Differential growth rate, water-use efficiency and climate sensitivity between males and females of <i>Ilex aquifolium</i> in north-western Spain

  1. Sánchez Vilas, Julia 34
  2. Hernández-Alonso, Héctor 12
  3. Rozas, Vicente 1
  4. Retuerto, Rubén 3
  1. 1 EiFAB, iuFOR, Universidad de Valladolid , Campus Duques de Soria, 42004 Soria ,
  2. 2 CEFE, Univ Montpellier, CNRS, EPHE, IRD , Montpellier ,
  3. 3 Departamento de Bioloxía Funcional (Área de Ecoloxía), Facultade de Bioloxía, Universidade de Santiago de Compostela , c/ Lope Gómez de Marzoa s/n, 15782 Santiago de Compostela ,
  4. 4 School of Biosciences, Sir Martin Evans Building, Cardiff University , CF10 3AX Cardiff ,
Journal:
Annals of Botany

ISSN: 0305-7364 1095-8290

Year of publication: 2024

Type: Article

DOI: 10.1093/AOB/MCAE126 WoS: WOS:001299193200001 GOOGLE SCHOLAR lock_openOpen access editor HANDLE: https://hdl.handle.net/10347/42087

More publications in: Annals of Botany

Abstract

Background and aims Dioecious plant species, i.e. those in which male and female functions are housed in different individuals, are particularly vulnerable to global environmental changes. For long-lived plant species, such as trees, long-term studies are imperative to understand how growth patterns and their sensitivity to climate variability affect the sexes differentially.Methods Here, we explore long-term intersexual differences in wood traits, namely radial growth rates and water-use efficiency quantified as stable carbon isotope abundance of wood cellulose, and their climate sensitivity in Ilex aquifolium trees growing in a natural population in north-western Spain.Key results We found that sex differences in secondary growth rates were variable over time, with males outperforming females in both radial growth rates and water-use efficiency in recent decades. Summer water stress significantly reduced the growth of female trees in the following growing season, whereas the growth of male trees was favoured primarily by cloudy and rainy conditions in the previous autumn and winter combined with low cloud cover and warm conditions in summer. Sex-dependent lagged correlations between radial growth and water availability were found, with a strong association between tree growth and cumulative water availability in females at 30 months and in males at 10 months.Conclusions Overall, our results point to greater vulnerability of female trees to increasing drought, which could lead to sex-ratio biases threatening population viability in the future.

Funding information

Bibliographic References

  • Adams, (2017), Nature Ecology and Evolution, 1, pp. 1285, 10.1038/s41559-017-0248-x
  • Akaike, (1973), Second international symposium on information theory, pp. 267
  • Barrett, (2013), Journal of Experimental Botany, 64, pp. 67, 10.1093/jxb/ers308
  • Barton, (2022)
  • Beguería, (2017)
  • Benedí, (1997), Flora Ibérica, Vol. III. Haloragaceae–Euphorbiaceae, pp. 182
  • Benner, (1987), Nature, 329, pp. 708, 10.1038/329708a0
  • Biondi, (2008), Tree-Ring Research, 64, pp. 81, 10.3959/2008-6.1
  • Bram, (2000), American Journal of Botany, 87, pp. 1609, 10.2307/2656737
  • Brienen, (2022), Tree Physiology, 42, pp. 1131, 10.1093/treephys/tpab142
  • Brooks, (1998), Canadian Journal of Forest Research, 28, pp. 524, 10.1139/x98-018
  • Burnham, (2002), Model selection and multimodel inference: a practical information-theoretic approach
  • Campelo, (2012), Dendrochronologia, 30, pp. 57, 10.1016/j.dendro.2011.01.010
  • Cattaneo, (2013), Dendrochronologia, 31, pp. 147, 10.1016/j.dendro.2013.01.005
  • Cedro, (2011), Tree-Ring Research, 67, pp. 3, 10.3959/2009-9.1
  • Clark, (1967), HortScience, 2, pp. 115, 10.21273/HORTSCI.2.3.115
  • Cruden, (2000), Plant Systematics and Evolution, 222, pp. 143, 10.1007/BF00984100
  • Damesin, (1997), Oecologia, 111, pp. 26, 10.1007/s004420050204
  • Damesin, (1998), Functional Ecology, 12, pp. 778, 10.1046/j.1365-2435.1998.00259.x
  • Da Silveira, (1989), Modern methods of plant analysis, Vol. 10. Plant fibers, pp. 89
  • Dawson, (1989), Oecologia, 79, pp. 332, 10.1007/BF00384312
  • Dawson, (1993), Ecology, 74, pp. 798, 10.2307/1940807
  • Dawson, (2004), Functional Ecology, 18, pp. 212, 10.1111/j.0269-8463.2004.00838.x
  • De Candolle, (1855), Geographie Botanique Raisonee
  • DeClerk, (2006), Ecology, 87, pp. 2787, 10.1890/0012-9658(2006)87[2787:SRASSI]2.0.CO;2
  • Desoto, (2016), Frontiers in Plant Science, 7, pp. 173698, 10.3389/fpls.2016.00723
  • Díaz-Barradas, (2018), Environmental and Experimental Botany, 155, pp. 609, 10.1016/j.envexpbot.2018.08.011
  • Dupouey, (1993), Plant, Cell and Environment, 16, pp. 939, 10.1111/j.1365-3040.1993.tb00517.x
  • Eckes-Shephard, (2022), Frontiers in Plant Science, 13, pp. 837648, 10.3389/fpls.2022.837648
  • Ehleringer, (1993), Stable isotopes and plant carbon/water relations, pp. 155, 10.1016/B978-0-08-091801-3.50018-0
  • Farquhar, (1982), Functional Plant Biology, 9, pp. 121, 10.1071/PP9820121
  • Farquhar, (1989), Annual Review of Plant Physiology, 40, pp. 503, 10.1146/annurev.pp.40.060189.002443
  • Ferrio, (2003), Oecologia, 137, pp. 512, 10.1007/s00442-003-1372-7
  • Fleck, (1996), Oecologia, 105, pp. 286, 10.1007/BF00328730
  • Forrest, (2014), The American Naturalist, 184, pp. 338, 10.1086/677295
  • Garcia-Barreda, (2022), Dendrochronologia, 73, pp. 125944, 10.1016/j.dendro.2022.125944
  • Gessler, (2014), Tree Physiology, 34, pp. 796, 10.1093/treephys/tpu040
  • Granda, (2014), Oecologia, 174, pp. 307, 10.1007/s00442-013-2742-4
  • Guitián, (2006), Acta Oecologica, 30, pp. 151, 10.1016/j.actao.2006.02.009
  • Hacket-Pain, (2015), Tree Physiology, 35, pp. 319, 10.1093/treephys/tpv007
  • Harris, (2010), Journal of Ecology, 98, pp. 509, 10.1111/j.1365-2745.2009.01623.x
  • Harris, (2020), Scientific Data, 7, pp. 109, 10.1038/s41597-020-0453-3
  • Hartman, (2010), Oecologia, 162, pp. 837, 10.1007/s00442-009-1514-7
  • Hebbali, (2020), olsrr. Tools for building OLS regression models. R package version 0.5.3
  • Heilbuth, (2000), The American Naturalist, 156, pp. 221, 10.1086/303389
  • Heilman, (2021), Oecologia, 197, pp. 1095, 10.1007/s00442-021-04892-0
  • Holmes, (1983), Tree Ring Bulletin 43, pp. 69
  • Huang, (2018), Journal of Plant Ecology, 11, pp. 771, 10.1093/jpe/rtx048
  • Hultine, (2013), Global Change Biology, 19, pp. 3390, 10.1111/gcb.12230
  • Hultine, (2016), Nature Plants, 2, pp. 16109, 10.1038/nplants.2016.109
  • Hultine, (2018), Oecologia, 187, pp. 921, 10.1007/s00442-018-4190-7
  • IPCC., (2023), Climate change 2023: synthesis report. Contribution of working groups I, II and III to the sixth assessment report of intergovernmental panel on climate change
  • Iszkuło, (2011), Acta Oecologica, 37, pp. 99, 10.1016/j.actao.2011.01.001
  • Iszkuło, (2009), Plant Ecology, 200, pp. 229, 10.1007/s11258-008-9447-5
  • Iversen, (1944), Geologiska Föreningen i Stockholm Förhandlingar, 66, pp. 463, 10.1080/11035894409445689
  • Juvany, (2015), Journal of Experimental Botany, 66, pp. 6083, 10.1093/jxb/erv343
  • Körner, (1988), Oecologia, 74, pp. 623, 10.1007/BF00380063
  • Korol, (1999), Tree Physiology, 19, pp. 551, 10.1093/treephys/19.9.551
  • Kwak, (2016), Chemical Geology, 420, pp. 127, 10.1016/j.chemgeo.2015.11.015
  • Leavitt, (1993), Analytical Chemistry, 65, pp. 87, 10.1021/ac00049a017
  • Liu, (2014), Tree Physiology, 34, pp. 966, 10.1093/treephys/tpu067
  • Lloyd, (1977), Botanical Review, 43, pp. 177, 10.1007/BF02860717
  • Martins, (2021), Plant Ecology, 222, pp. 275, 10.1007/s11258-020-01105-1
  • Meagher, (2001), Evolutionary Ecology Research, 3, pp. 845
  • Mendoza, (2021), Scientific Reports, 11, pp. 21244, 10.1038/s41598-021-00555-5
  • Midgley, (2022), Scientific Reports, 12, pp. 1407, 10.1038/s41598-022-05558-4
  • Milla, (2006), Plant Biology (Stuttgart, Germany), 8, pp. 103, 10.1055/s-2005-872890
  • Montesinos, (2006), Annals of Botany, 98, pp. 885, 10.1093/aob/mcl172
  • Nock, (2011), Global Change Biology, 17, pp. 1049, 10.1111/j.1365-2486.2010.02222.x
  • Nuñez, (2008), Ecoscience, 15, pp. 73, 10.2980/1195-6860(2008)15[73:SSSAGI]2.0.CO;2
  • Obeso, (1997), Journal of Ecology, 85, pp. 159, 10.2307/2960648
  • Obeso, (2002), New Phytologist, 155, pp. 321, 10.1046/j.1469-8137.2002.00477.x
  • Obeso, (2002), Revista Chilena de Historia Natural, 75, pp. 67, 10.4067/S0716-078X2002000100007
  • Obeso, (1998), American Journal of Botany, 85, pp. 1602, 10.2307/2446488
  • Pannell, (2022), Annual Review of Ecology, Evolution, and Systematics, 53, pp. 183, 10.1146/annurev-ecolsys-102320-085812
  • Pearse, (2016), The New Phytologist, 212, pp. 546, 10.1111/nph.14114
  • Peltier, (2019), Global Change Biology, 25, pp. 3803, 10.1111/gcb.14720
  • Peltier, (2020), Ecology Letters, 23, pp. 1561, 10.1111/ele.13575
  • Peltier, (2023), Journal of Ecology, 111, pp. 1170, 10.1111/1365-2745.14116
  • Peterken, (1967), Journal of Ecology, 55, pp. 841, 10.2307/2258429
  • Petry, (2016), Science, 353, pp. 69, 10.1126/science.aaf2588
  • Pollo, (2005), Bird Conservation International, 15, pp. 397, 10.1017/S0959270905000626
  • Purrington, (1998), Journal of Ecology, 86, pp. 397, 10.1046/j.1365-2745.1998.00262.x
  • R Core Team., (2022), R: a language and environment for statistical computing
  • Renner, (2014), American Journal of Botany, 101, pp. 1588, 10.3732/ajb.1400196
  • Retuerto, (2000), Functional Ecology, 14, pp. 529, 10.1046/j.1365-2435.2000.t01-1-00454.x
  • Retuerto, (2006), International Journal of Plant Sciences, 167, pp. 279, 10.1086/498919
  • Retuerto, (2018), Environmental and Experimental Botany, 146, pp. 1, 10.1016/j.envexpbot.2017.12.006
  • Roddy, (2019), PeerJ, 7, pp. e6835, 10.7717/peerj.6835
  • Rovere, (2003), Ecoscience, 10, pp. 195, 10.1080/11956860.2003.11682767
  • Rozas, (2009), The New Phytologist, 182, pp. 687, 10.1111/j.1469-8137.2009.02770.x
  • Rozas, (2019), Agricultural and Forest Meteorology, 274, pp. 132, 10.1016/j.agrformet.2019.05.003
  • Rozas, (2021), Dendrochronologia, 68, pp. 125853, 10.1016/j.dendro.2021.125853
  • Sánchez Vilas, (2011), Annals of Botany, 107, pp. 119, 10.1093/aob/mcq209
  • Saurer, (1989), Dendrochronologia, 7, pp. 9
  • Schweingruber, (2011), Anatomy of European woods: an atlas for the identification of European trees, shrubs and dwarf shrubs
  • Seibt, (2008), Oecologia, 155, pp. 441, 10.1007/s00442-007-0932-7
  • Shestakova, (2016), Proceedings of the National Academy of Sciences of the United States of America, 113, pp. 662, 10.1073/pnas.1514717113
  • Tans, (1978), Nature, 271, pp. 234, 10.1038/271234a0
  • Tognetti, (2012), Tree Physiology, 32, pp. 1321, 10.1093/treephys/tps105
  • Tornos-Estupiña, (2023), Agricultural and Forest Meteorology, 341, pp. 109665, 10.1016/j.agrformet.2023.109665
  • Urrutia-Jalabert, (2022), Journal of Geophysical Research, Biogeosciences, 128, pp. e2022
  • Vamosi, (2003), Journal of Evolutionary Biology, 16, pp. 1006, 10.1046/j.1420-9101.2003.00559.x
  • Vicente-Serrano, (2010), Journal of Climate, 23, pp. 1696, 10.1175/2009JCLI2909.1
  • Ward, (1904), Trees: a handbook of forest-botany for the woodlands and the laboratory
  • Ward, (2002), Tree Physiology, 22, pp. 339, 10.1093/treephys/22.5.339
  • Warren, (2001), Oecologia, 127, pp. 476, 10.1007/s004420000609
  • Weiwei, (2018), Scientific Reports, 8, pp. 308, 10.1038/s41598-017-18694-z
  • Wu, (2015), Frontiers in Plant Science, 6, pp. 309, 10.3389/fpls.2015.00309