Angelino Carta1,2, Eduardo Fernández-Pascual3, Margherita Gioria4, Jonas V Müller5, Stéphane Rivière6, Sergey Rosbakh7, Arne Saatkamp8, Filip Vandelook9, Efisio Mattana5. 1. Department of Biology, Botany Unit, University of Pisa, Pisa, Italy. 2. CIRSEC - Centre for Climate Change Impact, University of Pisa, Pisa, Italy. 3. IMIB - Biodiversity Research Institute, University of Oviedo, Mieres, Spain. 4. Czech Academy of Sciences, Institute of Botany, Department of Invasion Ecology, Průhonice, Czech Republic. 5. Royal Botanic Gardens, Kew, Wakehurst, West Sussex, UK. 6. ENSCONET Consortium, Cambridge, UK. 7. Ecology and Conservation Biology, University of Regensburg, Regensburg, Germany. 8. Aix Marseille Université, Université d'Avignon, CNRS, IRD, IMBE, Marseille, France. 9. Meise Botanic Garden, Meise, Belgium.
Abstract
BACKGROUND AND AIMS: Interactions between ecological factors and seed physiological responses during the establishment phase shape the distribution of plants. Yet, our understanding of the functions and evolution of early-life traits has been limited by the scarcity of large-scale datasets. Here, we tested the hypothesis that the germination niche of temperate plants is shaped by their climatic requirements and phylogenetic relatedness, using germination data sourced from a comprehensive seed conservation database of the European flora (ENSCOBASE). METHODS: We performed a phylogenetically informed Bayesian meta-analysis of primary data, considering 18 762 germination tests of 2418 species from laboratory experiments conducted across all European geographical regions. We tested for the interaction between species' climatic requirements and germination responses to experimental conditions including temperature, alternating temperature, light and dormancy-breaking treatments, while accounting for between-study variation related to seed sources and seed lot physiological status. KEY RESULTS: Climate was a strong predictor of germination responses. In warm and seasonally dry climates the seed germination niche includes a cold-cued germination response and an inhibition determined by alternating temperature regimes and cold stratification, while in climates with high temperature seasonality opposite responses can be observed. Germination responses to scarification and light were related to seed mass but not to climate. We also found a significant phylogenetic signal in the response of seeds to experimental conditions, providing evidence that the germination niche is phylogenetically constrained. Nevertheless, phylogenetically distant lineages exhibited common germination responses under similar climates. CONCLUSION: This is the first quantitative meta-analysis of the germination niche at a continental scale. Our findings showed that the germination niches of European plants exhibit evolutionary convergence mediated by strong pressures at the macroclimatic level. In addition, our methodological approach highlighted how large datasets generated by conservation seed banking can be valuable sources to address questions in plant macroecology and evolution.
BACKGROUND AND AIMS: Interactions between ecological factors and seed physiological responses during the establishment phase shape the distribution of plants. Yet, our understanding of the functions and evolution of early-life traits has been limited by the scarcity of large-scale datasets. Here, we tested the hypothesis that the germination niche of temperate plants is shaped by their climatic requirements and phylogenetic relatedness, using germination data sourced from a comprehensive seed conservation database of the European flora (ENSCOBASE). METHODS: We performed a phylogenetically informed Bayesian meta-analysis of primary data, considering 18 762 germination tests of 2418 species from laboratory experiments conducted across all European geographical regions. We tested for the interaction between species' climatic requirements and germination responses to experimental conditions including temperature, alternating temperature, light and dormancy-breaking treatments, while accounting for between-study variation related to seed sources and seed lot physiological status. KEY RESULTS: Climate was a strong predictor of germination responses. In warm and seasonally dry climates the seed germination niche includes a cold-cued germination response and an inhibition determined by alternating temperature regimes and cold stratification, while in climates with high temperature seasonality opposite responses can be observed. Germination responses to scarification and light were related to seed mass but not to climate. We also found a significant phylogenetic signal in the response of seeds to experimental conditions, providing evidence that the germination niche is phylogenetically constrained. Nevertheless, phylogenetically distant lineages exhibited common germination responses under similar climates. CONCLUSION: This is the first quantitative meta-analysis of the germination niche at a continental scale. Our findings showed that the germination niches of European plants exhibit evolutionary convergence mediated by strong pressures at the macroclimatic level. In addition, our methodological approach highlighted how large datasets generated by conservation seed banking can be valuable sources to address questions in plant macroecology and evolution.
Authors: Sandra Díaz; Jens Kattge; Johannes H C Cornelissen; Ian J Wright; Sandra Lavorel; Stéphane Dray; Björn Reu; Michael Kleyer; Christian Wirth; I Colin Prentice; Eric Garnier; Gerhard Bönisch; Mark Westoby; Hendrik Poorter; Peter B Reich; Angela T Moles; John Dickie; Andrew N Gillison; Amy E Zanne; Jérôme Chave; S Joseph Wright; Serge N Sheremet'ev; Hervé Jactel; Christopher Baraloto; Bruno Cerabolini; Simon Pierce; Bill Shipley; Donald Kirkup; Fernando Casanoves; Julia S Joswig; Angela Günther; Valeria Falczuk; Nadja Rüger; Miguel D Mahecha; Lucas D Gorné Journal: Nature Date: 2015-12-23 Impact factor: 49.962
Authors: Arne Saatkamp; Anne Cochrane; Lucy Commander; Lydia K Guja; Borja Jimenez-Alfaro; Julie Larson; Adrienne Nicotra; Peter Poschlod; Fernando A O Silveira; Adam T Cross; Emma L Dalziell; John Dickie; Todd E Erickson; Alessandra Fidelis; Anne Fuchs; Peter J Golos; Michael Hope; Wolfgang Lewandrowski; David J Merritt; Ben P Miller; Russell G Miller; Catherine A Offord; Mark K J Ooi; Annisa Satyanti; Karen D Sommerville; Ryan Tangney; Sean Tomlinson; Shane Turner; Jeffrey L Walck Journal: New Phytol Date: 2018-10-25 Impact factor: 10.151
Authors: Riin Tamme; Lars Götzenberger; Martin Zobel; James M Bullock; Danny A P Hooftman; Ants Kaasik; Meelis Pärtel Journal: Ecology Date: 2014-02 Impact factor: 5.499
Authors: Jens Kattge; Gerhard Bönisch; Sandra Díaz; Sandra Lavorel; Iain Colin Prentice; Paul Leadley; Susanne Tautenhahn; Gijsbert D A Werner; Tuomas Aakala; Mehdi Abedi; Alicia T R Acosta; George C Adamidis; Kairi Adamson; Masahiro Aiba; Cécile H Albert; Julio M Alcántara; Carolina Alcázar C; Izabela Aleixo; Hamada Ali; Bernard Amiaud; Christian Ammer; Mariano M Amoroso; Madhur Anand; Carolyn Anderson; Niels Anten; Joseph Antos; Deborah Mattos Guimarães Apgaua; Tia-Lynn Ashman; Degi Harja Asmara; Gregory P Asner; Michael Aspinwall; Owen Atkin; Isabelle Aubin; Lars Baastrup-Spohr; Khadijeh Bahalkeh; Michael Bahn; Timothy Baker; William J Baker; Jan P Bakker; Dennis Baldocchi; Jennifer Baltzer; Arindam Banerjee; Anne Baranger; Jos Barlow; Diego R Barneche; Zdravko Baruch; Denis Bastianelli; John Battles; William Bauerle; Marijn Bauters; Erika Bazzato; Michael Beckmann; Hans Beeckman; Carl Beierkuhnlein; Renee Bekker; Gavin Belfry; Michael Belluau; Mirela Beloiu; Raquel Benavides; Lahcen Benomar; Mary Lee Berdugo-Lattke; Erika Berenguer; Rodrigo Bergamin; Joana Bergmann; Marcos Bergmann Carlucci; Logan Berner; Markus Bernhardt-Römermann; Christof Bigler; Anne D Bjorkman; Chris Blackman; Carolina Blanco; Benjamin Blonder; Dana Blumenthal; Kelly T Bocanegra-González; Pascal Boeckx; Stephanie Bohlman; Katrin Böhning-Gaese; Laura Boisvert-Marsh; William Bond; Ben Bond-Lamberty; Arnoud Boom; Coline C F Boonman; Kauane Bordin; Elizabeth H Boughton; Vanessa Boukili; David M J S Bowman; Sandra Bravo; Marco Richard Brendel; Martin R Broadley; Kerry A Brown; Helge Bruelheide; Federico Brumnich; Hans Henrik Bruun; David Bruy; Serra W Buchanan; Solveig Franziska Bucher; Nina Buchmann; Robert Buitenwerf; Daniel E Bunker; Jana Bürger; Sabina Burrascano; David F R P Burslem; Bradley J Butterfield; Chaeho Byun; Marcia Marques; Marina C Scalon; Marco Caccianiga; Marc Cadotte; Maxime Cailleret; James Camac; Jesús Julio Camarero; Courtney Campany; Giandiego Campetella; Juan Antonio Campos; Laura Cano-Arboleda; Roberto Canullo; Michele Carbognani; Fabio Carvalho; Fernando Casanoves; Bastien Castagneyrol; Jane A Catford; Jeannine Cavender-Bares; Bruno E L Cerabolini; Marco Cervellini; Eduardo Chacón-Madrigal; Kenneth Chapin; F Stuart Chapin; Stefano Chelli; Si-Chong Chen; Anping Chen; Paolo Cherubini; Francesco Chianucci; Brendan Choat; Kyong-Sook Chung; Milan Chytrý; Daniela Ciccarelli; Lluís Coll; Courtney G Collins; Luisa Conti; David Coomes; Johannes H C Cornelissen; William K Cornwell; Piermaria Corona; Marie Coyea; Joseph Craine; Dylan Craven; Joris P G M Cromsigt; Anikó Csecserits; Katarina Cufar; Matthias Cuntz; Ana Carolina da Silva; Kyla M Dahlin; Matteo Dainese; Igor Dalke; Michele Dalle Fratte; Anh Tuan Dang-Le; Jirí Danihelka; Masako Dannoura; Samantha Dawson; Arend Jacobus de Beer; Angel De Frutos; Jonathan R De Long; Benjamin Dechant; Sylvain Delagrange; Nicolas Delpierre; Géraldine Derroire; Arildo S Dias; Milton Hugo Diaz-Toribio; Panayiotis G Dimitrakopoulos; Mark Dobrowolski; Daniel Doktor; Pavel Dřevojan; Ning Dong; John Dransfield; Stefan Dressler; Leandro Duarte; Emilie Ducouret; Stefan Dullinger; Walter Durka; Remko Duursma; Olga Dymova; Anna E-Vojtkó; Rolf Lutz Eckstein; Hamid Ejtehadi; James Elser; Thaise Emilio; Kristine Engemann; Mohammad Bagher Erfanian; Alexandra Erfmeier; Adriane Esquivel-Muelbert; Gerd Esser; Marc Estiarte; Tomas F Domingues; William F Fagan; Jaime Fagúndez; Daniel S Falster; Ying Fan; Jingyun Fang; Emmanuele Farris; Fatih Fazlioglu; Yanhao Feng; Fernando Fernandez-Mendez; Carlotta Ferrara; Joice Ferreira; Alessandra Fidelis; Bryan Finegan; Jennifer Firn; Timothy J Flowers; Dan F B Flynn; Veronika Fontana; Estelle Forey; Cristiane Forgiarini; Louis François; Marcelo Frangipani; Dorothea Frank; Cedric Frenette-Dussault; Grégoire T Freschet; Ellen L Fry; Nikolaos M Fyllas; Guilherme G Mazzochini; Sophie Gachet; Rachael Gallagher; Gislene Ganade; Francesca Ganga; Pablo García-Palacios; Verónica Gargaglione; Eric Garnier; Jose Luis Garrido; André Luís de Gasper; Guillermo Gea-Izquierdo; David Gibson; Andrew N Gillison; Aelton Giroldo; Mary-Claire Glasenhardt; Sean Gleason; Mariana Gliesch; Emma Goldberg; Bastian Göldel; Erika Gonzalez-Akre; Jose L Gonzalez-Andujar; Andrés González-Melo; Ana González-Robles; Bente Jessen Graae; Elena Granda; Sarah Graves; Walton A Green; Thomas Gregor; Nicolas Gross; Greg R Guerin; Angela Günther; Alvaro G Gutiérrez; Lillie Haddock; Anna Haines; Jefferson Hall; Alain Hambuckers; Wenxuan Han; Sandy P Harrison; Wesley Hattingh; Joseph E Hawes; Tianhua He; Pengcheng He; Jacob Mason Heberling; Aveliina Helm; Stefan Hempel; Jörn Hentschel; Bruno Hérault; Ana-Maria Hereş; Katharina Herz; Myriam Heuertz; Thomas Hickler; Peter Hietz; Pedro Higuchi; Andrew L Hipp; Andrew Hirons; Maria Hock; James Aaron Hogan; Karen Holl; Olivier Honnay; Daniel Hornstein; Enqing Hou; Nate Hough-Snee; Knut Anders Hovstad; Tomoaki Ichie; Boris Igić; Estela Illa; Marney Isaac; Masae Ishihara; Leonid Ivanov; Larissa Ivanova; Colleen M Iversen; Jordi Izquierdo; Robert B Jackson; Benjamin Jackson; Hervé Jactel; Andrzej M Jagodzinski; Ute Jandt; Steven Jansen; Thomas Jenkins; Anke Jentsch; Jens Rasmus Plantener Jespersen; Guo-Feng Jiang; Jesper Liengaard Johansen; David Johnson; Eric J Jokela; Carlos Alfredo Joly; Gregory J Jordan; Grant Stuart Joseph; Decky Junaedi; Robert R Junker; Eric Justes; Richard Kabzems; Jeffrey Kane; Zdenek Kaplan; Teja Kattenborn; Lyudmila Kavelenova; Elizabeth Kearsley; Anne Kempel; Tanaka Kenzo; Andrew Kerkhoff; Mohammed I Khalil; Nicole L Kinlock; Wilm Daniel Kissling; Kaoru Kitajima; Thomas Kitzberger; Rasmus Kjøller; Tamir Klein; Michael Kleyer; Jitka Klimešová; Joice Klipel; Brian Kloeppel; Stefan Klotz; Johannes M H Knops; Takashi Kohyama; Fumito Koike; Johannes Kollmann; Benjamin Komac; Kimberly Komatsu; Christian König; Nathan J B Kraft; Koen Kramer; Holger Kreft; Ingolf Kühn; Dushan Kumarathunge; Jonas Kuppler; Hiroko Kurokawa; Yoko Kurosawa; Shem Kuyah; Jean-Paul Laclau; Benoit Lafleur; Erik Lallai; Eric Lamb; Andrea Lamprecht; Daniel J Larkin; Daniel Laughlin; Yoann Le Bagousse-Pinguet; Guerric le Maire; Peter C le Roux; Elizabeth le Roux; Tali Lee; Frederic Lens; Simon L Lewis; Barbara Lhotsky; Yuanzhi Li; Xine Li; Jeremy W Lichstein; Mario Liebergesell; Jun Ying Lim; Yan-Shih Lin; Juan Carlos Linares; Chunjiang Liu; Daijun Liu; Udayangani Liu; Stuart Livingstone; Joan Llusià; Madelon Lohbeck; Álvaro López-García; Gabriela Lopez-Gonzalez; Zdeňka Lososová; Frédérique Louault; Balázs A Lukács; Petr Lukeš; Yunjian Luo; Michele Lussu; Siyan Ma; Camilla Maciel Rabelo Pereira; Michelle Mack; Vincent Maire; Annikki Mäkelä; Harri Mäkinen; Ana Claudia Mendes Malhado; Azim Mallik; Peter Manning; Stefano Manzoni; Zuleica Marchetti; Luca Marchino; Vinicius Marcilio-Silva; Eric Marcon; Michela Marignani; Lars Markesteijn; Adam Martin; Cristina Martínez-Garza; Jordi Martínez-Vilalta; Tereza Mašková; Kelly Mason; Norman Mason; Tara Joy Massad; Jacynthe Masse; Itay Mayrose; James McCarthy; M Luke McCormack; Katherine McCulloh; Ian R McFadden; Brian J McGill; Mara Y McPartland; Juliana S Medeiros; Belinda Medlyn; Pierre Meerts; Zia Mehrabi; Patrick Meir; Felipe P L Melo; Maurizio Mencuccini; Céline Meredieu; Julie Messier; Ilona Mészáros; Juha Metsaranta; Sean T Michaletz; Chrysanthi Michelaki; Svetlana Migalina; Ruben Milla; Jesse E D Miller; Vanessa Minden; Ray Ming; Karel Mokany; Angela T Moles; Attila Molnár; Jane Molofsky; Martin Molz; Rebecca A Montgomery; Arnaud Monty; Lenka Moravcová; Alvaro Moreno-Martínez; Marco Moretti; Akira S Mori; Shigeta Mori; Dave Morris; Jane Morrison; Ladislav Mucina; Sandra Mueller; Christopher D Muir; Sandra Cristina Müller; François Munoz; Isla H Myers-Smith; Randall W Myster; Masahiro Nagano; Shawna Naidu; Ayyappan Narayanan; Balachandran Natesan; Luka Negoita; Andrew S Nelson; Eike Lena Neuschulz; Jian Ni; Georg Niedrist; Jhon Nieto; Ülo Niinemets; Rachael Nolan; Henning Nottebrock; Yann Nouvellon; Alexander Novakovskiy; Kristin Odden Nystuen; Anthony O'Grady; Kevin O'Hara; Andrew O'Reilly-Nugent; Simon Oakley; Walter Oberhuber; Toshiyuki Ohtsuka; Ricardo Oliveira; Kinga Öllerer; Mark E Olson; Vladimir Onipchenko; Yusuke Onoda; Renske E Onstein; Jenny C Ordonez; Noriyuki Osada; Ivika Ostonen; Gianluigi Ottaviani; Sarah Otto; Gerhard E Overbeck; Wim A Ozinga; Anna T Pahl; C E Timothy Paine; Robin J Pakeman; Aristotelis C Papageorgiou; Evgeniya Parfionova; Meelis Pärtel; Marco Patacca; Susana Paula; Juraj Paule; Harald Pauli; Juli G Pausas; Begoña Peco; Josep Penuelas; Antonio Perea; Pablo Luis Peri; Ana Carolina Petisco-Souza; Alessandro Petraglia; Any Mary Petritan; Oliver L Phillips; Simon Pierce; Valério D Pillar; Jan Pisek; Alexandr Pomogaybin; Hendrik Poorter; Angelika Portsmuth; Peter Poschlod; Catherine Potvin; Devon Pounds; A Shafer Powell; Sally A Power; Andreas Prinzing; Giacomo Puglielli; Petr Pyšek; Valerie Raevel; Anja Rammig; Johannes Ransijn; Courtenay A Ray; Peter B Reich; Markus Reichstein; Douglas E B Reid; Maxime Réjou-Méchain; Victor Resco de Dios; Sabina Ribeiro; Sarah Richardson; Kersti Riibak; Matthias C Rillig; Fiamma Riviera; Elisabeth M R Robert; Scott Roberts; Bjorn Robroek; Adam Roddy; Arthur Vinicius Rodrigues; Alistair Rogers; Emily Rollinson; Victor Rolo; Christine Römermann; Dina Ronzhina; Christiane Roscher; Julieta A Rosell; Milena Fermina Rosenfield; Christian Rossi; David B Roy; Samuel Royer-Tardif; Nadja Rüger; Ricardo Ruiz-Peinado; Sabine B Rumpf; Graciela M Rusch; Masahiro Ryo; Lawren Sack; Angela Saldaña; Beatriz Salgado-Negret; Roberto Salguero-Gomez; Ignacio Santa-Regina; Ana Carolina Santacruz-García; Joaquim Santos; Jordi Sardans; Brandon Schamp; Michael Scherer-Lorenzen; Matthias Schleuning; Bernhard Schmid; Marco Schmidt; Sylvain Schmitt; Julio V Schneider; Simon D Schowanek; Julian Schrader; Franziska Schrodt; Bernhard Schuldt; Frank Schurr; Galia Selaya Garvizu; Marina Semchenko; Colleen Seymour; Julia C Sfair; Joanne M Sharpe; Christine S Sheppard; Serge Sheremetiev; Satomi Shiodera; Bill Shipley; Tanvir Ahmed Shovon; Alrun Siebenkäs; Carlos Sierra; Vasco Silva; Mateus Silva; Tommaso Sitzia; Henrik Sjöman; Martijn Slot; Nicholas G Smith; Darwin Sodhi; Pamela Soltis; Douglas Soltis; Ben Somers; Grégory Sonnier; Mia Vedel Sørensen; Enio Egon Sosinski; Nadejda A Soudzilovskaia; Alexandre F Souza; Marko Spasojevic; Marta Gaia Sperandii; Amanda B Stan; James Stegen; Klaus Steinbauer; Jörg G Stephan; Frank Sterck; Dejan B Stojanovic; Tanya Strydom; Maria Laura Suarez; Jens-Christian Svenning; Ivana Svitková; Marek Svitok; Miroslav Svoboda; Emily Swaine; Nathan Swenson; Marcelo Tabarelli; Kentaro Takagi; Ulrike Tappeiner; Rubén Tarifa; Simon Tauugourdeau; Cagatay Tavsanoglu; Mariska Te Beest; Leho Tedersoo; Nelson Thiffault; Dominik Thom; Evert Thomas; Ken Thompson; Peter E Thornton; Wilfried Thuiller; Lubomír Tichý; David Tissue; Mark G Tjoelker; David Yue Phin Tng; Joseph Tobias; Péter Török; Tonantzin Tarin; José M Torres-Ruiz; Béla Tóthmérész; Martina Treurnicht; Valeria Trivellone; Franck Trolliet; Volodymyr Trotsiuk; James L Tsakalos; Ioannis Tsiripidis; Niklas Tysklind; Toru Umehara; Vladimir Usoltsev; Matthew Vadeboncoeur; Jamil Vaezi; Fernando Valladares; Jana Vamosi; Peter M van Bodegom; Michiel van Breugel; Elisa Van Cleemput; Martine van de Weg; Stephni van der Merwe; Fons van der Plas; Masha T van der Sande; Mark van Kleunen; Koenraad Van Meerbeek; Mark Vanderwel; Kim André Vanselow; Angelica Vårhammar; Laura Varone; Maribel Yesenia Vasquez Valderrama; Kiril Vassilev; Mark Vellend; Erik J Veneklaas; Hans Verbeeck; Kris Verheyen; Alexander Vibrans; Ima Vieira; Jaime Villacís; Cyrille Violle; Pandi Vivek; Katrin Wagner; Matthew Waldram; Anthony Waldron; Anthony P Walker; Martyn Waller; Gabriel Walther; Han Wang; Feng Wang; Weiqi Wang; Harry Watkins; James Watkins; Ulrich Weber; James T Weedon; Liping Wei; Patrick Weigelt; Evan Weiher; Aidan W Wells; Camilla Wellstein; Elizabeth Wenk; Mark Westoby; Alana Westwood; Philip John White; Mark Whitten; Mathew Williams; Daniel E Winkler; Klaus Winter; Chevonne Womack; Ian J Wright; S Joseph Wright; Justin Wright; Bruno X Pinho; Fabiano Ximenes; Toshihiro Yamada; Keiko Yamaji; Ruth Yanai; Nikolay Yankov; Benjamin Yguel; Kátia Janaina Zanini; Amy E Zanne; David Zelený; Yun-Peng Zhao; Jingming Zheng; Ji Zheng; Kasia Ziemińska; Chad R Zirbel; Georg Zizka; Irié Casimir Zo-Bi; Gerhard Zotz; Christian Wirth Journal: Glob Chang Biol Date: 2019-12-31 Impact factor: 10.863
Authors: Margherita Gioria; Angelino Carta; Carol C Baskin; Wayne Dawson; Franz Essl; Holger Kreft; Jan Pergl; Mark van Kleunen; Patrick Weigelt; Marten Winter; Petr Pyšek Journal: Ecol Lett Date: 2021-05-24 Impact factor: 9.492
Authors: Steven B Janssens; Thomas L P Couvreur; Arne Mertens; Gilles Dauby; Leo-Paul M J Dagallier; Samuel Vanden Abeele; Filip Vandelook; Maurizio Mascarello; Hans Beeckman; Marc Sosef; Vincent Droissart; Michelle van der Bank; Olivier Maurin; William Hawthorne; Cicely Marshall; Maxime Réjou-Méchain; Denis Beina; Fidele Baya; Vincent Merckx; Brecht Verstraete; Olivier Hardy Journal: Biodivers Data J Date: 2020-01-21