Skip to main content
Log in

Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and plant genotype

  • Plant Animal Interactions
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

This study examined the effects of carbon dioxide (CO2)-, ozone (O3)-, and genotype-mediated changes in quaking aspen (Populus tremuloides) chemistry on performance of the forest tent caterpillar (Malacosoma disstria) and its dipteran parasitoid (Compsilura concinnata) at the Aspen Free-Air CO2 Enrichment (FACE) site. Parasitized and non-parasitized forest tent caterpillars were reared on two aspen genotypes under elevated levels of CO2 and O3, alone and in combination. Foliage was collected for determination of the chemical composition of leaves fed upon by forest tent caterpillars during the period of endoparasitoid larval development. Elevated CO2 decreased nitrogen levels but had no effect on concentrations of carbon-based compounds. In contrast, elevated O3 decreased nitrogen and phenolic glycoside levels, but increased concentrations of starch and condensed tannins. Foliar chemistry also differed between aspen genotypes. CO2, O3, genotype, and their interactions altered forest tent caterpillar performance, and differentially so between sexes. In general, enriched CO2 had little effect on forest tent caterpillar performance under ambient O3, but reduced performance (for insects on one aspen genotype) under elevated O3. Conversely, elevated O3 improved forest tent caterpillar performance under ambient, but not elevated, CO2. Parasitoid larval survivorship decreased under elevated O3, depending upon levels of CO2 and aspen genotype. Additionally, larval performance and masses of mature female parasitoids differed between aspen genotypes. These results suggest that host-parasitoid interactions in forest systems may be altered by atmospheric conditions anticipated for the future, and that the degree of change may be influenced by plant genotype.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

References

  • Arnaud PH (1978) A host-parasitoid catalog of North American Tachinidae (Diptera). US Dept Agric Misc Publ 1319:1–860

    Google Scholar 

  • Arteel GE, Lindroth RL (1992) Effects of aspen phenolic glycosides on gypsy moth (Lepidoptera: Lymantriidae) susceptibility to Bacillus thuringiensis. Great Lakes Entomol 25:239–244

    Google Scholar 

  • Barbosa P, Saunders JA, Waldvogel M (1982) Plant-mediated variation in herbivore suitability and parasitoid fitness. In: Visser JH, Minks AK (eds) Proceedings of the 5th International Symposium in Insect-Plant Relationships. Center for Agricultural Publishing and Documentation, Wageningen, pp 63–71

  • Bezemer TM, Jones TH (1998) Plant-insect herbivore interactions in elevated atmospheric CO2: quantitative analyses and guild effects. Oikos 82:212–222

    Google Scholar 

  • Bourchier RS (1991) Growth and development of Compsilura concinnata (Meigan) (Diptera: Tachinidae) parasitizing gypsy moth larvae feeding on tannin diets. Can Entomol 123:1047–1055

    Google Scholar 

  • Cannon WN (1993) Gypsy moth (Lepidoptera: Lymantriidae) consumption and utilization of northern red oak and white oak foliage exposed to simulated acid rain and ozone. Environ Entomol 22:669–673

    Google Scholar 

  • Ceulemans R, Janssens IA, Jach ME (1999) Effects of CO2 enrichment on trees and forests: lessons to be learned in view of future ecosystem studies. Ann Bot 84:577–590

    CAS  Google Scholar 

  • Chappelka AH, Kraemer ME, Mebrahtu T, Rangappa M, Benepal PS (1988) Effects of ozone on soybean resistance to the Mexican bean beetle (Epilachna varivestris Mulsant). Environ Exp Bot 28:53–60

    CAS  Google Scholar 

  • Cheng L (1970) Timing of attack of Lypha dubia Fall (Diptera: Tachinidae) on the winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae) as a factor affecting parasite success. J Anim Ecol 39:313–320

    Google Scholar 

  • Coleman JS, Jones CG (1988) Plant stress and insect performance: cottonwood, ozone and a leaf beetle. Oecologia 76:57–61

    Google Scholar 

  • Coviella CE, Trumble JT (1999) Effects of elevated atmospheric carbon dioxide on insect-plant interactions. Conserv Biol 13:700–712

    Article  Google Scholar 

  • Culver JJ (1919) A study of Compsilura concinnata, an imported tachinid parasite of the gipsy moth and the brown-tail moth. USDA Bull 766:1–27

    Google Scholar 

  • Dickson RE, Lewin KF, Isebrands JG, Coleman MD, Heilman WE, Riemenschneider DE, Sober J, Host GE, Hendrey GR, Pregitzer KS, Karnosky DF, Zak DR (2000) Forest Atmosphere Carbon Transfer and Storage (FACTS-II)—The Aspen Free-air CO2 and O3 Enrichment (FACE) project: an overview. General Technical Report NC−214. USDA Forest Service, St Paul, Minn.

  • Ellers J, van Alphen JM (2002) A trade-off between diapause duration and fitness in female parasitoids. Ecol Entomol 27:279–284

    Article  Google Scholar 

  • English-Loeb GM, Brody AK, Karban R (1993) Host-plant-mediated interactions between a generalist folivore and its tachinid parasitoid. J Anim Ecol 62:465–471

    Google Scholar 

  • Filion M, Dutilleul P, Potvin C (2000) Optimum experimental design for Free-Air Carbon Dioxide Enrichment (FACE) studies. Global Change Biol 6:843–854

    Article  Google Scholar 

  • Fowler D, Cape JN, Coyle M, Flechard C, Kuylenstierna J, Hicks K, Derwent D, Johnson C, Stevenson D (1999) The global exposure of forests to air pollutants. Water Air Soil Pollut 116:5–32

    CAS  Google Scholar 

  • Gate IM, McNeill S, Ashmore MR (1995) Effects of air pollution on the searching behaviour of an insect parasitoid. Water Air Soil Pollut 85:1425–1430

    CAS  Google Scholar 

  • Goverde M, Bazin A, Shykoff JA, Erhardt A (1999) Influence of leaf chemistry of Lotus corniculatus (Fabaceae) on larval development of Polyommatus icarus (Lepidoptera: Lycaenidae): effects of elevated CO2 and plant genotype. Funct Ecol 13:801–810

    Article  Google Scholar 

  • Greenblatt JA, Barbosa P (1981) Effects of host's diet on two pupal parasitoids of the gypsy moth, Brachymeria intermedia (Nees) and Coccygomimus turionellae (L.). J Appl Ecol 18:1–10

    Google Scholar 

  • Greenblatt JA, Barbosa P, Montegomery ME (1982) Host's diet effects on nitrogen utilization efficiency for two parasitoid species: Brachymeria intermedia and Coccygomimus turionellae. Physiol Entomol 7:263–267

    Google Scholar 

  • Hagerman AE, Butler LG (1980) Condensed tannin purification and characterization of tannin-associated proteins. J Agric Food Chem 28:947–952

    CAS  PubMed  Google Scholar 

  • Hemming JDC, Lindroth RL (1995) Intraspecific variation in aspen phytochemistry: effects on performance of gypsy moths and forest tent caterpillars. Oecologia 103:79–88

    Google Scholar 

  • Herms DA, Mattson WJ, Karowe DN, Coleman MD, Trier TM, Birr BA, Isebrands JG 1995. Variable performance of outbreak defoliators on aspen clones exposed to elevated CO2 and O3. General Technical Report NE-214:43–55. USDA Forest Service, NE Forest Experiment Station

  • Hodson AC (1941) An ecological study of the forest tent caterpillar, Malacosoma disstria Hbn., in northern Minnesota. Univ Minn Agric Exp Stn Bull 148:1–55

    Google Scholar 

  • Hwang SY, Lindroth RL (1997) Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia 111:99–108

    Article  Google Scholar 

  • Jackson DM, Rufty TW, Heagle AS, Severson RF, Eckel RVW (2000) Survival and development of tobacco hornworm larvae on tobacco plants grown under elevated levels of ozone. J Chem Ecol 26:1–19

    Article  CAS  Google Scholar 

  • Kangasjärvi J, Talvinen J, Utriainen M, Karjalainen R (1994) Plant defence systems induced by ozone. Plant Cell Environ 17:783–794

    Google Scholar 

  • Karnosky DF, Gagnon ZE, Dickson RE, Coleman MD, Lee EH, Isebrands JG (1996) Changes in growth, leaf abscission, and biomass associated with seasonal tropospheric ozone exposures of Populus tremuloides clones and seedlings. Can J For Res 26:23–37

    CAS  Google Scholar 

  • Karnosky DF, Zak DR, Pregitzer KS, Awmack CS, Bockheim JG, Dickson RE, Hendrey GR, Host GE, King JS, Kopper BJ, Kruger EL, Kubiske ME, Lindroth RL, Mattson WJ, McDonald EP, Noormets A, Oksanen E, Parsons WFJ, Percy KE, Podila GK, Riemenschneider DE, Sharma P, Sober A, Sober J, Jones WS, Anttonen S, Vapaavuori E, Isebrands JG (2003) Low levels of tropospheric O3 moderate responses of temperate hardwood forests to elevated CO2: a synthesis of results from the Aspen FACE project. Funct Ecol (in press)

    Google Scholar 

  • Karowe DN, Schoonhoven LM (1992) Interactions among three trophic levels: the influence of host plant on performance of Pieris brassicae and its parasitoid, Cotesia glomerata. Entomol Exp Appl 62:241–251

    Google Scholar 

  • Keinanen M, Julkunen-Tiitto R, Mutikainen P, Walls M (1999) Trade-offs in phenolic metabolism of silver birch: effects of fertilization, defoliation, and genotype. Ecology 80:1970–1986

    Google Scholar 

  • Kinney KK, Lindroth RL, Jung SM, Nordheim EV (1997) Effects of CO2- and NO3-availability on deciduous trees: phytochemistry and insect performance. Ecology 78:215–230

    Google Scholar 

  • Kopper BJ, Lindroth RL (2003a) Responses of trembling aspen (Populus tremuloides) phytochemistry and aspen blotch leafminer (Phyllonorycter tremuloidiella) performance to elevated levels of atmospheric CO2 and O3. Agric For Entomol 5:17–26

    Article  Google Scholar 

  • Kopper BJ, Lindroth RL (2003b) Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134:95–103

    Article  PubMed  Google Scholar 

  • Koricheva J, Larsson S, Haukioja E, Keinänen M (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos 83:212–226

    CAS  Google Scholar 

  • Lavola A, Julkunen-Tiitto RPE (1994) Does ozone stress change the primary or secondary metabolites of birch (Betula pendula Roth)? New Phytol 126:637–642

    Google Scholar 

  • Lindroth RL (1996a) Consequences of elevated atmospheric CO2 for forest insects. In: Koch GW, Mooney HA (eds) Carbon dioxide and terrestrial ecosystems. Academic Press, San Diego, pp 105–120

  • Lindroth RL (1996b) CO2-mediated changes in tree chemistry and tree-Lepidoptera interactions. In: Körner C, Bazzaz FA (eds) Carbon dioxide, populations, and communities. Academic Press, San Diego, pp 347–361

  • Lindroth RL, Bloomer MS (1991) Biochemical ecology of the forest tent caterpillar: responses to dietary protein and phenolic glycosides. Oecologia 86:408–413

    Google Scholar 

  • Lindroth RL, Hwang SY (1996) Clonal variation in foliar chemistry of quaking aspen (Populus tremuloides Michx). Biochem Syst Ecol 24:357–364

    Google Scholar 

  • Lindroth RL, Kinney KK, Platz CL (1993a) Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry, and insect performance. Ecology 74:763–777

    CAS  Google Scholar 

  • Lindroth RL, Reich PB, Tjoelker MG, Volin JC, Oleksyn J (1993b) Light environment alters response to ozone stress in Acer saccharum Marsh. and hybrid Populus L. seedlings. III. Consequences for gypsy moth performance. New Phytol 124:647–651

    CAS  Google Scholar 

  • Lindroth RL, Roth S, Kruger EL, Volin JC, Koss PA (1997) CO2-mediated changes in aspen chemistry: effects on gypsy moth performance and susceptibility to virus. Global Change Biol 3:279–289

    Google Scholar 

  • Lindroth RL, Roth S, Nordheim EV (2001a) Genotypic variation in response of quaking aspen (Populus tremuloides) to atmospheric CO2 enrichment. Oecologia 126:371–376

    Article  Google Scholar 

  • Lindroth RL, Kopper BJ, Parsons WFJ, Bockheim JG, Karnosky DF, Hendrey GR, Pregitzer KS, Isebrands JG, Sober J (2001b) Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Environ Pollut 115:395–404

    Article  CAS  PubMed  Google Scholar 

  • Lindroth RL, Osier TL, Wood SA, Barnhill HRA (2002a) Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochem Syst Ecol 30:297–307

    CAS  Google Scholar 

  • Lindroth RL, Wood SA, Kopper BJ (2002b) Responses of quaking aspen genotypes to enriched CO2: foliar chemistry and tussock moth performance. Agric For Entomol 4:315–323

    Article  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, N.C.

  • Loponen J, Ossipov V, Lempa K, Haukioja E, Pihlaja K (1998) Concentrations and among-compound correlations of individual phenolics in white birch leaves under air pollution stress. Chemosphere 37:1445–1456

    Article  CAS  Google Scholar 

  • Mallampalli N, Barbosa P, Weinges K (1996) Effects of condensed tannins and catalpol on growth and development of Compsilura concinnata (Diptera: Tachinidae) reared in gypsy moth (Lepidoptera: Lymantriidae). J Entomol Sci 31:289–300

    Google Scholar 

  • Mansfield JL, Curtis PS, Zak DR, Pregitzer KS (1999) Genotypic variation for condensed tannin production in trembling aspen (Populus tremuloides, Salicaceae) under elevated CO2 and in high- and low-fertility soil. Am J Bot 86:1154–1159

    CAS  PubMed  Google Scholar 

  • Mattson WJ, Palmer SR (1988) Changes in foliar minerals and phenolics in trembling aspen, Populus tremuloides, in response to artificial defoliation. In: Mattson WJ, Levieux J, Bernard-Dagan C (eds) Mechanisms of woody plant defenses against insects: search for pattern. Springer, Berlin Heidelberg New York, pp 157–169

  • Muggli JM (1974) Sex identification of Malacosoma disstria pupae (Lepidoptera: Lasiocampidae). Ann Entomol Soc Am 67:521–522

    Google Scholar 

  • Palo RT (1984) Distribution of birch (Betula spp.), willow (Salix spp.), and poplar (Populus spp.) secondary metabolites and their potential role as chemical defense against herbivores. J Chem Ecol 10:499–520

    CAS  Google Scholar 

  • Parry D, Spence JR, Volney WJA (1998) Budbreak phenology and natural enemies mediate survival of first-instar forest tent caterpillar (Lepidoptera: Lasiocampidae). Environ Entomol 27:1368–1374

    Google Scholar 

  • Percy KE, Awmack CS, Lindroth RL, Kubiske ME, Kopper BJ, Isebrands JG, Pregitzer KS, Hendrey GR, Dickson RE, Zak DR, Oksanen E, Sober J, Harrington R., Karnosky DF (2002) Altered performance of forest pests under atmospheres enriched by CO2 and O3. Nature 420:403–407

    Article  CAS  PubMed  Google Scholar 

  • Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230

    CAS  Google Scholar 

  • Prado FE, González JA, Boero C, Sampierto AR (1998) A simple and sensitive method for determining reducing sugars in plant tissues. Application to quantify the sugar content in quinoa (Chenopodium quinoa Willd.) seedlings. Phytochem Anal 9:58–62

    CAS  Google Scholar 

  • Riemer J, Whittaker JB (1989) Air pollution and insect herbivores: observed interactions and possible mechanisms. In: Insect-plant interactions, vol 1. CRC, Boca Raton, pp 73–105

  • Roth SK, Lindroth RL (1995) Elevated atmospheric CO2 effects on phytochemistry, insect performance and insect-parasitoid interactions. Global Change Biol 1:173–182

    Google Scholar 

  • Roth S, Knorr C, Lindroth RL (1997) Dietary phenolics affect performance of the gypsy moth (Lepidoptera: Lymantriidae) and its parasitoid Cotesia melanoscela (Hymenoptera: Braconidae). Environ Entomol 26:668–671

    CAS  Google Scholar 

  • Roth S, Lindroth RL, Volin JC, Kruger EL (1998) Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance. Global Change Biol 4:419–430

    Article  Google Scholar 

  • SAS Institute (1989) SAS User's Guide: Statistics. SAS Institute, Cary, N.C.

  • Scriber JM, Slansky F (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26:183–211

    Article  Google Scholar 

  • Stehr FW, Cook EF (1968) A revision of the genus Malcosoma Hübner in North America (Lepidoptera: Lasiocampidae): systematics, biology, immatures, and parasites. US Natl Mus Bull 276:1–321

    Google Scholar 

  • Stiling P, Rossi AM, Hungate B, Dukstra P, Hinkle CR, Knott WM, Drake B (1999) Decreased leaf-miner abundance in elevated CO2: reduced leaf quality and increased parasitoid attack. Ecol Appl 9:240–244

    CAS  PubMed  Google Scholar 

  • Stiling P, Moon DC, Hunter MD, Colson J, Rossi AM, Hymus GJ, Drake BG (2003) Elevated CO2 lowers relative and absolute herbivore density across all species of a scrub-oak forest. Oecologia 134:82–87

    Article  PubMed  Google Scholar 

  • Trumble JT, Hare JD, Musselman PC, McCool PM (1987) Ozone-induced changes in host-plant suitability: interactions of Keiferia lycopersicella and Lycopersicon esculentum. J Chem Ecol 13:203–218

    CAS  Google Scholar 

  • Turlings TCJ, Benrey B (1998) Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5:321–333

    Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vinson SB, Barbosa P (1987) Interrelationships of nutritional ecology of parasitoids. In: Slansky F, Rodriguez JG (eds) Nutritional quality of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 673–695

  • Warren JH, Raupp MJ, Sadoff CS, Odell TM (1992) Host plants used by gypsy moths affect survival and development of the parasitoid Cotesia melanoscela. Environ Entomol 21:173–177

    Google Scholar 

  • Williams RS, Norby RJ, Lincoln DE (2000) Effects of elevated CO2 and temperature-grown red and sugar maple on gypsy moth performance. Global Change Biol 6:685–695

    Article  Google Scholar 

  • Zak DR, Pregitzer KS, Curtis PS, Vogel CS, Holmes WE, Lussenhop J (2000) Atmospheric CO2, soil-N availability, and allocation of biomass and nitrogen by Populus tremuloides. Ecol Appl 10:34–46

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice Hall, New Jersey

Download references

Acknowledgements

We thank Kate Zachman, Aimee Weldon, Kelly Krein, Brian Kopper, Heidi Barnhill, and the Aspen FACE Experiment staff for assistance in the field and laboratory. We also thank Brian Rehill for suggestions on this work, Peter Crump for assistance with SAS, and John Dedes for advice on rearing Compsilura concinnata. Bob McCron and Kees van Frankenheyzen (Canadian Forest Service, Sault Ste. Marie, Canada) provided Malacosoma disstria egg masses and C. concinnata puparia, respectively. This work was supported by McIntire-Stennis grant WIS04457 and National Science Foundation grant DEB-9707263. The FACE facility was supported by the U.S. Department of Energy (Office of Biological and Environmental Research grant DE-FG02–95ER62125), the U.S. Forest Service Global Change Program, and the U.S. Forest Service North Central Research Station.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard L. Lindroth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holton, M.K., Lindroth, R.L. & Nordheim, E.V. Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and plant genotype. Oecologia 137, 233–244 (2003). https://doi.org/10.1007/s00442-003-1351-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-003-1351-z

Keywords

Navigation