Abstract
Seedlings of loblolly pine Pinus taeda (L.), were grown in open-topped field chambers under three CO2 regimes: ambient, 150 μl l−1 CO2 above ambient, and 300 μl l−1 CO2 above ambient. A fourth, non-chambered ambient treatment was included to assess chamber effects. Needles were used in 96 h feeding trials to determine the performance of young, second instar larvae of loblolly pine's principal leaf herbivore, red-headed pine sawfly, Neodiprion lecontei (Fitch). The relative consumption rate of larvae significantly increased on plants grown under elevated CO2, and needles grown in the highest CO2 regime were consumed 21% more rapidly than needles grown in ambient CO2. Both the significant decline in leaf nitrogen content and the substantial increase in leaf starch content contributed to a significant increase in the starch:nitrogen ratio in plants grown in elevated CO2. Insect consumption rate was negatively related to leaf nitrogen content and positively related to the starch:nitrogen ratio. Of the four volatile leaf monoterpenes measured, only β-pinene exhibited a significant CO2 effect and declined in plants grown in elevated CO2. Although consumption changed, the relative growth rates of larvae were not different among CO2 treatments. Despite lower nitrogen consumption rates by larvae feeding on the plants grown in elevated CO2, nitrogen accumulation rates were the same for all treatments due to a significant increase in nitrogen utilization efficiency. The ability of this insect to respond at an early, potentially susceptible larval stage to poorer food quality and declining levels of a leaf monoterpene suggest that changes in needle quality within pines in future elevated-CO2 atmospheres may not especially affect young insects and that tree-feeding sawflies may respond in a manner similar to herb-feeding lepidopterans.
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References
Annila E, Hiltunen R, Löyttyniemi R (1984) Defoliation by Neodiprion sertifer (Hymenoptera, Diprionidae) in relation to terpene composition of Pinus contorta Ann Entomol Fenn 50: 33–36
Bazzaz FA (1990) The response of natural ecosystems to the rising CO2 levels. Annu Rev Ecol Syst 21: 167–196
Benjamin DM (1955) The biology and ecology of the red-headed pine sawfly (US Dept Agric Tech Bull 1118). US Department of Agriculture, Washington DC
Bray JR (1964) Primary consumption in three forest canopies. Ecology 45: 165–167
Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357–368
Cates RG, Henderson CB, Redak RA (1987) Responses of the western spruce budworm to varying levels of nitrogen and terpenes. Oecologia 73: 312–316
Coleman JS, McConnaughay KDM, Bazzaz FA (1993) Elevated CO2 and plant nitrogen-use:is reduced tissue nitrogen concentration size-dependent? Oecologia 93: 195–200
Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53: 209–233
Coppel HC, Benjamin DM (1964) Bionomics of the nearctic pinefeeding diprionids. Annu Rev Entomol 10: 69–91
Fajer ED (1989) The effects of enriched CO2 atmospheres on plant-insect herbivore interactions: growth responses of larvae of the specialist butterfly, Junonia coenia (Lepidoptera: Nymphalidae). Oecologia 81: 514–520
Fajer ED, Bowers MD, Bazzaz FA (1989) The effects of enriched carbon dioxide atmospheres on plant-insect herbivore interactions. Science 243: 1198–1200
Fajer ED, Bowers MD, Bazzaz FA (1991) The effects of enriched CO2 atmospheres on the buckeye butterfly Junonia coenia. Ecology 72: 751–754
Fajer ED, Bowers MD, Bazzaz FA (1992) The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago: a test of the carbon/nutrient balance hypothesis. Am Nat 140: 707–723
Fogal WH (1974) Nutritive value of pine foliage for some Diprionid sawflies. Proc Entomol Soc Ont 105: 101–118
Gershenzon J, Croteau R (1992) Terpenoids. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, San Diego, pp 165–219
Griffin KL, Thomas RB, Strain BR (1993) Effects of nitrogen supply and elevated carbon dioxide on construction cost in leaves of Pinus taeda (L.) seedlings. Oecologia 95:575–580
Haissig BE, Dickson RE (1979) Starch measurement in plant tissue using enzymatic hydrolysis Physiol Plant 47: 151–157
Hanover JW (1975) Physiology of tree resistance to insects. Annu Rev Entomol 20: 75–95
Ikeda TF, Matsumura F, Benjamin DM (1977) Mechanism of feeding discrimination between matured and juvenile foliage by two species of pine sawflies. J Chem Ecol 3: 677–694
Isaac RA, Johnson WC (1976) Determination of total nitrogen in plant tissue using a block digester. J Assoc Off Anal Chem 59: 98–100
Johnson RH, Lincoln DE (1990) Sagebrush and grasshopper responses to atmospheric carbon dioxide concentration. Oecologia 84: 103–110
Johnson RH, Lincoln DE (1991) Sagebrush carbon allocation patterns and grasshopper nutrition: the influence of CO2 enrichment and soil mineral limitation. Oecologia 87:127–134
Kimball BA (1983) Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agron J 75: 779–786
Kuehny JS, Peet MM, Nelson PV, Willits DH (1991) Nutrient dilution by starch in CO2-enriched Chrysanthenum. J Exp Bot 42: 711–716
Langenheim JH, Hall GD (1983) Sesquiterpene deterrence of a leaf-tying lepidopteran, Stenoma ferrocanella, on Hymenaea stigonocarpa in central Brazil. Biochem Syst Ecol 11: 29–36
Larsson S, Björkman C, Gref R (1986) Responses of Neodiprion sertifer (Hym., Diprionidae) larvae to variation in needle resin acid concentration in Scots pine. Oecologia 70: 77–84
Lincoln DE, Couvet D (1989) The effect of carbon supply on allocation to allelochemicals and caterpillar consumption of peppermint. Oecologia 78: 112–114
Lincoln DE, Sionit N, Strain BR (1984) Growth and feeding responses of Pseudoplusia includens (Lepidoptera: Noctuiidae) to host plants in controlled carbon dioxide atmospheres. Environ Entomol 13: 1527–1530
Lincoln DE, Couvet D, Sionit N (1986) Response of an insect herbivore to host plants grown in enriched carbon dioxide atmospheres. Oecologia 69: 556–560
Lindroth RL, Kinney KK, Platz CL (1993) Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry, and insect performance. Ecology 74: 763–777
Loon JJA van (1991) Measuring food utilization in plant-feeding insects toward a metabolic and dynamic approach. In: Bernays E (ed) Insect-plant interactions, Vol III. CRC Press, Boca Raton, pp 79–124
Mattson JW (1980) Nitrogen and herbivory. Annu Rev Ecol Syst 11: 119–162
Mihaliak CA, Couvet D, Lincoln DE (1987) Inhibition of feeding by a generalist insect due to increased volatile leaf terpenes under nitrate-limiting conditions. J Chem Ecol 13: 2059–2067
Morrow PA, Fox LR (1980) Effects of variation in Eucalyptus essential oil yield on insect growth and grazing damage. Oecologia 45: 209–219
Osbrink WLA, Trumble JT, Wagner RE (1987) Host suitability of Phaseolus lunata for Trichoplusia ni (Lepidoptera: Noctuiidae) in controlled carbon dioxide atmospheres. Environ Entomol 16: 210–215
Parra JR, Kogan M (1981) Comparative analysis of methods for measurements of food intake and utilization using the soybean looper, Pseudoplusia includens and artificial media. Entomol Exp Appl 30: 45
Redak RA, Cates RG (1984) Douglas-fir (Pseudotsuga menziesii)-spruce budworm (Choristoneura occidentalis) interactions: the effect of nutrition, chemical defenses, tissue phenology, and tree physical parameters on budworm success. Oecologia 62: 61–67
SAS Institute Inc (1990) SAS/STAT User's Guide: volume 2, version 6, 4th edition. SAS Institute, Cary NC
Schmidt DJ, Reese JC (1986) Sources of error in nutritional index studies of insects on artificial diet. J Insect Physiol 32: 193–198
Schuh BA, Benjamin DM (1984) The chemical feeding ecology of Neodiprion dubiosus Schedl., N. rugifrons Midd., and N. lecontei Fitch on jack pine (Pinus banksiana Lamb.) J Chem Ecol 10: 1071–1079
Scriber JM, Slansky F (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26: 183–211
Sionit N (1983) Response of soybean to two levels of mineral nutrition in CO2-enriched atmosphere. Crop Sci 23: 329–333
Slansky F (1992) Allelochemical-nutrient interactions in herbivore nutritional ecology. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. vol. II. Academic Press, San Diego, pp 135–174
Slansky F, Feeny PP (1977) Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol Monogr 47: 209–228
Slansky F, Rodriguez JG (eds) (1987) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley-Interscience, New York
Slansky F, Wheeler GS (1989) Compensatory increases in food consumption and utilization efficiencies by velvethean caterpillars mitigate impact of diluted diets on growth. Entomol Exp Appl 51: 175–187
Slansky F, Wheeler GS (1991) Food consumption and utilization responses to dietary dilution with cellulose and water by velvetbean caterpillars, Anticarsia gemmatalis. Physiol Entomol 16: 99–116
Strain BR, Cure JD (eds) (1985) Direct effects of increasing carbon dioxide on vegetation (DOE/ER-0238). U S Dept Energy, Washington DC
Tans PP, Fung IY, Takahashi T (1990) Observational constraints on the global atmospheric CO2 budget. Science 247: 1431–1438
Tissue DT, Thomas RB, Strain BR (1993) Long-term effects of elevated CO2 and nutrients on photosynthesis and rubisco in loblolly pine seedlings. Plant Cell Environ 16: 859–865
Wagner MR, Benjamin DM, Clancy KM, Schuh BA (1983) Influence of diterpene resin acids on feeding and growth of larch sawfly, Pristiphora erichsonii (Hartig). J Chem Ecol 9: 119–127
Waldbauer GP (1968) The consumption and utilization of food by insects. Adv Insect Physiol 5: 229–288
Wheeler GS, Slansky F (1991) Compensatory feeding responses of the fall armyworm (Spodoptera frugiperda) when fed water-and cellulose-diluted diets. Physiol Entomol 16: 361–374
Wilson LF, Wilkinson RC, Averill RC (1992) Redheaded pine sawfly-its ecology and management (U S Dept Agric For Serv Agri Man 694), US Department of Agriculture, Washington DC
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Williams, R.S., Lincoln, D.E. & Thomas, R.B. Loblolly pine grown under elevated CO2 affects early instar pine sawfly performance. Oecologia 98, 64–71 (1994). https://doi.org/10.1007/BF00326091
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DOI: https://doi.org/10.1007/BF00326091