Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands

Anne Ebeling; Alex T. Strauss; Peter B. Adler; Carlos A. Arnillas; Isabel C Barrio; Lori A. Biederman; Elizabeth T. Borer; Miguel N. Bugalho; Maria C Caldeira; Marc W. Cadotte; Pedro Daleo; Nico Eisenhauer; Anu Eskelinen; Philip A. Fay; Jennifer Firn; Pamela Graff; Nicole Hagenah; Sylvia Haider; Kimberly J. Komatsu; Rebecca L McCulley; Charles E. Mitchell; Joslin L. Moore; Jesus Pascual; Pablo L. Peri; Sally A. Power; Suzanne M. Prober; Anita C Risch; Christiane Roscher; Mahesh Sankaran; Eric W Seabloom; Holger Schielzeth; Martin Schütz; Karina L. Speziale; Michelle Tedder; Risto Virtanen; Dana M. Blumenthal

doi:10.1111/1365-2745.13801

Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands

Anne Ebeling, Alex T. Strauss, Peter B. Adler, Carlos A. Arnillas, Isabel C Barrio, Lori A. Biederman, Elizabeth T. Borer, Miguel N. Bugalho, Maria C Caldeira, Marc W. Cadotte, Pedro Daleo, Nico Eisenhauer, Anu Eskelinen, Philip A. Fay, Jennifer Firn, Pamela Graff, Nicole Hagenah, Sylvia Haider, Kimberly J. Komatsu, Rebecca L McCulleyCharles E. Mitchell, Joslin L. Moore, Jesus Pascual, Pablo L. Peri, Sally A. Power, Suzanne M. Prober, Anita C Risch, Christiane Roscher, Mahesh Sankaran, Eric W Seabloom, Holger Schielzeth, Martin Schütz, Karina L. Speziale, Michelle Tedder, Risto Virtanen, Dana M. Blumenthal

Plant and Soil Sciences

Research output: Contribution to journal › Article › peer-review

34 Scopus citations

Abstract

Plant damage by invertebrate herbivores and pathogens influences the dynamics of grassland ecosystems, but anthropogenic changes in nitrogen and phosphorus availability can modify these relationships. Using a globally distributed experiment, we describe leaf damage on 153 plant taxa from 27 grasslands worldwide, under ambient conditions and with experimentally elevated nitrogen and phosphorus. Invertebrate damage significantly increased with nitrogen addition, especially in grasses and non-leguminous forbs. Pathogen damage increased with nitrogen in grasses and legumes but not forbs. Effects of phosphorus were generally weaker. Damage was higher in grasslands with more precipitation, but climatic conditions did not change effects of nutrients on leaf damage. On average, invertebrate damage was relatively higher on legumes and pathogen damage was relatively higher on grasses. Community-weighted mean damage reflected these functional group patterns, with no effects of N on community-weighted pathogen damage (due to opposing responses of grasses and forbs) but stronger effects of N on community-weighted invertebrate damage (due to consistent responses of grasses and forbs). Synthesis. As human-induced inputs of nitrogen and phosphorus continue to increase, understanding their impacts on invertebrate and pathogen damage becomes increasingly important. Our results demonstrate that eutrophication frequently increases plant damage and that damage increases with precipitation across a wide array of grasslands. Invertebrate and pathogen damage in grasslands is likely to increase in the future, with potential consequences for plant, invertebrate and pathogen communities, as well as the transfer of energy and nutrients across trophic levels.

Original language	English
Pages (from-to)	327-339
Number of pages	13
Journal	Journal of Ecology
Volume	110
Issue number	2
DOIs	https://doi.org/10.1111/1365-2745.13801
State	Published - Feb 2022

Bibliographical note

Publisher Copyright:
© 2021 The Authors. Journal of Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society

Funding

This work was conducted using data from the NutNet collaborative experiment, funded at the site scale by individual researchers. Coordination and data management have been supported by funding to E.B. and E.S. from the National Science Foundation Research Coordination Network (NSF-DEB-1042132) and Long Term Ecological Research (NSF-DEB-1234162 to Cedar Creek LTER) programmes, and the Institute on the Environment (DG-0001-13). We thank Eric Lind and Ashley Asmus for support in data management and preparation. We further thank Dan LeCain for organizing and shipping equipment, required for the add-on study, and Julie Kray for creating Figure 1. At the Mt Caroline site, we thank Georg Wiehl for assistance with data collection, Denise and Malcolm French, and the Terrestrial Ecosystems Research Network (TERN) Great Western Woodlands Supersite for support. Furthermore, we thank Rui Alves for the logistic support on the establishment of the Companhia das Lezírias site. For the Indian site, we thank Yadugiri V. T. for assistance with data collection. This manuscript is an outcome of a workshop kindly supported by sDiv, the Synthesis Centre of the German Centre for Integrative Biodiversity Research Halle-Jena-Leipzig (DFG FZT 118). This work was conducted using data from the NutNet collaborative experiment, funded at the site scale by individual researchers. Coordination and data management have been supported by funding to E.B. and E.S. from the National Science Foundation Research Coordination Network (NSF‐DEB‐1042132) and Long Term Ecological Research (NSF‐DEB‐1234162 to Cedar Creek LTER) programmes, and the Institute on the Environment (DG‐0001‐13). We thank Eric Lind and Ashley Asmus for support in data management and preparation. We further thank Dan LeCain for organizing and shipping equipment, required for the add‐on study, and Julie Kray for creating Figure 1 . At the Mt Caroline site, we thank Georg Wiehl for assistance with data collection, Denise and Malcolm French, and the Terrestrial Ecosystems Research Network (TERN) Great Western Woodlands Supersite for support. Furthermore, we thank Rui Alves for the logistic support on the establishment of the Companhia das Lezírias site. For the Indian site, we thank Yadugiri V. T. for assistance with data collection. This manuscript is an outcome of a workshop kindly supported by sDiv, the Synthesis Centre of the German Centre for Integrative Biodiversity Research Halle‐Jena‐Leipzig (DFG FZT 118).

Funders	Funder number
TERN Great Western Woodlands Supersite
Hawkesbury Institute for the Environment	DG‐0001‐13
Long-Term Ecological Research	NSF‐DEB‐1234162
Synthesis Centre of the German Centre for Integrative Biodiversity Research Halle-Jena-Leipzig
Synthesis Centre of the German Centre for Integrative Biodiversity Research Halle-Jena-Leipzig	DFG FZT 118
Terrestrial Ecosystems Research Network
National Science Foundation Arctic Social Science Program	NSF‐DEB‐1042132
National Science Foundation Arctic Social Science Program
Deutsche Forschungsgemeinschaft	FZT 118
Deutsche Forschungsgemeinschaft

Keywords

fungi
grasslands
insects
nitrogen
nutrient network
phosphorus
precipitation gradient
temperature gradient

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Ecology
Plant Science

Access to Document

10.1111/1365-2745.13801

Cite this

Ebeling, A., Strauss, A. T., Adler, P. B., Arnillas, C. A., Barrio, IC., Biederman, L. A., Borer, E. T., Bugalho, M. N., Caldeira, MC., Cadotte, M. W., Daleo, P., Eisenhauer, N., Eskelinen, A., Fay, P. A., Firn, J., Graff, P., Hagenah, N., Haider, S., Komatsu, K. J., ... Blumenthal, D. M. (2022). Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands. Journal of Ecology, 110(2), 327-339. https://doi.org/10.1111/1365-2745.13801

@article{aa46d4991a76489d96b4724a6a54ac2f,

title = "Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands",

abstract = "Plant damage by invertebrate herbivores and pathogens influences the dynamics of grassland ecosystems, but anthropogenic changes in nitrogen and phosphorus availability can modify these relationships. Using a globally distributed experiment, we describe leaf damage on 153 plant taxa from 27 grasslands worldwide, under ambient conditions and with experimentally elevated nitrogen and phosphorus. Invertebrate damage significantly increased with nitrogen addition, especially in grasses and non-leguminous forbs. Pathogen damage increased with nitrogen in grasses and legumes but not forbs. Effects of phosphorus were generally weaker. Damage was higher in grasslands with more precipitation, but climatic conditions did not change effects of nutrients on leaf damage. On average, invertebrate damage was relatively higher on legumes and pathogen damage was relatively higher on grasses. Community-weighted mean damage reflected these functional group patterns, with no effects of N on community-weighted pathogen damage (due to opposing responses of grasses and forbs) but stronger effects of N on community-weighted invertebrate damage (due to consistent responses of grasses and forbs). Synthesis. As human-induced inputs of nitrogen and phosphorus continue to increase, understanding their impacts on invertebrate and pathogen damage becomes increasingly important. Our results demonstrate that eutrophication frequently increases plant damage and that damage increases with precipitation across a wide array of grasslands. Invertebrate and pathogen damage in grasslands is likely to increase in the future, with potential consequences for plant, invertebrate and pathogen communities, as well as the transfer of energy and nutrients across trophic levels.",

keywords = "fungi, grasslands, insects, nitrogen, nutrient network, phosphorus, precipitation gradient, temperature gradient",

author = "Anne Ebeling and Strauss, {Alex T.} and Adler, {Peter B.} and Arnillas, {Carlos A.} and Isabel C Barrio and Biederman, {Lori A.} and Borer, {Elizabeth T.} and Bugalho, {Miguel N.} and Maria C Caldeira and Cadotte, {Marc W.} and Pedro Daleo and Nico Eisenhauer and Anu Eskelinen and Fay, {Philip A.} and Jennifer Firn and Pamela Graff and Nicole Hagenah and Sylvia Haider and Komatsu, {Kimberly J.} and Rebecca L McCulley and Mitchell, {Charles E.} and Moore, {Joslin L.} and Jesus Pascual and Peri, {Pablo L.} and Power, {Sally A.} and Prober, {Suzanne M.} and Anita C Risch and Christiane Roscher and Mahesh Sankaran and Eric W Seabloom and Holger Schielzeth and Martin Sch{\"u}tz and Speziale, {Karina L.} and Michelle Tedder and Risto Virtanen and Blumenthal, {Dana M.}",

note = "Publisher Copyright: {\textcopyright} 2021 The Authors. Journal of Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society",

year = "2022",

month = feb,

doi = "10.1111/1365-2745.13801",

language = "English",

volume = "110",

pages = "327--339",

number = "2",

}

Ebeling, A, Strauss, AT, Adler, PB, Arnillas, CA, Barrio, IC, Biederman, LA, Borer, ET, Bugalho, MN, Caldeira, MC, Cadotte, MW, Daleo, P, Eisenhauer, N, Eskelinen, A, Fay, PA, Firn, J, Graff, P, Hagenah, N, Haider, S, Komatsu, KJ, McCulley, RL, Mitchell, CE, Moore, JL, Pascual, J, Peri, PL, Power, SA, Prober, SM, Risch, AC, Roscher, C, Sankaran, M, Seabloom, EW, Schielzeth, H, Schütz, M, Speziale, KL, Tedder, M, Virtanen, R & Blumenthal, DM 2022, 'Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands', Journal of Ecology, vol. 110, no. 2, pp. 327-339. https://doi.org/10.1111/1365-2745.13801

TY - JOUR

T1 - Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands

AU - Ebeling, Anne

AU - Strauss, Alex T.

AU - Adler, Peter B.

AU - Arnillas, Carlos A.

AU - Barrio, Isabel C

AU - Biederman, Lori A.

AU - Borer, Elizabeth T.

AU - Bugalho, Miguel N.

AU - Caldeira, Maria C

AU - Cadotte, Marc W.

AU - Daleo, Pedro

AU - Eisenhauer, Nico

AU - Eskelinen, Anu

AU - Fay, Philip A.

AU - Firn, Jennifer

AU - Graff, Pamela

AU - Hagenah, Nicole

AU - Haider, Sylvia

AU - Komatsu, Kimberly J.

AU - McCulley, Rebecca L

AU - Mitchell, Charles E.

AU - Moore, Joslin L.

AU - Pascual, Jesus

AU - Peri, Pablo L.

AU - Power, Sally A.

AU - Prober, Suzanne M.

AU - Risch, Anita C

AU - Roscher, Christiane

AU - Sankaran, Mahesh

AU - Seabloom, Eric W

AU - Schielzeth, Holger

AU - Schütz, Martin

AU - Speziale, Karina L.

AU - Tedder, Michelle

AU - Virtanen, Risto

AU - Blumenthal, Dana M.

PY - 2022/2

Y1 - 2022/2

N2 - Plant damage by invertebrate herbivores and pathogens influences the dynamics of grassland ecosystems, but anthropogenic changes in nitrogen and phosphorus availability can modify these relationships. Using a globally distributed experiment, we describe leaf damage on 153 plant taxa from 27 grasslands worldwide, under ambient conditions and with experimentally elevated nitrogen and phosphorus. Invertebrate damage significantly increased with nitrogen addition, especially in grasses and non-leguminous forbs. Pathogen damage increased with nitrogen in grasses and legumes but not forbs. Effects of phosphorus were generally weaker. Damage was higher in grasslands with more precipitation, but climatic conditions did not change effects of nutrients on leaf damage. On average, invertebrate damage was relatively higher on legumes and pathogen damage was relatively higher on grasses. Community-weighted mean damage reflected these functional group patterns, with no effects of N on community-weighted pathogen damage (due to opposing responses of grasses and forbs) but stronger effects of N on community-weighted invertebrate damage (due to consistent responses of grasses and forbs). Synthesis. As human-induced inputs of nitrogen and phosphorus continue to increase, understanding their impacts on invertebrate and pathogen damage becomes increasingly important. Our results demonstrate that eutrophication frequently increases plant damage and that damage increases with precipitation across a wide array of grasslands. Invertebrate and pathogen damage in grasslands is likely to increase in the future, with potential consequences for plant, invertebrate and pathogen communities, as well as the transfer of energy and nutrients across trophic levels.

AB - Plant damage by invertebrate herbivores and pathogens influences the dynamics of grassland ecosystems, but anthropogenic changes in nitrogen and phosphorus availability can modify these relationships. Using a globally distributed experiment, we describe leaf damage on 153 plant taxa from 27 grasslands worldwide, under ambient conditions and with experimentally elevated nitrogen and phosphorus. Invertebrate damage significantly increased with nitrogen addition, especially in grasses and non-leguminous forbs. Pathogen damage increased with nitrogen in grasses and legumes but not forbs. Effects of phosphorus were generally weaker. Damage was higher in grasslands with more precipitation, but climatic conditions did not change effects of nutrients on leaf damage. On average, invertebrate damage was relatively higher on legumes and pathogen damage was relatively higher on grasses. Community-weighted mean damage reflected these functional group patterns, with no effects of N on community-weighted pathogen damage (due to opposing responses of grasses and forbs) but stronger effects of N on community-weighted invertebrate damage (due to consistent responses of grasses and forbs). Synthesis. As human-induced inputs of nitrogen and phosphorus continue to increase, understanding their impacts on invertebrate and pathogen damage becomes increasingly important. Our results demonstrate that eutrophication frequently increases plant damage and that damage increases with precipitation across a wide array of grasslands. Invertebrate and pathogen damage in grasslands is likely to increase in the future, with potential consequences for plant, invertebrate and pathogen communities, as well as the transfer of energy and nutrients across trophic levels.

KW - fungi

KW - grasslands

KW - insects

KW - nitrogen

KW - nutrient network

KW - phosphorus

KW - precipitation gradient

KW - temperature gradient

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U2 - 10.1111/1365-2745.13801

DO - 10.1111/1365-2745.13801

M3 - Article

AN - SCOPUS:85118257832

SN - 0022-0477

VL - 110

SP - 327

EP - 339

JO - Journal of Ecology

JF - Journal of Ecology

IS - 2

ER -

Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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