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Soil carbon and nitrogen mineralization following deposition of insect frass and greenfall from forests under elevated CO2 and O3

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Abstract

Elevated CO2 and O3 alter tree quality and the quality of herbivore inputs, such as frass, to forest soil. Altered quality or quantity of herbivore inputs to the forest floor can have large impacts on belowground processes. We collected green leaves and frass from whitemarked tussock moth caterpillars from aspen-birch stands at the Aspen Free Air CO2 Enrichment (FACE) site near Rhinelander, WI, USA. Small or large quantities of frass, greenfall, or a 1:1 ratio of frass and greenfall were added to microcosms for each FACE treatment (control, +CO2, +O3, +CO2+O3). We measured initial frass and greenfall quality, and recorded microbial respiration, and nitrate leaching over 40 days. Elevated carbon dioxide (eCO2) and tropospheric ozone (eO3) significantly altered the carbon, nitrogen, and condensed tannin content of insect frass and green leaves. Although FACE treatments affected input quality, they had minimal effect on microbial respiration and no effect on nitrogen leaching. In contrast, input quantity substantially influenced microbial respiration and nitrate leaching. Respiratory carbon loss and nitrate immobilization were nearly double in microcosms receiving large amounts of herbivore inputs than those receiving no herbivore inputs. Small amounts of herbivore inputs, however, did not significantly alter microbial respiration or immobilization, suggesting that effects of herbivore inputs on soil processes will be detected only at moderate to high herbivory/input levels. These results suggest that subtle changes in frass and greenfall quality may not affect soil nutrient cycling. In contrast, environmental change induced increases in insect population size or frass and greenfall inputs to the soil may substantially impact nutrient cycling.

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References

  • Akimoto H (2003) Global air quality and pollution. Science 302:1716–1719

    Article  CAS  PubMed  Google Scholar 

  • Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1156–1168

    Article  Google Scholar 

  • Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Natl Acad Sci 97:14414–14417

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Burrows SN, Gower ST, Clayton MK, Mackay DS, Ahl DE, Norman JM, Diak G (2002) Application of geostatistics to characterize leaf area index (LAI) from flux tower to landscape scales using a cyclic sampling design. Ecosystems 5:667–679

    Google Scholar 

  • Carpenter SR (1996) Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77:677–690

    Article  Google Scholar 

  • Christenson LM, Lovett GM, Mitchell MJ, Groffman PM (2002) The fate of nitrogen in gypsy moth frass deposited to an oak forest floor. Oecologia 131:444–452

    Article  Google Scholar 

  • Constantinides M, Fownes JH (1994) Nitrogen mineralization from leaves and litter of tropical plants: relationship to nitrogen, lignin, and soluble polyphenol concentrations. Soil Biol Biochem 26:49–55

    Article  CAS  Google Scholar 

  • Davidson EA, Savage K, Bolstad P, Clark DA, Curtis PS, Ellsworth DS, Hanson PJ, Luo Y, Pregitzer KS, Randolph JC, Zak DR (2002) Belowground carbon allocation in forests estimated from litterfall and IRGA-based soil respiration measurements. Agric For Meteorol 113:39–51

    Article  Google Scholar 

  • Dickson RE, Lewin KF, Isebrands JG, Coleman MD, Heilman WE, Riemenschneider DE, Sober J, Host GE, Zak DR, Hendry GR, Pregitzer KS, Karnosky DF (2000) Forest atmosphere carbon transfer storage-II (FACTS II)—the aspen free-air CO2 and O3 enrichment (FACE) project: an overview, General Technical Report NC-214, USDA Forest Service, North Central Research Station, Rhinelander, WI

  • Doane TA, Horwath WR (2003) Spectrophotometric determination of nitrate with a single reagent. Analytical Letters 36:2713–2722

    Article  CAS  Google Scholar 

  • Eshleman KN, Morgan RP II, Webb JR, Deviney FA, Galloway JN (1998) Temporal patterns of nitrogen leakage from mid-Appalachian forested watersheds: role of insect defoliation. Water Resour Res 34:2005–2016

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Fogal WH, Slansky F Jr (1984) Contribution of feeding by European pine sawfly larvae to litter production and element flux in Scots pine plantations. Can J For Res 15:484–487

    Google Scholar 

  • Fonte SJ, Schowalter TD (2004) Decomposition of greenfall vs. senescent foliage in a tropical forest ecosystem in Puerto Rico. Biotropica 36:474–482

    Google Scholar 

  • Frost CJ, Hunter MD (2004) Insect canopy herbivory and frass deposition affect soil nutrient dynamics and export in oak mesocosms. Ecology 85:3335–3347

    Article  Google Scholar 

  • Frost CJ, Hunter MD (2007) Recycling of nitrogen in herbivore feces: plant recovery, herbivore assimilation, soil retention, and leaching losses. Oecologia 151:42–53

    Article  PubMed  Google Scholar 

  • Grace JR (1986) The influence of gypsy moth on the composition and nutrient content of litter fall in a Pennsylvania oak forest. For Sci 32:855–870

    Google Scholar 

  • Hollinger DY (1986) Herbivory and the cycling of nitrogen and phosphorus in isolated California oak trees. Oecologia 70:291–297

    Article  Google Scholar 

  • Holton MK, Lindroth RL, Nordheim EV (2003) Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and genotype. Oecologia 137:233–244

    Article  PubMed  Google Scholar 

  • Hunter MD (2001) Insect population dynamics meets ecosystem ecology: effects of herbivory on soil nutrient dynamics. Agric For Entomol 3:77–84

    Article  Google Scholar 

  • Hunter MD, Linnen CR, Reynolds BC (2003) Effects of endemic densities of canopy herbivores on nutrient dynamics along a gradient in elevation in the southern Appalachians. Pedobiologia 47:231–244

    Article  Google Scholar 

  • Intergovernmental Panel on Climate Change (2007) Climate Change 2007: The Physical Scientific Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • Karnosky DF (1976) Threshold levels for foliar injury to Populus tremuloides Michx. by sulfur dioxide and ozone. Can J For Res 6:166–169

    Article  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, Thakur RC, Sober A, Sober J, Jones WS, Anttonen S, Vapaavuori E, Mankovska B, Heilman WE, Isebrands JG (2003) Tropospheric O3 moderates responses of temperate hardwood forests to elevated CO2: a synthesis of molecular to ecosystem results from the Aspen FACE project. Funct Ecol 17:289–304

    Article  Google Scholar 

  • King JS, Hanson PJ, Bernhardt E, DeAngelis P, Norby RJ, Pregitzer KS (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Glob Change Biol 10:1027–1042

    Article  Google Scholar 

  • Knepp RG, Hamilton JG, Zangerl AR, Berenbaum MR, DeLucia EH (2007) Foliage of oaks grown under elevated CO2 reduced performance of Antheraea polyphemus (Lepidoptera: Saturniidae). Environ Entomol 36:609–617

    Article  PubMed  Google Scholar 

  • Kopper BJ, Lindroth RL (2003) 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 

  • Kopper BJ, Jakobi VN, Osier TL, Lindroth RL (2002) Effects of paper birch condensed tannin on whitemarked tussock moth (Lepidoptera: Lymantriidae) performance. Environ Entomol 31:10–14

    Article  CAS  Google Scholar 

  • Liebhold AM, Elkinton JS (1988) Techniques for estimating the density of late-instar gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae), populations using frass drop and frass production measurements. Environ Entomol 17:381–384

    Google Scholar 

  • Lightfoot DC, Whitford WG (1990) Phytophagous insects enhance nitrogen flux in a desert creosote bush community. Oecologia 82:18–25

    Article  Google Scholar 

  • Lindroth RL (1996) Consequences of elevated atmospheric CO2 for forest insects. In: Korner C, Bazzaz FA (eds) Carbon dioxide, populations, and communities. Physiological Ecology Series, Academic Press, San Diego, pp 347–361

    Chapter  Google Scholar 

  • Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36:2–21

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lindroth RL, Roth S, Nordheim EV (2001) Genotypic variation in response of quaking aspen (Populus tremuloides) to atmospheric CO2 enrichment. Oecologia 126:371–379

    Article  Google Scholar 

  • Liu LL, King JS, Giardina CP (2005) Effects of elevated concentrations of atmospheric CO2 and tropospheric O3 on leaf litter production and chemistry in trembling aspen and paper birch communities. Tree Physiol 25:1511–1522

    CAS  PubMed  Google Scholar 

  • Liu LL, King JS, Booker FL, Giardina CP, Allen HL, Hu S (2009) Enhanced litter input rather than changes in litter chemistry drive soil carbon and nitrogen cycles under elevated CO2: a microcosm study. Glob Change Biol 15:441–453

    Article  Google Scholar 

  • Lovett GM, Ruesink AE (1995) Carbon and nitrogen mineralization from decomposing gypsy moth frass. Oecologia 104:133–138

    Article  Google Scholar 

  • Lovett GM, Hart JE, Christenson LM, Jones CG (1998) Caterpillar gut and ammonia volatilization: retention of nitrogen by gypsy moth larvae consuming oak foliage. Oecologia 117:513–516

    Article  Google Scholar 

  • Lovett GM, Christenson LM, Groffman PM, Jones CG, Hart JE, Mitchell JM (2002) Insect defoliation and nitrogen cycling in forests. Bioscience 52:335–341

    Article  Google Scholar 

  • Madritch MD, Donaldson JR, Lindroth RL (2007a) Canopy herbivory can mediate the influence of plant genotype on soil processes through frass deposition. Soil Biol Biochem 29:1192–1201

    Article  Google Scholar 

  • Madritch MD, Jordan LM, Lindroth RL (2007b) Interactive effects of condensed tannin and cellulose additions on soil respiration. Can J For Res 37:2063–2067

    Article  CAS  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide-Biol Chem 5:62–71

    Article  CAS  Google Scholar 

  • Parsons WFJ, Lindroth RL, Bockheim JG (2004) Decomposition of Betula papyrifera leaf litter under the independent and interactive effects of elevated CO2 and O3. Glob Change Biol 10:1666–1677

    Article  Google Scholar 

  • Parsons WFJ, Bockheim JG, Lindroth RL (2008) Independent, interactive, and species-specific responses of leaf litter decomposition to elevated CO2 and O3 in a northern hardwood forest. Ecosystems 11:505–519

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Raich JW, Nadelhoffer KJ (1989) Belowground carbon allocation in forest ecosystems: global trends. Ecology 70:1346–1354

    Article  Google Scholar 

  • Reynolds BC, Hunter MD (2001) Responses of soil respiration, soil nutrients, and litter decomposition to inputs from canopy herbivores. Soil Biol Biochem 33:1641–1652

    Article  CAS  Google Scholar 

  • Reynolds BC, Hunter MD, Crossley DA Jr (2000) Effects of canopy herbivory on nutrient cycling in a northern hardwood forest in western North Carolina. Selbyana 21:74–78

    Google Scholar 

  • Risely LS, Crossley DA Jr (1993) Contribution of herbivore-caused greenfall to litterfall nitrogen flux in several southern Appalachian forested watersheds. Am Midl Nat 129:67–74

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139:395–436

    Article  Google Scholar 

  • Schowalter TD (2000) Insect ecology: an ecosystem approach. Academic Press, New York

    Google Scholar 

  • Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008) Plant-soil-microorganism interactions: heritable relationship between plant genotype and associate soil microorganisms. Ecology 89:773–781

    Article  PubMed  Google Scholar 

  • Stadler B, Solinger S, Michalzik B (2001) Insect herbivores and the nutrient flow from the canopy to the soil in coniferous and deciduous forests. Oecologia 126:104–113

    Article  Google Scholar 

  • Stadler B, Muller T, Orwig D (2006) The ecology of energy and nutrient fluxes in hemlock forests invaded by hemlock woolly adelgid. Ecology 87:1792–1804

    Article  PubMed  Google Scholar 

  • Steele SJ, Gower ST, Vogel JG, Norman JM (1997) Root mass, net primary production and turnover in aspen, jack pine and black spruce forest in Saskatchewan and Manitoba, Canada. Tree Physiol 17:577–587

    CAS  PubMed  Google Scholar 

  • Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant-herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob Change Biol 13:1–20

    Article  Google Scholar 

  • Swank WT, Crossley DA Jr (1988) Forest ecology and hydrology at Coweeta. Springer, New York

    Google Scholar 

  • Valkama E, Koricheva J, Oksanen E (2007) Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Change Biol 13:184–201

    Article  Google Scholar 

  • Verhoef HA (1996) The role of soil microcosms in the study of ecosystem processes. Ecology 77:685–690

    Article  Google Scholar 

  • Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974

    Article  CAS  Google Scholar 

  • Wittig VE, Ainsworth EA, Naidu SL, Karnosky DF, Long SP (2009) Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta-analysis. Glob Change Biol 15:396–424

    Article  Google Scholar 

  • Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a metaanalysis. Glob Change Biol 12:27–41

    Article  Google Scholar 

Download references

Acknowledgments

Aspen FACE is principally supported by the Office of Science (BER), U.S. Department of Energy, Grant No. DE-FG02-95ER62125 to Michigan Technological University, and Contract No. DE-AC02-98CH10886 to Brookhaven National Laboratory, the U.S. Forest Service Northern Global Change Program and North Central Research Station, Michigan Technological University, and Natural Resources Canada—Canadian Forest Service. We thank the members of the Lindroth Lab, especially Mike Madritch, for input into study design and lab techniques, Adam Gusse and Andy Vogelzang for help raising whitemarked tussock moth larvae, and Leanne Vigue for collecting senesced leaves from the Aspen FACE site. We also thank the two anonymous reviewers for their helpful comments on the manuscript. This work was supported by U.S. Department of Energy (Office of Science, BER) grant DE-FG02-06ER64232, and University of Wisconsin Hatch grant WIS04898 to R.L. Lindroth.

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  1. Department of Entomology, University of Wisconsin, 237 Russell Labs, 1630 Linden Drive, Madison, WI, 53706-1598, USA

    Michael Hillstrom, Timothy D. Meehan, Kristine Kelly & Richard L. Lindroth

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  1. Michael Hillstrom
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  2. Timothy D. Meehan
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  4. Richard L. Lindroth
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Correspondence to Michael Hillstrom.

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Hillstrom, M., Meehan, T.D., Kelly, K. et al. Soil carbon and nitrogen mineralization following deposition of insect frass and greenfall from forests under elevated CO2 and O3 . Plant Soil 336, 75–85 (2010). https://doi.org/10.1007/s11104-010-0449-4

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