Article

Willems, F. M., J. F. Scheepens, and O. Bossdorf. 2022. Forest wildflowers bloom earlier as Europe warms: lessons from herbaria and spatial modelling. New Phytologist 235: 52–65. https://doi.org/10.1111/nph.18124

Today plants often flower earlier due to climate warming. Herbarium specimens are excellent witnesses of such long‐term changes. However, the magnitude of phenological shifts may vary geographically, and the data are often clustered. Therefore, large‐scale analyses of herbarium data are prone to pseudoreplication and geographical biases.We studied over 6000 herbarium specimens of 20 spring‐flowering forest understory herbs from Europe to understand how their phenology had changed during the last century. We estimated phenology trends with or without taking spatial autocorrelation into account.On average plants now flowered over 6 d earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Flowering time advanced 3.6 d per 1°C warming. Spatial modelling showed that, in some parts of Europe, plants flowered earlier or later than expected. Without accounting for this, the estimates of phenological shifts were biased and model fits were poor.Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change. However, these phenological shifts differ geographically. This shows that it is crucial to combine the analysis of herbarium data with spatial modelling when testing for long‐term phenology trends across large spatial scales.

Robert Stephen Adamson
Robert Stephen Adamson

March 02, 1885 – November 06, 1965

United Kingdom; Union of South Africa; United Kingdom of Great Britain and Ireland

Poaceae

Collected Poaceae and identified Juncaceae

Paul Aellen

May 13, 1896 – August 19, 1973

Switzerland

Asteraceae

Collected Asteraceae and identified Amaranthaceae

Jacob Georg Agardh
Jacob Georg Agardh

December 08, 1813 – January 17, 1901

Sweden

Asteraceae

Collected Asteraceae and identified Asteraceae

Ernst Almquist
Ernst Almquist

August 10, 1852 – May 16, 1946

Sweden

Parmeliaceae

Collected Parmeliaceae and identified Parmeliaceae

Collected Poaceae

Marie Andree-Eysn

November 11, 1847 – January 13, 1929

Austria

Ranunculaceae

Collected Ranunculaceae and identified Rosaceae

Eleonora Armitage

December 11, 1865 – October 24, 1961

United Kingdom of Great Britain and Ireland; United Kingdom

Caryophyllaceae

Collected Caryophyllaceae and identified Rubiaceae

Erik Asplund

October 09, 1888 – July 30, 1974

Sweden

Poaceae

Collected Poaceae and identified Poaceae

Cardale Babington
Cardale Babington

November 23, 1808 – July 22, 1895

United Kingdom of Great Britain and Ireland

Caryophyllaceae

Collected Caryophyllaceae and identified Rosaceae

Charles Bailey

June 18, 1838 – September 14, 1924

Characeae

Collected Characeae and identified Cyperaceae

Edward Benedict Bangerter

May 22, 1911 – August 21, 2001

United Kingdom

Poaceae

Collected Poaceae and identified Fabaceae

Joseph Banks
Joseph Banks

February 13, 1743 – June 19, 1820

United Kingdom of Great Britain and Ireland

Poaceae

Collected Poaceae and identified Dermestidae

Arthur Bennett

1843 – 1929

United Kingdom; United Kingdom of Great Britain and Ireland

Cyperaceae

Collected Cyperaceae and identified Potamogetonaceae

Alfred William Bennett
Alfred William Bennett

June 24, 1833 – January 23, 1902

United Kingdom of Great Britain and Ireland

Caryophyllaceae

Collected Caryophyllaceae and identified Polygalaceae

Sven Berggren
Sven Berggren

August 12, 1837 – June 28, 1917

Sweden

Pottiaceae

Collected Pottiaceae and identified Pottiaceae

Spencer Henry Bickham

November 15, 1840 – April 07, 1933

United Kingdom of Great Britain and Ireland

Caryophyllaceae

Collected Caryophyllaceae and identified Asteraceae

Dominik Bilimek
Dominik Bilimek

February 25, 1813 – August 03, 1884

Austrian Empire

Asteraceae

Collected Asteraceae and identified Fabaceae

Stig Blixt

January 02, 1930 – 2009

Sweden

Asteraceae

Collected Asteraceae and identified Asteraceae

Thomas Bates Blow

November 08, 1853 – January 16, 1941

Characeae

Collected Characeae and identified Ceratophyllaceae

Matthias Numsen Blytt
Matthias Numsen Blytt

April 26, 1789 – July 26, 1862

Norway

Asteraceae

Collected Asteraceae and identified Asteraceae

Torsten Alvin Borgvall

1884 – 1975

Sweden

Asteraceae

Collected Asteraceae and identified Poaceae

Joseph Friedrich Nicolaus Bornmüller
Joseph Friedrich Nicolaus Bornmüller

February 06, 1862 – December 19, 1948

Germany; Saxe-Meiningen

Asteraceae

Collected Asteraceae and identified Asteraceae

Arnold Eastwood Bradley

February 18, 1873 – November 13, 1944

Rosaceae

Collected Rosaceae and identified Lamiaceae

John Patrick Micklethwait Brenan

June 19, 1917 – September 26, 1985

United Kingdom; United Kingdom of Great Britain and Ireland

Fabaceae

Collected Fabaceae and identified Fabaceae

Elizabeth Raymond Ewing

1860 – 1951

Caryophyllaceae

Collected Caryophyllaceae

Christian Christener

1810 – 1872

Asteraceae

Collected Asteraceae and identified Salicaceae

John Christoffersson

1930 – January 27, 2013

Sweden

Asteraceae

Collected Asteraceae and identified Hylocomiaceae

Ingvar Christoffersson

1924 – 2003

Sphagnaceae

Collected Sphagnaceae and identified Poaceae

Judith Christoffersson

1896 – 1988

Sweden

Sphagnaceae

Collected Sphagnaceae and identified Neckeraceae

Beatrice Olive Corfe

January 19, 1866 – January 09, 1947

United Kingdom of Great Britain and Ireland; United Kingdom

Caryophyllaceae

Collected Caryophyllaceae and identified Poaceae