Plants face many challenges due to climate change, and in response need to acclimate, adapt or migrate. Temperature is a major factor limiting the growth, biochemistry and ultimately range distribution of species,
therefore changes in the thermal growing season conditions can have
large impacts on forests. In the past, during the late Quaternary deglaciation, tree species’ range shifts followed climatic cycles closely, suggesting a good capacity for forests to do so in a relatively slowly
changing environment. However, the current rate of climate change means that migratory success and survival will depend not only on migration potential but strongly on adaptive capacity, and especially trailing edge populations (those persisting on-site despite changing climate) will benefit from large within-population variation (Davis and Shaw 2001, Aitken et al.
2008). However, the scope of the changes taking place test the boundaries of adaptive capacity, as more extreme risks of herbivory, droughts, floods and heat and cold spells will increase, and migratory populations from the south to the north face new photoperiods at new latitudes.
The among- and within-population genetic variation visible in today’s tree populations has been shaped by past historical events. North European post-glacial recolonization history of tree species, such as birches, is different from that of North America (Petit et al. 2003, Breen et al. 2012, Jadwiszczak 2012). North American tree species survived the last glacial maximum mainly south of the glacial sheet and afterwards
gradually spread northward (Williams et al. 2004, Breen et al. 2012). For example, refugial Populus populations in Beringia contributed only little to the diversity of current populations (Breen et al. 2012). On the other hand, Finland was probably recolonized from two directions, from the west and from the east. Nowadays, high genetic variation in and rare haplotypes of European B. pendula are mainly concentrated in regions north of the Alps and near the Ural Mountains (Palmé et al. 2003, Jadwiszczak 2012), and since ancient populations are thought to be genetically the most diverse, it is possible that these sites acted as primary glacial refugia during the Last Glacial Maximum. Other sites of high variation do exist, possibly due to post-glacial population admixing (Petit et al. 2003) or, controversially, even
‘cryptic refugia’ (Stewart and Lister 2001, but see Tzedakis et al. 2013 for a critique).
In the current climate, silver birch provenances separated by latitude seem to have several key differences. Whether these are strong local adaptations and exactly how plastically these traits can acclimate, remain
open questions. Reciprocal transplantation to other common gardens is necessary for a complete demonstration of local adaptation (Kawecki and Ebert 2004), as otherwise the responses to the translocation itself, i.e.
phenotypic plasticity (due to varying changes in, e.g., herbivory pressure, climate, light and temperature), are not possible to quantify. Irrespective of latitudinal adaptations (but probably as a related phenomenon), boreal tree species (including Betula spp.) have been suggested to exhibit a close coupling of metabolic and morphological traits at a whole-tree –level. High resource acquisition rates (carbon assimilation and nitrogen uptake), high respiration rates, high tissue %N concentration and high root specific length but low LMA may exist together in an individual tree, or, depending on resource availability, the opposite traits may do (Reich et al. 1998).
Some of these correlations could stem from rather direct causal linkages between morphology and metabolism, while some may be more indirectly correlated with other traits such as relative growth rate (RGR). While the northern silver birches exhibited signs of a ‘polar day syndrome’ of traits including high GE rates (I, II, III), efficient photochemistry (II), high RGR (I, III) and high allocation to the below-ground mass fraction (II), there was no indication of co-occurring low LMA, and CCI (as a proxy of tissue N or [Chl]) did not differ among provenances. The GE rates of the southern 61°PU may have been lower in CL than in NCL, while biomass accumulation was not negatively affected in CL. Instead, total DW increased but relative allocation to roots was decreased (III). Thus, although there are risks, these southern silver birches may in the future survive a northward transfer to areas of CL, which would agree with survival-rates seen in the field (Possen et al. 2021). However, as many leaf traits were not affected by photoperiod, it is possible that in the future they will be shaped more by warming.
In the future, long-distance pollen dispersal could promote gene flow among birch species or provenances and aid in adapting to the new climate, as the pollen of birch species behaves almost similarly to anthropogenic coarse aerosols and can spread hundreds of kilometers (Sofiev et al. 2006). However, mismatched flowering times probably limit effective gene flow between distant provenances (Rousi et al. 2011, 2019).
Therefore, it is possible that genotypic (within-stand) variation will be more
important as a genetic reservoir. Genotypic variation in Finnish silver birch provenances is repeatedly encountered in various traits (Laitinen et al.
2005, Silfver 2009, Mäenpää 2012, Possen 2014), and high genotypic
variation was visible in many traits in all of the experiments of this thesis as well. High genotypic variation has biological but also economic importance, as it means that the progeny of trees from a particular latitude do not necessarily boast the average physiological characteristics of that provenance. Mäenpää et al. (2013) used the same 61°PU provenance of silver birch used here (and one of the same genotypes, Pu17) and noted that gas exchange and biomass allocation patterns were highly genotype- specific. They highlight that one of their genotypes had low Anet, gs and LMA, concurrent with high LMF and low RMF (Mäenpää et al. 2013).
Although these genotype-level patterns were not specifically looked for, some of the genotypes were clearly distinct, for example the genotype Pu30 which in (III) in both treatments had relatively high Anet and Amass, low LMA and high root, stem, leaf and total plant DWs.
Along with temperature, climate change affects precipitation and air humidity. These affect the moisture supply from the soil to the plant and evaporative demand out of the plant. These two processes happen at different time scales because while soils dry out slowly, VPD can change rapidly. VPD is an indicator of atmospheric water stress or desiccation strength, and as climate warming is expected to increase VPD, trees will be predisposed to events of drought stress and mortality (Williams et al.
2012). Stomata close in response to higher evaporative demand to
maintain a minimum leaf water potential and to prevent xylem cavitation (Hogg et al. 1999), which in turn reduces gs and Anet irrespective of soil moisture (Dang et al. 1997, Hogg et al. 1999) and this has been associated with recent aspen growth declines in Alaska (Trugman et al. 2018 and references therein). On the other hand, if rainfall and cloudiness increase locally, this would decrease VPD (Lihavainen 2016). In article (II), the silver birch provenances were found not to differ in their leaf-level response to VPD in regard to either stomatal conductance (gs – VPD) or internal CO2
partial pressure (Ci – VPD) and both gs and Ci steadily decreased with increasing VPD. However, on a whole-tree level, northern silver birches
could in principle be less susceptible to desiccation (or more generally to changes in VPD), as they have less leaves and more relative root biomass.
Trees from cold climates may also have more absorptive roots (Zadworny et al. 2016), and could therefore be able to take up more water.
Insect herbivore pressure on northern silver birches is currently typically low (Silfver et al. 2020) but is predicted to increase in the future (Heimonen 2015). As northern silver birches have less leaves than southern ones (I, II, III), it is presumable that even a small increase in defoliation can decrease survival. In addition, Silfver et al. (2020) found that artificially reducing the already low levels of insect herbivory in the Subarctic increased the ecosystem carbon uptake potential considerably, further supporting the idea that northern trees have high stakes riding on a small number of leaves. Further, the LMA of these leaves may change in the future, and thus noticeably affect herbivory and gas exchange. High-LMA leaves are not preferentially eaten by herbivores, as they are usually structurally more durable and may contain more defense compounds such as
phenolics (Poorter et al. 2009). However, the direction of possible changes depends on many factors, because while direct climate change factors such as warming and air humidity will cause acclimation pressure for LMA, also species and provenance range shifts will play a role.
4 Concluding remarks
’How will silver birch cope in the future’ is a difficult question and one that still evokes various answers. In a changing climate it is exceedingly
important to understand within-species provenance responses to latitude and the warming-by-photoperiod –interaction should be of interest for future studies. Silver birch faces a longer, warmer growing season with increased variation in moisture availability, while areas of continuous light (CL) will become suitable for plants that did not habit them before.
This thesis provides insight on how silver birch has adapted to the current climate and also on the future outlooks for this species. Based on the results:
Northern silver birches may exhibit a ‘polar day syndrome’ of traits, making them clearly distinct from geographically separated southern provenances even when translocated to a common environment. Northern silver birches showed higher maximal area-based gas exchange rates (Anet, Aopt, gs) and higher maximum quantum yield of photochemistry (Fv/Fm) than southern ones. In addition, northern silver birches had higher relative height growth rates (RGR), lower stomatal density and higher allocation to below-ground biomass and lesser allocation to above-ground biomass than southern ones.
In the future, it is likely that silver birch can plastically acclimate several traits to new environmental conditions. Apart from the higher Aopt in 67°KI than in 61°PU, the provenances did not differ in their responses of gas exchange to temperature or light. Additionally, many leaf traits did not differ among all provenances, including leaf longevity, leaf mass per area (LMA) and chlorophyll content. These observations may indicate capacity for acclimation, and especially likely traits to exhibit plasticity are the photosynthetic gas exchange temperature optimum (Topt), leaf longevity, LMA and the relative allocation to roots (RMF, which may be plastic to photoperiod). However, severe risks are associated with the unknown limits of acclimation capacity, i.e. the range of values each trait can easily achieve in response to a change.
The findings of this thesis have significance both for basic biological research and for practical applied forestry. The results present a basis for predicting the future of silver birch carbon assimilation and growth and provide new understanding for studies tackling northern trait syndromes.
Silver birch has great potential for carbon uptake in the changing climate, but it should be recognized that provenances have differences in
photosynthetic traits and biomass allocation properties, and that these may change depending on photoperiod. Thus, knowledge of the
differences and similarities among provenances and of the high genotypic variation as a source of plasticity can be applied for the needs of the forestry sector when planning new transfers of tree material, but are also highly important for the success of the species facing a changing
environment.
Bibliography
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: 95–111.
Ashraf, M. & Harris, P.J.C. 2013. Photosynthesis under stressful environments: An overview. Photosynthetica 51: 163–190.
Barber, S.A. 1962. A diffusion and mass-flow concept of soil nutrient availability. Soil Science 93: 39–49.
Bates, D., Maechler, M., Bolker, B. & Walker, S. 2015. Fitting linear mixed- effects models using lme4. Journal of Statistical Software 67: 1–48.
Bernacchi, C.J., Calfapietra, C., Centritto, M. & Valladares, F. 2012. Global change and photosynthesis. In: Flexas, J., Loreto, F. & Medrano, H.
(eds): Terrestrial photosynthesis in a changing environment, a molecular, physiological and ecological approach. Cambridge University Press, Cambridge, UK, pp 537–545.
Blume‐Werry, G., Wilson, S.D., Kreyling, J. & Milbau, A. 2016. The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient. New Phytologist 209: 978–986.
Breen, A.L., Murray, D.F. & Olson, M.S. 2012. Genetic consequences of glacial survival: the late Quaternary history of balsam poplar (Populus balsamifera L.) in North America. Journal of Biogeography 39: 918–928.
Brelsford, C.C., Nybakken, L., Kotilainen, T.K. & Robson, T.M. 2019. The influence of spectral composition on spring and autumn phenology in trees. Tree Physiology 39: 925–950.
Burnham, K.P. & Anderson, D.R. 2002. Model selection and multi-model inference: A practical information-theoretic approach, 2nd edn.
Springer, New York, USA.
von Caemmerer, S. & Farquhar, G.D. 1981. Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves.
Planta 153: 376–387.
Chiang, C., Olsen, J.E., Basler, D., Bånkestad, D. & Hoch, G. 2019. Latitude and weather influences on sun light quality and the relationship to tree growth. Forests 10: 1–12.
Cox, R.M. & Zhu, X.B. 2003. Effects of simulated thaw on xylem cavitation, residual embolism, spring dieback and shoot growth in yellow birch.
Tree Physiology 23: 615–624.
Cramer, M.D., Hawkins, H.-J. & Verboom, G.A. 2009. The importance of nutritional regulation of plant water flux. Oecologia 161: 15–24.
Croft, H., Chen, J.M., Luo, X., Bartlett, P., Chen, B. & Staebler, R.M. 2017. Leaf chlorophyll content as a proxy for leaf photosynthetic capacity.
Global Change Biology 23: 3513–3524.
Crous, K.Y., Drake, J.E., Aspinwall, M.J., Sharwood, R.E., Tjoelker, M.G. &
Ghannoum, O. 2018. Photosynthetic capacity and leaf nitrogen decline along a controlled climate gradient in provenances of two widely distributed Eucalyptus species. Global Change Biology 24:
4626–4644.
Dang, Q.L., Margolis, H.A., Coyea, M.R., Sy, M. & Collatz, G.J. 1997.
Regulation of branch-level gas exchange of boreal trees: roles of shoot water potential and vapor pressure difference. Tree physiology 17: 521–535.
Davis, M.B. & Shaw, R.G. 2001. Range shifts and adaptive responses to quaternary climate change. Science 292: 673–679.
Deepak, M. 2020. Intraspecific variation in silver birch leaf spectral reflectance and surface secondary metabolites. PhD thesis, University of Eastern Finland, Faculty of Science and Forestry, Department of Environmental and Biological Sciences.
https://erepo.uef.fi/handle/123456789/23890 (22 December 2022, date last accessed).
Deepak, M., Keski-Saari, S., Fauch, L., Granlund, L., Oksanen, E. & Keinänen, M. 2019. Leaf canopy layers affect spectral reflectance in silver birch. Remote Sensing 11: 2884.
Deepak, M., Lihavainen, J., Keski-Saari, S., Kontunen-Soppela, S., Salojärvi, J., Tenkanen, A., Heimonen, K., Oksanen, E. & Keinänen, M. 2018.
Genotype- and provenance-related variation in the leaf surface
secondary metabolites of silver birch. Canadian Journal of Forest Research 48: 494–505.
Eckert, C.G., Samis, K.E. & Lougheed, S.C. 2008. Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Molecular Ecology 17: 1170–1188.
Ellsworth, D.S. & Reich, P.B. 1992. Leaf mass per area, nitrogen content and photosynthetic carbon gain in Acer saccharum seedlings in contrasting forest light environments. Functional Ecology 6: 423–
435.
Epron, D., Dreyer, E. & Bréda, N. 1992. Photosynthesis of oak trees [Quercus petraea (Matt.) Liebl.] during drought under field conditions: diurnal course of net CO2 assimilation and photochemical efficiency of photosystem II. Plant, Cell &
Environment 15: 809–820.
Fernández-Marín, B., Atherton, J., Olascoaga, B., Kolari, P., Porcar-Castell, A.
& García-Plazaola, J.I. 2018. When the sun never sets: daily changes in pigment composition in three subarctic woody plants during the summer solstice. Trees 32: 615–630.
Finnish Meteorological Institute 2017. Open data, weather observations.
http://catalog.fmi.fi/geonetwork/srv/eng/catalog.search#/home (22 December 2022, date last accessed).
Flexas, J., Barbour, M.M., Brendel, O., Cabrera, H.M., Carriquí, M., Díaz- Espejo, A., Douthe, C., Dreyer, E., Ferrio, J.P., Gago, J., Gallé, A., Galmés, J., Kodama, N., Medrano, H., Niinemets, Ü., Peguero-Pina, J.J., Pou, A., Ribas-Carbó, M., Tomás, M., Tosens, T. & Warren, C.R.
2012a. Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis. Plant Science 193–194: 70–84.
Flexas, J., Loreto, F. & Medrano, H. 2012b. Terrestrial photosynthesis in a changing environment: A molecular, physiological, and ecological approach. Cambridge University Press, Cambridge, UK.
Fox, J. & Weisberg, S. 2019. An R companion to applied regression, third
edition. Thousand Oaks CA: Sage.
https://socialsciences.mcmaster.ca/jfox/Books/Companion/ (22 December 2022, date last accessed).
Foyer, C.H. & Harbinson, J. 2012. Photosynthetic regulation. In: Flexas, J., Loreto, F. & Medrano, H. (eds): Terrestrial photosynthesis in a changing environment. A molecular, physiological and ecological approach. Cambridge University Press, Cambridge, UK, pp 20–40.
Ghimire, R.P., Silfver, T., Myller, K., Oksanen, E., Holopainen, J.K. & Mikola, J.
2022. BVOC emissions from a subarctic ecosystem, as controlled by insect herbivore pressure and temperature. Ecosystems 25: 872–
891.
Gornall, J.L. & Guy, R.D. 2007. Geographic variation in ecophysiological traits of black cottonwood (Populus trichocarpa). Can J Bot 85:
1202–1213.
Govindjee & Govindjee, R. 1974. The absorption of light in photosynthesis.
Scientific American 231: 68–82.
Hall, D., Luquez, V., Garcia, V.M., St Onge, K.R., Jansson, S. & Ingvarsson, P.K. 2007. Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): A comparison of neutral markers, candidate genes and phenotypic traits. Evolution 61: 2849–2860.
Heimonen, K. 2015. Plant-insect interactions on silver birch under a warming climate: A latitudinal translocation experiment. PhD thesis, University of Eastern Finland, Faculty of Science and Forestry,
Department of Biology.
https://erepo.uef.fi/handle/123456789/16226 (22 December 2022, date last accessed).
Heimonen, K., Valtonen, A., Kontunen-Soppela, S., Keski-Saari, S., Rousi, M., Oksanen, E. & Roininen, H. 2015a. Insect herbivore damage on latitudinally translocated silver birch (Betula pendula) – predicting the effects of climate change. Climatic Change 131: 245–257.
Heimonen, K., Valtonen, A., Kontunen-Soppela, S., Keski-Saari, S., Rousi, M., Oksanen, E. & Roininen, H. 2015b. Colonization of a host tree by herbivorous insects under a changing climate. Oikos 124: 1013–
1022.
Heimonen, K., Valtonen, A., Kontunen-Soppela, S., Keski-Saari, S., Rousi, M., Oksanen, E. & Roininen, H. 2017. Susceptibility of silver birch (Betula
pendula) to herbivorous insects is associated with the size and phenology of birch – implications for climate warming. Scandinavian Journal of Forest Research 32: 95–104.
Hetemäki, L., Kangas, J. & Peltola, H. (eds) 2022. Forest bioeconomy and climate Change. Springer International Publishing, Cham.
Hogg, E.H., Saugier, B., Pontailler, J.Y., Black, T.A., Chen, W., Hurdle, P.A. &
Wu, A. 1999. Responses of trembling aspen and hazelnut to vapor pressure deficit in a boreal deciduous forest. Tree Physiology 20:
725–734.
Hoshika, Y., Watanabe, M., Inada, N., Mao, Q. & Koike, T. 2013.
Photosynthetic response of early and late leaves of white birch (Betula platyphylla var. japonica) grown under free-air ozone exposure. Environmental Pollution 182: 242–247.
Hubbard, R.M., Ryan, M.G., Stiller, V. & Sperry, J.S. 2001. Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell & Environment 24: 113–
121.
Jadwiszczak, K. 2012. What can molecular markers tell us about the glacial and postglacial histories of European birches? Silva Fennica 46: 733–
745.
Jalkanen, R., Aalto, T. & Kurkela, T. 1995. Development of needle retention in Scots pine (Pinus sylvestris) in 1957–1991 in northern and southern Finland. Trees 10: 125–133.
Jankowski, A., Wyka, T., Żytkowiak, R., Danusevičius, D. & Oleksyn, J. 2019.
Does climate-related in situ variability of Scots pine (Pinus sylvestris L.) needles have a genetic basis? Evidence from common garden experiments. Tree Physiology 39: 573–589.
Jansen, E., Christensen, J.H., Dokken, T., Nisancioglu, K.H., Vinther, B.M., Capron, E., Guo, C., Jensen, M.F., Langen, P.L., Pedersen, R.A., Yang, S., Bentsen, M., Kjær, H.A., Sadatzki, H., Sessford, E. & Stendel, M.
2020. Past perspectives on the present era of abrupt Arctic climate change. Nature Climate Change 10: 714–721.
Järvinen, P., Lemmetyinen, J., Savolainen, O. & Sopanen, T. 2003. DNA sequence variation in BpMADS2 gene in two populations of Betula pendula. Molecular Ecology 12: 369–384.
Jia, G., Shevliakova, E., Artaxo, P., De Noblet-Ducoudré, N., Houghton, R., House, J., Kitajima, K., Lennard, C., Popp, A., Sirin, A., Sukumar, R. &
Verchot, L. 2019. Land–climate interactions. In: Shukla, P.R., Skea, J., Calvo Buendia, E., Masson-Delmotte, V., Pörtner, H.-O., Roberts, D.C., Zhai, P., Slade, R., Connors, S., van Diemen, R., Ferrat, M., Haughey, E., Luz, S., Neogi, S., Pathak, M., Petzold, J., Portugal Pereira, J., Vyas, P., Huntley, E., Kissick, K., Belkacemi, M. & Malley, J.
(eds.): Climate change and land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems.
Johnsen, K.H. & Seiler, J.R. 1996. Growth, shoot phenology and physiology of diverse seed sources of black spruce: I. Seedling responses to varied atmospheric CO2 concentrations and photoperiods. Tree Physiology 16: 367–373.
Jones, H.G. 1999. Use of thermography for quantitative studies of spatial and temporal variation of stomatal conductance over leaf surfaces.
Plant, Cell & Environment 22: 1043–1055.
Jones, M. & Harper, J.L. 1987. The influence of neighbours on the growth of trees: II. The fate of buds on long and short shoots in Betula pendula. Proceedings of the Royal Society of London, Series B, Biological Sciences 232: 19–33.
June, T., Evans, J.R. & Farquhar, G.D. 2004. A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf. Functional Plant Biology 31:
275–283.
Junker, A., Muraya, M.M., Weigelt-Fischer, K., Arana-Ceballos, F., Klukas, C., Melchinger, A.E., Meyer, R.C., Riewe, D. & Altmann, T. 2015.
Optimizing experimental procedures for quantitative evaluation of crop plant performance in high throughput phenotyping systems.
Frontiers in Plant Science 5: 1–21.