The impact of insect herbivory on biogeochemical cycling in broadleaved forests varies with temperature

. 2024 Jul 17 ; 15 (1) : 6011. [epub] 20240717

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39019847

Grantová podpora
682707 EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
871120 EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
NE/R016860/1 RCUK | Natural Environment Research Council (NERC)

Odkazy

PubMed 39019847
PubMed Central PMC11254921
DOI 10.1038/s41467-024-50245-9
PII: 10.1038/s41467-024-50245-9
Knihovny.cz E-zdroje

Herbivorous insects alter biogeochemical cycling within forests, but the magnitude of these impacts, their global variation, and drivers of this variation remain poorly understood. To address this knowledge gap and help improve biogeochemical models, we established a global network of 74 plots within 40 mature, undisturbed broadleaved forests. We analyzed freshly senesced and green leaves for carbon, nitrogen, phosphorus and silica concentrations, foliar production and herbivory, and stand-level nutrient fluxes. We show more nutrient release by insect herbivores at non-outbreak levels in tropical forests than temperate and boreal forests, that these fluxes increase strongly with mean annual temperature, and that they exceed atmospheric deposition inputs in some localities. Thus, background levels of insect herbivory are sufficiently large to both alter ecosystem element cycling and influence terrestrial carbon cycling. Further, climate can affect interactions between natural populations of plants and herbivores with important consequences for global biogeochemical cycles across broadleaved forests.

Appalchian State University 572 Rivers Street Boone NC 28608 USA

Asociación Civil Sin Fines De Lucro Para La Biodiversidad Investigación Y Desarrollo Ambiental En Ecosistemas Tropicales Urbanización Ucchullo Grande Avenida Argentina F 9 Cusco Perú

CAS Key Laboratory of Forest Ecology and Management Institute of Applied Ecology Chinese Academy of Sciences Shenyang 110016 China

Centre for Horticultural Science Queensland Alliance for Agriculture and Food Innovation The University of Queensland 47 Mayers Road Nambour 4056 Australia

College of Science and Engineering and Centre for Tropical Environmental and Sustainability Science James Cook University Qld Australia

CongoPeat Project Ecole Nationale Supérieure d'Agronomie et de Foresterie Université Marien Ngouabi Brazzaville République du Congo

CONICET CENAC APN Universidad Nacional del Comahue Argentina

CSIR Forestry Research Institute of Ghana Kumasi Ashanti Ghana

Department of Ecology and Environmental Science Umeå University Linnaeus väg 6 Umeå Sweden

Department of Ecology Faculty of Biology University of Warsaw Żwirki i Wigury 101 02 086 Warsaw Poland

Department of Ecology University of Innsbruck Sterwartestraße 15 Innsbruck Austria

Department of Geography University College London London UK

Department of Natural Resources Management CSIR College of Science and Technology Kumasi Ghana

Department of Physical Geography and Ecosystem Science Lund University Lund Sweden

Department of Physical Geography and Environmental Management Problems Institute of Geography Russian Science Academy Moscow Russia

Department of Plant Systematics University of Bayreuth Bayreuth Germany

Department of Science and Conservation National Tropical Botanical Garden 3530 Papalina Road Kalāheo HI 96741 USA

Ecole Nationale Supérieure d'Agronomie et de Foresterie Université Marien Ngouabi Brazzaville République du Congo

Environmental Change Institute School of Geography and the Environment University of Oxford Oxford OX1 3QY UK

Escuela de Ingeniería Forestal Tecnológico de Costa Rica Cartago Costa Rica

Facultad de Ciencias Biológicas Universidad Nacional de San Antonio Abad del Cusco Av de La Cultura 773 Cusco Cusco Province 08000 Peru

Faculty of Silviculture and Forest Engineering Transilvania University of Brașov Șirul Beethoven 1 500123 Brașov Romania

Forest Research Institute University of Quebec in Abitibi Témiscamingue QC Canada

Forest Research Institute University of the Sunshine Coast Sippy Downs Queensland Australia

Grupo de Ecología de Invasiones Instituto de Investigaciones en Biodiversidad y Medioambiente CONICET Universidad Nacional del Comahue Bariloche Argentina

Institute of Ecology Ilia State University 3 5 Cholokashvili Ave 0169 Tbilisi Georgia

Institute of Geology and Nature Management Far Eastern Branch of Russian Academy of Sciences Relochny lane 1 Blagoveshchensk 675000 Russia

Institute of Pacific Islands Forestry Pacific Southwest Research Station USDA Forest Service Hilo HI USA

Institute of Zoology Ilia State University 3 5 Cholokashvili Ave 0169 Tbilisi Georgia

Instituto de Ciencias Ambientales y Evolutivas Universidad Austral de Chile Campus Isla Teja Valdivia Chile

Kevo Subarctic Research Institute Biodiversity Unit University of Turku 20014 Turku Finland

Laboratoire de Biodiversité de Gestion des Ecosystèmes et de l'Environnement Faculté des Sciences et techniques Université Marien Ngouabi Brazzaville République du Congo

Mammal Research Institute Polish Academy of Sciences Ul Stoczek 1 17‑230 Białowieża Poland

Pacific Southwest Research Station USDA Forest Service Hilo Hawai'i USA

Pitirim Sorokin Syktyvkar State University 455 Oktyabrsky prosp 167001 Syktyvkar Russia

Reforest Africa PO Box 5 Mang'ula Kilombero District Tanzania

Research Institute of Tropical Forestry Chinese Academy of Forestry Guangzhou 510520 China

Rubenstein School of Environment and Natural Resources University of Vermont Burlington VT 05405 USA

School of Geography University of Leeds Leeds UK

Senckenberg Biodiversity and Climate Research Centre Frankfurt Germany

Siberian Institute of Plant Physiology and Biochemistry SB RAS 664033 Irkutsk Lermontova str 132 Russia

Swiss Federal Institute for Forest Snow and Landscape Research WSL Birmensdorf 8903 Switzerland

The Silva Tarouca Research Institute Květnové náměstí 391 Průhonice 252 43 Czech Republic

Ugyen Wangchuk Institute for Forest Research and Training Department of Forests and Park Services Ministry of Energy and Natural Resources Lamai Goempa Bumthang Bhutan

Yugra State University 628012 Chekhova street 16 Khanty Mansiysk Russia

Zobrazit více v PubMed

McNaughton SJ, Oesterheld M, Frank DA, Williams KJ. Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats. Nature. 1989;34:142–144. doi: 10.1038/341142a0. PubMed DOI

Huntly N. Herbivores and the dynamics of communities and ecosystems. Annu. Rev. Ecol. Evol. Syst. 1991;22:477–503. doi: 10.1146/annurev.es.22.110191.002401. DOI

Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Q. Rev. Biol. 1992;67:283–335. doi: 10.1086/417659. DOI

Anderegg WR, et al. Tree mortality from drought, insects, and their interactions in a changing climate. N. Phytol. 2015;208:674–683. doi: 10.1111/nph.13477. PubMed DOI

Pringle RM, et al. Impacts of large herbivores on terrestrial ecosystems. Curr. Biol. 2023;33:R584–R610. doi: 10.1016/j.cub.2023.04.024. PubMed DOI

Kozlov, M. V. & Zvereva, E. L. in Progress In Botany Vol. 79 (eds Cánovas, F., Lüttge, U., Matyssek, R.) 313–355 (Springer, Cham, 2017).

Risch AC, et al. Size-dependent loss of aboveground animals differentially affects grassland ecosystem coupling and functions. Nat. Commun. 2018;9:3684. doi: 10.1038/s41467-018-06105-4. PubMed DOI PMC

Bardgett, R. D. & Wardle, D. A. Aboveground–Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change 312 (OUP Oxford, 2010).

Hartley, S. E. & Jones, T. H. in Insects And Ecosystem Function Vol. 173 (eds Weisser, W.W. & Siemann, E.) 27–52 (Springer–Verlag, Heidelberg, 2008).

Metcalfe DB, et al. Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol. Lett. 2014;17:324–332. doi: 10.1111/ele.12233. PubMed DOI

Chapin FS. The mineral nutrition of wild plants. Annu. Rev. Ecol. Evol. Syst. 1980;11:233–260. doi: 10.1146/annurev.es.11.110180.001313. DOI

Johnson DW, Turner J. Tamm review: nutrient cycling in forests: a historical look and newer developments. Ecol. Manag. 2019;444:344–373. doi: 10.1016/j.foreco.2019.04.052. DOI

Street‐Perrott F, Barker P. Biogenic silica: a neglected component of the coupled global continental biogeochemical cycles of carbon and silicon. Earth Surf. Process. Landf. 2008;33:1436–1457. doi: 10.1002/esp.1712. DOI

Cooke J, Leishman MR. Is plant ecology more siliceous than we realise? Trends Plant Sci. 2011;16:61–68. doi: 10.1016/j.tplants.2010.10.003. PubMed DOI

Hwang BC, Metcalfe DB. Reviews and syntheses: impacts of plant-silica–herbivore interactions on terrestrial biogeochemical cycling. Biogeosciences. 2021;18:1259–1268. doi: 10.5194/bg-18-1259-2021. DOI

Kozlov MV, Lanta V, Zverev V, Zvereva EL. Global patterns in background losses of woody plant foliage to insects. Glob. Ecol. Biogeogr. 2015;24:1126–1135. doi: 10.1111/geb.12347. DOI

Schmitt CB, et al. Global analysis of the protection status of the world’s forests. Biol. Conserv. 2009;142:2122–2130. doi: 10.1016/j.biocon.2009.04.012. DOI

Fagan WF, et al. Nitrogen in insects: implications for trophic complexity and species diversification. Am. Nat. 2002;160:784–802. doi: 10.1086/343879. PubMed DOI

Connahs H, Aiello A, Van Bael S, Rodríguez–Castañeda G. Caterpillar abundance and parasitism in a seasonally dry versus wet tropical forest of Panama. J. Trop. Ecol. 2011;27:51–58. doi: 10.1017/S0266467410000568. DOI

Lemoine NP, Burkepile DE, Parker JD. Variable effects of temperature on insect herbivory. PeerJ. 2012;2:e376. doi: 10.7717/peerj.376. PubMed DOI PMC

Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO. Changing sources of nutrients during four million years of ecosystem development. Nature. 1999;397:491–497. doi: 10.1038/17276. DOI

Du E, et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 2020;13:221–226. doi: 10.1038/s41561-019-0530-4. DOI

Reyer C. Forest productivity under environmental change—a review of stand–scale modeling studies. Curr. Rep. 2015;1:53–68. doi: 10.1007/s40725-015-0009-5. DOI

Seidl R, et al. Forest disturbances under climate change. Nat. Clim. Chang. 2017;7:395–402. doi: 10.1038/nclimate3303. PubMed DOI PMC

Kristensen JA, Michelsen A, Metcalfe DB. Background insect herbivory increases with local elevation but makes minor contribution to element cycling along natural gradients in the Subarctic. Ecol. Evol. 2020;10:11684–11698. doi: 10.1002/ece3.6803. PubMed DOI PMC

Lovett GM, et al. Insect defoliation and nitrogen cycling in forests: laboratory, plot, and watershed studies indicate that most of the nitrogen released from forest foliage as a result of defoliation by insects is redistributed within the ecosystem, whereas only a small fraction of nitrogen is lost by leaching. Biosci. 2002;52:335–341. doi: 10.1641/0006-3568(2002)052[0335:IDANCI]2.0.CO;2. DOI

Boulanger Y, et al. Dendrochronological reconstruction of spruce budworm (Choristoneura fumiferana) outbreaks in southern quebec for the last 400 years. Can. J. Res. 2012;42:1264–1276. doi: 10.1139/x2012-069. DOI

Sackett TE, Smith SM, Basiliko N. Indirect and direct effects of exotic earthworms on soil nutrient and carbon pools in north American temperate forests. Soil Biol. Biochem. 2013;57:459–467. doi: 10.1016/j.soilbio.2012.08.015. DOI

Jonsson M, Wardle DA. Context dependency of litter‐mixing effects on decomposition and nutrient release across a long‐term chronosequence. Oikos. 2008;117:1674–1682. doi: 10.1111/j.1600-0706.2008.16810.x. DOI

Metcalfe DB, Crutsinger GM, Kumordzi BB, Wardle DA. Nutrient fluxes from insect herbivory increase during ecosystem retrogression in boreal forest. Ecology. 2016;97:124–132. doi: 10.1890/15-0302.1. PubMed DOI

Garcia LC, Eubanks MD. Overcompensation for insect herbivory: a review and meta‐analysis of the evidence. Ecology. 2019;100:e02585. doi: 10.1002/ecy.2585. PubMed DOI

Visakorpi K, et al. Small–scale indirect plant responses to insect herbivory could have major impacts on canopy photosynthesis and isoprene emission. N. Phytol. 2019;220:799–810. doi: 10.1111/nph.15338. PubMed DOI

Harvey JA, Heinen R, Gols R, Thakur MP. Climate change‐mediated temperature extremes and insects: from outbreaks to breakdowns. Clim. Chang. Biol. 2020;26:6685–6701. doi: 10.1111/gcb.15377. PubMed DOI PMC

Weissflog A, Markesteijn L, Lewis OT, Comita LS, Engelbrecht BM. Contrasting patterns of insect herbivory and predation pressure across a tropical rainfall gradient. Biotrop. 2018;50:302–311. doi: 10.1111/btp.12513. DOI

Matthews B, et al. Transpiration deficits increase host susceptibility to bark beetle attack: experimental observations and practical outcomes for Ips typographus hazard assessment. Agric. Meteorol. 2018;263:69–89. doi: 10.1016/j.agrformet.2018.08.004. DOI

Mezei P, Potterf M, Škvarenina J, Rasmussen JG, Jakuš R. Potential solar radiation as a driver for bark beetle infestation on a landscape scale. Forests. 2019;10:604. doi: 10.3390/f10070604. DOI

Loughnan D, Williams JL. Climate and leaf traits, not latitude, explain variation in plant–herbivore interactions across a species’ range. J. Ecol. 2019;107:913–922. doi: 10.1111/1365-2745.13065. DOI

Pincebourde S, Woods HA. There is plenty of room at the bottom: microclimates drive insect vulnerability to climate change. Curr. Opin. Insect Sci. 2020;41:63–70. doi: 10.1016/j.cois.2020.07.001. PubMed DOI

Fürstenberg-Hägg J, Zagrobelny M, Bak S. Plant defense against insect herbivores. Int. J. Mol. Sci. 2013;14:10242–10297. doi: 10.3390/ijms140510242. PubMed DOI PMC

Souri Z, Khanna K, Karimi N, Ahmad P. Silicon and plants: current knowledge and future prospects. J. Plant Growth Regul. 2021;40:906–925. doi: 10.1007/s00344-020-10172-7. DOI

Clissold FJ, Sanson GD, Read J, Simpson SJ. Gross vs. net income: how plant toughness affects performance of an insect herbivore. Ecology. 2009;90:3393–3405. doi: 10.1890/09-0130.1. PubMed DOI

Hou E, et al. Global meta–analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nat. Commun. 2020;11:1–9. doi: 10.1038/s41467-020-14492-w. PubMed DOI PMC

Huang X, et al. Global distributions of foliar nitrogen and phosphorus resorption in forest ecosystems. Sci. Total Environ. 2023;871:162075. doi: 10.1016/j.scitotenv.2023.162075. PubMed DOI

Ostle NJ, et al. Integrating plant–soil interactions into global carbon cycle models. J. Ecol. 2009;97:851–863. doi: 10.1111/j.1365-2745.2009.01547.x. DOI

Kyker‐Snowman E, et al. Increasing the spatial and temporal impact of ecological research: a roadmap for integrating a novel terrestrial process into an earth system model. Glob. Chang. Biol. 2022;28:665–684. doi: 10.1111/gcb.15894. PubMed DOI PMC

Loidi J, Navarro-Sánchez G, Vynokurov D. A vector map of the world’s terrestrial biotic units: subbiomes, biomes, ecozones and domains. Veg. Classif. Surv. 2023;4:59–61.

Vola, J., Rautio, P. & Rantala, O. in Researching With Proximity: Relational Methodologies For The Anthropocene (eds. Rantala, O., Kinnunen, V., Höckert, E.) 147–164 (Springer Nature, Cham, 2023).

Breuning–Madsen H, Ehlers CB, Borggaard OK. The impact of perennial cormorant colonies on soil phosphorus status. Geoderma. 2008;148:51–54. doi: 10.1016/j.geoderma.2008.09.002. DOI

Zahajská, P. Diatom–Rich Sediment Formation In Lakes, 132 (Lund University, 2021).

Alliende MC. Demographic studies of a dioecious tree. II. The distribution of leaf predation within and between trees. J. Ecol. 1989;77:1048–1058. doi: 10.2307/2260822. DOI

Johnson MT, Bertrand JA, Turcotte MM. Precision and accuracy in quantifying herbivory. Ecol. Entomol. 2016;41:112–121. doi: 10.1111/een.12280. DOI

Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol. Monogr. 2012;82:205–220. doi: 10.1890/11-0416.1. DOI

Wiegert RG, Petersen CE. Energy transfer in insects. Ann. Rev. Entomol. 1983;28:455–486. doi: 10.1146/annurev.en.28.010183.002323. DOI

Brahney J, Mahowald N, Ward DS, Ballantyne AP, Neff JC. Is atmospheric phosphorus pollution altering global alpine Lake stoichiometry? global biogeochem. Cycles. 2015;29:1369–1383. doi: 10.1002/2015GB005137. DOI

Hartmann J, Moosdorf N, Lauerwald R, Hinderer M, West AJ. Global chemical weathering and associated P–release—the role of lithology, temperature and soil properties. Chem. Geol. 2014;363:145–163. doi: 10.1016/j.chemgeo.2013.10.025. DOI

Zhang L, Dawes WR, Walker GR. Response of mean annual evapotranspiration to vegetation changes at catchment scale. Water Resour. Res. 2001;37:701–708. doi: 10.1029/2000WR900325. DOI

Singer MB, et al. Hourly potential evapotranspiration at 0.1 resolution for the global land surface from 1981-present. Sci. Data. 2021;8:224. doi: 10.1038/s41597-021-01003-9. PubMed DOI PMC

R Core Team. R: A Language And Environment For Statistical Computing. https://www.r-project.org/ (2023).

Fox, J. & Weisberg, S. An R Companion To Applied Regression 3rd edn, 308 (SAGE Publications, 2019).

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed–effects models using ime4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

Schielzeth H, et al. Robustness of linear mixed-effects models to violations of distributional assumptions. Methods Ecol. Evol. 2020;11:1141–1152. doi: 10.1111/2041-210X.13434. DOI

Luke SG. Evaluating significance in linear mixed–effects models in R. Behav. Res. Methods. 2017;49:1494–1502. doi: 10.3758/s13428-016-0809-y. PubMed DOI

Barton, K. & Barton, M. K. Package ‘Mumin’. Version 1.47.5https://cran.r-project.org/web/packages/MuMIn/index.html (2023).

Hwang, B. et al. Datasets and R code for Hwang, B. et al. The impact of insect herbivory on biogeochemical cycling in broadleaved forests varies with temperature. Figshare10.6084/m9.figshare.25725594 (2024). PubMed PMC

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The impact of insect herbivory on biogeochemical cycling in broadleaved forests varies with temperature

. 2024 Jul 17 ; 15 (1) : 6011. [epub] 20240717

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