The fall of the summer truffle: Recurring hot, dry summers result in declining fruitbody production of Tuber aestivum in Central Europe
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
PubMed
36200354
PubMed Central
PMC9828532
DOI
10.1111/gcb.16424
Knihovny.cz E-zdroje
- Klíčová slova
- climate change, drought extremes, ecological niche, global warming, mycorrhizal fungi, truffles,
- MeSH
- Ascomycota * fyziologie MeSH
- mykorhiza * fyziologie MeSH
- roční období MeSH
- stromy MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Evropa MeSH
Global warming is pushing populations outside their range of physiological tolerance. According to the environmental envelope framework, the most vulnerable populations occur near the climatic edge of their species' distributions. In contrast, populations from the climatic center of the species range should be relatively buffered against climate warming. We tested this latter prediction using a combination of linear mixed effects and machine learning algorithms on an extensive, citizen-scientist generated dataset on the fruitbody productivity of the Burgundy (aka summer) truffle (Tuber aestivum Vittad.), a keystone, ectomycorrhizal tree-symbiont occurring on a wide range of temperate climates. T. aestivum's fruitbody productivity was monitored at 3-week resolution over up to 8 continuous years at 20 sites distributed in the climatic center of its European distribution in southwest Germany and Switzerland. We found that T. aestivum fruitbody production is more sensitive to summer drought than would be expected from the breadth of its species' climatic niche. The monitored populations occurring nearly 5°C colder than the edge of their species' climatic distribution. However, interannual fruitbody productivity (truffle mass year-1 ) fell by a median loss of 22% for every 1°C increase in summer temperature over a site's 30-year mean. Among the most productive monitored populations, the temperature sensitivity was even higher, with single summer temperature anomalies of 3°C sufficient to stop fruitbody production altogether. Interannual truffle productivity was also related to the phenology of host trees, with ~22 g less truffle mass for each 1-day reduction in the length of the tree growing season. Increasing summer drought extremes are therefore likely to reduce fruiting among summer truffle populations throughout Central Europe. Our results suggest that European T. aestivum may be a mosaic of vulnerable populations, sensitive to climate-driven declines at lower thresholds than implied by its species distribution model.
Agrifood Research and Technology Centre of Aragon CITA Zaragoza Spain
Department of Ecology University of Konstanz Konstanz Germany
Department of Geography Faculty of Science Masaryk University Brno Czech Republic
Department of Geography University of Cambridge Cambridge UK
Deutsche Trüffelbäume Bodman Germany
European Mycological Institute EGTC EMI Soria Spain
Forest Growth Albert Ludwigs University Freiburg Germany
Forest Science and Technology Centre of Catalonia Solsona Spain
Global Change Research Centre Brno Czech Republic
Swiss Federal Institute for Forest Snow and Landscape Research WSL Birmensdorf Switzerland
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Aitken, S. N. , Yeaman, S. , Holliday, J. A. , Wang, T. , & Curtis‐McLane, S. (2008). Adaptation, migration or extirpation: Climate change outcomes for tree populations. Evolutionary Applications, 1(1), 95–111. 10.1111/j.1752-4571.2007.00013.x PubMed DOI PMC
Alexander, L. (2011). Extreme heat rooted in dry soils. Nature Geoscience, 4(1), 12–13. 10.1038/ngeo1045 DOI
Anderson, I. C. , & Cairney, J. W. G. (2007). Ectomycorrhizal fungi: Exploring the mycelial frontier. FEMS Microbiology Reviews, 31(4), 388–406. 10.1111/j.1574-6976.2007.00073.x PubMed DOI
Araújo, M. B. , Whittaker, R. J. , Ladle, R. J. , & Erhard, M. (2005). Reducing uncertainty in projections of extinction risk from climate change. Global Ecology and Biogeography, 14(6), 529–538. 10.1111/j.1466-822X.2005.00182.x DOI
Atkins, K. E. , & Travis, J. M. J. (2010). Local adaptation and the evolution of species' ranges under climate change. Journal of Theoretical Biology, 266(3), 449–457. 10.1016/j.jtbi.2010.07.014 PubMed DOI
Austin, M. (2007). Species distribution models and ecological theory: A critical assessment and some possible new approaches. Ecological Modelling, 200(1), 1–19. 10.1016/j.ecolmodel.2006.07.005 DOI
Baragatti, M. , Grollemund, P.‐M. , Montpied, P. , Dupouey, J.‐L. , Gravier, J. , Murat, C. , & Le Tacon, F. (2019). Influence of annual climatic variations, climate changes, and sociological factors on the production of the Périgord black truffle (Tuber melanosporum Vittad.) from 1903–1904 to 1988–1989 in the Vaucluse (France). Mycorrhiza, 29(2), 113–125. 10.1007/s00572-018-0877-1 PubMed DOI
Bates, D. , Mächler, M. , Bolker, B. , & Walker, S. (2015). Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67(1), 1–48. 10.18637/jss.v067.i01 DOI
Beaumont, L. J. , Hughes, L. , & Poulsen, M. (2005). Predicting species distributions: Use of climatic parameters in BIOCLIM and its impact on predictions of species' current and future distributions. Ecological Modelling, 186(2), 251–270. 10.1016/j.ecolmodel.2005.01.030 DOI
Benucci, G. M. N. , Raggi, L. , Albertini, E. , Grebenc, T. , Bencivenga, M. , Falcinelli, M. , & Di Massimo, G. (2011). Ectomycorrhizal communities in a productive Tuber aestivum Vittad. Orchard: Composition, host influence and species replacement. FEMS Microbiology Ecology, 76(1), 170–184. 10.1111/j.1574-6941.2010.01039.x PubMed DOI
Büntgen, U. , Egli, S. , Camarero, J. J. , Fischer, E. M. , Stobbe, U. , Kauserud, H. , Tegel, W. , Sproll, L. , & Stenseth, N. C. (2012). Drought‐induced decline in Mediterranean truffle harvest. Nature Climate Change, 2(12), 827–829. 10.1038/nclimate1733 DOI
Büntgen, U. , Lendorff, H. , Lendorff, A. , Leuchtmann, A. , Peter, M. , Bagi, I. , & Egli, S. (2019). Truffles on the move. Frontiers in Ecology and the Environment, 17(4), 200–202. 10.1002/fee.2033 DOI
Büntgen, U. , Tegel, W. , Egli, S. , Stobbe, U. , Sproll, L. , & Stenseth, N. C. (2011). Truffles and climate change. Frontiers in Ecology and the Environment, 9(3), 150–151. 10.1890/11.WB.004 DOI
Čejka, T. , Trnka, M. , Krusic, P. J. , Stobbe, U. , Oliach, D. , Václavík, T. , Tegel, W. , & Büntgen, U. (2020). Predicted climate change will increase the truffle cultivation potential in Central Europe. Scientific Reports, 10(1), 21281. 10.1038/s41598-020-76177-0 PubMed DOI PMC
Chen, I.‐C. , Hill, J. K. , Ohlemüller, R. , Roy, D. B. , & Thomas, C. D. (2011). Rapid range shifts of species associated with high levels of climate warming. Science, 333(6045), 1024–1026. 10.1126/science.1206432 PubMed DOI
Christidis, N. , Jones, G. S. , & Stott, P. A. (2015). Dramatically increasing chance of extremely hot summers since the 2003 European heatwave. Nature Climate Change, 5(1), 46–50. 10.1038/nclimate2468 DOI
Copernicus Climate Change Service . (2019). ERA5‐land hourly data from 2001 to present [data set]. ECMWF. 10.24381/CDS.E2161BAC DOI
Čufar, K. , Prislan, P. , de Luis, M. , & Gričar, J. (2008). Tree‐ring variation, wood formation and phenology of beech (Fagus sylvatica) from a representative site in Slovenia, SE Central Europe. Trees, 22(6), 749–758. 10.1007/s00468-008-0235-6 DOI
Diez, J. , Kauserud, H. , Andrew, C. , Heegaard, E. , Krisai‐Greilhuber, I. , Senn‐Irlet, B. , Høiland, K. , Egli, S. , & Büntgen, U. (2020). Altitudinal upwards shifts in fungal fruiting in the Alps. Proceedings of the Royal Society B: Biological Sciences, 287(1919), 20192348. 10.1098/rspb.2019.2348 PubMed DOI PMC
Dongmo, M. A. K. , Hanna, R. , Smith, T. B. , Fiaboe, K. K. M. , Fomena, A. , & Bonebrake, T. C. (2021). Local adaptation in thermal tolerance for a tropical butterfly across ecotone and rainforest habitats. Biology Open, 10(4), bio058619. 10.1242/bio.058619 PubMed DOI PMC
Douhan, G. W. , Vincenot, L. , Gryta, H. , & Selosse, M.‐A. (2011). Population genetics of ectomycorrhizal fungi: From current knowledge to emerging directions. Fungal Biology, 115(7), 569–597. 10.1016/j.funbio.2011.03.005 PubMed DOI
Dyderski, M. K. , Paź, S. , Frelich, L. E. , & Jagodziński, A. M. (2018). How much does climate change threaten European forest tree species distributions? Global Change Biology, 24(3), 1150–1163. 10.1111/gcb.13925 PubMed DOI
Ebenman, B. , & Jonsson, T. (2005). Using community viability analysis to identify fragile systems and keystone species. Trends in Ecology and Evolution, 20(10), 568–575. 10.1016/j.tree.2005.06.011 PubMed DOI
Elith, J. , Phillips, S. J. , Hastie, T. , Dudík, M. , Chee, Y. E. , & Yates, C. J. (2011). A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17(1), 43–57. 10.1111/j.1472-4642.2010.00725.x DOI
Fick, S. E. , & Hijmans, R. J. (2017). WorldClim 2: New 1‐km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315. 10.1002/joc.5086 DOI
Gárate‐Escamilla, H. , Hampe, A. , Vizcaíno‐Palomar, N. , Robson, T. M. , & Benito Garzón, M. (2019). Range‐wide variation in local adaptation and phenotypic plasticity of fitness‐related traits in Fagus sylvatica and their implications under climate change. Global Ecology and Biogeography, 28(9), 1336–1350. 10.1111/geb.12936 DOI
Grinnell, J. (1914). An account of the mammals and birds of the lower Colorado Valley: With especial reference to the distributional problems presented (classic reprint). Fb&c Limited.
Gryndler, M. , Černá, L. , Bukovská, P. , Hršelová, H. , & Jansa, J. (2014). Tuber aestivum association with non‐host roots. Mycorrhiza, 24(8), 603–610. 10.1007/s00572-014-0580-9 PubMed DOI
Guidot, A. , Debaud, J.‐C. , Effosse, A. , & Marmeisse, R. (2004). Below‐ground distribution and persistence of an ectomycorrhizal fungus. New Phytologist, 161(2), 539–547. 10.1046/j.1469-8137.2003.00945.x PubMed DOI
Hagedorn, F. , Joseph, J. , Peter, M. , Luster, J. , Pritsch, K. , Geppert, U. , Kerner, R. , Molinier, V. , Egli, S. , Schaub, M. , Liu, J.‐F. , Li, M. , Sever, K. , Weiler, M. , Siegwolf, R. T. W. , Gessler, A. , & Arend, M. (2016). Recovery of trees from drought depends on belowground sink control. Nature Plants, 2(8), 1–5. 10.1038/nplants.2016.111 PubMed DOI
Harrison, P. A. , Berry, P. M. , Butt, N. , & New, M. (2006). Modelling climate change impacts on species' distributions at the European scale: Implications for conservation policy. Environmental Science and Policy, 9(2), 116–128. 10.1016/j.envsci.2005.11.003 DOI
Hersbach, H. , Bell, B. , Berrisford, P. , Hirahara, S. , Horányi, A. , Muñoz‐Sabater, J. , Nicolas, J. , Peubey, C. , Radu, R. , Schepers, D. , Simmons, A. , Soci, C. , Abdalla, S. , Abellan, X. , Balsamo, G. , Bechtold, P. , Biavati, G. , Bidlot, J. , Bonavita, M. , … Thépaut, J.‐N. (2020). The ERA5 global reanalysis. Quarterly Journal of the Royal Meteorological Society, 146(730), 1999–2049. 10.1002/qj.3803 DOI
Hilszczańska, D. , Szmidla, H. , Sikora, K. , & Rosa‐Gruszecka, A. (2019). Soil properties conducive to the formation of Tuber aestivum Vitt. Fruiting bodies. Polish Journal of Environmental Studies, 28(3), 1713–1718. 10.15244/pjoes/89588 DOI
Hutchinson, G. E. (1959). Homage to Santa Rosalia or why are there so many kinds of animals? The American Naturalist, 93(870), 145–159. 10.1086/282070 DOI
Joseph, J. , Gao, D. , Backes, B. , Bloch, C. , Brunner, I. , Gleixner, G. , Haeni, M. , Hartmann, H. , Hoch, G. , Hug, C. , Kahmen, A. , Lehmann, M. M. , Li, M.‐H. , Luster, J. , Peter, M. , Poll, C. , Rigling, A. , Rissanen, K. A. , Ruehr, N. K. , … Gessler, A. (2020). Rhizosphere activity in an old‐growth forest reacts rapidly to changes in soil moisture and shapes whole‐tree carbon allocation. Proceedings of the National Academy of Sciences of the United States of America, 117(40), 24885–24892. 10.1073/pnas.2014084117 PubMed DOI PMC
Kane, K. , Debinski, D. M. , Anderson, C. , Scasta, J. D. , Engle, D. M. , & Miller, J. R. (2017). Using regional climate projections to guide grassland community restoration in the face of climate change. Frontiers in Plant Science, 8, 1–11. https://www.frontiersin.org/article/10.3389/fpls.2017.00730 PubMed DOI PMC
Kaspari, M. , Clay, N. A. , Lucas, J. , Yanoviak, S. P. , & Kay, A. (2015). Thermal adaptation generates a diversity of thermal limits in a rainforest ant community. Global Change Biology, 21(3), 1092–1102. 10.1111/gcb.12750 PubMed DOI
Kelly, M. W. , Sanford, E. , & Grosberg, R. K. (2012). Limited potential for adaptation to climate change in a broadly distributed marine crustacean. Proceedings of the Royal Society B: Biological Sciences, 279(1727), 349–356. 10.1098/rspb.2011.0542 PubMed DOI PMC
Knutzen, F. , Dulamsuren, C. , Meier, I. C. , & Leuschner, C. (2017). Recent climate warming‐related growth decline impairs European beech in the center of its distribution range. Ecosystems, 20(8), 1494–1511. 10.1007/s10021-017-0128-x DOI
Lenoir, J. , & Svenning, J.‐C. (2015). Climate‐related range shifts–A global multidimensional synthesis and new research directions. Ecography, 38(1), 15–28. 10.1111/ecog.00967 DOI
Leonardi, P. , Iotti, M. , Donati Zeppa, S. , Lancellotti, E. , Amicucci, A. , & Zambonelli, A. (2017). Morphological and functional changes in mycelium and mycorrhizas of Tuber borchii due to heat stress. Fungal Ecology, 29, 20–29. 10.1016/j.funeco.2017.05.003 DOI
Lian, C. , Narimatsu, M. , Nara, K. , & Hogetsu, T. (2006). Tricholoma matsutake in a natural Pinus densiflora forest: Correspondence between above‐ and below‐ground genets, association with multiple host trees and alteration of existing ectomycorrhizal communities. New Phytologist, 171(4), 825–836. 10.1111/j.1469-8137.2006.01801.x PubMed DOI
Liaw, A. , & Wiener, M. (2002). Classification and regression by randomForest. R News, 2(3), 18–22.
Matsuki, K. , Kuperman, V. , & Dyke, J. A. V. (2016). The random forests statistical technique: An examination of its value for the study of reading. Scientific Studies of Reading, 20(1), 20–33. 10.1080/10888438.2015.1107073 PubMed DOI PMC
McDowell, N. G. (2011). Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology, 155(3), 1051–1059. 10.1104/pp.110.170704 PubMed DOI PMC
Molinier, V. , Murat, C. , Baltensweiler, A. , Büntgen, U. , Martin, F. , Meier, B. , Moser, B. , Sproll, L. , Stobbe, U. , Tegel, W. , Egli, S. , & Peter, M. (2016). Fine‐scale genetic structure of natural Tuber aestivum sites in southern Germany. Mycorrhiza, 26(8), 895–907. 10.1007/s00572-016-0719-y PubMed DOI
Molinier, V. , Peter, M. , Stobbe, U. , & Egli, S. (2016). The Burgundy truffle (Tuber aestivum syn. Uncinatum): A truffle species with a wide habitat range over Europe. In Zambonelli A., Iotti M., & Murat C. (Eds.), True truffle (tuber spp.) in the world: Soil ecology, systematics and biochemistry (pp. 33–47). Springer International Publishing. 10.1007/978-3-319-31436-5_3 DOI
Murat, C. , Vizzini, A. , Bonfante, P. , & Mello, A. (2005). Morphological and molecular typing of the below‐ground fungal community in a natural tuber magnatum truffle‐ground. FEMS Microbiology Letters, 245(2), 307–313. 10.1016/j.femsle.2005.03.019 PubMed DOI
Nadeau, C. P. , Urban, M. C. , & Bridle, J. R. (2017). Climates past, present, and yet‐to‐come shape climate change vulnerabilities. Trends in Ecology and Evolution, 32(10), 786–800. 10.1016/j.tree.2017.07.012 PubMed DOI
Ovaskainen, O. , Schigel, D. , Ali‐Kovero, H. , Auvinen, P. , Paulin, L. , Nordén, B. , & Nordén, J. (2013). Combining high‐throughput sequencing with fruit body surveys reveals contrasting life‐history strategies in fungi. The ISME Journal, 7(9), 1696–1709. 10.1038/ismej.2013.61 PubMed DOI PMC
Pearson, R. G. , & Dawson, T. P. (2003). Predicting the impacts of climate change on the distribution of species: Are bioclimate envelope models useful? Global Ecology and Biogeography, 12(5), 361–371. 10.1046/j.1466-822X.2003.00042.x DOI
Piñuela, Y. , Alday, J. G. , Oliach, D. , Castaño, C. , Bolaño, F. , Colinas, C. , & Bonet, J. A. (2021). White mulch and irrigation increase black truffle soil mycelium when competing with summer truffle in young truffle orchards. Mycorrhiza, 31(3), 371–382. 10.1007/s00572-020-01018-x PubMed DOI
Prober, S. , Byrne, M. , McLean, E. , Steane, D. , Potts, B. , Vaillancourt, R. , & Stock, W. (2015). Climate‐adjusted provenancing: A strategy for climate‐resilient ecological restoration. Frontiers in Ecology and Evolution, 3, 1–5. 10.3389/fevo.2015.00065 DOI
Pucko, C. , Beckage, B. , Perkins, T. , & Keeton, W. S. (2011). Species shifts in response to climate change: Individual or shared responses? 1, 2. The Journal of the Torrey Botanical Society, 138(2), 156–176. 10.3159/TORREY-D-10-00011.1 DOI
Reich, P. B. , Sendall, K. M. , Rice, K. , Rich, R. L. , Stefanski, A. , Hobbie, S. E. , & Montgomery, R. A. (2015). Geographic range predicts photosynthetic and growth response to warming in co‐occurring tree species. Nature Climate Change, 5(2), 148–152. 10.1038/nclimate2497 DOI
Reyna, S. , & Garcia‐Barreda, S. (2014). Black truffle cultivation: A global reality. Forest Systems, 23(2), 317–328. 10.5424/fs/2014232-04771 DOI
Reyna‐Domenech, S. , & García‐Barreda, S. (2009). European black truffle: Its potential role in agroforestry development in the marginal lands of Mediterranean Calcareous Mountains. In Rigueiro‐Rodróguez A., McAdam J., & Mosquera‐Losada M. R. (Eds.), Agroforestry in Europe: Current status and future prospects (pp. 295–317). Springer Netherlands. 10.1007/978-1-4020-8272-6_14 DOI
Robin, C. , Goutal‐Pousse, N. , & Le Tacon, F. (2016). Soil characteristics for Tuber aestivum (syn. T. uncinatum). In Zambonelli A., Iotti M., & Murat C. (Eds.), True truffle (tuber spp.) in the world: Soil ecology, systematics and biochemistry (pp. 211–231). Springer International Publishing. 10.1007/978-3-319-31436-5_13 DOI
RStudio Team . (2022). RStudio: Integrated development environment for R. RStudio, PBC. http://www.rstudio.com/
Sánchez, S. , de Miguel, A. M. , Sáez, R. , Martín‐Santafé, M. , Águeda, B. , Barriuso, J. , García‐Barreda, S. , Salvador‐Alcalde, D. , & Reyna, S. (2016). Summer truffle in the Iberian Peninsula: Current status and crop potential. ITEA, 112(1), 20–33.
Schneider‐Maunoury, L. , Taschen, E. , Richard, F. , & Selosse, M.‐A. (2019). Soil spore bank in tuber melanosporum: Up to 42% of fruitbodies remain unremoved in managed truffle grounds. Mycorrhiza, 29(6), 663–668. 10.1007/s00572-019-00912-3 PubMed DOI
Selosse, M.‐A. , Schneider‐Maunoury, L. , Taschen, E. , Rousset, F. , & Richard, F. (2017). Black truffle, a hermaphrodite with forced unisexual behaviour. Trends in Microbiology, 25(10), 784–787. 10.1016/j.tim.2017.05.010 PubMed DOI
Soberón, J. , & Nakamura, M. (2009). Niches and distributional areas: Concepts, methods, and assumptions. Proceedings of the National Academy of Sciences of the United States of America, 106(Suppl 2), 19644–19650. 10.1073/pnas.0901637106 PubMed DOI PMC
Somero, G. N. (2010). The physiology of climate change: How potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. Journal of Experimental Biology, 213(6), 912–920. 10.1242/jeb.037473 PubMed DOI
Steidinger, B. , & Peter, M. (2022). Data from: The fall of the summer truffle: Recurring hot, dry summers result in declining fruitbody production of Tuber aestivum in Central Europe. Dryad. 10.5061/dryad.zs7h44jd3 PubMed DOI PMC
Steinbauer, M. J. , Grytnes, J.‐A. , Jurasinski, G. , Kulonen, A. , Lenoir, J. , Pauli, H. , Rixen, C. , Winkler, M. , Bardy‐Durchhalter, M. , Barni, E. , Bjorkman, A. D. , Breiner, F. T. , Burg, S. , Czortek, P. , Dawes, M. A. , Delimat, A. , Dullinger, S. , Erschbamer, B. , Felde, V. A. , … Wipf, S. (2018). Accelerated increase in plant species richness on mountain summits is linked to warming. Nature, 556(7700), 231–234. 10.1038/s41586-018-0005-6 PubMed DOI
Stobbe, U. , Büntgen, U. , Sproll, L. , Tegel, W. , Egli, S. , & Fink, S. (2012). Spatial distribution and ecological variation of re‐discovered German truffle habitats. Fungal Ecology, 5(5), 591–599. 10.1016/j.funeco.2012.02.001 DOI
Stobbe, U. , Egli, S. , Tegel, W. , Peter, M. , Sproll, L. , & Büntgen, U. (2013). Potential and limitations of Burgundy truffle cultivation. Applied Microbiology and Biotechnology, 97(12), 5215–5224. 10.1007/s00253-013-4956-0 PubMed DOI
Stott, P. A. , Stone, D. A. , & Allen, M. R. (2004). Human contribution to the European heatwave of 2003. Nature, 432(7017), 610–614. 10.1038/nature03089 PubMed DOI
Streiblová, E. , Gryndlerová, H. , & Gryndler, M. (2012). Truffle brûlé: An efficient fungal life strategy. FEMS Microbiology Ecology, 80(1), 1–8. 10.1111/j.1574-6941.2011.01283.x PubMed DOI
Strobl, C. , Malley, J. , & Tutz, G. (2009). An introduction to recursive partitioning: Rationale, application, and characteristics of classification and regression trees, bagging, and random forests. Psychological Methods, 14(4), 323–348. 10.1037/a0016973 PubMed DOI PMC
Suz, L. M. , Martín, M. P. , Oliach, D. , Fischer, C. R. , & Colinas, C. (2008). Mycelial abundance and other factors related to truffle productivity in tuber melanosporum–Quercus ilex orchards. FEMS Microbiology Letters, 285(1), 72–78. 10.1111/j.1574-6968.2008.01213.x PubMed DOI
Tacon, F. L. , Zeller, B. , Plain, C. , Hossann, C. , Bréchet, C. , & Robin, C. (2013). Carbon transfer from the host to tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse‐labeling technique. PLoS ONE, 8(5), e64626. 10.1371/journal.pone.0064626 PubMed DOI PMC
Taschen, E. , Sauve, M. , Vincent, B. , Parladé, J. , van Tuinen, D. , Aumeeruddy‐Thomas, Y. , Assenat, B. , Selosse, M.‐A. , & Richard, F. (2020). Insight into the truffle brûlé: Tripartite interactions between the black truffle (Tuber melanosporum), holm oak (Quercus ilex) and arbuscular mycorrhizal plants. Plant and Soil, 446(1), 577–594. 10.1007/s11104-019-04340-2 DOI
Thomas, C. D. , Cameron, A. , Green, R. E. , Bakkenes, M. , Beaumont, L. J. , Collingham, Y. C. , Erasmus, B. F. N. , de Siqueira, M. F. , Grainger, A. , Hannah, L. , Hughes, L. , Huntley, B. , van Jaarsveld, A. S. , Midgley, G. F. , Miles, L. , Ortega‐Huerta, M. A. , Townsend Peterson, A. , Phillips, O. L. , & Williams, S. E. (2004). Extinction risk from climate change. Nature, 427(6970), 145–148. 10.1038/nature02121 PubMed DOI
Todesco, F. , Belmondo, S. , Guignet, Y. , Laurent, L. , Fizzala, S. , Le Tacon, F. , & Murat, C. (2019). Soil temperature and hydric potential influences the monthly variations of soil Tuber aestivum DNA in a highly productive orchard. Scientific Reports, 9(1), 12964. 10.1038/s41598-019-49602-2 PubMed DOI PMC
Wedén, C. , Danell, E. , & Tibell, L. (2005). Species recognition in the truffle genus tuber–The synonyms Tuber aestivum and tuber uncinatum. Environmental Microbiology, 7(10), 1535–1546. 10.1111/j.1462-2920.2005.00837.x PubMed DOI
Welling, S. H. , Refsgaard, H. H. F. , Brockhoff, P. B. , & Clemmensen, L. H. (2016). Forest floor visualizations of random forests. ArXiv:1605.09196 [cs, stat], 1–25. http://arxiv.org/abs/1605.09196
Zampieri, E. , Mello, A. , Bonfante, P. , & Murat, C. (2009). PCR primers specific for the genus tuber reveal the presence of several truffle species in a truffle‐ground. FEMS Microbiology Letters, 297(1), 67–72. 10.1111/j.1574-6968.2009.01655.x PubMed DOI
Zhou, Z. , Miwa, M. , Matsuda, Y. , & Hogetsu, T. (2001). Spatial distribution of the subterranean mycelia and Ectomycorrhizae of Suillus grevillei genets. Journal of Plant Research, 114(2), 179–185. 10.1007/PL00013981 DOI
Zizka, A. , Silvestro, D. , Andermann, T. , Azevedo, J. , Duarte Ritter, C. , Edler, D. , Farooq, H. , Herdean, A. , Ariza, M. , Scharn, R. , Svantesson, S. , Wengström, N. , Zizka, V. , & Antonelli, A. (2019). CoordinateCleaner: Standardized cleaning of occurrence records from biological collection databases. Methods in Ecology and Evolution, 10(5), 744–751. 10.1111/2041-210X.13152 DOI
Zweifel, R. , Haeni, M. , Buchmann, N. , & Eugster, W. (2016). Are trees able to grow in periods of stem shrinkage? New Phytologist, 211(3), 839–849. 10.1111/nph.13995 PubMed DOI
Zweifel, R. , Sterck, F. , Braun, S. , Buchmann, N. , Eugster, W. , Gessler, A. , Häni, M. , Peters, R. L. , Walthert, L. , Wilhelm, M. , Ziemińska, K. , & Etzold, S. (2021). Why trees grow at night. New Phytologist, 231(6), 2174–2185. 10.1111/nph.17552 PubMed DOI PMC
Zweifel, R. , Zimmermann, L. , & Newbery, D. M. (2005). Modeling tree water deficit from microclimate: An approach to quantifying drought stress. Tree Physiology, 25(2), 147–156. 10.1093/treephys/25.2.147 PubMed DOI