functional types, species and genotypes of plants from fertile permanent grassland. Oecologia 113:37–45
Marc J, Gifford FM (1984) Floral initiation in wheat, sunflower and sorghum under carbon dioxide enrichment. Can J Bot 62:9–14
Moore BD, Cheng S-H, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582
Morison JIL, Lawlor DW (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant Cell Environ 22:659–682
Navas M-L, Sonie L, Richarte J, Roy J (1997) The influence of elevated CO2 on species phenology, growth and reproduction in a Mediterranean old-field community. Global Change Biol 3:523–530
Norby RJ, Wullschleger SD, Gunderson CA, Johnson DW, Ceulemans R (1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell Environ 22:683–714
Poorter H (1998) Do slow-growing species and nutrient-stressed plants respond relatively strongly to elevated CO2? Global Change Biol 4:693–698
Poorter H, Pérez-Soba M (2001) The growth response of plants to elevated CO2 under non-optimal environmental conditions. Oecologia 129:1–20
Purohit AN, Treguna EB (1974) Effects of carbon dioxide on Pharbitus, Xanthium, and Silene in short days. Can J Bot 52:1283–1291
Reekie EG (1998) An explanation for size-dependent reproductive allocation in Plantago major. Can J Bot 76:43–50
Reekie EG, Bazzaz FA (1991) Phenology and growth in four annual species grown in ambient and elevated CO2. Can J Bot 69:2475–2481
Reekie JYC, Hicklenton PR, Reekie EG (1994) Effects of elevated CO2 on time of flowering in four short-day and four long-day species. Can J Bot 71:533–538
Reekie EG, MacDougall G, Wong I, Hicklenton PR (1998) Effect of sink size on growth response to elevated atmospheric CO2 within the genus Brassica. Can J Bot 76:829–835
Reuveni J, Gale J, Zeroni M (1997) Differentiating day from night effects of high ambient CO2 on the gas exchange and growth of Xanthium strumarium L. exposed to salinity stress. Ann Bot 79:191–196
Rusterholz PH, Erhardt A (1998) Effects of elevated CO2 on flowering phenology and nectar production of nectar plants important for butterflies of calcareous grasslands. Oecologia 113:341–349
Salisbury FB, Ross CW (1985) Plant physiology. Wadsworth, Belmont, Calif.
Samson DA, Werk KS (1986) Size-dependent effects in the analysis of reproductive effort in plants. Am Nat 127:667–680
Shitaka Y, Hirose T (1993) Timing of seed germination and the reproductive effort in Xanthium canadense. Oecologia 95:334–339
Shitaka Y, Hirose T (1998) Effects of shift in flowering time on the reproductive output of Xanthium canadense in a seasonal environment. Oecologia 114:361–367
Stocklin J, Favre P (1994) Effects of plant size and morphological constraints on variation in reproductive components in two related species of Epilobium. J Ecol 82:735–746
Sugiyama H, Hirose T (1991) Growth schedule of Xanthium canadense: does it optimize the timing of reproduction? Oecologia 88:55–60
Tissue DT, Wright SJ (1995) Effect of seasonal water availability on phenology and the annual shoot carbohydrate cycle of tropical forest shrubs. Funct Ecol 9:518–527
Wagner J, Lüscher A, Hillebrand C, Kobald B, Spitaler N, Larcher W (2001) Sexual reproduction of Lolium perenne L. and Trifolium repens L. under free air CO2 enrichment (FACE) at two levels of nitrogen application. Plant Cell Environ 24:957–965
Wang X, Lewis JD, Tissue DT, Seemann JR, Griffin KL (2001) Effects of elevated atmospheric CO2 concentration on leaf respiration of Xanthium strumarium in light and in darkness. Proc Natl Acad Sci USA 98:2479–2484
Ward JK, Strain BR (1997) Effects of low and elevated CO2 partial pressure on growth and reproduction of Arabidopsis thaliana from different elevations. Plant Cell Environ 20:254–260
Ward JK, Strain BR (1999) Elevated CO2 studies: past, present and future. Tree Physiol 19:211–220
Weber H, Borisjuk L, Wobus U (1997) Sugar import and metobolism during seed development. Trends Plant Sci 2:169–174
Willson MF (1983) Plant reproductive ecology. Wiley, New York
Winer BJ (1971) Statistical principles in experimental design. McGraw-Hill, New York
Acknowledgements
We thank Ardis Thompson, Laura Watt and Brent Wehner for their technical support. Drs Rob Jackson, Jacqui Johnson and an anonymous reviewer improved an earlier draft of this manuscript. This project was supported in part by funding from Fordham University to J. D. L., by a National Science Foundation grant (IBN-9603940) to K. L. G., and by a grant to D. T. T. from the U.S. Department of Energy's Office of Biological and Environmental Research (BER) through the Program for Ecosystem Research (PER). This is contribution no. 217 from the Louis Calder Center and Biological Station, Fordham University.
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Lewis, J.D., Wang, X., Griffin, K.L. et al. Age at flowering differentially affects vegetative and reproductive responses of a determinate annual plant to elevated carbon dioxide. Oecologia 135, 194–201 (2003). https://doi.org/10.1007/s00442-003-1186-7
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DOI: https://doi.org/10.1007/s00442-003-1186-7