Journal of Plant Ecology Advance Access published online on June 17, 2008
Journal of Plant Ecology, doi:10.1093/jpe/rtn015
N availability does not modify plant-mediated responses of Trichoplusia ni to elevated CO2
1 Department of Integrative Biology, 3060 Valley Life Sciences Building, University of California, Berkeley, CA 94720-3140, USA
2 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
(Deceased, 6 February, 2008)
* Correspondence address: Tel: 510-643-5430; Fax: 510-643-6264; E-mail: sudderth{at}berkeley.edu
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Aims: Elevated CO2 and increased N availability can alter a variety of plant physiological processes leading to changes in the nutritional quality of leaf tissue for herbivores. Numerous experiments have examined the responses of herbivores to environmental change; however the potential effects of simultaneous change in multiple factors on leaf-chewing insect herbivores are less well understood. The plant-mediated effects of elevated CO2 and high N on the performance of a generalist leaf-chewing insect herbivore, Trichoplusia ni, were investigated.
Methods: Newly hatched T. ni larvae were introduced to Amaranthus viridis and Polygonum persicaria plants grown under ambient and elevated CO2 and low and high N conditions. Insect performance was assessed by measuring larvae weight after ten days of feeding. Plant photosynthesis, biomass, leaf area and specific leaf weight were measured to determine the effects of elevated CO2, N and insect feeding on plant performance.
Important Findings: Elevated CO2 did not have strong effects on plant or insect performance, only affecting a few responses under low or high N conditions, but not both. Growth under high nitrogen improved almost all measures of plant performance. Trichoplusia ni performed significantly better on Amaranthus viridis (C4) compared to Polygonum persicaria (C3), despite similar leaf C:N ratios in both species. The performance of T. ni caterpillars was only improved by the high nitrogen treatment when they were feeding on P. persicaria, the host they performed poorly on. The only interactions between N and CO2 affecting plant performance were seen for leaf photosynthesis of P. persicaria and leaf area of A. viridis. Contrary to the predictions, there were no significant CO2 by N interactions affecting T. ni performance.
Keywords: herbivory • insect performance • Polygonum persicaria • Amaranthus viridis
Received: 26 January 2008 Revised: 6 May 2008 Accepted: 15 May 2008
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Environmental factors influence plant and insect physiology, leading to both direct and indirect effects on the interactions between plant species and their insect herbivores. Anthropogenic modification of the global climate and virtually all natural habitats is well documented and predicted to intensify in the future (Foley et al. 2005; Vitousek et al. 1997). Extensive research has led to a range of detailed predictions regarding plant and herbivore response to increases in global temperature (Bale et al. 2002; Veteli et al. 2002), atmospheric CO2 (Bezemer and Jones 1998; Coviella and Trumble 1999; Hunter 2001) and nitrogen availability (Throop and Lerdau 2004). Hundreds of single-factor experiments have been completed. In many cases, the precise response of a plant species and its herbivores to global change factors are species specific and even experiment specific, making it difficult to predict how future environmental conditions will affect species interactions (Bale et al. 2002; Bezemer and Jones 1998; Coviella and Trumble 1999; Throop and Lerdau 2004; Whittaker 1999, 2001; Zvereva and Kozlov 2006).
While the responses of insects in different feeding guilds vary widely, leaf-chewing insects have shown the most consistent responses to global change factors (Bezemer and Jones 1998). When feeding on plants grown in elevated CO2, leaf-chewing herbivores generally increase tissue consumption. They can sometimes compensate for lower tissue quality (Williams et al. 1994), but often development time increases and insect fitness is reduced (Hunter 2001; Zvereva and Kozlov 2006). The negative impacts of elevated CO2 on leaf-chewing insect herbivores are thought to be mediated by reduced leaf N, increased leaf toughness and, in some cases, an increase in defense compounds (Bezemer and Jones 1998; Coviella and Trumble 1999; Hunter 2001; Lincoln et al. 1993; Watt et al. 1995; Zvereva and Kozlov 2006).
General trends in herbivore response to elevated CO2 have been documented but the responses of leaf-chewing herbivore species to simultaneous change in multiple environmental factors are less well understood. A meta-analysis of the effects of elevated CO2 and temperature on plants and their insect herbivores found that overall insect performance declined in elevated CO2, improved in elevated temperature and was not affected by simultaneous change in both factors. Therefore, temperature increases could mitigate the predicted negative effects of elevated CO2 on insect herbivores (Zvereva and Kozlov 2006). Plant-mediated responses of leaf-chewing herbivores to elevated CO2 and N has been investigated in several studies, primarily for insects feeding on trees (Hattenschwiler and Schafellner 1999; Kinney et al. 1997; Saxon et al. 2004) and shrubs (Johnson and Lincoln 1991; Kerslake et al. 1998). These studies have often found additive, not interactive effects of CO2 and N on leaf nutrition and insect performance (Throop and Lerdau 2004). The few experiments using herbaceous plant species have shown CO2 by N interactions affecting leaf N content. Studies with cotton have demonstrated a corresponding CO2 by N interaction affecting the development time of Spodoptera exigua (Coviella et al. 2002; Coviella and Trumble 2000; Mevi-Schutz et al. 2003).
The patterns that can be identified when the results of many global change studies are compiled highlight the importance of examining the response of additional plant–insect species pairs, particularly to simultaneous change in multiple environmental factors. This experiment investigated how the performance of a generalist insect herbivore (Trichoplusia ni Hübner, Lepidoptera: Noctuidae) can be affected by the physiological responses of host plants to elevated CO2 and high N availability. Despite their importance as key agricultural pests (Bailey and Mukerji 1976; Maxwell and Fadamiro 2006), no studies published to date have examined the effects of elevated CO2 and increased N on T. ni. The response of insects feeding on two herbaceous host plants was compared. Species that utilize different photosynthetic physiologies, the C3 Polygonum persicaria L. (Polygonales: Polygonaceae) and the C4 Amaranthus viridis L. (Caryophyllales: Amaranthaceae), were used. Based on previous experiments, it was expected that these host plants would be differentially affected by the selected treatments (Bazzaz 1990; Sudderth et al. 2005). The experiment was designed to test the hypotheses that changes in leaf nitrogen content would cause leaf chewer performance to decrease when feeding on plants grown under elevated CO2 and increase on plants grown under high N. CO2 by N interactions affecting leaf nitrogen content were expected to correspond to significant interactions affecting insect performance. Based on the photosynthetic physiologies of the plant species, greater plant-mediated responses to elevated CO2 but similar responses to N were expected for insects feeding on P. persicaria (C3) compared to A. viridis (C4).
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Study species
Trichoplusia ni (cabbage looper) is a highly dispersive noctuid moth found throughout North America. In addition to crucifers, T. ni feeds on a wide variety of plants including cotton, legumes and Solanum species (Capinera 2001). Polygonum persicaria (spotted ladysthumb) is an annual herbaceous plant that was introduced to USA from Europe. It grows in all US states excluding Hawaii and is considered invasive in some regions (USDA, PLANTS database: http://plants.usda.gov). Amaranthus viridis (slender amaranth) is a pantropical C4 weed found in warm temperate regions, with an obscure origin (USDA, Germplasm Resources Information Network, Taxonomy for plants: http://www.ars-grin.gov/). Both plant species are common agricultural weeds. Preliminary work showed that T. ni was able to complete development on both plant species used in the experiment.
Plant growth conditions
Seeds of A. viridis and P. persicaria were planted in flats containing a 2:1 mixture of Promix to sand and placed in four environmentally controlled greenhouse zones to germinate. Before planting, Polygonum persicaria seeds were first scarified by removing a small portion of the seed tips with a razor blade and then stratified on moist filter paper at 5°C for 2 weeks. Two greenhouse zones were maintained at ambient CO2 (370 ppm) and two were maintained at elevated CO2 (750 ppm). Air temperatures averaged 25°C day and 20°C night, with a 16:8 hour day to night light regime. When light levels dropped below 600 µmol m–2s–1 during the daytime period, ambient light was supplemented with 1000-W high-density discharge lights. Daytime light levels averaged between 700 and 800 µmol m–2s–2 during the course of the experiment. Plants were watered and fertilized every 1–2 days via two parallel automatic watering systems (The Drip Store, Escondido, CA, USA). A water-soluble fertilizer (MiracleGro EXCEL Cal-Mag 15-5-15) mixed to deliver 25 ppm N was used for both nutrient treatments. The high N treatment received an additional 50 ppm ammonium nitrate, for a total treatment level of 75 ppm N. The nutrient treatments were delivered via two continuous feed injectors connected to the watering systems (Dosatron International, Bordeaux, France). Two weeks after germination, 64 A. viridis and P. persicaria seedlings were transplanted into 2.5-l pots containing the 2:1 Promix to sand mixture. The pots were randomly distributed between the two zones maintained at the same CO2 level (ambient or elevated) in which the plants were germinated.
Insect performance
Four weeks after the plants had germinated, one freshly hatched T. ni caterpillar (Entopath, PA, USA) was introduced onto half of the plants in each CO2 x N treatment combination. There were eight replicates of each CO2 x N x infestation treatment combination in the experiment (four replicates in each of the two blocks at each CO2 level). All plants were caged with custom lightweight nets constructed from paint-strainer material (DC May, GA, USA) supported with collapsible wire frames (Pacific Wire, CA, USA). Caterpillar performance was determined by measuring the final biomass of each caterpillar after 10 days of feeding. Determining how caterpillar feeding affected plant performance was a primary objective of the experiment; therefore, insects were all harvested on the same day, rather when they began pupating. The caterpillars were collected and dried at 65°C to a constant mass and weighed. The newly hatched caterpillars had a very low initial biomass; therefore, the final biomass of each individual was used as a proxy for total weight gain during the experiment.
Data collection
The plants were harvested in a random order over 3 days, beginning on the date that the caterpillars were removed. One plant from each N x infestation treatment combination in each block at both CO2 levels (16 plants total) was randomly selected for photosynthesis measurements. The maximum photosynthesis rate of one fully expanded leaf was measured using a Licor 6400 photosynthesis system. Total leaf area of all plants in the experiment was measured with a Licor 3100 leaf area meter (Li-Cor Biosciences, NE, USA). The plants were dried at 65°C for biomass analysis. The leaf carbon to nitrogen ratio of two randomly selected plants from each block and treatment (48 plants total) was analyzed by the University of Georgia Soil Lab using a C/H/N analyzer (NA1500, Carlo Erba Strumentazione, Milan, Italy).
Statistical analyses
Plant performance (above ground biomass, leaf area, specific leaf weight, C:N ratio, and leaf %N) was analyzed using four-factor analysis of variance (ANOVA) (JMP, SAS Institute, NC, USA).
The split-plot model (shown below) includes CO2 and block as whole plot effects and a factorial combination of low and high N and insect presence or absence as sub-plot effects.
ANOVA model:
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The effects of CO2 and N on caterpillar weight gain were tested by three-factor ANOVA using a split-plot design with CO2 and block (nested in CO2) as the main effects and N as the sub-plot effect. Caterpillars were only retrieved from 14 of the 24 infested P. persicaria plants, presumably due to insect death. Infested plants from which the caterpillar was not retrieved at harvest, and an equal number of randomly selected uninfested plants, were excluded from the analysis. Data were transformed (log, arc sin or box-cox) if necessary for ANOVA. Box-cox transformations were performed using the Factor Profiling/Box-Cox Y transformation function in JMP. Linear regression was used to determine if final caterpillar weight was correlated with leaf C:N ratio or N content. The LSMeans contrast function of JMP was used to examine the effects of CO2, nitrogen and infestation under a fixed level of the other two factors (planned contrasts).
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Results |
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Trichoplusia ni caterpillars gained twice as much biomass during the 10-day period when feeding on A. viridis compared to P. persicaria (Fig. 1). High N conditions only improved T. ni performance when the caterpillars were feeding on the poor host plant (P. persicaria). On P. persicaria they had higher biomass when feeding on plants grown under high N conditions, while in contrast, high N did not significantly increase T. ni biomass when feeding on A. viridis (Table 1). Elevated CO2 tended to decrease T. ni biomass on P. persicaria at high N, but did not affect the performance of caterpillars feeding on A. viridis. There were no significant CO2 x N interactions affecting T. ni performance. There was a significant positive correlation between leaf N content and caterpillar biomass (data not shown) for A. viridis (r2 = 0.24, P = 0.012) and P. persicaria (r2 = 0.27, P = 0.001).
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ANOVA results showed that elevated CO2 did not affect plant performance, while N had large significant effects on most measures of performance in P. persicaria and A. viridis (Table 2). Increased nitrogen availability increased the maximum photosynthesis rates (Fig. 2a) and leaf area (Fig. 2b) while reducing the leaf C:N ratios (Fig. 3b) of both plant species and reducing the specific leaf weight of A. viridis (Fig. 3a). Changes in leaf C:N ratios were driven by changes in leaf N content: the C content of the leaves remained relatively constant across all treatments (data not shown). The only significant interactions between N and CO2 affecting plant performance were seen for the leaf photosynthesis response of P. persicaria and the leaf area of A. viridis. Planned contrasts showed that elevated CO2 increased the leaf area of P. persicaria plants grown under high nitrogen (F1,2 = 24.07, P = 0.04) but not low nitrogen.
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Infestation by T. ni reduced the leaf area of both plant species (Fig. 2b). There was a significant N x infestation interaction affecting the leaf area of P. persicaria plants. Caterpillar feeding reduced P. persicaria leaf area under high N, but not under low N (Table 2). Insect feeding also reduced photosynthetic rates in P. persicaria under ambient CO2, high N growth conditions (LSMeans contrast: F1,2 = 28.79, P = 0.03). Insect feeding significantly increased the specific leaf weight of A. viridis, while high N reduced leaf thickness (Fig. 3a). Elevated CO2 only increased leaf C:N ratios under low nitrogen when the plants were not infested (LSMeans contrast: F1,2 = 29.12, P = 0.03 for P. persicaria, and F1,2 = 60.89, P = 0.02 for A. viridis). Feeding by T. ni had no effect on the C:N ratio of leaf tissue in either plant species (Fig. 3b). Trichoplusia ni had larger effects than increased N on the specific leaf weight of A. viridis, but did not affect the specific leaf weight of P. persicaria. This result is not surprising given the much larger final size of the T. ni larvae feeding on A. viridis compared to P. persicaria (Fig. 1).
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Increased nitrogen availability significantly altered numerous measures of performance in both plant species. In contrast to a previous study using A. viridis (C4) and Solanum dulcamara (C3) (Sudderth et al. 2005), the CO2 and N treatments had similar effects on both the C3 (P. persicaria) and the C4 (A. viridis) species. There were very few CO2 by N interactions affecting the performance of either plant species, but leaf C:N ratios increased more in response to elevated CO2 at low nitrogen compared to high nitrogen when the plants were not infested. There were no CO2 by N interactions affecting caterpillar performance (Table 1). Trichoplusia ni larvae were substantially larger when feeding on A. viridis compared to P. persicaria. Notably, the caterpillars were more affected by the nitrogen treatment when feeding on the poor host, P. persicaria (Fig. 1). The leaf C:N ratios (Fig. 3b) of both plant species were similar; therefore, the dramatic difference in insect performance was likely due to an unmeasured factor, such as secondary chemicals.
Whole plants were used in the experiment because previous studies have shown that leaf chemistry is altered in detached leaves (Schmelz et al. 2001). The disadvantage of this approach is the difficulty of assessing the amount of leaf area consumed by the insects due to the potential of compensatory growth. In addition, it is not possible to distinguish whether differences in insect performance are due to variation in the amount of leaf tissue consumed or in the efficiency of conversion of ingested food (ECI). However, differences in final plant and insect biomass between the treatment groups indicate how overall performance is affected. Further experiments can then examine the mechanisms that produce the observed results.
On A. viridis, where caterpillars grew quite large, insect feeding reduced the leaf area of plants grown under high nitrogen by over 10%. Furthermore, A. viridis had higher specific leaf weight when attacked by caterpillars, particularly under high nitrogen conditions. This result provides evidence of an induced growth response to insect feeding. Increasing cell wall thickness and an increase in the concentration of total non-structural carbohydrates is often associated with a reduction in SLA under elevated CO2 (Yin 2002). Increased leaf toughness can decrease the palatability of leaf tissue for leaf-chewing herbivores (Bernays and Simpson 1990). Trichoplusia ni reduced the leaf area of plants grown in high nitrogen, even on P. persicaria where final caterpillar biomass was low (Fig. 2b). However, they did not affect the leaf area of plants grown in low nitrogen. The leaf area data indicate that the caterpillars did not exhibit compensatory feeding; it is not likely that the plants could compensate for additional feeding by producing more leaf area at low nitrogen but not high nitrogen.
A positive relationship between leaf N content across all treatments and the final biomass of T. ni caterpillars feeding on A. viridis and P. persicaria was observed. Percent N explained 24% and 27%, respectively, of the variation in final caterpillar biomass. However, there is not always a clear relationship between leaf traits and herbivore performance or consumption patterns. Previous studies have found either increased (Bentz et al. 1995; Minkenberg and Fredrix 1989; Minkenberg and Ottenheim 1990) or decreased (Ayres 1993; Peters et al. 2000) consumption by leaf-chewing herbivores feeding on plants grown under elevated CO2 conditions. It is well established that plant responses to elevated CO2 are highly dependent on nutrient availability (Bazzaz 1990; Fajer et al. 1992; Poorter et al. 1988; Reich et al. 2006; Trumble et al. 1993). Therefore, some of the species-specific responses observed in previous studies may be attributed to the lack of consistent fertilization levels between experiments (Newman et al. 2003; Sudderth et al. 2005).
Elevated CO2 generally increases leaf C:N ratios and herbivores can show no response, compensatory feeding or host switching, all of which may result in increased or decreased performance. Compensatory feeding of herbivores in response to elevated CO2 and reduced nitrogen conditions has primarily been observed in non-choice experiments, rather than in studies where herbivores can choose between plants in a community (Peters et al. 2006). In community-choice experiments, elevated CO2 has been shown to modify the relative consumption of grass and forb species by gastropod herbivores, potentially altering species composition of grassland communities (Cleland et al. 2006; Peters et al. 2000, 2006). Another study with gastropods and aphids did not find altered herbivore preferences in response to elevated CO2 (Diaz et al. 1998), potentially because the most significant declines in N content under elevated CO2 were not observed in the preferred plant species (Cleland et al. 2006). In contrast to this hypothesis, our study showed greater effects of the N treatment on caterpillars feeding on the host they performed poorly on, P. persicaria.
Experiments in open systems (free-air CO2 enrichment) have indicated that despite predicted increases in leaf tissue consumption under elevated CO2, damage to tree species may decrease due to reduced performance and a lower abundance of leaf-chewing insects (Knepp et al. 2005; Stiling et al. 2002, 2003). In the current experiment the only evidence that elevated atmospheric CO2 conditions might modify insect damage to herbaceous plant species was the trend toward interactions between insect infestation and elevated CO2 affecting the leaf C:N ratios of P. persicaria. Elevated CO2 did not affect caterpillar performance, while increased N significantly improved caterpillar performance on P. persicaria. Contrary to the predictions, there were no significant interactions between CO2 and N affecting plant or caterpillar performance.
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Many research papers and reviews have discussed the need for experiments examining the interactive effects of simultaneous change in multiple environmental factors on insect herbivores (Johns and Hughes 2002; Newman et al. 2003; Williams et al. 2000; Zvereva and Kozlov 2006). While previous studies have not found evidence of CO2 by N interactions affecting leaf-chewing herbivores feeding on trees and shrubs (Hattenschwiler and Schafellner 1999; Johnson and Lincoln 1991; Kerslake et al. 1998; Kinney et al. 1997; Mevi-Schutz et al. 2003; Saxon et al. 2004), interactions have been observed for insects feeding on herbaceous cotton plants (Coviella et al. 2002; Coviella and Trumble 2000). In contrast to the results for cotton, this experiment did not find evidence for significant CO2 by N interactions affecting the response of a caterpillar species feeding on two herbaceous plant species. Trichoplusia ni performance was substantially higher on A. viridis compared to P. persicaria, but high N only improved caterpillar performance on the poor host. The results support other findings that N availability strongly affects leaf-chewing herbivores. However, there was not evidence that N significantly modifies plant-mediated herbivore response to elevated CO2.
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Funding |
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NSF grant (#9903808 to FAB), an NSF doctoral fellowship (EAS), and a student dissertation grant from the Department of Organismic and Evolutionary Biology, Harvard University (EAS).
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Acknowledgements |
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We thank Shirley Dong for her assistance in completing the experiments, Kristin Lewis and Rachel Spicer for discussion of the experimental design and results and Leslie Hughes for helpful comments on the manuscript.
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