Effects of increased atmospheric CO2 on nutritional contents in poplar (Populus pseudo-simonii [Kitag.]) tissues and larval growth of gypsy moth (Lymantria dispar)

ACTA ECOLOGICA SINICA Volume 26, Issue 10, October 2006 Online English edition of the Chinese language journal Cite this article as: Acta Ecologica Sinica, 2006, 26(10), 3166−3174

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RESEARCH PAPER

Effects of increased atmospheric CO2 on nutritional contents in poplar (Populus pseudo-simonii [Kitag.]) tissues and larval growth of gypsy moth (Lymantria dispar) Wang Xiaowei1,2, Ji Lanzhu1,*, Liu Yan3 1 Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China 2 Graduate School of Chinese Academy of Sciences, Beijing 100039, China 3 Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China

Abstract: Changes in the concentrations of phytochemical compounds usually occur when plants are grown under elevated atmospheric CO2. CO2-induced changes in foliar chemistry tend to reduce leaf quality and may further affect insect herbivores. Increased atmospheric CO2 also has a potential influence on decomposition because it causes variations in chemical components of plant tissues. To investigate the effects of increased atmospheric CO2 on the nutritional contents of tree tissues and the activities of leaf-chewing forest insects, samples of Populus pseudo-simonii [Kitag.] grown in open-top chambers under ambient and elevated －

CO2 (650 µmol mol 1) conditions were collected for measuring concentrations of carbon, nitrogen, C︰N ratio, soluble sugar and starch in leaves, barks, coarse roots (>2 mm in diameter) and fine roots (<2 mm in diameter). Gypsy moth (Lymantria dispar) larvae were reared on a single branch of experimental trees in a nylon bag with 1 mm × 1 mm grid. The response of larval growth was observed in situ. Elevated CO2 resulted in significant reduction in nitrogen concentration and increase in C︰N ratio of all poplar tissues. In all tissues, total carbon contents were not affected by CO2 treatments. Soluble sugar and nonstructural carbohydrate (TNC) in the poplar leaves significantly increased with CO2 enrichment, whereas starch concentration increased only on partial sampling dates. Carbohydrate concentration in roots and barks was generally not affected by elevated CO2, whereas soluble sugar contents in fine roots decreased in response to elevated CO2. When second instar gypsy moth larvae consuming poplars grew under elevated CO2 for the first 13 days, their body weight was 30.95% lower than that of larvae grown at ambient CO2, but no significant difference was found when larvae were fed in the same treatment for the next 11 days. Elevated atmospheric CO2 had adverse effects on the nutritional quality of Populus pseudo-simonii [Kitag.] tissues and the resultant variations in foliar chemical components had a significant but negative effect on the growth of early instar gypsy moth larvae. Key Words:

elevated CO2; Populus pseudo-simonii [Kitag.]; nutritional content; nitrogen; Carbohydrate; Lymantria dispar

Since the industrial revolution, atmospheric concentrations － of CO2 have steadily increased from 280 µmol mol 1 to the － current level of 368 µmol mol 1, and this level is expected to －1 － range from 540 µmol mol up to 970 µmol mol 1 by the year [1] 2100 . Atmospheric CO2 enrichment has been shown to stimulate both photosynthesis and growth and thereby causes increase in biomass[2], and to bring about changes in the － chemical components of many plant tissues[2 6]. The variations in the tissue phytochemical compounds of primary producers may influence species interactions and biogeochemical

cycling in ecosystems through alteration in competition, consumption and decomposition processes. The feeding activities of phytophagous insects affect forest productivity, species composition, energy flow, and nutrient cycling. Therefore, the research on and the prediction of tree–insect interactions under a CO2-enriched atmosphere is of particular importance[7]. Theoretically, the effect of rising levels of atmospheric CO2 on phytophagous insects can be attributed to the following approaches: the direct effect of enriched CO2, the indirect effect of changes in phytochemical com-

Received date: 2006-02-25; Accepted date 2006-06-27 *Corresponding author. E-mail: [email protected] Copyright © 2006, Ecological Society of China. Published by Elsevier BV. All rights reserved.

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pounds induced by elevated CO2, and the top–down effect of the third trophic level species, such as parasitoids, predators, and pathogens. However, it is generally believed that CO2induced changes in foliar phytochemical compounds play the most important role in the activities of phytophagous insects[7]. Foliar carbohydrate and carbon-based secondary metabolites, especially phenolics, generally increase under elevated CO2, and the accumulation of these components reduces the concentration of nitrogen and increases the C︰N ratio of green － leaves[3, 8 12]. Several experiments showed that CO2-mediated changes in foliar phytochemical compounds had a negative － effect on the activities of leaf-chewing insects[13 16], typically resulting in decreased growth rate, reduced weights of larvae or pupae, prolonged larval development, and reduced food processing efficiencies. Although several other researchers have found a decline in the palatability of leaves under elevated CO2 compared with those under ambient CO2 but the － insect were not affected or little affected[17 19]. The results of these and other related studies suggest that the responses of phytophagous insects to increased CO2 concentrations are species- and system- specific and that they are usually affected by independent or interactive effects of other environmental and biological factors[12]. Whether the CO2-induced changes in the chemistry of green leaves can remain unaltered in the senescent leaves has significant influences on the decomposition and nutrient cycling in an ecosystem[4,11,20]. Various conclusions have been reported regarding the changes in the chemistry of senescent leaves under conditions of elevated CO2, and the decomposition rate of senescent leaves was reduced or unaffected in response to － high CO2 concentrations[4,20 23]. Changes in the chemical levels of other tree tissues have also been reported to occur under elevated CO2 conditions. Cotrufo and Ineson[6] noted that elevated CO2 significantly influenced the chemical components of Fagus sylvatica L. twigs, but its decomposition rates remained unchanged. Several experiments showed that fine root nitrogen concentration reduced and C︰N ratio increased under elevated CO2 conditions, as reported by King et al. [24] and Parsons et al. [5]. The review by Cotrufo and Ineson[3] indicated a greater reduction in nitrogen contents in belowground tissues than in aboveground tissues. Because the effects of elevated CO2 on the chemistry of tree tissues have important implications for revealing and predicting the changes in the herbivory and decomposition of forest ecosystems, field-based open-top chambers were used in this study to examine the effects of elevated atmospheric CO2 on the tissue phytochemical compounds of native tree species (Populus pseudo-simonii [Kitag.]) and the growth of gypsy moth (Lymantria dispar) larvae reared on experimental trees under ambient and elevated CO2 concentrations. These two species were chosen in this experiment considering the fol-

lowing two factors: China possesses the largest area of poplar plantations and poplars play an important role in environmental protection, afforestation, and wood production; the gypsy moth is a worldwide forest pest, and its host plants exceed 300 species of trees and shrubs[26].

1

Materials and methods

1.1 Experimental system This study was carried out at the Changbaishan Forest Ecosystem Research Station of the Chinese Academy of Sciences. Open-top chambers (OTCs) were used to expose experimental trees and insects under elevated and ambient CO2 levels. The octagonal OTCs are 2.4 m in diameter by 2.8 m in height. Its frames are made of square steel and are covered with 0.02cm transparent polyvinyl chloride film. Four vertical PVC tubes (2 cm in diameter by 100 cm in height) that were connected with each other, with several 2mm ventages symmetrically distributed on each vertical PVC tube, served as the CO2 exposure system (Fig. 1). CO2 in a gas cylinder was allowed to flow into PVC tubes through CO2 reductors. A fan fixed 1.5 m above ground in the center of OTCs was used to mix CO2 with air. Levels of CO2 were controlled by regulating the flowmeter of the CO2 reductor and monitoring with an infrared gas analyzer (CI-301, CID Inc., USA). A plastic CO2-monitoring tube was attached on each of the four vertical PVC tubes (Fig. 1). The CO2 concentrations in high-CO2 － chambers were maintained at (650 ± 80) µl L 1. The CO2 concentrations in control chambers were those of the ambient CO2. For each CO2 level, two chambers were used to reduce the potential influence of other environmental variables. CO2 exposure was maintained from 7:00 to 19:00 everyday from 1 June to 27 September, 2005. 1.2 Experimental materials One-year-old Populus pseudo-simonii [Kitag.] saplings of

Fig. 1 Perspective drafting of CO2 exposure system

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similar shoot and root lengths were randomly transplanted into each OTC on 12 May, 2005. Ten saplings were planted in each chamber. The 0–25 cm soil of chambers was replaced with humus-topsoil of broad-leaved Korean pine mixed forest on Changbaishan to reduce the soil heterogeneity. Masses of Gypsy moth egg were collected in the field and stored in a refrigerator at 4℃. Egg hatch was deferred to meet the requirements of this experiment. First-stage larvae were reared with immature foliage of Quercus mongolica. 1.3 Sampling and analysis of phytochemical compounds Six poplar saplings were randomly selected from each chamber on 1 July for rearing gypsy moth larvae. For each sapling, one or two branches that extended toward the south were enclosed in a 35cm × 20cm nylon mesh bag (1 mm × 1 mm grid size). Four newly molted second-instar larvae were transferred to each bag, and the bag was large enough to allow for free movement of the larvae within the bag. The bags and caterpillars were moved to the next closest branches on the same sapling when more than half of the leaves in the bags were consumed. The average weight of each larva in each bag was determined on 13 July and 24 July, respectively. Leaves for the analysis of phytochemical compounds were collected thrice (20 July, 11 August, and 25 September, 2005) from each of the six experimental saplings in each chamber. Leaves from one individual sapling were made up a separate sample. The first leaf sampling was carried out around the fourth instar of larval development. So as to exactly represent the leaves fed upon by caterpillars, branches used for foliar collection were at the same relative position (south-facing and in the middle of the canopy) on which the insect bag was placed. On the latter two leaf sampling dates, the fifth to the tenth leaves were removed, down from the apex of the main stem. Leaves were all cleanly excised at the petiole. Leaves were then put into valve bags, immediately transported to the laboratory, and dried at 60℃. Roots and barks were collected on 26 September. Three insect-feeding trees were selected for root and bark analyses. Around the center of the taproot, all the roots (<20 cm in diameter) were harvested. Then, the fine

roots (<2 mm in diameter) and the coarse roots (>2 mm in diameter) were separated. Barks of each sapling were peeled off. All samples were dried at 60℃. The concentrations of all phytochemical compounds were expressed on the basis of percentage of tissue dry weight. The concentrations of carbon and nitrogen of all tissues were measured with an elemental analyzer (Elementar, Vario EL Ⅲ, Germany). C︰N ratios were calculated from the respective carbon and nitrogen tissue concentrations. Tissue dry powders were extracted thrice, 10 min for each extraction, with 80% ethanol in water bath maintained at 100℃. After each extrac－ tion, the samples were centrifuged (10 min, 4000 r·min 1) and the supernatant was used for the determination of soluble sugar[27]. The pellet was resuspended in 5 ml of 35% perchloric acid for 1 h to hydrolyze the starch. The soluble material represented the starch-rich fraction[28]. The sugar content of the various supernatants was quantified colorimetrically at 490 nm using the phenol-sulfuric acid method[29] and using glucose as the standard. Starch concentrations were calculated as the product of sugar content in pellet and coefficient 0.9. Total nonstructural carbohydrate (TNC) was the sum of soluble sugar and starch. 1.4 Statistical analysis Independent-Samples T test (SPSS 10.0 for windows) was used for statistical analysis. Results were represented as mean value ± 1 standard error.

2

Results

2.1 The effects of elevated CO2 on nitrogen, carbon contents, and C︰N ratio in poplar tissues The concentrations of foliar nitrogen significantly decreased with elevation in CO2 (Fig. 2a). Foliar nitrogen concentrations in high-CO2 trees declined 14.19% (P < 0.001) and 7.71% (P < 0.001) relative to the control on 20 July and 11 August, respectively. Leaf nitrogen contents slightly reduced by 4.93% (P = 0.075) on 25 September. The proportion of CO2-induced reduction in foliar nitrogen concentrations decreased with time (Fig. 2a). Elevated CO2 reduced foliar ni-

Fig. 2 Effect of elevated CO2 on total nitrogen contents (a), total carbon contents (b) and C/N ratio (c) in poplar leaves over three sampling dates *** indicates significance at P < 0.001; Error bars indicate ±1 standard error

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trogen levels by 8.94% on average over three sampling dates. The concentrations of total foliar carbon remained unchanged by CO2 enrichments (Fig. 2b). However, leaf C︰N ratios increased significantly in response to elevated CO2 (Fig. 2c). Elevated CO2 increased foliar C︰N ratio by 16.70% (P < 0.001) and 8.24% (P < 0.001) relative to controls on 20 July and 11 August, respectively. Leaf C︰N ratios were slightly reduced by 5.01% (P = 0.072) on 25 September. Elevated CO2 increased foliar C︰N ratios by 9.98% on average over three sampling dates. Elevated CO2 also significantly reduced the nitrogen concentrations in barks, fine roots, and coarse roots by 9.13% (P < 0.05), 5.35% (P < 0.05), and 10.53% (P < 0.05), respectively (Fig. 3a). Total carbon contents in these tissues were not affected by CO2 enrichment (Fig. 3b). Elevated CO2 significantly increased C︰N ratios in barks (+9.54%, P < 0.05) and coarse roots (+10.27%, P < 0.05). C︰N ratios of fine roots increased (+4.12%, P = 0.113) but not significantly in response to enriched CO2 (Fig. 3c). 2.2 The effects of increased CO2 on carbohydrate concentrations in poplar tissues The concentrations of total soluble sugar in poplar leaves significantly increased under conditions of elevated CO2. Enriched CO2 increased concentrations of foliar soluble sugar by 21.74% (P < 0.001), 13.04% (P < 0.05), and 6.88% (P < 0.05) relative to controls on 20 July, 11 August, and 25 September, respectively (Fig. 4a). It suggested that the proportion of the

CO2-induced changes in foliar soluble sugar decreased with time. Starch concentration increased by 24.67% (P < 0.05) only on 20 July but did not change significantly on 11 August and 25 September (Fig. 4b). The trend of changes in the total nonstructural carbohydrate concentrations of leaves was similar to that of soluble sugar in response to CO2 effect and time effect (Fig. 4). Enriched CO2 increased foliar total nonstructural carbohydrate concentrations by 22.34% (P < 0.001), 11.17% (P < 0.001), and 4.50% (P = 0.141) on 20 July, 11 August, and 25 September, respectively. Carbohydrate concentrations (total soluble sugar, starch, and total nonstructural carbohydrate) in poplar coarse roots and barks did not show significant difference among CO2 treatments, and the starch and total nonstructural carbohydrate concentrations in fine roots also remained unchanged under conditions of enriched CO2, but total soluble sugar contents in fine roots decreased by 10.54% (P < 0.05) in response to elevated CO2 (Fig. 5). As a major reservoir of carbon nutrients, the starch and total nonstructural carbohydrate contents in coarse roots were substantially higher than those in other tree tissues (Fig. 5). The ratio of foliar total soluble sugar to total nonstructural carbohydrate was substantially higher than that in other tree tissues (Fig. 5). 2.3 Growth response of gypsy moth larvae to enriched CO2 When the second instar gypsy moth larvae consuming poplars were grown under conditions of increased CO2 for the

Fig. 3 Effect of elevated CO2 on total nitrogen (a), total carbon contents (b) and C/N ratio (c) in bark, fine roots and coarse roots of poplars. * indicate significance at P < 0.05; Error bars indicate ±1 standard error

Fig. 4 Effect of elevated CO2 on total soluble sugar (a), starch (b), and total nonstructural carbohydrate (c) concentrations in poplar leaves over three sampling dates

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Fig. 5 The concentrations of total soluble sugar (a), starch (b), and total nonstructural carbohydrate (c) in bark, fine roots, and coarse roots of poplars at ambient CO2 and elevated CO2 *indicates significance at P < 0.05; Error bars indicate ±1 standard error

first 13 days (from 1 July to 13 July), their body weight was 30.95% (P < 0.05) lower than that of larvae at ambient CO2, but when larvae were fed in the same treatment for the next 11 days (from 13 July to 24 July), there was no significant difference in their body weight (Fig. 6).

Fig. 6 Mean larval weight of gypsy moth fed on poplars at ambient CO2 and elevated CO2

3

Discussion

3.1 The effects of increased CO2 on the concentrations of foliar phytochemical compounds The concentrations of nitrogen in Populus pseudo-simonii [Kitag.] leaves declined significantly in response to CO2 enrichment, which was in accordance with the conclusions of other researchers. Norby et al. [11] summarized the responses of foliar nitrogen concentration to elevated CO2 in field-grown trees and found considerable variation with an overall average decline of 11% in gymnosperms and 14% in angiosperms. The reduction in foliar nitrogen may be a limitation factor for the sustained enhancement of photosynthesis and growth, as noted by Norby et al [11]. The soil used in this study was the humus-topsoil of broadleaved Korean pine mixed forest on Changbaishan and was highly fertile. This could be the reason for the higher nitrogen content in Populus pseudo-simonii [Kitag.] leaves than those of poplars grown in moderate or barren soil but were similar

to the nitrogen values of aspen grown under CO2 enrichment conditions[16,30,31]. It was assumed that the foliar nitrogen contents are closely associated with the soil nutrient availability of these experiments. It was found that the C︰N ratio of green leaves significantly increased in response to elevated CO2. According to the prediction of the carbon/nutrient (C/N) balance theory[32], the increase in C︰N ratio probably results in the accumulation of carbon-based secondary compounds (e.g. phenolics and terpenoids) and structural carbohydrates (e.g. cellulose and hemicellulose)[10,33]. The potential changes in these compounds play the most important role in the plant-insect interactions and the litter decomposition in ecosystems[10]. Higher C︰N ratio probably increases carbon allocation to some special organs and tissues (e.g. thickening of cell wall and increase of trichomes). Thus, the toughness of leaves may increase under conditions of elevated CO2, which makes the consumption of these leaves more difficult for leaf-chewing insects[34]. The concentrations of foliar soluble sugar and total nonstructural carbohydrate increased significantly in response to CO2 enrichment, but foliar starch contents increased significantly only at the first sampling date. Higher concentrations of foliar nonstructural carbohydrates may be a stimulus for the herbivory and assimilation of phytophagous insects. 3.2 The effect of CO2-induced changes in foliar chemical components on the larval growth of gypsy moth The body weight of the early instar gypsy moth larvae that were fed under conditions of elevated CO2 for the first 13 days was significantly lower than that of their counterparts fed at ambient levels of CO2, whereas the body weight of the larvae that were fed for the next 11 days in the same treatment did not show significant difference; this may be attributed to the following factors. (1) The effect of CO2-induced phytochemical changes on the growth of early instar larvae is stronger than that of old instar larvae. Bezemer and Jones[8] reviewed 61 plant-insect interactions under enriched CO2 conditions and found that this trend certainly exists. The diverse responses of different instar larvae under CO2 enrichment were generally

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attributed to the difference in the compensatory feeding ability[8,35] or the nitrogen utilization efficiency (NUE)[36]. (2) The male or female caterpillars were not distinguished in this experiment, but the body weight of male and female larvae visually differed, especially when larvae molted into the fourth instar. The weight of female larvae was substantially larger than that of male larvae. Because the gypsy moth larvae reared on trees did not constitute a large sample in this experiment, sex-induced differences in larval body weight probably obscured the actual responses under conditions of enriched CO2. (3) It was also recognized that changing the host plant species from Quercus mongolica to Populus pseudo-simonii [Kitag.] probably resulted in the maladjustment for early instar larvae, but the CO2-induced changes in foliar chemistry probably intensified these responses. Leaf nitrogen concentrations play the most important role in the consumption, digestion, growth, development, and reproduction of leaf-chewing insects. Although higher nonstructural carbohydrate is beneficial for insects, it may not counteract the negative effects of lower concentrations in nitrogen. The carbon-based secondary metabolites (e.g. condensed tannin) and structural carbohydrates (e.g. cellulose) were not measured in this article, but according to the prediction of the carbon/nutrient (C/N) balance theory[32], these compounds probably increase under conditions of enriched CO2[10,33] and can cause a decline in the growth of insects by influencing the consumption and assimilation abilities of the insects. Therefore, poor nutritional quality may be the major reason that restrained the growth of early instar gypsy moth larvae in this study, and the old instar larvae probably can partly compensate the depreciation in nutrient quality by increasing consumption or improving the nitrogen-utilization efficiency. However, the effects of sex-induced differences of insects on the growth of the gypsy moth larvae were not excluded in this study. 3.3 The effects of increased CO2 on the concentrations of phytochemical compounds of poplar barks and roots It was found that the nitrogen concentrations of Populus pseudo-simonii [Kitag.] barks and coarse roots reduced significantly in response to elevated CO2, and the C︰N ratio of coarse roots slightly increased, which partly consisted with the findings of some previous researches. In theory, the changes in the C︰N ratio and the nitrogen concentration of roots may alter the decomposition processes and the cycling of matter between plants and soil; yet, thus far, there are no sufficient evidences available to confirm this hypothesis. Johnson et al.[37] reported that the elevated CO2 did not affect the decomposition rate of fine roots, and Chapman et al.[38] found that elevated CO2 induced only small changes in fine root chemistry that were insufficient to significantly influence fine root decomposition. Thus far, data regarding the effects of elevated CO2 on car-

bohydrates of tree roots are particularly limited and no uniform conclusions have been achieved. King et al.[24] reported that the starch and soluble sugar concentrations in fine roots of Populus tremuloides and Acer saccharum were generally unresponsive to elevated CO2. Parsons et al.[5] found that fine root starch concentrations of Betula papyrifera and Acer saccharum were not affected by CO2 enrichment. This study also reports that there were no significant changes in the concentrations of root soluble sugar, starch, and total nonstructural carbohydrates in response to CO2 enrichment. An exceptional change was the reduction of fine root soluble sugar under conditions of enriched CO2. The analysis of bark nutritional contents showed that elevated CO2 resulted in decreased nitrogen concentration and increased C︰N ratio, whereas bark carbohydrates were not affected. The bark structure and chemistry are closely associated with the resistance of trees to trunk pests (e.g. longhorned beetles). Yang et al.[39] showed that long-horned beetles were apparently addicted to low-nitrogen aspen variety compared with high-nitrogen variety. Therefore, it is inferred that elevated CO2 would probably result in high resistance of aspen to trunk pests in the future. 3.4 The changes in the response intensity of foliar phytochemical concentrations to elevated CO2 The degree of CO2-induced reduction in foliar nitrogen concentrations decreased with time and the proportion of increased concentrations of foliar soluble sugar and total nonstructural carbohydrates also decreased in response to CO2 enrichment with time. In this study, two possible explanations were put forth. First, the effects of CO2 on the concentration of phytochemical compounds weaken with the prolonged exposure to CO2. Second, the effect of leaf sampling position (the first time in middle of the canopy and the next two times at the top of the canopy) on the phytochemistry was probably combined with the effect of CO2 enrichment. Nitrogen concentration (on the basis of leaf mass ) was lower in CO2-enriched forest plots than in ambient plots at every canopy depth, but the CO2 effect was greater toward the top of the canopy, as reported by Norby and Iversen[40]. The observations of Mandre et al.[41] also showed that leaf-soluble sugar and starch contents were significantly correlated with canopy depth. Therefore, it is still unclear whether the change in the response intensity of foliar phytochemical concentrations resulted from the weakening of CO2 effects or from the sampling position effects.

Acknowledgements This research was supported by the National Natural Science Foundation of China (No. 30670306), the Knowledge Innovation Program of Chinese Academy of Sciences (No. KZCX1-SW- 19) and the Open Foundation of Changbaishan Forest Ecosystem Research Station of Chinese Academy of

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Sciences. The authors thank Hao Zhanqing, Han Shijie, and Wang Lihua from the Institute of Applied Ecology, Chinese Academy of Sciences and Professor Wang Zhiying from the Northeast Forest University, China. The authors also thank Professor Shao Guofan from Purdue University for his help in revising this manuscript and Mr. Gu Jianhui for his help in drawing the sketch-map of CO2 exposure system.

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