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Elevated atmospheric-carbon dioxide concentration increases soil respiration in a mid-successional lowland forest
Soil Biology & Biochemistry 32 (2000) 721±723
www.elsevier.com/locate/soilbio
Short communication
Elevated atmospheric-carbon dioxide concentration increases soil respiration in a mid-successional lowland forest A.S. Ball a,*, E. Milne a, B.G. Drake b a
Department of Biological Sciences, John Tabor Laboratories, University of Essex, Wivenhoe Park, Colchester, Essex CO4 3SQ, UK b Smithsonian Environmental Research Center, Edgewater, MD 21037, USA Accepted 8 October 1999
Signi®cant increases in both soil respiration and root biomass (50 and 30%, respectively) were detected in a mid-successional lowland forest soil exposed to elevated atmospheric [CO2] compared with soil exposed to ambient [CO2]. Many studies have focused on the way in which elevated atmospheric [CO2] will aect vegetation processes. Photosynthesis has been shown to be enhanced by elevated [CO2] in plants using the C3 pathway (Kimball et al., 1993). In many instances this can lead to an increase in dry biomass and, particularly in crop species, an accumulation of carbohydrates in the green tissues of the plant (Allen, 1990; Kimball et al., 1993). However, one area of which relatively little is known is the eect of elevated [CO2] on belowground processes. There have been a number of reports citing an increase in total root biomass which accompanies increases in total plant biomass of C3 species grown in elevated [CO2] (Curtis et al., 1989; Berryman et al., 1993). Reports of changes in the root-to-shoot ratio are less consistent, although a number of studies do show a greater allocation of biomass to roots in elevated [CO2] (Rogers et al., 1983; Hocking and Meyer, 1991). Of daily photosynthetic carbon production 30 to 60% is lost in respiration and a signi®cant portion (between 10 and 50%) of this carbon is released from roots (Lambers, 1985) but studies on the eects of elevated [CO2] on soil and root respiration are few in number and generally based on short-term exposure. Results from these studies have shown a decrease (Callaway et * Corresponding author. Tel.: +44-1206-873-332; fax: +44-1206873-416. E-mail address: [email protected] (A.S. Ball).
al., 1994), an increase or no eect (Giord et al., 1985), depending on species and growing conditions. Stimulation of soil respiration by elevated [CO2] has also been observed for marsh vegetation (Ball and Drake, 1998). This increase in soil respiration in swards of Scirpus olneyi was accompanied by an 83% increase in root biomass. However increased soil respiration was also observed in swards of Spartina patens, although no increase in root biomass was detected (Ball and Drake, 1998). Further work is required to establish the long-term eects of elevated [CO2] on soil and root respiration. We have examined the eects of long-term exposure of elevated atmospheric [CO2] on in situ soil respiration and root respiration within a natural population of the temperate zone shrub Lindera benzoin (spicebush). The study site was mid-successional lowland forest located 300 m inland from the Rhode River, a subsidiary of the Chesapeake Bay, MD, at a latitude of 36853 'N and longitude of 76833 'W. The site, which was dominated by mature L. tulipifera and L. styraci¯ua in the overstorey, was occupied almost exclusively by the C3 shrub, L. benzoin on Adelphia sandy loam (Kirby and Matthews, 1973). Plots at this site were exposed to elevated atmospheric [CO2] during every growing season (May to October) from 1991 until 1996. Within this site a 60 30 m area was divided into three 20 30 m blocks arranged in parallel along a slight slope (approx. 3%). Within each block, plants were grouped into three experimental treatments: control, ambient and elevated. The control treatment is not relevant to this study. For elevated and ambient treatments, plants were enclosed within 3.4 m tall 3.8
0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 3 8 - 0 7 1 7 ( 9 9 ) 0 0 1 9 8 - 4
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A.S. Ball et al. / Soil Biology & Biochemistry 32 (2000) 721±723
m wide octagonal footprint chambers. One of the two paired chambered plots per block received enough additional CO2 to increase its concentration by 340 mmol CO2 molÿ1. The mean [CO2] recorded in ambient and elevated chambers during the experimental period was 352 mmol CO2 molÿ1 and 693 mmol CO2 molÿ1, respectively. Additional details of the ®eld chamber design and microclimate, and the method for determining ecosystem gas exchange, can be found in Cipollini et al. (1993). In situ measurements of soil respiratory activity were recorded from July±August 1995 (3 weeks, Julian days 208±230) using a portable environmental gas monitor (EGM-1, PP Systems, UK) connected to a soil respiration chamber (SRC-1, PP Systems, UK). At the same time, soil temperature at a depth of 1.5 cm was measured using a battery-operated digital thermometer (HH-25TC, Omega, USA) and a thermocouple (Type T Cu±Cu±Ni, Omega, USA) Measurements were taken ®ve times on each sample day beginning at 10.30 h. Each individual measurement took about 5 min, and was made by placing the respiration chamber (dia 10 cm) over the naturally bare soil surface between plants. Respiratory activity was calculated from CO2 accumulation rates, as described by the manufacturer, (Anon, 1990), and expressed as mmol CO2 mÿ2 sÿ1. For soil respiration measurements, the ®ve readings taken from each plot were used to obtain a mean value for that ®eld chamber. The three ®eld chambers were treated as replicates. Repeated measures ANOVA was used to interpret the results presented in Fig. 1. Root respiration measurements were taken on material obtained on ®ve separate occasions (Julian dates 208, 210, 212, 216 and 230). Following soil respiration measurements, 5.5 cm dia cores (depth 10 cm, n 5
Fig. 1. Mean soil respiration rate (mmol CO2 produced mÿ2 sÿ1) from ®eld chambers exposed to ambient (q) or elevated (Q) atmospheric [CO2] in stands dominated by L. benzoin. Results are the means of ®ve replicates. indicates a signi®cant dierences (P < 0.05) between soil respiration rates in ®eld chambers exposed to ambient and elevated [CO2].
were obtained using an auger. All root material was removed by washing the core over a ®ne mesh net (1 mm) with Ca2Cl (0.2 mM), to counteract membrane damage sustained during separation. Root respiration was measured using a dark-type oxygen electrode (Rank Brothers, Cambridge, UK) with a high sensitivity membrane (Yellow Springs Instrument Co. Inc., OH, USA). The roots were washed in distilled water prior to being placed in a buer solution of 10 mM MES (2[N-morpholino] ethanesulphonic acid, pH 6) and the oxygen concentration monitored over time at 208C. Following each measurement and rewashing in water, the dry weight of the root material used was assessed by placing the roots in an oven at 608C until a constant dry weight was obtained. Root respiration was determined as mmol of O2 utilised g dry root biomass sÿ1. The results (Fig. 1) are based on the mean daily respiration rate. Variations in soil respiration over the 3 weeks may have been caused by changes in water availability (not determined) because, although soil temperature varied between 17 and 258C during the taking of soil respiration measurements, no correlation could be detected between soil temperature and soil respiration r2 0:30). Mean soil respiration rates measured in ®eld chambers maintained at elevated [CO2] ranged from 1.8 to 5.0 mmol CO2 mÿ2 sÿ1 and were signi®cantly greater (P < 0.05) on eight of the 10 sampling dates than the rates of 1.2 to 3.8 mmol mÿ2 sÿ1 in chambers containing L. benzoin exposed to ambient [CO2] (Fig. 1). This general increase in in situ soil respiration in ®eld chambers exposed to elevated [CO2] con®rms previous ®ndings based on other natural ecosystems (Ball and Drake, 1998) and supports the hypothesis of Zak et al. (1993) that stimulation of soil processes occurs as a consequence of the eects of elevated [CO2] on plant physiological processes. At this site, L. benzoin showed only a slight, nonsigni®cant enhancement of aboveground growth when exposed to elevated [CO2] (Cipollini et al., 1993). However, the authors concluded that nitrogen limitation might have led the plants to store any increased carbon assimilated in belowground growth. Increased root biomass may therefore account for the increased soil respiration observed in Fig. 1. To examine this hypothesis, root respiration was assessed from soil cores taken from ®eld chambers. In all cores, between 70 and 80% (by volume) of the roots were identi®ed as being from L. benzoin, con®rming the dominant nature of this plant in this soil (data not shown). When respiration was expressed per unit dried weight of roots, no signi®cant dierence was observed between the ambient and elevated [CO2] systems (4626 and 5228 mmol O2 sÿ1 g dry weight rootsÿ1 respectively), suggesting that elevated [CO2] does not aect root res-
A.S. Ball et al. / Soil Biology & Biochemistry 32 (2000) 721±723
piration in L. benzoin-dominated systems. However, when these values were expressed in terms per unit of soil, a signi®cant increase was observed in root respiration in samples from ®eld chambers exposed to elevated [CO2] (70 2 9 mmol O2 sÿ1 kg dry weight soilÿ1 compared to 44 2 8 mmol O2 sÿ1 kg dry weight soilÿ1 for samples from ®eld chambers exposed to ambient [CO2]). This resulted from a 30% increase in the dry weight of roots present in ®eld chambers exposed to elevated [CO2]. Similar increases in root biomass in plants grown in elevated atmospheric [CO2] were described by Fitter et al. (1996, 1997). Interestingly the % increase in both soil respiration and root respiration (on a soil weight basis) in samples from ®eld chambers exposed to elevated atmospheric [CO2] were both around 50%. These results imply that both an increase in root respiration per unit of soil and an increase in microbial respiration per unit area occurred in soils exposed to elevated [CO2]. However root respiration did not respond to elevated [CO2] on a root dry weight basis. Further work is necessary to establish the eects of elevated [CO2] on the size and activity of the soil microbial community. Acknowledgements We would like to express our thanks to G. Peresta, M. Gonzalez-Meyler and R. Matamala. Smithsonian Environmental Research Center for helpful advice and discussions. This work was supported by funds from the Smithsonian Institute, the UK Natural Environment Research Council, the US Department of Energy, the North Atlantic Treaty Organisation and the University of Essex. References Allen, L.H., 1990. Plant responses to rising carbon dioxide and potential interactions with air pollutants. Journal of Environmental Quality 19, 13±34. Anon, 1990. Operators Manual Version 1.8. PP Systems, Hitchin, UK.
723
Ball, A.S., Drake, B.G., 1998. Stimulation of soil respiration by carbon dioxide enrichment of marsh vegetation. Soil Biology & Biochemistry 30, 1203±1205. Berryman, C.A., Eamus, D., Du, G.A., 1993. The in¯uence of CO2 enrichment on growth, nutrient content and biomass allocation of Maranthus corymbosa. Australian Journal of Botany 41, 195±209. Callaway, R.M., De Lucia, E.H., Thomas, E.M., Schlesinger, W.H., 1994. Compensatory response of CO2 exchange and biomass allocation and their eects on the relative growth rates of ponderosa pine in dierent CO2 and temperature regimes. Oecologia 98, 159±166. Cipollini, M.L., Drake, B.G., Whigham, D., 1993. Eects of elevated CO2 on growth and carbon/nutrient balance in the deciduous woody shrub Lindera benzoin (L.) Blume (Lauraceae). Oecologia 96, 339±346. Curtis, P.S., Drake, B.G., Whigham, D.F., 1989. Nitrogen and carbon dynamics in C3 and C4 estuarine marsh plants grown under elevated CO2 in situ. Oecologia 78, 297±301. Fitter, A.H., Graves, J.D., Wolfenden, J., Self, G.K., Brown, T.K., Bogie, D., Mans®eld, T.A., 1997. Root production and turnover and carbon budgets of two contrasting grasslands under ambient and elevated atmospheric carbon dioxide concentrations. New Phytologist 137, 247±255. Fitter, A.H., Self, G.K., Wolfenden, J., van Vururen, M.M.I., Broen, T.K., Williamson, L., Graves, J.D., Robinson, D., 1996. Root production and mortality under elevated atmospheric carbon dioxide. Plant and Soil 187, 299±306. Giord, R.M., Lambers, H., Morison, J.I.L., 1985. Respiration of crop species under CO2 enrichment. Physiologia Plantarum 63, 351±356. Hocking, P.J., Meyer, C.P., 1991. Eects of CO2 enrichment and nitrogen stress on growth and partitioning of dry matter and N in wheat and maize. Australian Journal of Plant Physiology 18, 339±356. Kimball, B.A., Mauney, J.R., Nakayama, F.S., Idso, S.B., 1993. Eects of increasing atmospheric CO2 on vegetation. Vegetatio 104/105, 65±75. Kirby, R.M., Matthews, E.D., 1973. Soil Survey of Anne Arundel County, MD. USDA Soil Conservation Service, Washington DC. Lambers, H. 1985. Respiration in intact plants and tissues and dependence on environmental factors, metabolism and invaded organisms. In: Douce, R., Day, D.A. (Eds.), Encyclopaedia of Plant Physiology. Springer-Verlag, Berlin, pp. 418±473. Rogers, H.H., Bingham, G.E., Cure, J.D., Smith, J.M., Surano, K.A., 1983. Responses of selected plant species to elevated CO2 in the ®eld. Journal of Environmental Quality 12, 569±574. Zak, D.R.R., Pregistzer, K.S., Curtis, P.S., Teeri, J.A., Pogel, R., Randiett, D.L., 1993. Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant and Soil 151, 105±117.
www.elsevier.com/locate/soilbio
Short communication
Elevated atmospheric-carbon dioxide concentration increases soil respiration in a mid-successional lowland forest A.S. Ball a,*, E. Milne a, B.G. Drake b a
Department of Biological Sciences, John Tabor Laboratories, University of Essex, Wivenhoe Park, Colchester, Essex CO4 3SQ, UK b Smithsonian Environmental Research Center, Edgewater, MD 21037, USA Accepted 8 October 1999
Signi®cant increases in both soil respiration and root biomass (50 and 30%, respectively) were detected in a mid-successional lowland forest soil exposed to elevated atmospheric [CO2] compared with soil exposed to ambient [CO2]. Many studies have focused on the way in which elevated atmospheric [CO2] will aect vegetation processes. Photosynthesis has been shown to be enhanced by elevated [CO2] in plants using the C3 pathway (Kimball et al., 1993). In many instances this can lead to an increase in dry biomass and, particularly in crop species, an accumulation of carbohydrates in the green tissues of the plant (Allen, 1990; Kimball et al., 1993). However, one area of which relatively little is known is the eect of elevated [CO2] on belowground processes. There have been a number of reports citing an increase in total root biomass which accompanies increases in total plant biomass of C3 species grown in elevated [CO2] (Curtis et al., 1989; Berryman et al., 1993). Reports of changes in the root-to-shoot ratio are less consistent, although a number of studies do show a greater allocation of biomass to roots in elevated [CO2] (Rogers et al., 1983; Hocking and Meyer, 1991). Of daily photosynthetic carbon production 30 to 60% is lost in respiration and a signi®cant portion (between 10 and 50%) of this carbon is released from roots (Lambers, 1985) but studies on the eects of elevated [CO2] on soil and root respiration are few in number and generally based on short-term exposure. Results from these studies have shown a decrease (Callaway et * Corresponding author. Tel.: +44-1206-873-332; fax: +44-1206873-416. E-mail address: [email protected] (A.S. Ball).
al., 1994), an increase or no eect (Giord et al., 1985), depending on species and growing conditions. Stimulation of soil respiration by elevated [CO2] has also been observed for marsh vegetation (Ball and Drake, 1998). This increase in soil respiration in swards of Scirpus olneyi was accompanied by an 83% increase in root biomass. However increased soil respiration was also observed in swards of Spartina patens, although no increase in root biomass was detected (Ball and Drake, 1998). Further work is required to establish the long-term eects of elevated [CO2] on soil and root respiration. We have examined the eects of long-term exposure of elevated atmospheric [CO2] on in situ soil respiration and root respiration within a natural population of the temperate zone shrub Lindera benzoin (spicebush). The study site was mid-successional lowland forest located 300 m inland from the Rhode River, a subsidiary of the Chesapeake Bay, MD, at a latitude of 36853 'N and longitude of 76833 'W. The site, which was dominated by mature L. tulipifera and L. styraci¯ua in the overstorey, was occupied almost exclusively by the C3 shrub, L. benzoin on Adelphia sandy loam (Kirby and Matthews, 1973). Plots at this site were exposed to elevated atmospheric [CO2] during every growing season (May to October) from 1991 until 1996. Within this site a 60 30 m area was divided into three 20 30 m blocks arranged in parallel along a slight slope (approx. 3%). Within each block, plants were grouped into three experimental treatments: control, ambient and elevated. The control treatment is not relevant to this study. For elevated and ambient treatments, plants were enclosed within 3.4 m tall 3.8
0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 3 8 - 0 7 1 7 ( 9 9 ) 0 0 1 9 8 - 4
722
A.S. Ball et al. / Soil Biology & Biochemistry 32 (2000) 721±723
m wide octagonal footprint chambers. One of the two paired chambered plots per block received enough additional CO2 to increase its concentration by 340 mmol CO2 molÿ1. The mean [CO2] recorded in ambient and elevated chambers during the experimental period was 352 mmol CO2 molÿ1 and 693 mmol CO2 molÿ1, respectively. Additional details of the ®eld chamber design and microclimate, and the method for determining ecosystem gas exchange, can be found in Cipollini et al. (1993). In situ measurements of soil respiratory activity were recorded from July±August 1995 (3 weeks, Julian days 208±230) using a portable environmental gas monitor (EGM-1, PP Systems, UK) connected to a soil respiration chamber (SRC-1, PP Systems, UK). At the same time, soil temperature at a depth of 1.5 cm was measured using a battery-operated digital thermometer (HH-25TC, Omega, USA) and a thermocouple (Type T Cu±Cu±Ni, Omega, USA) Measurements were taken ®ve times on each sample day beginning at 10.30 h. Each individual measurement took about 5 min, and was made by placing the respiration chamber (dia 10 cm) over the naturally bare soil surface between plants. Respiratory activity was calculated from CO2 accumulation rates, as described by the manufacturer, (Anon, 1990), and expressed as mmol CO2 mÿ2 sÿ1. For soil respiration measurements, the ®ve readings taken from each plot were used to obtain a mean value for that ®eld chamber. The three ®eld chambers were treated as replicates. Repeated measures ANOVA was used to interpret the results presented in Fig. 1. Root respiration measurements were taken on material obtained on ®ve separate occasions (Julian dates 208, 210, 212, 216 and 230). Following soil respiration measurements, 5.5 cm dia cores (depth 10 cm, n 5
Fig. 1. Mean soil respiration rate (mmol CO2 produced mÿ2 sÿ1) from ®eld chambers exposed to ambient (q) or elevated (Q) atmospheric [CO2] in stands dominated by L. benzoin. Results are the means of ®ve replicates. indicates a signi®cant dierences (P < 0.05) between soil respiration rates in ®eld chambers exposed to ambient and elevated [CO2].
were obtained using an auger. All root material was removed by washing the core over a ®ne mesh net (1 mm) with Ca2Cl (0.2 mM), to counteract membrane damage sustained during separation. Root respiration was measured using a dark-type oxygen electrode (Rank Brothers, Cambridge, UK) with a high sensitivity membrane (Yellow Springs Instrument Co. Inc., OH, USA). The roots were washed in distilled water prior to being placed in a buer solution of 10 mM MES (2[N-morpholino] ethanesulphonic acid, pH 6) and the oxygen concentration monitored over time at 208C. Following each measurement and rewashing in water, the dry weight of the root material used was assessed by placing the roots in an oven at 608C until a constant dry weight was obtained. Root respiration was determined as mmol of O2 utilised g dry root biomass sÿ1. The results (Fig. 1) are based on the mean daily respiration rate. Variations in soil respiration over the 3 weeks may have been caused by changes in water availability (not determined) because, although soil temperature varied between 17 and 258C during the taking of soil respiration measurements, no correlation could be detected between soil temperature and soil respiration r2 0:30). Mean soil respiration rates measured in ®eld chambers maintained at elevated [CO2] ranged from 1.8 to 5.0 mmol CO2 mÿ2 sÿ1 and were signi®cantly greater (P < 0.05) on eight of the 10 sampling dates than the rates of 1.2 to 3.8 mmol mÿ2 sÿ1 in chambers containing L. benzoin exposed to ambient [CO2] (Fig. 1). This general increase in in situ soil respiration in ®eld chambers exposed to elevated [CO2] con®rms previous ®ndings based on other natural ecosystems (Ball and Drake, 1998) and supports the hypothesis of Zak et al. (1993) that stimulation of soil processes occurs as a consequence of the eects of elevated [CO2] on plant physiological processes. At this site, L. benzoin showed only a slight, nonsigni®cant enhancement of aboveground growth when exposed to elevated [CO2] (Cipollini et al., 1993). However, the authors concluded that nitrogen limitation might have led the plants to store any increased carbon assimilated in belowground growth. Increased root biomass may therefore account for the increased soil respiration observed in Fig. 1. To examine this hypothesis, root respiration was assessed from soil cores taken from ®eld chambers. In all cores, between 70 and 80% (by volume) of the roots were identi®ed as being from L. benzoin, con®rming the dominant nature of this plant in this soil (data not shown). When respiration was expressed per unit dried weight of roots, no signi®cant dierence was observed between the ambient and elevated [CO2] systems (4626 and 5228 mmol O2 sÿ1 g dry weight rootsÿ1 respectively), suggesting that elevated [CO2] does not aect root res-
A.S. Ball et al. / Soil Biology & Biochemistry 32 (2000) 721±723
piration in L. benzoin-dominated systems. However, when these values were expressed in terms per unit of soil, a signi®cant increase was observed in root respiration in samples from ®eld chambers exposed to elevated [CO2] (70 2 9 mmol O2 sÿ1 kg dry weight soilÿ1 compared to 44 2 8 mmol O2 sÿ1 kg dry weight soilÿ1 for samples from ®eld chambers exposed to ambient [CO2]). This resulted from a 30% increase in the dry weight of roots present in ®eld chambers exposed to elevated [CO2]. Similar increases in root biomass in plants grown in elevated atmospheric [CO2] were described by Fitter et al. (1996, 1997). Interestingly the % increase in both soil respiration and root respiration (on a soil weight basis) in samples from ®eld chambers exposed to elevated atmospheric [CO2] were both around 50%. These results imply that both an increase in root respiration per unit of soil and an increase in microbial respiration per unit area occurred in soils exposed to elevated [CO2]. However root respiration did not respond to elevated [CO2] on a root dry weight basis. Further work is necessary to establish the eects of elevated [CO2] on the size and activity of the soil microbial community. Acknowledgements We would like to express our thanks to G. Peresta, M. Gonzalez-Meyler and R. Matamala. Smithsonian Environmental Research Center for helpful advice and discussions. This work was supported by funds from the Smithsonian Institute, the UK Natural Environment Research Council, the US Department of Energy, the North Atlantic Treaty Organisation and the University of Essex. References Allen, L.H., 1990. Plant responses to rising carbon dioxide and potential interactions with air pollutants. Journal of Environmental Quality 19, 13±34. Anon, 1990. Operators Manual Version 1.8. PP Systems, Hitchin, UK.
723
Ball, A.S., Drake, B.G., 1998. Stimulation of soil respiration by carbon dioxide enrichment of marsh vegetation. Soil Biology & Biochemistry 30, 1203±1205. Berryman, C.A., Eamus, D., Du, G.A., 1993. The in¯uence of CO2 enrichment on growth, nutrient content and biomass allocation of Maranthus corymbosa. Australian Journal of Botany 41, 195±209. Callaway, R.M., De Lucia, E.H., Thomas, E.M., Schlesinger, W.H., 1994. Compensatory response of CO2 exchange and biomass allocation and their eects on the relative growth rates of ponderosa pine in dierent CO2 and temperature regimes. Oecologia 98, 159±166. Cipollini, M.L., Drake, B.G., Whigham, D., 1993. Eects of elevated CO2 on growth and carbon/nutrient balance in the deciduous woody shrub Lindera benzoin (L.) Blume (Lauraceae). Oecologia 96, 339±346. Curtis, P.S., Drake, B.G., Whigham, D.F., 1989. Nitrogen and carbon dynamics in C3 and C4 estuarine marsh plants grown under elevated CO2 in situ. Oecologia 78, 297±301. Fitter, A.H., Graves, J.D., Wolfenden, J., Self, G.K., Brown, T.K., Bogie, D., Mans®eld, T.A., 1997. Root production and turnover and carbon budgets of two contrasting grasslands under ambient and elevated atmospheric carbon dioxide concentrations. New Phytologist 137, 247±255. Fitter, A.H., Self, G.K., Wolfenden, J., van Vururen, M.M.I., Broen, T.K., Williamson, L., Graves, J.D., Robinson, D., 1996. Root production and mortality under elevated atmospheric carbon dioxide. Plant and Soil 187, 299±306. Giord, R.M., Lambers, H., Morison, J.I.L., 1985. Respiration of crop species under CO2 enrichment. Physiologia Plantarum 63, 351±356. Hocking, P.J., Meyer, C.P., 1991. Eects of CO2 enrichment and nitrogen stress on growth and partitioning of dry matter and N in wheat and maize. Australian Journal of Plant Physiology 18, 339±356. Kimball, B.A., Mauney, J.R., Nakayama, F.S., Idso, S.B., 1993. Eects of increasing atmospheric CO2 on vegetation. Vegetatio 104/105, 65±75. Kirby, R.M., Matthews, E.D., 1973. Soil Survey of Anne Arundel County, MD. USDA Soil Conservation Service, Washington DC. Lambers, H. 1985. Respiration in intact plants and tissues and dependence on environmental factors, metabolism and invaded organisms. In: Douce, R., Day, D.A. (Eds.), Encyclopaedia of Plant Physiology. Springer-Verlag, Berlin, pp. 418±473. Rogers, H.H., Bingham, G.E., Cure, J.D., Smith, J.M., Surano, K.A., 1983. Responses of selected plant species to elevated CO2 in the ®eld. Journal of Environmental Quality 12, 569±574. Zak, D.R.R., Pregistzer, K.S., Curtis, P.S., Teeri, J.A., Pogel, R., Randiett, D.L., 1993. Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant and Soil 151, 105±117.