Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes

Lina Herbertsson; Johan Ekroos; Matthias Albrecht; Ignasi Bartomeus; Péter Batáry; Riccardo Bommarco; Paul Caplat; Tim Diekötter; Jenny M. Eikestam; Martin H. Entling; Sunniva Farbu; Nina Farwig; Juan P. Gonzalez-Varo; Annika L. Hass; Andrea Holzschuh; Sebastian Hopfenmüller; Anna Jakobsson; Birgit Jauker; Anikó Kovács-Hostyánszki; Wera Kleve; William E. Kunin; Sandra A.M. Lindström; Sarah Mullen; Erik Öckinger; Theodora Petanidou; Simon G. Potts; Eileen F. Power; Maj Rundlöf; Kathrin Seibel; Virve Sõber; Annika Söderman; Ingolf Steffan-Dewenter; Jane C. Stout; Tiit Teder; Teja Tscharntke; Henrik G. Smith

doi:10.5091/PLECEVO.2021.1884

Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes

Lina Herbertsson^*, Johan Ekroos, Matthias Albrecht, Ignasi Bartomeus, Péter Batáry, Riccardo Bommarco, Paul Caplat, Tim Diekötter, Jenny M. Eikestam, Martin H. Entling, Sunniva Farbu, Nina Farwig, Juan P. Gonzalez-Varo, Annika L. Hass, Andrea Holzschuh, Sebastian Hopfenmüller, Anna Jakobsson, Birgit Jauker, Anikó Kovács-Hostyánszki, Wera KleveWilliam E. Kunin, Sandra A.M. Lindström, Sarah Mullen, Erik Öckinger, Theodora Petanidou, Simon G. Potts, Eileen F. Power, Maj Rundlöf, Kathrin Seibel, Virve Sõber, Annika Söderman, Ingolf Steffan-Dewenter, Jane C. Stout, Tiit Teder, Teja Tscharntke, Henrik G. Smith

^*Corresponding author for this work

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

13 Citations (Scopus)

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Abstract

Background and aims – Agricultural intensification and loss of farmland heterogeneity have contributed to population declines of wild bees and other pollinators, which may have caused subsequent declines in insect-pollinated wild plants.

Material and methods – Using data from 37 studies on 22 pollinator-dependent wild plant species across Europe, we investigated whether flower visitation and seed set of insect-pollinated plants decline with an increasing proportion of arable land within 1 km.

Key results – Seed set increased with increasing flower visitation by bees, most of which were wild bees, but not with increasing flower visitation by other insects. Increasing proportion of arable land had a strongly variable effect on seed set and flower visitation by bees across studies.

Conclusion – Factors such as landscape configuration, local habitat quality, and temporally changing resource availability (e.g. due to mass-flowering crops or honey bee hives) could have modified the effect of arable land on pollination. While our results highlight that the persistence of wild bees is crucial to maintain plant diversity, we also show that pollen limitation due to declining bee populations in homogenized agricultural landscapes is not a universal driver causing parallel losses of bees and insect-pollinated plants.

Original language	English
Pages (from-to)	341-350
Number of pages	10
Journal	Plant Ecology and Evolution
Volume	154
Issue number	3
DOIs	https://doi.org/10.5091/PLECEVO.2021.1884
Publication status	Published - 23 Nov 2021

Bibliographical note

Funding Information:
We thank Carole Chateil, Volker Gaebele, Emmanuelle Porcher, and Marie Winsa for data contribution; Yann Clough and Peter Olsson for help on analyses and extraction of landscape data. The original idea was conceived as part of the project ?STEP-Status and trends of European pollinators? funded by the European Union in the 7th Framework Programme (grant 244090), which funded RB, ISD, HGS, SP, MR, LH, JME, and KS. JE and PC were funded by MULTAGRI/FORMAS. MA was funded by the EU FP5 project ?Evaluating current European agri-environment schemes to quantify and improve nature conservation efforts in agricultural landscapes? (EASY; QLRT-2001-01495) and the Swiss Federal Office for Science and Technology (01?0524-2). AJ and E? were funded by FORMAS. TTe and VS were supported by institutional research funding IUT (IUT20-33) of the Estonian Ministry of Education and Research, and TTe also received funding (grant no. 42900/1312/3166) from the Internal Grant Agency of the Faculty of Environmental Sciences, Czech University of Life Sciences Prague. IB was funded by MC-CIG BeeFun project: PCIG14-GA-2013-631653 and thanks the Do?ana NP staff members for granting access to the Park and Curro Molina for conducting the field work. JS, EFP, and SM were funded by DAFM and IRC. LH was funded by a grant from Formas to HGS and by a mobility grant from Formas (2018-01466). ALH was funded by the FarmLand project supported by the German Ministry of Research and Education (FKZ: 01LC1104A). AKH was supported by the NKFIH project (FK123813) and was a Bolyai Fellow of MTA. PB was supported by the NKFIH (KKP 133839).

Funding Information:
We thank Carole Chateil, Volker Gaebele, Emmanuelle Porcher, and Marie Winsa for data contribution; Yann Clough and Peter Olsson for help on analyses and extraction of landscape data. The original idea was conceived as part of the project ‘STEP - Status and trends of European pollinators’ funded by the European Union in the 7th Framework Programme (grant 244090), which funded RB, ISD, HGS, SP, MR, LH, JME, and KS. JE and PC were funded by MULTAGRI/FORMAS. MA was funded by the EU FP5 project ‘Evaluating current European agri-environment schemes to quantify and improve nature conservation efforts in agricultural landscapes’ (EASY; QLRT-2001-01495) and the Swiss Federal Office for Science and Technology (01·0524-2). AJ and EÖ were funded by FORMAS. TTe and VS were supported by institutional research funding IUT (IUT20-33) of the Estonian Ministry of Education and Research, and TTe also received funding (grant no. 42900/1312/3166) from the Internal Grant Agency of the Faculty of Environmental Sciences, Czech University of Life Sciences Prague. IB was funded by MC-CIG BeeFun project: PCIG14-GA-2013-631653 and thanks the Doñana NP staff members for granting access to the Park and Curro Molina for conducting the field work. JS, EFP, and SM were funded by DAFM and IRC. LH was funded by a grant from Formas to HGS and by a mobility grant from Formas (2018-01466). ALH was funded by the FarmLand project supported by the German Ministry of Research and Education (FKZ: 01LC1104A). AKH was supported by the NKFIH project (FK123813) and was a Bolyai Fellow of MTA. PB was supported by the NKFIH (KKP 133839).

Publisher Copyright:
© 2021 Lina Herbertsson, Johan Ekroos, Matthias Albrecht, Ignasi Bartomeus, Péter Batáry, Riccardo Bommarco, Paul Caplat, Tim Diekötter, Jenny M. Eikestam, Martin H. Entling, Sunniva Farbu, Nina Farwig, Juan P. Gonzalez-Varo, Annika L. Hass, Andrea Holzschuh, Sebastian Hopfenmüller, Anna Jakobsson, Birgit Jauker, Anikó Kovács-Hostyánszki, Wera Kleve, William E. Kunin, Sandra A.M. Lindström, Sarah Mullen, Erik Öckinger, Theodora Petanidou, Simon G. Potts, Eileen F. Power, Maj Rundlöf, Kathrin Seibe, Virve Sõber, Annika Söderman, Ingolf Steffan-Dewenter, Jane C. Stout, Tiit Teder, Teja Tscharntke, Henrik G. Smith.

Keywords

Habitat loss
Landscape complexity
Landscape simplification
Pollinating insects
Pollination
Semi-natural

ASJC Scopus subject areas

Plant Science

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Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes
Copyright 2021 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
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Cite this

Herbertsson, L., Ekroos, J., Albrecht, M., Bartomeus, I., Batáry, P., Bommarco, R., Caplat, P., Diekötter, T., Eikestam, J. M., Entling, M. H., Farbu, S., Farwig, N., Gonzalez-Varo, J. P., Hass, A. L., Holzschuh, A., Hopfenmüller, S., Jakobsson, A., Jauker, B., Kovács-Hostyánszki, A., ... Smith, H. G. (2021). Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes. Plant Ecology and Evolution, 154(3), 341-350. https://doi.org/10.5091/PLECEVO.2021.1884

@article{e7f6e048b9944a1f974a6a0524791064,

title = "Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes",

abstract = "Background and aims – Agricultural intensification and loss of farmland heterogeneity have contributed to population declines of wild bees and other pollinators, which may have caused subsequent declines in insect-pollinated wild plants. Material and methods – Using data from 37 studies on 22 pollinator-dependent wild plant species across Europe, we investigated whether flower visitation and seed set of insect-pollinated plants decline with an increasing proportion of arable land within 1 km. Key results – Seed set increased with increasing flower visitation by bees, most of which were wild bees, but not with increasing flower visitation by other insects. Increasing proportion of arable land had a strongly variable effect on seed set and flower visitation by bees across studies. Conclusion – Factors such as landscape configuration, local habitat quality, and temporally changing resource availability (e.g. due to mass-flowering crops or honey bee hives) could have modified the effect of arable land on pollination. While our results highlight that the persistence of wild bees is crucial to maintain plant diversity, we also show that pollen limitation due to declining bee populations in homogenized agricultural landscapes is not a universal driver causing parallel losses of bees and insect-pollinated plants.",

keywords = "Habitat loss, Landscape complexity, Landscape simplification, Pollinating insects, Pollination, Semi-natural",

author = "Lina Herbertsson and Johan Ekroos and Matthias Albrecht and Ignasi Bartomeus and P{\'e}ter Bat{\'a}ry and Riccardo Bommarco and Paul Caplat and Tim Diek{\"o}tter and Eikestam, {Jenny M.} and Entling, {Martin H.} and Sunniva Farbu and Nina Farwig and Gonzalez-Varo, {Juan P.} and Hass, {Annika L.} and Andrea Holzschuh and Sebastian Hopfenm{\"u}ller and Anna Jakobsson and Birgit Jauker and Anik{\'o} Kov{\'a}cs-Hosty{\'a}nszki and Wera Kleve and Kunin, {William E.} and Lindstr{\"o}m, {Sandra A.M.} and Sarah Mullen and Erik {\"O}ckinger and Theodora Petanidou and Potts, {Simon G.} and Power, {Eileen F.} and Maj Rundl{\"o}f and Kathrin Seibel and Virve S{\~o}ber and Annika S{\"o}derman and Ingolf Steffan-Dewenter and Stout, {Jane C.} and Tiit Teder and Teja Tscharntke and Smith, {Henrik G.}",

note = "Funding Information: We thank Carole Chateil, Volker Gaebele, Emmanuelle Porcher, and Marie Winsa for data contribution; Yann Clough and Peter Olsson for help on analyses and extraction of landscape data. The original idea was conceived as part of the project ?STEP-Status and trends of European pollinators? funded by the European Union in the 7th Framework Programme (grant 244090), which funded RB, ISD, HGS, SP, MR, LH, JME, and KS. JE and PC were funded by MULTAGRI/FORMAS. MA was funded by the EU FP5 project ?Evaluating current European agri-environment schemes to quantify and improve nature conservation efforts in agricultural landscapes? (EASY; QLRT-2001-01495) and the Swiss Federal Office for Science and Technology (01?0524-2). AJ and E? were funded by FORMAS. TTe and VS were supported by institutional research funding IUT (IUT20-33) of the Estonian Ministry of Education and Research, and TTe also received funding (grant no. 42900/1312/3166) from the Internal Grant Agency of the Faculty of Environmental Sciences, Czech University of Life Sciences Prague. IB was funded by MC-CIG BeeFun project: PCIG14-GA-2013-631653 and thanks the Do?ana NP staff members for granting access to the Park and Curro Molina for conducting the field work. JS, EFP, and SM were funded by DAFM and IRC. LH was funded by a grant from Formas to HGS and by a mobility grant from Formas (2018-01466). ALH was funded by the FarmLand project supported by the German Ministry of Research and Education (FKZ: 01LC1104A). AKH was supported by the NKFIH project (FK123813) and was a Bolyai Fellow of MTA. PB was supported by the NKFIH (KKP 133839). Funding Information: We thank Carole Chateil, Volker Gaebele, Emmanuelle Porcher, and Marie Winsa for data contribution; Yann Clough and Peter Olsson for help on analyses and extraction of landscape data. The original idea was conceived as part of the project {\textquoteleft}STEP - Status and trends of European pollinators{\textquoteright} funded by the European Union in the 7th Framework Programme (grant 244090), which funded RB, ISD, HGS, SP, MR, LH, JME, and KS. JE and PC were funded by MULTAGRI/FORMAS. MA was funded by the EU FP5 project {\textquoteleft}Evaluating current European agri-environment schemes to quantify and improve nature conservation efforts in agricultural landscapes{\textquoteright} (EASY; QLRT-2001-01495) and the Swiss Federal Office for Science and Technology (01·0524-2). AJ and E{\"O} were funded by FORMAS. TTe and VS were supported by institutional research funding IUT (IUT20-33) of the Estonian Ministry of Education and Research, and TTe also received funding (grant no. 42900/1312/3166) from the Internal Grant Agency of the Faculty of Environmental Sciences, Czech University of Life Sciences Prague. IB was funded by MC-CIG BeeFun project: PCIG14-GA-2013-631653 and thanks the Do{\~n}ana NP staff members for granting access to the Park and Curro Molina for conducting the field work. JS, EFP, and SM were funded by DAFM and IRC. LH was funded by a grant from Formas to HGS and by a mobility grant from Formas (2018-01466). ALH was funded by the FarmLand project supported by the German Ministry of Research and Education (FKZ: 01LC1104A). AKH was supported by the NKFIH project (FK123813) and was a Bolyai Fellow of MTA. PB was supported by the NKFIH (KKP 133839). Publisher Copyright: {\textcopyright} 2021 Lina Herbertsson, Johan Ekroos, Matthias Albrecht, Ignasi Bartomeus, P{\'e}ter Bat{\'a}ry, Riccardo Bommarco, Paul Caplat, Tim Diek{\"o}tter, Jenny M. Eikestam, Martin H. Entling, Sunniva Farbu, Nina Farwig, Juan P. Gonzalez-Varo, Annika L. Hass, Andrea Holzschuh, Sebastian Hopfenm{\"u}ller, Anna Jakobsson, Birgit Jauker, Anik{\'o} Kov{\'a}cs-Hosty{\'a}nszki, Wera Kleve, William E. Kunin, Sandra A.M. Lindstr{\"o}m, Sarah Mullen, Erik {\"O}ckinger, Theodora Petanidou, Simon G. Potts, Eileen F. Power, Maj Rundl{\"o}f, Kathrin Seibe, Virve S{\~o}ber, Annika S{\"o}derman, Ingolf Steffan-Dewenter, Jane C. Stout, Tiit Teder, Teja Tscharntke, Henrik G. Smith.",

year = "2021",

month = nov,

day = "23",

doi = "10.5091/PLECEVO.2021.1884",

language = "English",

volume = "154",

pages = "341--350",

journal = "Plant Ecology and Evolution",

issn = "2032-3913",

publisher = "Societe Royale de Botanique de Belgique",

number = "3",

}

Herbertsson, L, Ekroos, J, Albrecht, M, Bartomeus, I, Batáry, P, Bommarco, R, Caplat, P, Diekötter, T, Eikestam, JM, Entling, MH, Farbu, S, Farwig, N, Gonzalez-Varo, JP, Hass, AL, Holzschuh, A, Hopfenmüller, S, Jakobsson, A, Jauker, B, Kovács-Hostyánszki, A, Kleve, W, Kunin, WE, Lindström, SAM, Mullen, S, Öckinger, E, Petanidou, T, Potts, SG, Power, EF, Rundlöf, M, Seibel, K, Sõber, V, Söderman, A, Steffan-Dewenter, I, Stout, JC, Teder, T, Tscharntke, T & Smith, HG 2021, 'Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes', Plant Ecology and Evolution, vol. 154, no. 3, pp. 341-350. https://doi.org/10.5091/PLECEVO.2021.1884

TY - JOUR

T1 - Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes

AU - Herbertsson, Lina

AU - Ekroos, Johan

AU - Albrecht, Matthias

AU - Bartomeus, Ignasi

AU - Batáry, Péter

AU - Bommarco, Riccardo

AU - Caplat, Paul

AU - Diekötter, Tim

AU - Eikestam, Jenny M.

AU - Entling, Martin H.

AU - Farbu, Sunniva

AU - Farwig, Nina

AU - Gonzalez-Varo, Juan P.

AU - Hass, Annika L.

AU - Holzschuh, Andrea

AU - Hopfenmüller, Sebastian

AU - Jakobsson, Anna

AU - Jauker, Birgit

AU - Kovács-Hostyánszki, Anikó

AU - Kleve, Wera

AU - Kunin, William E.

AU - Lindström, Sandra A.M.

AU - Mullen, Sarah

AU - Öckinger, Erik

AU - Petanidou, Theodora

AU - Potts, Simon G.

AU - Power, Eileen F.

AU - Rundlöf, Maj

AU - Seibel, Kathrin

AU - Sõber, Virve

AU - Söderman, Annika

AU - Steffan-Dewenter, Ingolf

AU - Stout, Jane C.

AU - Teder, Tiit

AU - Tscharntke, Teja

AU - Smith, Henrik G.

N1 - Funding Information: We thank Carole Chateil, Volker Gaebele, Emmanuelle Porcher, and Marie Winsa for data contribution; Yann Clough and Peter Olsson for help on analyses and extraction of landscape data. The original idea was conceived as part of the project ?STEP-Status and trends of European pollinators? funded by the European Union in the 7th Framework Programme (grant 244090), which funded RB, ISD, HGS, SP, MR, LH, JME, and KS. JE and PC were funded by MULTAGRI/FORMAS. MA was funded by the EU FP5 project ?Evaluating current European agri-environment schemes to quantify and improve nature conservation efforts in agricultural landscapes? (EASY; QLRT-2001-01495) and the Swiss Federal Office for Science and Technology (01?0524-2). AJ and E? were funded by FORMAS. TTe and VS were supported by institutional research funding IUT (IUT20-33) of the Estonian Ministry of Education and Research, and TTe also received funding (grant no. 42900/1312/3166) from the Internal Grant Agency of the Faculty of Environmental Sciences, Czech University of Life Sciences Prague. IB was funded by MC-CIG BeeFun project: PCIG14-GA-2013-631653 and thanks the Do?ana NP staff members for granting access to the Park and Curro Molina for conducting the field work. JS, EFP, and SM were funded by DAFM and IRC. LH was funded by a grant from Formas to HGS and by a mobility grant from Formas (2018-01466). ALH was funded by the FarmLand project supported by the German Ministry of Research and Education (FKZ: 01LC1104A). AKH was supported by the NKFIH project (FK123813) and was a Bolyai Fellow of MTA. PB was supported by the NKFIH (KKP 133839). Funding Information: We thank Carole Chateil, Volker Gaebele, Emmanuelle Porcher, and Marie Winsa for data contribution; Yann Clough and Peter Olsson for help on analyses and extraction of landscape data. The original idea was conceived as part of the project ‘STEP - Status and trends of European pollinators’ funded by the European Union in the 7th Framework Programme (grant 244090), which funded RB, ISD, HGS, SP, MR, LH, JME, and KS. JE and PC were funded by MULTAGRI/FORMAS. MA was funded by the EU FP5 project ‘Evaluating current European agri-environment schemes to quantify and improve nature conservation efforts in agricultural landscapes’ (EASY; QLRT-2001-01495) and the Swiss Federal Office for Science and Technology (01·0524-2). AJ and EÖ were funded by FORMAS. TTe and VS were supported by institutional research funding IUT (IUT20-33) of the Estonian Ministry of Education and Research, and TTe also received funding (grant no. 42900/1312/3166) from the Internal Grant Agency of the Faculty of Environmental Sciences, Czech University of Life Sciences Prague. IB was funded by MC-CIG BeeFun project: PCIG14-GA-2013-631653 and thanks the Doñana NP staff members for granting access to the Park and Curro Molina for conducting the field work. JS, EFP, and SM were funded by DAFM and IRC. LH was funded by a grant from Formas to HGS and by a mobility grant from Formas (2018-01466). ALH was funded by the FarmLand project supported by the German Ministry of Research and Education (FKZ: 01LC1104A). AKH was supported by the NKFIH project (FK123813) and was a Bolyai Fellow of MTA. PB was supported by the NKFIH (KKP 133839). Publisher Copyright: © 2021 Lina Herbertsson, Johan Ekroos, Matthias Albrecht, Ignasi Bartomeus, Péter Batáry, Riccardo Bommarco, Paul Caplat, Tim Diekötter, Jenny M. Eikestam, Martin H. Entling, Sunniva Farbu, Nina Farwig, Juan P. Gonzalez-Varo, Annika L. Hass, Andrea Holzschuh, Sebastian Hopfenmüller, Anna Jakobsson, Birgit Jauker, Anikó Kovács-Hostyánszki, Wera Kleve, William E. Kunin, Sandra A.M. Lindström, Sarah Mullen, Erik Öckinger, Theodora Petanidou, Simon G. Potts, Eileen F. Power, Maj Rundlöf, Kathrin Seibe, Virve Sõber, Annika Söderman, Ingolf Steffan-Dewenter, Jane C. Stout, Tiit Teder, Teja Tscharntke, Henrik G. Smith.

PY - 2021/11/23

Y1 - 2021/11/23

N2 - Background and aims – Agricultural intensification and loss of farmland heterogeneity have contributed to population declines of wild bees and other pollinators, which may have caused subsequent declines in insect-pollinated wild plants. Material and methods – Using data from 37 studies on 22 pollinator-dependent wild plant species across Europe, we investigated whether flower visitation and seed set of insect-pollinated plants decline with an increasing proportion of arable land within 1 km. Key results – Seed set increased with increasing flower visitation by bees, most of which were wild bees, but not with increasing flower visitation by other insects. Increasing proportion of arable land had a strongly variable effect on seed set and flower visitation by bees across studies. Conclusion – Factors such as landscape configuration, local habitat quality, and temporally changing resource availability (e.g. due to mass-flowering crops or honey bee hives) could have modified the effect of arable land on pollination. While our results highlight that the persistence of wild bees is crucial to maintain plant diversity, we also show that pollen limitation due to declining bee populations in homogenized agricultural landscapes is not a universal driver causing parallel losses of bees and insect-pollinated plants.

AB - Background and aims – Agricultural intensification and loss of farmland heterogeneity have contributed to population declines of wild bees and other pollinators, which may have caused subsequent declines in insect-pollinated wild plants. Material and methods – Using data from 37 studies on 22 pollinator-dependent wild plant species across Europe, we investigated whether flower visitation and seed set of insect-pollinated plants decline with an increasing proportion of arable land within 1 km. Key results – Seed set increased with increasing flower visitation by bees, most of which were wild bees, but not with increasing flower visitation by other insects. Increasing proportion of arable land had a strongly variable effect on seed set and flower visitation by bees across studies. Conclusion – Factors such as landscape configuration, local habitat quality, and temporally changing resource availability (e.g. due to mass-flowering crops or honey bee hives) could have modified the effect of arable land on pollination. While our results highlight that the persistence of wild bees is crucial to maintain plant diversity, we also show that pollen limitation due to declining bee populations in homogenized agricultural landscapes is not a universal driver causing parallel losses of bees and insect-pollinated plants.

KW - Habitat loss

KW - Landscape complexity

KW - Landscape simplification

KW - Pollinating insects

KW - Pollination

KW - Semi-natural

U2 - 10.5091/PLECEVO.2021.1884

DO - 10.5091/PLECEVO.2021.1884

M3 - Article

AN - SCOPUS:85123110620

SN - 2032-3913

VL - 154

SP - 341

EP - 350

JO - Plant Ecology and Evolution

JF - Plant Ecology and Evolution

IS - 3

ER -

Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes

Abstract

Bibliographical note

Keywords

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