In general, Populus species are highly plastic to environmental conditions.
The results of this study (I–III) showed that both female and male individuals of P. tremula increased height, diameter, and biomass growth in response to moderate elevation of temperature in greenhouse and field conditions.
Moreover, the combined effects of elevated CO2 concentration and temperature promoted diameter growth in the plants in the greenhouses.
Therefore, we may expect that ongoing climate warming in the future would increase the growth of P. tremula in boreal conditions. However, the positive impact of elevated temperature on growth stimulation may reduce to some degree due to thermal acclimation over time. In the field experiment, the stimulating effect of elevated temperature on the diameter growth rate in P.
tremula seedlings decreased as the time progresses during the three-year growth period. Moreover, it is important to recognize that other environmental conditions, particularly drought, could modify the stimulating effect of elevated temperature on growth in P. tremula (Ruosteenoja et al. 2018). There is a positive correlation between increased temperature and drier growing seasons, and this may lead to a decrease in the growth of P. tremula in boreal conditions, because Populus species are particularly sensitive to water deficit (Niinemets and Valladares 2006;
Buermann et al. 2013).
The plants exposed to elevated CO2 concentration increased the concentration of salicylates, phenolic acids, and total low-molecular-weight phenolics in stem bark of both females and males in the greenhouses. This may imply that elevated levels of CO2 concentrations would lower the quality of P. tremula as a host and reduce the palatability of this species to insect and/or mammalian herbivores in boreal forests because of changing climate. However, elevated temperature may negate the stimulating effect of elevated CO2 concentration on phenolic accumulation in P. tremula in the future. In this study, temperature-treated plants had a lower concentration
48
of total low-molecular-weight phenolics in stem bark in the greenhouse experiment, and in stems and leaves in the field experiment. Under the combined treatment, elevated temperature cancelled out the CO2-induced effect on phenolics in the greenhouses. Although elevated UVB radiation often increases UV-induced phenolic compounds in boreal tree species, we did not identify any strong effect in stems and leaves in P. tremula.
The findings of this study partially support Robinson et al. (2014), who claimed that there is no evidence of sexual dimorphism in P. tremula. In this study, male and female individuals of P. tremula showed no discrepancy in growth traits in the field experiment, but females had greater concentrations of low-molecular-weight phenolics in stem bark and stems in greenhouse and field studies, respectively. However, based on this study, ongoing climate warming might drive sex-based discrepancies in P. tremula in the future. Temperature-induced growth stimulation was considerably higher in females grown in greenhouses and in bud-removed females grown in the field. If dimorphism in non-reproductive features of P. tremula is influenced by increased temperature in the future, global warming and the associated increase in herbivore (insect) population might alter sex ratios and population dynamics of this tree species.
Based on the present findings, it is apparent that there is no general answer regarding how P. tremula seedlings would perform in the projected climate change scenarios in the boreal conditions. Because climate change involves many different factors, and one factor can offset or be additive to the impact of another, the combined impact is difficult to predict. Elevated temperature might increase the growth and extend the range of P. tremula further north in the boreal forests, while increased drought and insect population outbreaks due to climate warming might cause this species to become increasingly threatened.
49
Bibliography
Agrawal A.A. 2011. Current trends in the evolutionary ecology of plant defence. Functional Ecology 25: 420–432.
Ballaré C.L., Caldwell M.M., Flint S.D., Robinson S.A. & Bornman J.F. 2011.
Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochemical &
Photobiological Sciences 10: 226–241.
Barton K.E. & Koricheva J. 2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. The American Naturalist 175: 481–493.
Bryant J., Chapin F. & Klein D. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357–368.
Boeckler G.A., Gershenzon J. & Unsicker S.B. 2011. Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:
1497–1509.
Boege K. & Marquis R.J. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution 20: 441–448.
Buermann W., Bikash P.R., Jung M., Burn D.H. & Reichstein M. 2013. Earlier springs decrease peak summer productivity in North American boreal forests. Environmental Research Letters 8: 024027.
Caldwell M.M., Bornman J.F., Ballaré C.L., Flint S.D. & Kulandaivelu G. 2007.
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with bother climate change factors. Photochemical &
Photobiological Sciences 6: 252–266.
Carmona D., Lajeunesse M.J. & Johnson M.T.J. 2011. Evolutionary ecology of plant defences: plant traits that predict resistance to herbivores.
Functional Ecology 25: 358–367.
Caudullo G. & de Rigo D. 2016. Populus tremula in Europe: distribution, habitat, usage and threats. In San-Miguel-Ayanz J., de Rigo D., Caudullo
50
G., Houston Durrant T. & Mauri A. (Eds) European Atlas of Forest Tree Species. Publ. Off. EU, Luxembourg, pp. e01f148+
Cepeda-Cornejo V. & Dirzo R. 2010. Sex-related differences in reproductive allocation, growth, defense and herbivory in three dioecious neotropical palms. PLoS One 5: e9824.
Cole C.T., Stevens M.T., Anderson J.E. & Lindroth R.L. 2016. Heterozygosity, gender, and the growth-defense trade-off in quaking aspen. Oecologia 181: 381–390.
Coley P. D., Massa M., Lovelock C. E. & Winter K. 2002. Effects of elevated CO2
on foliar chemistry of saplings of nine species of tropical tree. Oecologia 133: 62–69.
Conroy J.P., Milham P.J., Mazur M. & Barlow E.W. 1990. Growth, dry weight partitioning and wood properties of Pinus radiate D. Don after 2 years of CO2 enrichment. Plant, Cell & Environment 13: 329–337.
Cope O.L., Kruger E.L., Rubert-Nason K.F. & Lindroth R.L. 2019. Chemical defense over decadal scales: ontogenetic allocation trajectories and consequences for fitness in a foundation tree species. Functional Ecology 33: 2105–2115.
Cornelissen T. & Stiling P. 2005. Sex-biased herbivory: A meta-analysis of the effects of gender on plant-herbivore interactions. Oikos 111: 488–500.
Day T.A., Vogelmann T.C. & DeLucia E.H. 1992. Are some plant life forms more effective than others in screening out ultraviolet-B radiation?
Oecologia 92: 513–519.
Delph L. F. 1999. Sexual dimorphism in life history. In Geber M.A., Dawson T.E. & Delph L.F. (Eds) Gender and Sexual Dimorphism in Flowering Plants. Springer, Berlin, pp. 149–173.
Dieleman W.I.J., Vicca S., Dijkstra F.A., Hagedorn F., Hovenden M.J., Larsen K.S., Morgan J.A., Volder A., Beier C., Dukes J.S., King J., Leuzinger S., Linder S., Luo Y., Oren R., De Angelis P., Tingey D., Hoosbeek M.R. &
Janssens I.A. 2012. Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Global Change Biology 18:
2681–2693.
51 Donaldson J.R., Stevens M.T., Barnhill H.R. & Lindroth R.L. 2006. Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). Journal of Chemical Ecology 32: 1415–1429.
Endara M.J. & Coley P.D. 2011. The resource availability hypothesis revisited:
a meta-analysis. Functional Ecology 25: 389–398.
Erwin E.A., Turner M.G., Lindroth R.L. & Romme W.H. 2001. Secondary plant compounds in seedling and mature aspen (Populus tremuloides) in Yellowstone National Park, Wyoming. The American Midland Naturalist 145: 299–308.
Farrar J.F. & Williams M.L. 1991. The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source-sink relations and respiration. Plant, Cell & Environment 14: 819–830.
Fineblum W.L. & Rausher M.D. 1995. Evidence for a trade-off between resistance and tolerance to herbivore damage in a morning glory.
Nature 377: 517–520.
Fritz C., Palacios-Rojas N., Feil R. & Stitt M. 2006. Regulation of secondary metabolism by the carbon–nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. The Plant Journal 46:
533–548.
Gherlenda A.N., Haigh A.M., Moore B.D., Johnson S.N. & Riegler M. 2015.
Responses of leaf beetle larvae to elevated [CO₂] and temperature depend on Eucalyptus species. Oecologia 177: 607–617.
Goodger J.Q.D., Gleadow R.M. & Woodrow I.E. 2006. Growth cost and ontogenetic expression patterns of defence in cyanogenic Eucalyptus spp. Trees 20: 757–765.
Goralka R.J.L. & Langenheim, J.H. 1996. Implications of foliar monoterpenoid variation among ontogenetic stages of the California bay tree (Umbellularia california) for deer herbivory. Biochemical Systematics and Ecology 24: 13–23.
Gowda J.H. 1997. Physical and chemical response of juvenile Acacia tortilis trees to browsing: experimental evidence. Functional Ecology 11: 106–
111.
52
Gronemeyer P.A., Dilger B.J., Bouzat J.L. & Paige K.N. 1997. The effects of herbivory on paternal fitness in scarlet gilia: Better moms also make better pops. The American Naturalist 150: 592–602.
Hagerman A.E. 2011. The Tannin Handbook. Department of Chemistry and Biochemistry, Miami University, Oxford, OH. Available at http://www.users.miamioh.edu/hagermae/.
Handa I.T., Körner C. & Hättenschwiler S. 2005. A test of the treeline carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology 86: 1288–1300.
Hanley M.E., Fenner M., Whibley H. & Darvil B. 2004. Early plant growth:
identifying the end point of the seedling phase. New Phytologist 163:
61–66.
Hemming J.D.C. & Lindroth R.L. 1999. Effects of light and nutrient availability on aspen: growth, phytochemistry, and insect performance. Journal of Chemical Ecology 25: 1687–1714.
Herms D. & Mattson W. 1992. The dilemma of plants – to grow or defend.
The Quarterly Review of Biology 67: 283–335.
Hikosaka K., Takashima T., Kabeyay D., Hirose T. & Kamata N. 2005. Biomass allocation and leaf chemical defence in defoliated seedlings of Quercus serrata with respect to carbon–nitrogen balance. Annals of Botany 95:
1025–1032.
Hjältén J. 1992. Plant sex and hare feeding preferences. Oecologia 89: 253–
256.
Honkanen T., Haukioja E. & Suomela J. 1994. Effects of simulated defoliation and debudding on needle and shoot growth in Scots pine (Pinus sylvestris): implications of plant source/sink relationships for plant-herbivore. Functional Ecology 8: 631–639.
Hood S. & Sala A. 2015. Ponderosa pine resin defenses and growth: metrics matter. Tree Physiology 35: 1223–1235.
Huttunen L., Ayres M.P., Niemelä P., Heiska S., Tegelberg R., Rousi M. &
Kellomäki S. 2013. Interactive effects of defoliation and climate change on compensatory growth of silver birch seedlings. Silva Fennica 47: 1–
14.
53 Huttunen L., Niemelä P., Peltola H., Heiska S., Rousi M. & Kellomäki S. 2007.
Is a defoliated silver birch seedling able to overcompensate the growth under changing climate? Environmental Experimental Botany 60: 227–
238.
IPCC. 2014. Summary for policymakers. In Core Writing Team, Pachauri R.K.
& Meyer L.A. (Eds), Climate Change 2014: Synthesis Report.
Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, pp. 1–31.
Izaguirre M.M., Mazza C.A., Svatosˇ A., Baldwin I.T. & Ballaré C.L. 2007. Solar ultraviolet-B radiation and insect herbivory trigger partially overlapping phenolic responses in Nicotiana attenuate and Nicotiana longiflora. Annals of Botany 99:103–109.
Jacquet J.-S., Bosc A., O’Grady A.P. & Jactel H. 2013. Pine growth response to processionary moth defoliation across a 40-year chronosequence.
Forest Ecology and Management 293: 29–38.
Jiang D., Wang Y.-y., Dong X.-w. & Yan S.-c. 2018. Inducible defense responses in Populus alba berolinensis to Pb stress. South African Journal of Botany 119: 295–300.
Jiang H., Zhang S., Lei Y., Xu G. & Zhang D. 2016. Alternative growth and defensive strategies reveal potential and gender specific trade-offs in dioecious plants Salix paraplesia to nutrient availability. Frontiers in Plant Science 7: 1064.
Jing S.W. & Coley P.D. 1990. Dioecy and herbivory: the effect of growth rate on plant defense in Acer negundo. Oikos 58: 369–377.
Johnson W.T. & Lyon H.H. 1988. Insects that feed on trees and shrubs.
Cornell University Press, Ithaca, NY.
Jones M.H., MacDonald S.E. & Henry G.H.R. 1999. Sex- and habitat-specific responses of a high arctic willow, Salix arctica, to experimental climate change. Oikos 87:129–138.
de Jong T.J. & van der Meijden E. 2000. On the correlation of defence and regrowth in plants. Oikos 88: 503–508.
54
Julkunen-Tiitto R. 1989. Phenolic compounds of the genus Salix: a chemotaxonomical survey of further Finnish species. Phytochemistry 28: 2115–2125.
Julkunen-Tiitto R., Häggman H., Aphalo P.J., Lavola A., Tegelberg R. & Veteli T.
2005. Growth and defense in deciduous trees and shrubs under UV-B.
Environmental Pollution 137: 404–414.
Juvany M. & Munné-Bosch S. 2015. Sex-related differences in stress tolerance in dioecious plants: a critical appraisal in a physiological context. Journal of Experimental Botany 66: 6083–6092.
Kellomäki S. 2017. Managing Boreal Forests in the Context of Climate Change Impacts, Adaptation and Climate Change Mitigation. CRC Press, Boca Raton, FL.
Kessler A. & Baldwin I.T. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53: 299–
328.
Kim H.Y., Lieffering M., Kobayashi K., Okada M., Mitchell M.W. & Gumpertz M. 2003. Effects of free-air CO2 enrichment and nitrogen supply on the yield of temperate paddy rice crops. Field Crop Research 83: 261–270.
Kuokkanen K., Yan S. C. & Niemela P. 2003. Effects of elevated CO2 and temperature on the leaf chemistry of birch Betula pendula (Roth) and the feeding behaviour of the weevil Phyllobius maculicornis. Agricultural and Forest Entomology 5: 209–217.
Lavigne M.B., Little C.H.A. & Major J.E. 2001. Increasing the sink: source balance enhances photosynthetic rate of 1-year-old balsam fir foliage by increasing allocation of mineral nutrients. Tree Physiology 21: 417–
426.
Lavola A., Nybakken L., Rousi M., Pusenius J., Petrelius M., Kellomäki S. &
Julkunen- Tiitto R. 2013. Combination treatment of elevated UVB radiation, CO2 and temperature has little effect on silver birch (Betula pendula) growth and phytochemistry. Physiologia Plantarum 149: 499–
514.
Lavola A., Julkunen-Tiitto R., Roininen H. & Aphalo P. 1998. Host–plant preference of an insect herbivore mediated by UV-B and CO2 in
55 relation to plant secondary metabolites. Biochemical Systematics and Ecology 26: 1–12.
Lehtilä K. 2000. Modelling compensatory regrowth with bud dormancy and gradual activation of buds. Evolutionary Ecology 14: 315–330.
Lemoine N.P., Drews W.A., Burkepile D.E. & Parker J.D. 2013. Increased temperature alters feeding behavior of a generalist herbivore. Oikos 122: 1669–1678.
Leuzinger S., Luo Y., Beier C., Dieleman W., Vicca S. & Korner C. 2011. Do global change experiments overestimate impacts on terrestrial ecosystems? Trends in Ecology and Evolution 26: 236–241.
Lindroth R.L. 2010. Impacts of elevated atmospheric CO2 and O3 on forests:
phytochemistry, trophic interactions, and ecosystem dynamics. Journal of Chemical Ecology 36: 2–21.
Lindroth R.L. 2012. Atmospheric change, plant secondary metabolites and ecological interactions. In Iason G.R., Dicke M. & Hartley S.E. (Eds), The Ecology of Plant Secondary Metabolites: From Genes to Global Processes. Cambridge University Press, Cambridge, pp. 120–153.
Lindroth R.L., Donaldson J.R., Stevens M.T. & Gusse A.C. 2007. Browse quality in quaking aspen (Populus tremuloides): Effects of genotype, nutrients, defoliation, and coppicing. Journal of Chemical Ecology 33: 1049–1064.
Maldonado-Lopez Y., Cuevas-Reyes P., Sanchez-Montoya G., Oyama K. &
Quesada M. 2014. Growth, plant quality and leaf damage patterns in a dioecious tree species: is gender important? Arthropod-Plant Interaction 8: 241–251.
Maschinski J. & Whitham T.G. 1989. The continuum of plant responses to herbivory. The influence of plant association, nutrient availability, and timing. The American Naturalist 134: 1–19.
Matsuki M. 1996. Regulation of plant phenolic synthesis: from biochemistry to ecology and evolution. Australian Journal of Botany 44: 613-634.
McCloud E.S. & Berenbaum M. 1994. Stratospheric ozone depletion and plant-insect interactions: effects of UVB radiation on foliage quality of Citrus jambhiri for Trichoplusia ni. Journal of Chemical Ecology 20: 525–
539.
56
McDonald E.P., Agrell J. & Lindroth R.L. 1999. CO2 and light effects on deciduous trees: growth, foliar chemistry, and insect performance.
Oecologia 119: 389–399.
Miranda M., Ralph S.G., Mellway R., White R., Heath M.C., Bohlmann J., Constabel C.P. 2007. The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Molecular Plant-Microbe Interactions. 20: 816–831.
Mittler R. 2006. Abiotic stress, the field environment and stress combination.
Trends in Plant Science 11: 15–19.
Morison J.I.L. & Lawlor D.W. 1999. Interactions between increasing CO2
concentration and temperature on plant growth. Plant Cell &
Environment 22: 659–682.
Muola A., Mutikainen P., Laukkanen L., Lilley M. & Leimu R. 2010. Genetic variation in herbivore resistance and tolerance: The role of plant life-history stage and type of damage. Journal of Evolutionary Biology 23:
2185–2196.
Myking T. Bøhler F. Austrheim G. & Solberg E.J. 2011. Life history strategies of aspen (Populus tremula L.) and browsing effects: a literature review.
Forestry 84: 61–71.
Newsham K.K. & Robinson S.A. 2009. Responses of plants in polar regions to UVB exposure: a meta-analysis. Global Change Biology 15: 2574–2589.
Niinemets Ü. & Valladares F. 2006. Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs.
Ecological Monographs 46: 521–547.
Nissinen K., Nybakken L., Virjamo V. & Julkunen-Tiitto R. 2016. Slow-growing Salix repens (Salicaceae) benefits from changing climate. Environmental and Experimental Botany 128: 59–68.
Nissinen K., Virjamo V., Kilpelainen A., Ikonen V., Pikkarainen L., Arvas L., Kirsikka-aho S., Peltonen A., Sobuj N., Sivadasan U., Zhou X., Ge Z., Salminen T., Julkunen-Tiitto R. & Petola H. (2020). Growth responses of boreal Scots pine, Norway spruce and silver birch seedlings to
57 simulated climate warming over three growing seasons in a controlled field experiment. Forests 11: 943.
Nissinen K., Virjamo V., Mehtätalo L., Lavola A., Valtonen A., Nybakken L. &
Julkunen-Tiitto R. 2018. A seven-year study of phenolic concentrations of the dioecious Salix myrsinifolia. Journal of Chemical Ecology 44: 416–
430.
Nissinen K., Virjamo V., Randriamanana T., Sobuj N., Sivadasan U., Mehtätalo L., Beuker E., Julkunen-Tiitto R. & Nybakken L. 2017. Responses of growth and leaf phenolics in European aspen (Populus tremula) to climate change during juvenile phase change. Canadian Journal of Forest Research 47: 1350–1363.
Norby R.J., Warren J.M., Iversen C.M., Medlyn B.E. & McMurtrie R.E. 2010. CO2
enhancement of forest productivity constrained by limited nitrogen availability. Proceedings of the National Academy of Sciences of the United States of America 107: 19368–19373.
Nybakken L., Hörkkä R. & Julkunen-Tiitto R. 2012. Combined enhancements of temperature and UVB influence growth and phenolics in clones of the sexually dimorphic Salix myrsinifolia. Physiologia Plantarum 145:
551–564.
Nybakken L. & Julkunen-Tiitto R. 2013. Gender differences in Salix myrsinifolia at the pre-reproductive stage are little affected by simulated climatic change. Physiologia Plantarum 147: 465–476.
Nykänen H. & Koricheva J. 2004. Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis.
Oikos 104: 247–268.
Obeso J.R. 2002. The costs of reproduction in plants. New Phytologist 155:
321–348.
Ochoa-Lopez S., Villamil N., Zedillo-Avellryra P. & Boege K. 2015. Plant defence as a complex and changing phenotype throughout ontogeny.
Annals of Botany 116: 797–806.
O’Reilly-Wapstra J.M., Moore B.D., Brewer M., Beaton J., Sim D., Wiggins N.L.
and Iason G.R. 2014. Pinus sylvestris sapling growth and recovery from mammalian browsing. Forest Ecology and Management 325: 18–25.
58
Oren R., Ellsworth D.S., Johnsen K.H., Phillips N., Ewers B.E., Maier C., Schäfer K. V, McCarthy H., Hendrey G., McNulty S.G. & Katul G.G. 2001. Soil fertility limits carbon sequestration by forest ecosystems in a CO2 -enriched atmosphere. Nature 411: 469–472.
Osier T.L., Hwang S.-Y. & Lindroth R.L. 2000. Effects of clonal variation in quaking aspen, Populus tremuloides, phytochemistry on gypsy moth, Lymantria dispar, performance in the field and laboratory. Ecological Entomology 25: 197-207
Ozaki K., Saito H. & Yamamuro K. 2004. Compensatory photosynthesis as a response to partial debudding in Ezo spruce, Picea jezoensis, seedlings.
Ecological Research 19: 225–231.
Peltonen P.A., Vapaavuori E. & Julkunen-Tiitto R. 2005. Accumulation of phenolic compounds in birch leaves is changed by elevated carbon dioxide and ozone. Global Change Biology 11: 1305–1324.
Peñuelas J. & Estiarte M. 1998. Can elevated CO2 affect secondary metabolism and ecosystem function? Trends in Ecology & Evolution 13:
20–24.
Pilson D. 2000. The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evolutionary Ecology 14: 457–489.
Prittinen K., Pusenius J., Koivunoro K. & Roininen H. 2003. Genotypic variation in growth and resistance to insect herbivory in silver birch (Betula pendula) seedlings. Oecologia 137: 572–577.
R Core Team. 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available at http://www.R-project.org/.
Randriamanana T.R., Lavola A. & Julkunen-Tiitto R. 2015. Interactive effects of supplemental UV-B radiation and temperature in European aspen seedlings: implications for growth, leaf traits, phenolic defense and associated organisms. Plant Physiology and Biochemistry 93: 84–93.
Randriamanana T.R., Nybakken L., Lavola A., Aphalo P.J., Nissinen K. &
Julkunen- Tiitto R. 2014. Sex-related differences in growth and carbon
59 allocation to defence in Populus tremula as explained by current plant defence theories. Tree Physiology 34: 471–487.
Rasmussen H.N., Soerensen S. & Andersen L. 2003. Lateral bud and shoot removal affects leader growth in Abies nordmanniana Scand. Journal of Forestry Research 18: 127–132.
Reich P.B., Walters M.B., Krause S.C., Vanderklein D.W., Raffa K.F. & Tabone T. 1993. Growth, nutrition and gas exchange of Pinus resinosa following artificial defoliation. Trees 7: 67–77.
Renner S.S. 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany 101: 1588–1596.
Renner S.S. & Ricklefs R.E. 1995. Dioecy and its correlates in the flowering plants. American Journal of Botany 82: 596–606.
Robinson K.M., Delhomme N., Mähler N., Schiffthaler B., Önskog J., Albrectsen B.R., Ingvarsson P.K., Hvidsten T.R., Jansson S. & Street N.R.
2014. Populus tremula (European aspen) shows no evidence of sexual dimorphism. BMC Plant Biology 14: 276.
Roth S.K., Lindroth R.L., Volin J.C. & Kruger E.L. 1998. Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance.
Global Change Biology 4: 419–430.
Rousseaux M.C., Julkunen-Tiitto R., Searles P.S., Scopel A.L., Aphalo P.J. &
Ballaré, C. L. 2004. Solar UV-B radiation affects leaf quality and insect herbivory in the southern beech tree Nothofagus antarctica. Oecologia 138: 505–512.
Rozema J., Boelen P., Solheim B., Zielke M., Buskens A., Doorenbosch M., Fijn R., Herder J., Callaghan T., Björns L.O., Jones D.G., Broekman R., Blokker P. & van de Poll W. 2006. Stratospheric ozone depletion: high arctic tundra plant growth on Svalbard is not affected by enhanced UV-B after 7 years of UV-B supplementation in the field. Plant Ecology 182:
121–135.
Ruosteenoja K., Markkanen T., Venäläinen A., Räisänen P. & Peltola H. 2018.
Seasonal soil moisture and drought occurrence in Europe in CMIP5 projections for the 21st century. Climate Dynamics 50: 1177–1192.
60
Ruuhola T., Nybakken L., Randriamananaa T., Lavola A. & Julkunen-Tiitto R.
2018. Effects of long-term UV exposure and plant sex on the leaf phenoloxidase activities and phenolic concentrations of Salix myrsinifolia (Salisb.). Plant Physiology and Biochemistry 126: 55–62.
2018. Effects of long-term UV exposure and plant sex on the leaf phenoloxidase activities and phenolic concentrations of Salix myrsinifolia (Salisb.). Plant Physiology and Biochemistry 126: 55–62.