Shoot senescence in herbaceous perennials of the temperate zone: Identifying drivers of senescence pace and shape
Tereza Mašková
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Ecology and Conservation Biology, Institute of Plant Sciences, University of Regensburg, Regensburg, Germany
Search for more papers by this authorCorresponding Author
Tomáš Herben
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Institute of Botany, Academy of Science of the Czech Republic, Průhonice, Czech Republic
Correspondence
Tomáš Herben
Email: [email protected]
Search for more papers by this authorKristýna Hošková
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Search for more papers by this authorTomáš Koubek
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Search for more papers by this authorTereza Mašková
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Ecology and Conservation Biology, Institute of Plant Sciences, University of Regensburg, Regensburg, Germany
Search for more papers by this authorCorresponding Author
Tomáš Herben
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Institute of Botany, Academy of Science of the Czech Republic, Průhonice, Czech Republic
Correspondence
Tomáš Herben
Email: [email protected]
Search for more papers by this authorKristýna Hošková
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Search for more papers by this authorTomáš Koubek
Department of Botany, Faculty of Science, Charles University, Praha 2, Czech Republic
Search for more papers by this authorHandling Editor: Richard P. Shefferson
Abstract
- Perennial herbaceous species form their above-ground parts every year anew and discard them before the advent of winter. The senescence of above-ground structures is thus an inevitable part of their life cycle. This is also a key process that determines photosynthetic gain late in the season and the economy of soil-borne nutrients.
- Here we address patterns and drivers of the shoot senescence of perennial herbaceous plants. We present a comparative study of 231 temperate species, ranging from spring ephemeroids to species senescing in late autumn, in a common botanical garden collection. We assessed senescence by measuring size decline in the autumn part of the season.
- There were two main directions of variation in senescence trajectories: the pace–date axis, separating early and fast senescing species from late and slowly senescing species, and the shape-asynchrony axis, separating species with accelerating and synchronised senescence from constant senescence asynchronous among individual shoots. While accelerating senescence late in the season can be due to passive effects of the environment (e.g. frost), accelerating senescence early in the season is likely to be an indication of an active process driven by the enzymatic activity of the plant.
- The pace and shape of shoot senescence were associated with both leaf- and shoot-level traits. Species having leaves with high dry matter content senesced linearly and with higher asynchrony. Species with a larger specific leaf area senesced earlier and faster, while tall plants and plants with monocyclic shoots senesced later and in a more synchronous and accelerating manner.
- Species from different habitats varied in their senescence patterns. Forest species postpone their senescence relative to open-habitat species, presumably to boost their photosynthetic balance. We did not confirm the hypothesis that plants from nutrient-poor habitats senesce earlier to retain soil-borne nutrients before the winter.
- Synthesis. Shoot senescence in herbaceous plants is a neglected phenomenon in its own right, which bears only superficial similarity to autumn leaf shedding in trees. Individual species differ strongly in the pace, shape and synchrony of their senescence trajectories, with a potential bearing on the carbon and nutrient dynamics of their habitats.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
Open Research
PEER REVIEW
The peer review history for this article is available at https://publons.com/publon/10.1111/1365-2745.13870.
DATA AVAILABILITY STATEMENT
Data on species senescence trajectories are available from the Dryad Digital Repository https://doi.org/10.5061/dryad.fbg79cnwt (Mašková et al., 2022). All other data are from public sources.
Supporting Information
Filename | Description |
---|---|
jec13870-sup-0001-Appendices.docxWord 2007 document , 187.9 KB | Appendices |
jec13870-sup-0002-Appendix_S5.pdfPDF document, 775.8 KB | Appendix_S5 |
jec13870-sup-0003-Table_S1.txtplain text document, 12.1 KB | Table_S1 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Augspurger, C., Cheeseman, J., & Salk, C. (2005). Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Functional Ecology, 19(4), 537–546. https://doi.org/10.1111/j.1365-2435.2005.01027.x
- Balazadeh, S., Parlitz, S., Mueller-Roeber, B., & Meyer, R. C. (2008). Natural developmental variations in leaf and plant senescence in Arabidopsis thaliana. Plant Biology, 10(Suppl. 1), 136–147. https://doi.org/10.1111/j.1438-8677.2008.00108.x
- Bartoń, K. (2020). MuMIn: Multi-model inference. R package version 1.43.17. Retrieved from https://CRAN.R-project.org/package=MuMIn
- Baudisch, A., Salguero-Gómez, R., Jones, O. R., Wrycza, T., Mbeau-Ache, C., Franco, M., & Colchero, F. (2013). The pace and shape of senescence in angiosperms. Journal of Ecology, 101(3), 596–606. https://doi.org/10.1111/1365-2745.12084
- Beaulieu, J. M., Leitch, I. J., Patel, S., Pendharkar, A., & Knight, C. A. (2008). Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist, 179(4), 975–986. https://doi.org/10.1111/j.1469-8137.2008.02528.x
- Bennett, M. (1987). Variation in genomic form in plants and its ecological implications. New Phytologist, 106, 177–200. https://doi.org/10.1111/j.1469-8137.1987.tb04689.x
- Bucher, S. F., & Römermann, C. (2021). The timing of leaf senescence relates to flowering phenology and functional traits in 17 herbaceous species along elevational gradients. Journal of Ecology, 109(3), 1537–1548. https://doi.org/10.1111/1365-2745.13577
- Burns, J. H., & Strauss, S. Y. (2012). Effects of competition on phylogenetic signal and phenotypic plasticity in plant functional traits. Ecology, 93(8 SPEC. ISSUE), 126–137. https://doi.org/10.1890/11-0401.1
- Caswell, H., & Salguero-Gómez, R. (2013). Age, stage and senescence in plants. Journal of Ecology, 101(3), 585–595. https://doi.org/10.1111/1365-2745.12088
- Chytrý, M., Danihelka, J., Kaplan, Z., Wild, J., Holubová, D., Novotný, P., Řezníčková, M., Rohn, M., Dřevojan, P., Grulich, V., Klimešová, J., Lepš, J., Lososová, Z., Pergl, J., Sádlo, J., Šmarda, P., Štěpánková, P., Tichý, L., Axmanová, I., … Pyšek, P. (2021). Pladias database of the Czech flora and vegetation. Preslia, 93(1), 1–87. https://doi.org/10.23855/preslia.2021.001
- Damgaard, C., Weiner, J., & Nagashima, H. (2002). Modelling individual growth and competition in plant populations: Growth curves of Chenopodium album at two densities. Journal of Ecology, 90(4), 666–671. https://doi.org/10.1046/j.1365-2745.2002.00700.x
- Díaz, S., Kattge, J., Cornelissen, J. H. C., Wright, I. J., Lavorel, S., Dray, S., Reu, B., Kleyer, M., Wirth, C., Prentice, I. C., Garnier, E., Bönisch, G., Westoby, M., Poorter, H., Reich, P. B., Moles, A. T., Dickie, J., Gillison, A. N., Zanne, A. E., … Gorné, L. D. (2015). The global spectrum of plant form and function. Nature, 529(7585), 1–17. https://doi.org/10.1038/nature16489
- Diekmann, M. (2003). Species indicator values as an important tool in applied plant ecology—A review. Basic and Applied Ecology, 4(6), 493–506. https://doi.org/10.1078/1439-1791-00185
- Ellenberg, H., Weber, H. E., Duell, R., Wirth, W., Werner, W., & Paulissen, D. (1992). Zeigerwerte von Pflanzen in Mitteleuropa. In Scripta Geobotanica (Vol. 18, pp. 1–258). Erich Goltze.
- Estiarte, M., & Peñuelas, J. (2015). Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: Efects on nutrient proficiency. Global Change Biology, 21(3), 1005–1017. https://doi.org/10.1111/gcb.12804
- Fitzjohn, R. G., Pennell, M. W., Zanne, A. E., Stevens, P. F., Tank, D. C., & Cornwell, W. K. (2014). How much of the world is woody? Journal of Ecology, 102(5), 1266–1272. https://doi.org/10.1111/1365-2745.12260
- Francis, D., Davies, M. S., & Barlow, P. W. (2008). A strong nucleotypic effect on the cell cycle regardless of ploidy level. Annals of Botany, 101(6), 747–757. https://doi.org/10.1093/aob/mcn038
- Fridley, J. D. (2012). Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature, 485(7398), 359–362. https://doi.org/10.1038/nature11056
- Fu, Y. H., Piao, S., Delpierre, N., Hao, F., Hänninen, H., Liu, Y., Sun, W., Janssens, I. A., & Campioli, M. (2018). Larger temperature response of autumn leaf senescence than spring leaf-out phenology. Global Change Biology, 24(5), 2159–2168. https://doi.org/10.1111/gcb.14021
- Gaillard, J. M., & Lemaître, J. F. (2020). An integrative view of senescence in nature. Functional Ecology, 34(1), 4–16. https://doi.org/10.1111/1365-2435.13506
- Gallinat, A. S., Primack, R. B., & Wagner, D. L. (2015). Autumn, the neglected season in climate change research. Trends in Ecology & Evolution, 30(3), 169–176. https://doi.org/10.1016/j.tree.2015.01.004
- Gerdol, R., Iacumin, P., & Brancaleoni, L. (2019). Differential effects of soil chemistry on the foliar resorption of nitrogen and phosphorus across altitudinal gradients. Functional Ecology, 33(7), 1351–1361. https://doi.org/10.1111/1365-2435.13327
- Gregersen, P. L., Holm, P. B., & Krupinska, K. (2008). Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biology, 10(Suppl. 1), 37–49. https://doi.org/10.1111/j.1438-8677.2008.00114.x
- Grime, J. P., Thompson, K., Hunt, R., Hodgson, J. G., Cornelissen, J. H. C., Rorison, I. H., Hendry, G. A. F., Ashenden, T. W., Askew, A. P., Band, S. R., Booth, R. E., Bossard, C. C., Campbell, B. D., Cooper, J. E. L., Davison, A. W., Gupta, P. L., Hall, W., Hand, D. W., Hannah, M. A., … Whitehouse, J. (1997). Integrated screening validates primary axes of specialisation in plants. Oikos, 79(2), 259–281. https://doi.org/10.2307/3546011
- Großkinsky, D. K., Syaifullah, S. J., & Roitsch, T. (2018). Integration of multi-omics techniques and physiological phenotyping within a holistic phenomics approach to study senescence in model and crop plants. Journal of Experimental Botany, 69(4), 825–844. https://doi.org/10.1093/jxb/erx333
- Herben, T., Chytrý, M., & Klimešová, J. (2016). A quest for species-level indicator values for disturbance. Journal of Vegetation Science, 27(3), 628–636. https://doi.org/10.1111/jvs.12384
- Herben, T., Klimešová, J., & Chytrý, M. (2018). Philip Grime's fourth corner: Are there plant species adapted to high disturbance and low productivity? Oikos, 127(8), 1125–1131. https://doi.org/10.1111/oik.05090
- Hilty, J., Muller, B., Pantin, F., & Leuzinger, S. (2021). Plant growth: The what, the how, and the why. New Phytologist, 232, 25–41. https://doi.org/10.1111/nph.17610
- Huang, L., Koubek, T., Weiser, M., & Herben, T. (2018). Environmental drivers and phylogenetic constraints of growth phenologies across a large set of herbaceous species. Journal of Ecology, 106(4), 1621–1633. https://doi.org/10.1111/1365-2745.12927
- Huang, L., Xue, W., & Herben, T. (2019). Temporal niche differentiation among species changes with habitat productivity and light conditions. Journal of Vegetation Science, July 2018, 1–10. https://doi.org/10.1111/jvs.12741
- Killingbeck, K. T. (1996). Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency. Ecology, 77(6), 1716–1727. https://doi.org/10.2307/2265777
- Kim, J., Kim, J. H., Lyu, J. I., Woo, H. R., & Lim, P. O. (2018). New insights into the regulation of leaf senescence in Arabidopsis. Journal of Experimental Botany, 69(4), 787–799. https://doi.org/10.1093/jxb/erx287
- Kim, J., Woo, H. R. R., & Nam, H. G. G. (2016). Toward systems understanding of leaf senescence: An integrated multi-omics perspective on leaf senescence research. Molecular Plant, 9(6), 813–825. https://doi.org/10.1016/j.molp.2016.04.017
- Kleyer, M., Bekker, R. M., Knevel, I. C., Bakker, J. P., Thompson, K., Sonnenschein, M., Poschlod, P., Van Groenendael, J. M., Klimeš, L., Klimešová, J., Klotz, S., Rusch, G. M., Hermy, M., Adriaens, D., Boedeltje, G., Bossuyt, B., Dannemann, A., Endels, P., Götzenberger, L., … Peco, B. (2008). The LEDA Traitbase: A database of life-history traits of the Northwest European flora. Journal of Ecology, 96(6), 1266–1274. https://doi.org/10.1111/j.1365-2745.2008.01430.x
- Klimeš, A., Klimešová, L., Bartušková, A., & Klimešová, J. (2020). Climbing strategy in herbs does not necessarily lead to lower investments into stem biomass. Plant Ecology, 221(11), 1159–1166. https://doi.org/10.1007/s11258-020-01070-9
- Klimešová, J., Danihelka, J., Chrtek, J., de Bello, F., & Herben, T. (2017). CLO-PLA: A database of clonal and bud-bank traits of the central European flora. Ecology, 98(4), 1179. https://doi.org/10.1002/ecy.1745
- Klimešová, J., Nobis, M. P., & Herben, T. (2015). Senescence, ageing and death of the whole plant: Morphological prerequisites and constraints of plant immortality. New Phytologist, 206(1), 14–18. https://doi.org/10.1111/nph.13160
- Klimešová, J., Nobis, M. P., & Herben, T. (2016). Links between shoot and plant longevity and plant economics spectrum: Environmental and demographic implications. Perspectives in Plant Ecology, Evolution and Systematics, 22, 55–62. https://doi.org/10.1016/j.ppees.2016.09.002
- Krupinska, K., & Humbeck, K. (2008). Senescence processes and their regulation. Plant Biology, 10(Suppl. 1), 1–3. https://doi.org/10.1111/j.1438-8677.2008.00116.x
- Levey, S., & Wingler, A. (2005). Natural variation in the regulation of leaf senescence and relation to other traits in Arabidopsis. Plant, Cell and Environment, 28(2), 223–231. https://doi.org/10.1111/j.1365-3040.2004.01266.x
- Lim, P., Kim, H., & Nam, H. (2007). Leaf senescence. Annual Review of Plant Biology, 58, 115–136. https://doi.org/10.1146/annurev.arplant.57.032905.105316
- Makoto, K., Wilson, S. D., Sato, T., Blume-Werry, G., & Cornelissen, J. H. C. (2020). Synchronous and asynchronous root and shoot phenology in temperate woody seedlings. Oikos, 129, 643–650.
- Mašková, T., Herben, T., Hošková, K., & Koubek, T. (2022). Data from: Shoot senescence in herbaceous perennials of the temperate zone: Identifying drivers of senescence pace and shape. Dryad Digital Repository, https://doi.org/10.5061/dryad.fbg79cnwt
- Medan, D., & Bartoloni, N. (1998). Fecundity effects of dichogamy in an asynchronically flowering population: A genetic model. Annals of Botany, 81, 373–383.
- Niklas, K. J. (1994). Plant allometry: The scaling of form and process. Cornell University.
- O'Connell, E., & Savage, J. (2020). Extended leaf phenology has limited benefits for invasive species growing at northern latitudes. Biological Invasions, 22(10), 2957–2974. https://doi.org/10.1007/s10530-020-02301-w
- Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. (2020). Vegan: Community ecology package. R package version 2.5-7. Retrieved from https://CRAN.R-project.org/package=vegan
- Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., & Pearse, W. (2018). Caper: Comparative analyses of phylogenetics and evolution in R. R package version 1.0.1. Retrieved from https://CRAN.R-project.org/package=caper
- Panchen, Z. A., Primack, R. B., Nordt, B., Ellwood, E. R., Stevens, A. D., Renner, S. S., Willis, C. G., Fahey, R., Whittemore, A., Du, Y., & Davis, C. C. (2014). Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. New Phytologist, 203(4), 1208–1219. https://doi.org/10.1111/nph.12892
- Panchen, Z. A., Primack, R. B., Gallinat, A. S., Nordt, B., Stevens, A. D., Du, Y., & Fahey, R. (2015). Substantial variation in leaf senescence times among 1360 temperate woody plant species: Implications for phenology and ecosystem processes. Annals of Botany, 116(6), 865–873. https://doi.org/10.1093/aob/mcv015
- Penner, S., Dror, B., Aviezer, I., Bar-Lev, Y., Salman-Minkov, A., Mandakova, T., … Sapir, Y. (2020). Phenology and polyploidy in annual Brachypodium species (Poaceae) along the aridity gradient in Israel. Journal of Systematics and Evolution, 58(2), 189–199. https://doi.org/10.1111/jse.12489
- R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
- Rawlik, M., & Jagodziński, A. M. (2020). Seasonal dynamics of shoot biomass of dominant clonal herb species in an oak–hornbeam forest herb layer. Plant Ecology, 221(11), 1133–1142. https://doi.org/10.1007/s11258-020-01067-4
- Roach, D. A., & Smith, E. F. (2020). Life-history trade-offs and senescence in plants. Functional Ecology, 34(1), 17–25. https://doi.org/10.1111/1365-2435.13461
- Salguero-Gómez, R. (2018). Implications of clonality for ageing research. Evolutionary Ecology, 32(1), 9–28. https://doi.org/10.1007/s10682-017-9923-2
- Salguero-Gómez, R., Shefferson, R. P., & Hutchings, M. J. (2013). Plants do not count… Or do they? New perspectives on the universality of senescence. Journal of Ecology, 101(3), 545–554. https://doi.org/10.1111/1365-2745.12089.
- Schaffers, A. P., & Sýkora, K. V. (2000). Reliability of Ellenberg indicator values for moisture, nitrogen and soil reaction: A comparison with field measurements. Journal of Vegetation Science, 11(2), 225–244. https://doi.org/10.2307/3236802
- Schildhauer, J., Wiedemuth, K., & Humbeck, K. (2008). Supply of nitrogen can reverse senescence processes and affect expression of genes coding for plastidic glutamine synthetase and lysine-ketoglutarate reductase/saccharopine dehydrogenase. Plant Biology, 10(Suppl. 1), 76–84. https://doi.org/10.1111/j.1438-8677.2008.00075.x
- Schnablová, R., Huang, L., Klimešová, J., Šmarda, P., & Herben, T. (2021). Inflorescence preformation prior to winter: A surprisingly widespread strategy that drives phenology of temperate perennial herbs. New Phytologist, 229(1), 620–630. https://doi.org/10.1111/nph.16880
- Shefferson, R. P., & Roach, D. A. (2013). Longitudinal analysis in Plantago: Strength of selection and reverse age analysis reveal age-indeterminate senescence. Journal of Ecology, 101(3), 577–584. https://doi.org/10.1111/1365-2745.12079
- Shi, C., Silva, L. C. R., Zhang, H., Zheng, Q., Xiao, B., Wu, N., & Sun, G. (2015). Climate warming alters nitrogen dynamics and total non-structural carbohydrate accumulations of perennial herbs of distinctive functional groups during the plant senescence in autumn in an alpine meadow of the Tibetan plateau, China. Agricultural and Forest Meteorology, 200, 21–29. https://doi.org/10.1016/j.agrformet.2014.09.006
- Šmarda, P., Hejcman, M., Březinová, A., Horová, L., Steigerová, H., Zedek, F., Bureš, P., Hejcmanová, P., & Schellberg, J. (2013). Effect of phosphorus availability on the selection of species with different ploidy levels and genome sizes in a long-term grassland fertilization experiment. New Phytologist, 200, 911–921.
- Šmarda, P., Knápek, O., Březinová, A., Horová, L., Grulich, V., Danihelka, J., Veselý, P., Šmerda, J., Rotreklová, O., & Bureš, P. (2019). Genome sizes and genomic guanine+cytosine (GC) contents of the Czech vascular flora with new estimates for 1700 species. Preslia, 91(2), 117–142. https://doi.org/10.23855/preslia.2019.117
- Smith, L., Primack, R. B., Zipf, L., Pardo, S., Gallinat, A. S., & Panchen, Z. A. (2019). Leaf longevity in temperate evergreen species is related to phylogeny and leaf size. Oecologia, 191(3), 483–491. https://doi.org/10.1007/s00442-019-04492-z
- Sun, S., & Frelich, L. E. (2011). Flowering phenology and height growth pattern are associated with maximum plant height, relative growth rate and stem tissue mass density in herbaceous grassland species. Journal of Ecology, 99, 991–1000. https://doi.org/10.1111/j.1365-2745.2011.01830.x
- Swenson, N. G., & Enquist, B. J. (2009). Opposing assembly mechanisms in a neotropical dry forest: Implications for phylogenetic and functional community ecology. Ecology, 90(8), 2161–2170. https://doi.org/10.1890/08-1025.1
- Thomas, H. (2013). Senescence, ageing and death of the whole plant. New Phytologist, 197(3), 696–711. https://doi.org/10.1111/nph.12047
- Thomas, H., Huang, L., Young, M., & Ougham, H. (2009). Evolution of plant senescence. BMC Evolutionary Biology, 9(1), 1–33. https://doi.org/10.1186/1471-2148-9-163
- Thomas, H., & Ougham, H. (2016). Introduction to a virtual Issue on plant senescence. New Phytologist, 212(3), 531–536. https://doi.org/10.1111/nph.14248
- Valencia, E., de Bello, F., Lepš, J., Galland, T., E-Vojtkó, A., Conti, L., Danihelka, J., Dengler, J., Eldridge, D. J., Estiarte, M., García-González, R., Garnier, E., Gómez, D., Harrison, S., Herben, T., Ibáñez, R., Jentsch, A., Juergens, N., Kertész, M., … Götzenberger, L. (2020). Directional trends in species composition over time can lead to a widespread overemphasis of year-to-year asynchrony. Journal of Vegetation Science, 31(5), 792–802. https://doi.org/10.1111/jvs.12916
- Venus, J. C., & Causton, D. R. (1979). Plant growth analysis: A re-examination of the methods of calculation of relative growth and net assimilation rates without using fitted functions. Annals of Botany, 43(5), 633–638. https://doi.org/10.1093/oxfordjournals.aob.a085674
- Vergutz, L., Manzoni, S., Porporato, A., Novais, R. F., & Jackson, R. B. (2012). Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecological Monographs, 82(2), 205–220. https://doi.org/10.1890/11-0416.1
- Veselý, P., Bureš, P., Šmarda, P., & Pavlíček, T. (2012). Genome size and DNA base composition of geophytes: The mirror of phenology and ecology? Annals of Botany, 109(1), 65–75. https://doi.org/10.1093/aob/mcr267
- Wagner, M., Kahmen, A., Schlumprecht, H., Audorff, V., Perner, J., Buchmann, N., & Weisser, W. W. (2007). Prediction of herbage yield in grassland: How well do Ellenberg N-values perform? Applied Vegetation Science, 10(1), 15–24. https://doi.org/10.1111/j.1654-109X.2007.tb00499.x
- Watkinson, A. (1992). Plant senescence. Trends in Ecology & Evolution, 7(12), 417–420. https://doi.org/10.1016/0169-5347(92)90024-6
- Woo, H. R., Masclaux-Daubresse, C., & Lim, P. O. (2018). Plant senescence: How plants know when and how to die. Journal of Experimental Botany, 69(4), 715–718. https://doi.org/10.1093/jxb/ery011
- Wright, I. J., Reich, P. B., Westoby, M., Ackerly, D. D., Baruch, Z., Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, J. H. C., Diemer, M., Flexas, J., Garnier, E., Groom, P. K., Gulias, J., Hikosaka, K., Lamont, B. B., Lee, T., Lee, W., Lusk, C., … Villar, R. (2004). The worldwide leaf economics spectrum. Nature, 428(6985), 821–827. https://doi.org/10.1038/nature02403
- Wu, C., Chen, J. M., Black, T. A., Price, D. T., Kurz, W. A., Desai, A. R., Gonsamo, A., Jassal, R. S., Gough, C. M., Bohrer, G., Dragoni, D., Herbst, M., Gielen, B., Berninger, F., Vesala, T., Mammarella, I., Pilegaard, K., & Blanken, P. D. (2013). Interannual variability of net ecosystem productivity in forests is explained by carbon flux phenology in autumn. Global Ecology and Biogeography, 22(8), 994–1006. https://doi.org/10.1111/geb.12044
- Yan, E. R., Milla, R., Aarssen, L. A., & Wang, X. H. (2012). Functional relationships of leafing intensity to plant height, growth form and leaf habit. Acta Oecologica, 41, 20–29.
- Zohner, C. M., & Renner, S. S. (2017). Innately shorter vegetation periods in north American species explain native–non-native phenological asymmetries. Nature Ecology & Evolution, 1(11), 1655–1660. https://doi.org/10.1038/s41559-017-0307-3