Soil eutrophication shaped the composition of pollinator assemblages during the past century

Luísa G. Carvalheiro*, Jacobus C. Biesmeijer, Markus Franzén, Jesús Aguirre-Gutiérrez, Lucas A. Garibaldi, Aveliina Helm, Denis Michez, Juha Pöyry, Menno Reemer, Oliver Schweiger, Berg Leon van den, Michiel F. WallisDeVries, William E. Kunin

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Atmospheric nitrogen deposition and other sources of environmental eutrophication have increased substantially over the past century worldwide, notwithstanding the recent declining trends in Europe. Despite the recognized susceptibility of plants to eutrophication, few studies evaluated how impacts propagate to consumers, such as pollinators. Here we aim to test if soil eutrophication contributes to the temporal dynamics of pollinators and their larval resources. We used a temporally and spatially explicit historical dataset with information on species occurrences to test if soil eutrophication, and more specifically nitrogen deposition, contributes to the patterns of change of plant and pollinator richness in the Netherlands over an 80 yr period. We focus on bees and butterflies, two groups for which we have good knowledge of larval resources that allowed us to define groups of species with different nitrogen related diet preferences. For each group we estimated richness changes between different 20-yr periods at local, regional and national scale, using analytical methods developed for analyzing richness changes based on collection data. Our findings suggest that the impacts of soil eutrophication on plant communities propagate to higher trophic levels, but with a time-lag. Pollinators with nitrogen-related diet preferences were particularly affected, in turn potentially impairing the performance of pollinator-dependent plants. Pollinator declines continued even after their focal plants started to recover. In addition, our results suggest that current levels of nitrogen deposition still have a negative impact on most groups here analyzed, constraining richness recoveries and accentuating declines. Our results indicate that the global increase in nitrogen availability plays an important role in the ongoing pollinator decline. Consequently, species tolerances to soil nitrogen levels should be considered across all trophic levels in management plans that aim to halt biodiversity loss and enhance ecosystems services worldwide.

Original languageEnglish
Pages (from-to)209-221
JournalEcography
Volume43
Issue number2
Early online date7 Nov 2019
DOIs
Publication statusPublished - Feb 2020

Fingerprint

pollinating insects
pollinator
eutrophication
nitrogen
soil
soil test
food choices
trophic level
diet
species occurrence
resource
soil nitrogen
ecosystem service
butterfly
bee
ecosystem services
butterflies
analytical methods
plant community
plant communities

Keywords

  • extinction debt
  • herbivory
  • historical biodiversity changes
  • nitrogen deposition
  • nitrophily
  • pollinator communities

Cite this

Carvalheiro, L. G., Biesmeijer, J. C., Franzén, M., Aguirre-Gutiérrez, J., Garibaldi, L. A., Helm, A., ... Kunin, W. E. (2020). Soil eutrophication shaped the composition of pollinator assemblages during the past century. Ecography, 43(2), 209-221. https://doi.org/10.1111/ecog.04656
Carvalheiro, Luísa G. ; Biesmeijer, Jacobus C. ; Franzén, Markus ; Aguirre-Gutiérrez, Jesús ; Garibaldi, Lucas A. ; Helm, Aveliina ; Michez, Denis ; Pöyry, Juha ; Reemer, Menno ; Schweiger, Oliver ; Leon van den, Berg ; WallisDeVries, Michiel F. ; Kunin, William E. / Soil eutrophication shaped the composition of pollinator assemblages during the past century. In: Ecography. 2020 ; Vol. 43, No. 2. pp. 209-221.
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abstract = "Atmospheric nitrogen deposition and other sources of environmental eutrophication have increased substantially over the past century worldwide, notwithstanding the recent declining trends in Europe. Despite the recognized susceptibility of plants to eutrophication, few studies evaluated how impacts propagate to consumers, such as pollinators. Here we aim to test if soil eutrophication contributes to the temporal dynamics of pollinators and their larval resources. We used a temporally and spatially explicit historical dataset with information on species occurrences to test if soil eutrophication, and more specifically nitrogen deposition, contributes to the patterns of change of plant and pollinator richness in the Netherlands over an 80 yr period. We focus on bees and butterflies, two groups for which we have good knowledge of larval resources that allowed us to define groups of species with different nitrogen related diet preferences. For each group we estimated richness changes between different 20-yr periods at local, regional and national scale, using analytical methods developed for analyzing richness changes based on collection data. Our findings suggest that the impacts of soil eutrophication on plant communities propagate to higher trophic levels, but with a time-lag. Pollinators with nitrogen-related diet preferences were particularly affected, in turn potentially impairing the performance of pollinator-dependent plants. Pollinator declines continued even after their focal plants started to recover. In addition, our results suggest that current levels of nitrogen deposition still have a negative impact on most groups here analyzed, constraining richness recoveries and accentuating declines. Our results indicate that the global increase in nitrogen availability plays an important role in the ongoing pollinator decline. Consequently, species tolerances to soil nitrogen levels should be considered across all trophic levels in management plans that aim to halt biodiversity loss and enhance ecosystems services worldwide.",
keywords = "extinction debt, herbivory, historical biodiversity changes, nitrogen deposition, nitrophily, pollinator communities",
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Carvalheiro, LG, Biesmeijer, JC, Franzén, M, Aguirre-Gutiérrez, J, Garibaldi, LA, Helm, A, Michez, D, Pöyry, J, Reemer, M, Schweiger, O, Leon van den, B, WallisDeVries, MF & Kunin, WE 2020, 'Soil eutrophication shaped the composition of pollinator assemblages during the past century', Ecography, vol. 43, no. 2, pp. 209-221. https://doi.org/10.1111/ecog.04656

Soil eutrophication shaped the composition of pollinator assemblages during the past century. / Carvalheiro, Luísa G.; Biesmeijer, Jacobus C.; Franzén, Markus; Aguirre-Gutiérrez, Jesús; Garibaldi, Lucas A.; Helm, Aveliina; Michez, Denis; Pöyry, Juha; Reemer, Menno; Schweiger, Oliver; Leon van den, Berg; WallisDeVries, Michiel F.; Kunin, William E.

In: Ecography, Vol. 43, No. 2, 02.2020, p. 209-221.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Carvalheiro, Luísa G.

AU - Biesmeijer, Jacobus C.

AU - Franzén, Markus

AU - Aguirre-Gutiérrez, Jesús

AU - Garibaldi, Lucas A.

AU - Helm, Aveliina

AU - Michez, Denis

AU - Pöyry, Juha

AU - Reemer, Menno

AU - Schweiger, Oliver

AU - Leon van den, Berg

AU - WallisDeVries, Michiel F.

AU - Kunin, William E.

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KW - nitrophily

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Carvalheiro LG, Biesmeijer JC, Franzén M, Aguirre-Gutiérrez J, Garibaldi LA, Helm A et al. Soil eutrophication shaped the composition of pollinator assemblages during the past century. Ecography. 2020 Feb;43(2):209-221. https://doi.org/10.1111/ecog.04656