Circum‐Arctic distribution of chemical anti‐herbivore compounds suggests biome‐wide trade‐off in defence strategies in Arctic shrubs

Elin Lindén; Mariska Te Beest; Ilka Aubreu; Thomas Moritz; Maja K. Sundqvist; Isabel C. Barrio; Julia Boike; John P. Bryant; Kari Anne Bråthen; Agata Buchwal; C. Guillermo Bueno; Alain Currier; Dagmar D. Egelkraut; Bruce C. Forbes; Martin Hallinger; Monique Heijmans; Luise Hermanutz; David S. Hik; Annika Hofgaard; Milena Holmgren; Diane C. Huebner; Toke T. Høye; Ingibjörg S. Jónsdóttir; Elina Kaarlejärvi; Emilie Kissler; Timo Kumpula; Juul Limpens; Isla H. Myers‐smith; Signe Normand; Eric Post; Adrian V. Rocha; Niels Martin Schmidt; Anna Skarin; Eeva M. Soininen; Aleksandr Sokolov; Natalia Sokolova; James D. M. Speed; Lorna Street; Nikita Tananaev; Jean‐pierre Tremblay; Christine Urbanowicz; David A. Watts; Heike Zimmermann; Johan Olofsson

doi:10.1111/ecog.06166

Circum‐Arctic distribution of chemical anti‐herbivore compounds suggests biome‐wide trade‐off in defence strategies in Arctic shrubs

Elin Lindén, Mariska Te Beest, Ilka Aubreu, Thomas Moritz, Maja K. Sundqvist, Isabel C. Barrio, Julia Boike, John P. Bryant, Kari Anne Bråthen, Agata Buchwal, C. Guillermo Bueno, Alain Currier, Dagmar D. Egelkraut, Bruce C. Forbes, Martin Hallinger, Monique Heijmans, Luise Hermanutz, David S. Hik, Annika Hofgaard, Milena HolmgrenDiane C. Huebner, Toke T. Høye, Ingibjörg S. Jónsdóttir, Elina Kaarlejärvi, Emilie Kissler, Timo Kumpula, Juul Limpens, Isla H. Myers‐smith, Signe Normand, Eric Post, Adrian V. Rocha, Niels Martin Schmidt, Anna Skarin, Eeva M. Soininen, Aleksandr Sokolov, Natalia Sokolova, James D. M. Speed, Lorna Street, Nikita Tananaev, Jean‐pierre Tremblay, Christine Urbanowicz, David A. Watts, Heike Zimmermann, Johan Olofsson

School of Geosciences

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

Abstract / Description of output

Spatial variation in plant chemical defence towards herbivores can help us understand variation in herbivore top–down control of shrubs in the Arctic and possibly also shrub responses to global warming. Less defended, non-resinous shrubs could be more influenced by herbivores than more defended, resinous shrubs. However, sparse field measurements limit our current understanding of how much of the circum-Arctic variation in defence compounds is explained by taxa or defence functional groups (resinous/non-resinous). We measured circum-Arctic chemical defence and leaf digestibility in resinous (Betula glandulosa, B. nana ssp. exilis) and non-resinous (B. nana ssp. nana, B. pumila) shrub birches to see how they vary among and within taxa and functional groups. Using liquid chromatography–mass spectrometry (LC–MS) metabolomic analyses and in vitro leaf digestibility via incubation in cattle rumen fluid, we analysed defence composition and leaf digestibility in 128 samples from 44 tundra locations.

We found biogeographical patterns in anti-herbivore defence where mean leaf triterpene concentrations and twig resin gland density were greater in resinous taxa and mean concentrations of condensing tannins were greater in non-resinous taxa. This indicates a biome-wide trade-off between triterpene- or tannin-dominated defences. However, we also found variations in chemical defence composition and resin gland density both within and among functional groups (resinous/non-resinous) and taxa, suggesting these categorisations only partly predict chemical herbivore defence. Complex tannins were the only defence compounds negatively related to in vitro digestibility, identifying this previously neglected tannin group as having a potential key role in birch anti-herbivore defence.

We conclude that circum-Arctic variation in birch anti-herbivore defence can be partly derived from biogeographical distributions of birch taxa, although our detailed mapping of plant defence provides more information on this variation and can be used for better predictions of herbivore effects on Arctic vegetation.

Original language	English
Article number	e06166
Journal	Ecography
Volume	2022
Issue number	11
Early online date	30 Aug 2022
DOIs	https://doi.org/10.1111/ecog.06166
Publication status	Published - Nov 2022

Keywords / Materials (for Non-textual outputs)

Arctic
Betula
birch
herbivory
metabolomics
plant chemical defence
shrubs
tundra

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10.1111/ecog.06166Licence: CC BY

Linden et al. Ecography.
© 2022 The Authors. Ecography published by John Wiley & Sons Ltd on behalf of Nordic Society Oikos
Final published version, 1.34 MBLicence: Creative Commons: Attribution (CC-BY)

https://onlinelibrary.wiley.com/doi/10.1111/ecog.06166Licence: Creative Commons: Attribution (CC-BY)

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Lindén, E., Te Beest, M., Aubreu, I., Moritz, T., Sundqvist, M. K., Barrio, I. C., Boike, J., Bryant, J. P., Bråthen, K. A., Buchwal, A., Bueno, C. G., Currier, A., Egelkraut, D. D., Forbes, B. C., Hallinger, M., Heijmans, M., Hermanutz, L., Hik, D. S., Hofgaard, A., ... Olofsson, J. (2022). Circum‐Arctic distribution of chemical anti‐herbivore compounds suggests biome‐wide trade‐off in defence strategies in Arctic shrubs. Ecography, 2022(11), Article e06166. https://doi.org/10.1111/ecog.06166

@article{0b624cb50f9f40d183527fa2e3858fe8,

title = "Circum‐Arctic distribution of chemical anti‐herbivore compounds suggests biome‐wide trade‐off in defence strategies in Arctic shrubs",

abstract = "Spatial variation in plant chemical defence towards herbivores can help us understand variation in herbivore top–down control of shrubs in the Arctic and possibly also shrub responses to global warming. Less defended, non-resinous shrubs could be more influenced by herbivores than more defended, resinous shrubs. However, sparse field measurements limit our current understanding of how much of the circum-Arctic variation in defence compounds is explained by taxa or defence functional groups (resinous/non-resinous). We measured circum-Arctic chemical defence and leaf digestibility in resinous (Betula glandulosa, B. nana ssp. exilis) and non-resinous (B. nana ssp. nana, B. pumila) shrub birches to see how they vary among and within taxa and functional groups. Using liquid chromatography–mass spectrometry (LC–MS) metabolomic analyses and in vitro leaf digestibility via incubation in cattle rumen fluid, we analysed defence composition and leaf digestibility in 128 samples from 44 tundra locations.We found biogeographical patterns in anti-herbivore defence where mean leaf triterpene concentrations and twig resin gland density were greater in resinous taxa and mean concentrations of condensing tannins were greater in non-resinous taxa. This indicates a biome-wide trade-off between triterpene- or tannin-dominated defences. However, we also found variations in chemical defence composition and resin gland density both within and among functional groups (resinous/non-resinous) and taxa, suggesting these categorisations only partly predict chemical herbivore defence. Complex tannins were the only defence compounds negatively related to in vitro digestibility, identifying this previously neglected tannin group as having a potential key role in birch anti-herbivore defence.We conclude that circum-Arctic variation in birch anti-herbivore defence can be partly derived from biogeographical distributions of birch taxa, although our detailed mapping of plant defence provides more information on this variation and can be used for better predictions of herbivore effects on Arctic vegetation.",

keywords = "Arctic, Betula, birch, herbivory, metabolomics, plant chemical defence, shrubs, tundra",

author = "Elin Lind{\'e}n and {Te Beest}, Mariska and Ilka Aubreu and Thomas Moritz and Sundqvist, {Maja K.} and Barrio, {Isabel C.} and Julia Boike and Bryant, {John P.} and Br{\aa}then, {Kari Anne} and Agata Buchwal and Bueno, {C. Guillermo} and Alain Currier and Egelkraut, {Dagmar D.} and Forbes, {Bruce C.} and Martin Hallinger and Monique Heijmans and Luise Hermanutz and Hik, {David S.} and Annika Hofgaard and Milena Holmgren and Huebner, {Diane C.} and H{\o}ye, {Toke T.} and J{\'o}nsd{\'o}ttir, {Ingibj{\"o}rg S.} and Elina Kaarlej{\"a}rvi and Emilie Kissler and Timo Kumpula and Juul Limpens and Myers‐smith, {Isla H.} and Signe Normand and Eric Post and Rocha, {Adrian V.} and Schmidt, {Niels Martin} and Anna Skarin and Soininen, {Eeva M.} and Aleksandr Sokolov and Natalia Sokolova and Speed, {James D. M.} and Lorna Street and Nikita Tananaev and Jean‐pierre Tremblay and Christine Urbanowicz and Watts, {David A.} and Heike Zimmermann and Johan Olofsson",

note = "Funding Information: – We thank those who helped us reach out with our call for samples and of course all sample contributors without whom this study would not have been possible. We also thank the Swedish Metabolomics Centre for a great collaboration and all support for the metabolomic part of this study. Thanks also to the the local and indigenous people for the opportunity to conduct research on their land. – This study was mainly supported by FORMAS (grant no. 2015-01091) and the Swedish Research Council (grant no. 2017-04515) to JO, the Knut and Alice Wallenberg Foundation (grant no. KAW2014.0279) to TM and the Swedish Metabolomics Centre. Additional individual supporting grants: US National Science Foundation (grant no. 1556772) to AVR, Estonian Ministry of Education and Research (grant no. PRG1065) and the EU (Centre of Excellence: EcolChange) to CGB, Finnish Cultural Foundation to EK, Research Council of Norway (grant no. 262064) to JDMS, US National Science Foundation (grant no. 1107381) to EP, Nunatsiavut Government and Parks Canada (NSERC-ArcticNet grant Canada) to LH, UK NERC (grant no. NE/K000284/2) to LS, Carlsberg Foundation (grant no. CF14-0992) to TTH, UK NERC (grant no. NE/M016323/1) to IHM-S. Funding Information: – This study was mainly supported by FORMAS (grant no. 2015‐01091) and the Swedish Research Council (grant no. 2017‐04515) to JO, the Knut and Alice Wallenberg Foundation (grant no. KAW2014.0279) to TM and the Swedish Metabolomics Centre. Additional individual supporting grants: US National Science Foundation (grant no. 1556772) to AVR, Estonian Ministry of Education and Research (grant no. PRG1065) and the EU (Centre of Excellence: EcolChange) to CGB, Finnish Cultural Foundation to EK, Research Council of Norway (grant no. 262064) to JDMS, US National Science Foundation (grant no. 1107381) to EP, Nunatsiavut Government and Parks Canada (NSERC‐ArcticNet grant Canada) to LH, UK NERC (grant no. NE/K000284/2) to LS, Carlsberg Foundation (grant no. CF14‐0992) to TTH, UK NERC (grant no. NE/M016323/1) to IHM‐S. Publisher Copyright: {\textcopyright} 2022 The Authors. Ecography published by John Wiley & Sons Ltd on behalf of Nordic Society Oikos.",

year = "2022",

month = nov,

doi = "10.1111/ecog.06166",

language = "English",

volume = "2022",

journal = "Ecography",

issn = "0906-7590",

publisher = "Wiley-Blackwell",

number = "11",

}

Lindén, E, Te Beest, M, Aubreu, I, Moritz, T, Sundqvist, MK, Barrio, IC, Boike, J, Bryant, JP, Bråthen, KA, Buchwal, A, Bueno, CG, Currier, A, Egelkraut, DD, Forbes, BC, Hallinger, M, Heijmans, M, Hermanutz, L, Hik, DS, Hofgaard, A, Holmgren, M, Huebner, DC, Høye, TT, Jónsdóttir, IS, Kaarlejärvi, E, Kissler, E, Kumpula, T, Limpens, J, Myers‐smith, IH, Normand, S, Post, E, Rocha, AV, Schmidt, NM, Skarin, A, Soininen, EM, Sokolov, A, Sokolova, N, Speed, JDM, Street, L, Tananaev, N, Tremblay, J, Urbanowicz, C, Watts, DA, Zimmermann, H & Olofsson, J 2022, 'Circum‐Arctic distribution of chemical anti‐herbivore compounds suggests biome‐wide trade‐off in defence strategies in Arctic shrubs', Ecography, vol. 2022, no. 11, e06166. https://doi.org/10.1111/ecog.06166

TY - JOUR

T1 - Circum‐Arctic distribution of chemical anti‐herbivore compounds suggests biome‐wide trade‐off in defence strategies in Arctic shrubs

AU - Lindén, Elin

AU - Te Beest, Mariska

AU - Aubreu, Ilka

AU - Moritz, Thomas

AU - Sundqvist, Maja K.

AU - Barrio, Isabel C.

AU - Boike, Julia

AU - Bryant, John P.

AU - Bråthen, Kari Anne

AU - Buchwal, Agata

AU - Bueno, C. Guillermo

AU - Currier, Alain

AU - Egelkraut, Dagmar D.

AU - Forbes, Bruce C.

AU - Hallinger, Martin

AU - Heijmans, Monique

AU - Hermanutz, Luise

AU - Hik, David S.

AU - Hofgaard, Annika

AU - Holmgren, Milena

AU - Huebner, Diane C.

AU - Høye, Toke T.

AU - Jónsdóttir, Ingibjörg S.

AU - Kaarlejärvi, Elina

AU - Kissler, Emilie

AU - Kumpula, Timo

AU - Limpens, Juul

AU - Myers‐smith, Isla H.

AU - Normand, Signe

AU - Post, Eric

AU - Rocha, Adrian V.

AU - Schmidt, Niels Martin

AU - Skarin, Anna

AU - Soininen, Eeva M.

AU - Sokolov, Aleksandr

AU - Sokolova, Natalia

AU - Speed, James D. M.

AU - Street, Lorna

AU - Tananaev, Nikita

AU - Tremblay, Jean‐pierre

AU - Urbanowicz, Christine

AU - Watts, David A.

AU - Zimmermann, Heike

AU - Olofsson, Johan

N1 - Funding Information: – We thank those who helped us reach out with our call for samples and of course all sample contributors without whom this study would not have been possible. We also thank the Swedish Metabolomics Centre for a great collaboration and all support for the metabolomic part of this study. Thanks also to the the local and indigenous people for the opportunity to conduct research on their land. – This study was mainly supported by FORMAS (grant no. 2015-01091) and the Swedish Research Council (grant no. 2017-04515) to JO, the Knut and Alice Wallenberg Foundation (grant no. KAW2014.0279) to TM and the Swedish Metabolomics Centre. Additional individual supporting grants: US National Science Foundation (grant no. 1556772) to AVR, Estonian Ministry of Education and Research (grant no. PRG1065) and the EU (Centre of Excellence: EcolChange) to CGB, Finnish Cultural Foundation to EK, Research Council of Norway (grant no. 262064) to JDMS, US National Science Foundation (grant no. 1107381) to EP, Nunatsiavut Government and Parks Canada (NSERC-ArcticNet grant Canada) to LH, UK NERC (grant no. NE/K000284/2) to LS, Carlsberg Foundation (grant no. CF14-0992) to TTH, UK NERC (grant no. NE/M016323/1) to IHM-S. Funding Information: – This study was mainly supported by FORMAS (grant no. 2015‐01091) and the Swedish Research Council (grant no. 2017‐04515) to JO, the Knut and Alice Wallenberg Foundation (grant no. KAW2014.0279) to TM and the Swedish Metabolomics Centre. Additional individual supporting grants: US National Science Foundation (grant no. 1556772) to AVR, Estonian Ministry of Education and Research (grant no. PRG1065) and the EU (Centre of Excellence: EcolChange) to CGB, Finnish Cultural Foundation to EK, Research Council of Norway (grant no. 262064) to JDMS, US National Science Foundation (grant no. 1107381) to EP, Nunatsiavut Government and Parks Canada (NSERC‐ArcticNet grant Canada) to LH, UK NERC (grant no. NE/K000284/2) to LS, Carlsberg Foundation (grant no. CF14‐0992) to TTH, UK NERC (grant no. NE/M016323/1) to IHM‐S. Publisher Copyright: © 2022 The Authors. Ecography published by John Wiley & Sons Ltd on behalf of Nordic Society Oikos.

PY - 2022/11

Y1 - 2022/11

N2 - Spatial variation in plant chemical defence towards herbivores can help us understand variation in herbivore top–down control of shrubs in the Arctic and possibly also shrub responses to global warming. Less defended, non-resinous shrubs could be more influenced by herbivores than more defended, resinous shrubs. However, sparse field measurements limit our current understanding of how much of the circum-Arctic variation in defence compounds is explained by taxa or defence functional groups (resinous/non-resinous). We measured circum-Arctic chemical defence and leaf digestibility in resinous (Betula glandulosa, B. nana ssp. exilis) and non-resinous (B. nana ssp. nana, B. pumila) shrub birches to see how they vary among and within taxa and functional groups. Using liquid chromatography–mass spectrometry (LC–MS) metabolomic analyses and in vitro leaf digestibility via incubation in cattle rumen fluid, we analysed defence composition and leaf digestibility in 128 samples from 44 tundra locations.We found biogeographical patterns in anti-herbivore defence where mean leaf triterpene concentrations and twig resin gland density were greater in resinous taxa and mean concentrations of condensing tannins were greater in non-resinous taxa. This indicates a biome-wide trade-off between triterpene- or tannin-dominated defences. However, we also found variations in chemical defence composition and resin gland density both within and among functional groups (resinous/non-resinous) and taxa, suggesting these categorisations only partly predict chemical herbivore defence. Complex tannins were the only defence compounds negatively related to in vitro digestibility, identifying this previously neglected tannin group as having a potential key role in birch anti-herbivore defence.We conclude that circum-Arctic variation in birch anti-herbivore defence can be partly derived from biogeographical distributions of birch taxa, although our detailed mapping of plant defence provides more information on this variation and can be used for better predictions of herbivore effects on Arctic vegetation.

AB - Spatial variation in plant chemical defence towards herbivores can help us understand variation in herbivore top–down control of shrubs in the Arctic and possibly also shrub responses to global warming. Less defended, non-resinous shrubs could be more influenced by herbivores than more defended, resinous shrubs. However, sparse field measurements limit our current understanding of how much of the circum-Arctic variation in defence compounds is explained by taxa or defence functional groups (resinous/non-resinous). We measured circum-Arctic chemical defence and leaf digestibility in resinous (Betula glandulosa, B. nana ssp. exilis) and non-resinous (B. nana ssp. nana, B. pumila) shrub birches to see how they vary among and within taxa and functional groups. Using liquid chromatography–mass spectrometry (LC–MS) metabolomic analyses and in vitro leaf digestibility via incubation in cattle rumen fluid, we analysed defence composition and leaf digestibility in 128 samples from 44 tundra locations.We found biogeographical patterns in anti-herbivore defence where mean leaf triterpene concentrations and twig resin gland density were greater in resinous taxa and mean concentrations of condensing tannins were greater in non-resinous taxa. This indicates a biome-wide trade-off between triterpene- or tannin-dominated defences. However, we also found variations in chemical defence composition and resin gland density both within and among functional groups (resinous/non-resinous) and taxa, suggesting these categorisations only partly predict chemical herbivore defence. Complex tannins were the only defence compounds negatively related to in vitro digestibility, identifying this previously neglected tannin group as having a potential key role in birch anti-herbivore defence.We conclude that circum-Arctic variation in birch anti-herbivore defence can be partly derived from biogeographical distributions of birch taxa, although our detailed mapping of plant defence provides more information on this variation and can be used for better predictions of herbivore effects on Arctic vegetation.

KW - Arctic

KW - Betula

KW - birch

KW - herbivory

KW - metabolomics

KW - plant chemical defence

KW - shrubs

KW - tundra

U2 - 10.1111/ecog.06166

DO - 10.1111/ecog.06166

M3 - Article

SN - 0906-7590

VL - 2022

JO - Ecography

JF - Ecography

IS - 11

M1 - e06166

ER -

Circum‐Arctic distribution of chemical anti‐herbivore compounds suggests biome‐wide trade‐off in defence strategies in Arctic shrubs

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