INSTITUTIONEN FÖR BIOLOGI OCH MILJÖVETENSKAP

EFFECT OF CLIMATE CHANGE ON REGENERATION With emphasis on P. tremuloides and P. tremula

Elsa Scharin

Degree project for Bachelor of Science with a major in biology BIO602 Biology: Thesis Course 15 hp First cycle Semester/Year: Spring 2020 Supervisor: Åslög Dahl, department of Biology and Environmental Sciences Examiner: Mats Andersson, department of Biology and Environmental Sciences

Photo on front page: Daniel Romani / WTML

Index

Abstract...... 2 Sammanfattning ...... 3 Introduction...... 4 A widespread genus ...... 4 Future climate poses a challenge ...... 5 Growth, bud set and flowering in temperate ...... 6 Aim ...... 7 Method...... 7 Result ...... 8 ...... 8 Temperature ...... 8 Fire ...... 8 Drought ...... 9 Europe ...... 10 Temperature ...... 10 Fire ...... 10 Drought ...... 11 Discussion ...... 11 Difficult to predict the future ...... 11 Temperature changes can lead to frost damage - but also more light ...... 11 Severe fire is better than mild fire ...... 12 Phenotypic plasticity and climate changes ...... 12 Conservation and management ...... 12 Further studies ...... 13 Conclusions ...... 13 Acknowledgements ...... 14 References ...... 15

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Abstract In an era of abrupt climate change there is a strong need for understanding the impact on our environment. With increasing temperatures worldwide leading to more wildfire and drought in many regions, combined with more frequent heat spells, the effect of these factors on the health of our most common trees is crucial to include in planning of future forest management. Populus species are common globally and Quaking (Populus tremuloides) and European aspen () are two of the most widespread species in their respective distribution areas, North America and Europe. This review aims to offer an overview of how the regeneration of Populus species, specifically Quaking and European aspen, are affected by temperature, fire and drought. This was done through selecting and reading relevant articles on the subject. Results show a sensitivity towards drought, especially in Quaking aspen through Sudden Aspen Decline (SAD), and elevated temperature although some studies point to increased growth in high temperature scenarios if water availability is sufficient. Asexual regeneration is often negatively affected by drought, through decreased number of root suckers. Sexual regeneration may be positively influenced by high temperature and fire, especially severe fire. Bud set and bud break can become advanced or delayed due to changes in temperature which in turn affects the growth season. This could also lead to freezing damage. Further research is needed on how pollen processes are affected by these factors. In conclusion, regeneration of aspen is generally affected negatively by drought and raised temperatures and positively by fire.

Key words: Populus, climate change, regeneration, fire, drought, temperature

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Sammanfattning I en tid av abrupta klimatförändringar finns ett stort behov av att förstå hur vår miljö påverkas. I takt med att världens medeltemperatur stiger, ökar samtidigt risken för torka och skogsbränder utöver fler värmeböljor. Effekten av dessa faktorer på våra vanligaste trädarter är därför viktigt att inkludera i framtida skogsskötsel. Arter i släktet Populus har global spridning, Populus tremuloides (Amerikansk asp) och Populus tremula (Vanlig asp) täcker stora arealer i Nordamerika respektive Europa. Arterna är viktiga för många andra djur och växter, utöver deras ekosystemtjänster. Den här litteraturuppgiften syftar till att ge en överblick över hur regeneration hos Populus-arter, närmare bestämt asp, påverkas av klimatförändringar såsom eld, temperaturförändringar och torka. Studien gjordes genom sökning och läsning av relevanta källor. Resultaten visar en känslighet mot torka speciellt hos amerikansk asp, vilket syns mest i fenomenet Sudden Aspen Decline (SAD). Även förhöjd temperatur har negativ påverkan, men tillväxt kan även öka om vattentillgång är tillräcklig. Torka kan leda till färre rotskott och eld kan leda till bättre etablering av frön, särskilt omfattande eld. Även värme kan påverka sexuell förökning positivt. Knoppbildning och knoppsprickning kan förskjutas p.g.a. temperaturförändringar vilket kan påverka tillväxtsäsongen samt öka risken för frostskador. Fler studier behövs på hur pollen processer påverkas av framtida scenarier. I slutsats, regeneration påverkas generellt negativt av klimatförändringar, särskilt torka. Ökade skogsbränder kan dock medföra lokala ökningar av mängden asp.

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Introduction A widespread genus Populus is a genus of trees with around 29 species which occupy many different habitats globally although they are mainly found in the northern hemisphere, in temperate and boreal areas (see fig. 1.1). Common names for some species are cottonwood, poplar and aspen. These trees favour moist soils, are sensitive to shade and long lived. They are also ecological pioneers with a high growth rate enabling them to quickly occupy areas outcompeting slower-growing species (Jansson, 2010). Aspen trees, P. tremuloides and P.tremula, specifically favour low elevation sites, high humidity and relatively cool temperatures (Carter et al., 2017). Most Populus are

Fig. 1.1 Map showing global distribution of different Populus species (Rogers, 2020).

dioecious and flower early in the spring, before leaf burst and the bud dormancy is released. Pollen is dispersed by wind and events such as fires, floods or ice movements facilitate the establishment of seeds. Many species also reproduce asexually, and large quantities of clones originating from a single tree can be found together. Vegetative growth occurs through root suckers, shoots from shallow roots, or through shoots from broken branches (Jansson, 2010).

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Future climate poses a challenge The planet is experiencing a human-induced global warming which have led the world’s temperature to increase by 1℃ since pre-industrial times (see fig 1.2.). This change has had, and is causing, serious consequences for both animals and plants on a global scale. The impact on forests and more specifically on trees is a subject that is important to understand not only since forests occupy large areas and provide habitats, food sources and protection for many other species, but also because they are provide countless ecosystem services (Allen, 2018).

The Northern Hemisphere, where most Populus species are found, has already been exposed to regional rises in temperature which are more than double than the global average (Allen, 2018). The number of heat spells are predicted to increase, besides the increase in average temperature.

Figure 1.2 Graph showing the yearly temperature change in ℃ relative to 1850-1900 (pre-industrial time reference) (Allen, 2018) Furthermore, precipitation patterns are changing and leading to more heavy rainfall events in most regions although total precipitation is expected to decrease in some parts of the world (Seneviratne, 2012). The combination of altered temperatures and precipitation patterns is also influencing the development and seriousness of drought, causing changes in water availability (Clark, 2016). Anthropogenic influence has likely lead to increased risk of drought since the early 20th century (Marvel, 2019). Fires have increased in North America during the late 20th century due to increased temperatures (Handmer, 2012). In southern Europe there has been reduced fire activity during the 21st century due to changes in land use and protective measures. However, there has also been an increase of warm, dry weather during the same period, which in turn can cause wildfire (Dupuy, 2020). Additionally, there a high probability of wildfires overall increasing globally with a warmer climate since it has been observed in historical records that abrupt climate change lead to more fire activity (Marlon, 2009).

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Growth, bud set and flowering in temperate plants Plants in temperate areas maximise their growth during spring and summer and minimize the damage from cold temperatures during autumn and winter by shifting between an active state of development and a stage of halted growth, or dormancy. The bud formation and initiation of flowering during spring is regulated by two stages of dormancy: endodormancy which is controlled by internal causes and ectodormancy which depends upon environmental factors. When the buds are endodormant they cannot develop even if the external conditions are favourable, since they are regulated from the inside. Therefore, when the endodormant stage is substituted by the ectodormant stage an environmental cue is still required to initiate flowering (Dahl, 2013).

The main factors influencing the onset of flowering is photoperiod, temperature and water availability. Plants react to the photoperiod through photoreceptors which are sensitive to different wavelengths. These different wavelengths may in turn promote or repress flowering. Temperature on the other hand, is an important factor in all living creatures since it regulates many different processes. Plants in different parts of the world have adapted to perform optimally at a certain temperature; the flowering period (the time from the first to the last flower) is quickened by a temperature above the normal level of collected heat or slowed if the temperature does not reach this threshold (Dahl, 2013).

Readiness to Spring flower •Dormancy release Winter •Bud flush

Dormancy Flowering •Endodormancy •Production of pollen •Ectodormancy •Dispersal and deposition of pollen

Bud set Summer Autumn •Cessation of growth Growth •Bud formation

Figure 1.3 A simplified model of the annual life cycle of a Populus individual growing in a temperate or boreal region. Many parts of the annual growth of a tree is affected by changes in temperature. These include bud flush, growth, growth cessation, bud set, bud dormancy and dormancy release (see fig. 1.3) Bud set includes cessation of growth and bud formation. The decrease in growth is triggered by lengthening night and sometimes temperature. Bud formation, in turn, is made up of three processes: bud formation, cold acclimation and initiation of dormancy (Rohde, 2011). The bud growth and initiation of dormancy is primarily controlled by temperature unlike the cessation of growth which,

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as mentioned earlier, mainly depends upon photoperiod as the effect of temperature varies between different species (Cooke, 2012).

On a similar note, another important adaptation in temperate trees including Populus is freezing tolerance. This refers to the ability to handle stress induced by sub-zero temperatures, for example drought. The cold forces the water out of the cell along the water potential gradient, and leaves the cell exposed to drought. Adaptations to survive this stage involve decreased growth as well as certain protective proteins. This freezing tolerance is first induced by shorter photoperiod in the autumn and is thereafter deepened further by cold temperatures as winter arrives. Colder conditions in the temperature-controlled stage results in an increased freezing tolerance (Jansson, 2010).

In the , a recent decline in aspen (P. tremuloides) populations has been observed which has led to several studies. The phenomenon has been named Sudden Aspen Decline (SAD) and could be connected to climate change (Singer, 2019; J. J. Worrall, Keck, & Marchetti, 2015; J. J. Worrall, Rehfeldt, G. E., Hamann, A., Hogg, E. H., Marchetti, S. B., Michaelian, M. & Gray, L. K., 2013).

Aim The aim of this project is to review the current knowledge of how climate change affects the regeneration of Populus. To understand changing conditions is crucial when it comes to ensuring effective forest management. Climate change is a broad and multi-faceted subject with many factors influencing biology however this study will focus on temperature, drought and fire events and how they interact with P. tremuloides and P. tremula. Since fire enables seed establishment in many Populus species, this could have a positive impact on the development of seedlings. Temperature could influence dormancy and thus the timing and intensity of flowering. Changed precipitation patterns could lead to increased flooding or drought. These are all factors which will be reviewed in this essay.

Method The search for relevant information was mainly performed using Web of Science, as well as the search engine available through the university library’s webpage (https://www.ub.gu.se/sv). The search words initially used were: Populus, regeneration/ reproduction, climate and fire. In Web of Science, wildcards such as *, $, ?, search operators and phrase searching were utilized, for example: Populus AND (regeneration OR reproduction) AND “climate change”. Other frequently used

•Search •Notes words •List + End Note Search Selection Reading •Revise •Search •Revise search search design

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search words were phenology, pollen, temperature, fire and drought. Other words that were used fewer times were for example masting, budburst and freezing tolerance. The selection of information was made through searching, selecting articles with interesting titles and adding them to a list. Afterwards the abstract were read and if the article was considered relevant for the review it was downloaded into End Note and read more thoroughly. Occasionally when finding a suitable article, the references cited in it were explored as well as articles citing that article. Frequent notes where taken when reading. During both the selection and reading process, the search words and design was continuously revised.

Result The following text is the result connected to the search words presented in the method. Finding relevant information on the topic was challenging in some areas. For example, it was difficult to locate articles on how the reproductive processes such as flowering and pollen production might be influenced by climate change. Other areas were more thoroughly studied, such as the effect of drought on P. tremuloides in the U.S. Most articles found were made in North America and Europe, which is why the result is divided into these two regions with the factors investigated; temperature, fire and drought found beneath each region. This presentation was made to offer an overview of the studies made on each factor in the respective continents.

North America Temperature Carroll et al. studied establishment of seedlings of P. tremuloides planted along a temperature and elevation gradient in Colorado, U.S.A., and found a positive correlation between higher temperatures and the osmotic potential in the leaves, since higher temperatures lead to decreased soil moisture. This affected growth efficiency negatively. Instead the growth efficiency was optimal at a cooler temperature and highest at an intermediate temperature which was similar to the site from which the seeds originated. They concluded that Quaking aspen may experience reduced growth performance in the future, affecting its distribution in the area (Carroll, 2019).

Shinneman et al. found that clonal regeneration over time was connected to climate since establishment of Quaking aspen ramets depends on temperature and moisture (Shinneman, 2019). In , the distribution of Quaking aspen in northern latitudes was concentrated to southern slopes suggesting that microclimate affects the northern distribution line in the region. The southern tendency was weaker in mid and low latitudes, further strengthening the theory (Whitbeck, 2016). During a 7-decade long study performed in Canada where the flowering time was observed in relation to temperature, the bloom date of P. tremuloides occurred earlier and earlier in the spring. In the end flowering started two weeks earlier than it did at the start of the study (Beaubien, 2011).

Fire Gill et al. used algorithm modelling to investigate the settlement of Quaking aspen seedlings and how it is affected by different factors. Their result showed that fire had a positive impact on aspen seedlings and that in some cases severe fire had a more positive impact on young regeneration than a mild one (Gill, 2017). In another study made in , U.S.A., the effect of fire severity on

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regeneration and resilience to browsing was examined. More severe fire had a positive effect on regeneration. Furthermore, the seedlings developed stronger defence towards herbivores, caused by increased light conditions which in turn enabled stronger growth and chemical deterrence (H. Y. Wan, Rhodes, A. C. & St. Clair, S. B., 2014). Fire severity also had a positive effect on regeneration and recruitment. Seedlings were more frequent and larger in locations were fire had been severe (H. Y. Wan, Olson, A. C., Muncey, K. D. & St. Clair, S. B. , 2014). In a field study measuring seedling recruitment of mixed trees in Canada, aspen dominance was observed in areas that had burned and fire severity was positively correlated with dominance. The seedling density was measured one year after fire and re-measured three years after fire (Whitman, 2018).

Drought In 2004 in the United States an increased mortality in Quaking aspen involving rapid dieback of branches causing thinning of the crown, was first documented. This led to major stem mortality in many stands and in 2006 it was named “Sudden Aspen Decline” (SAD) due to its fast progression (J. J. Worrall, Marchetti, S. B., Egeland, L., Mask, R. A., Eager, T. & Howell, B., 2010). The term sudden is also to separate the decline from normal age-related mortality which takes place over the course of decades whereas SAD typically leads to complete mortality of a stand within 2-5 years (Singer, 2019). SAD gradually escalated and in 2008 it affected around 17% of the aspen cover in Colorado. When comparing the moisture status of healthy and damaged aspen, the trees which were suffering from SAD showed a deficit of moisture which led to the conclusion that drought

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Figure. 3.1. Graph showing mean mortality in % of healthy and SAD damaged plots in different sized groups of P. tremuloides: overstory (p < 0.001), large (p = 0.35), medium (p = 0.41) and small (p = 0.92) regeneration. DBH = stem diameter at breast height. (Worrall et al., 2010) was the primary cause (J. J. Worrall, Marchetti, S. B., Egeland, L., Mask, R. A., Eager, T. & Howell, B., 2010; J. J. Worrall, Rehfeldt, G. E., Hamann, A., Hogg, E. H., Marchetti, S. B., Michaelian, M. & Gray, L. K., 2013) and when combined with young age and dense structure of the stand, mortality increases (Bell, 2014). Other factors affecting the impact of SAD include the width of the stem and the type of site. Trees which grew higher up on slopes were more affected by the decline which was in line with drought being the main factor (J. J. Worrall, Marchetti, S. B., 9

Egeland, L., Mask, R. A., Eager, T. & Howell, B., 2010). Mortality caused by SAD mainly affected large individuals whereas smaller trees where less affected (see fig. 3.1.). However, SAD did not affect the mortality during regeneration significantly, when looking at all the sizes of regeneration together, although the mean mortality was a little higher in damaged plots compared to healthy ones (J. J. Worrall, Marchetti, S. B., Egeland, L., Mask, R. A., Eager, T. & Howell, B., 2010). Moreover, when the same plots were re-investigated in 2013, sick trees showed a continuing deterioration with substantial crown loss, many recently dead trees, and dead branches. The number of root suckers was also significantly lower in sick areas compared to that of healthy ones. An average of 500 stems ha-1 were lost during the study in the plots that contained sick trees (J. J. Worrall et al., 2015).

Besides studies of SAD, sensitivity to drought and temperature in Quaking aspen was also studied by Paudel et al. in Canada when they modelled how different factors affected regeneration. The result showed that increased precipitation was favourable and high temperature was disadvantageous. A similar result was observed for Balsam poplar, although if soil moisture was sufficient regeneration was not inhibited even when temperature was high (Paudel, 2015).

Europe Temperature In Sweden, European aspen has expanded along the alpine treeline in the subarctic region as a result of warmer summer temperatures. The increased temperature is believed to have favoured sexual reproduction in the species, thus enabling it to increase its colonisation of the area and competing with birch (Betula pubescens subsp. tortuosa) which is the normal occupant of the alpine treeline (Van Bogaert, 2010). Elevated temperature caused delayed bud set and advanced bud flush in young European aspen during an experimental study to investigate the effect of temperature and other factors on bud phenology (U. Sivadasan, Randriamanana, T., Chenhao, C., Virjamo, V., Nybakken, L. & Julkunen-Tiitto, R., 2017). It also caused greater total biomass as well as increased vertical growth and width in the treated plants compared to control plants (U. Sivadasan, Chenhao, C., Nissinen, K., Randriamanana, T., Nybakken, L. & Julkunen-Tiitto, R., 2018). Increased growth due to higher temperature was also observed in 2-year old aspen plants in an experimental field study made in Finland (Nissinen, 2017).

In another study, wild seedlings of European aspen were subjected to experiments in greenhouses to see how temperature and soil moisture affected the survival in terms of resilience to frost damage. The factors were modelled after the 2100 warming scenario of a 4℃ increase in world mean temperature. The result showed that the 4℃ treatment had a significant effect on the seedlings, by increasing the mortality. Although this treatment, combined with increased soil moisture initially caused an elevated growth scenario, the seedlings had a higher mortality after a freezing treatment than the ones that had been exposed to lower temperatures and the same soil moisture, both lower temperatures and soil moisture, and the control. However, some seedlings survived the freezing, which could be put to adaptive potential within the population (Zeps, 2017).

Fire Studies on the effect of fire on European aspen was mainly restricted to historical pollen and charcoal analyses of past fire events and studies where fire was used in forest management. Thus, finding relevant articles relating climate change-induced fire to regeneration proved a challenge. Latva-Karjanmaa et al. reported more seedlings in burned soil when looking at moisture and fire effects on seedling emergence and survival (Latva-Karjanmaa, 2006). In another study, seedlings

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were planted on different types of soil of which some types where burned. Other factors included soil moisture and protective cover of seedlings. Results showed that seedlings not always grow better in burned soil, as mineral soil yielded taller seedlings than burned organic substrate did (De Chantal, 2005).

Drought Seedlings of European aspen lost significant amounts of foliage when subjected to dry conditions. However, when they were exposed to a hot and wet treatment, they lost fewer leaves than the control seedlings. Also, water use efficiency (WUE) was higher in the aspen seedlings after the hot and dry conditions compared to some of the other species investigated (Pliura, 2018). As mentioned earlier, Zeps et al performed experiments on seedlings where drought was detrimental to height in seedlings. However, the effect of different soil moistures on survival was not significant (Zeps, 2017). The emergence and survival of seedlings was observed in experimental fields in Finland (Latva-Karjanmaa, 2006). This showed that seedlings favoured soil that had good water availability, as well as burned soil, as mentioned earlier.

Discussion Difficult to predict the future When comparing the different results included in this review it is apparent that there is no universal answer as to how aspen is affected by climate change. Since climate change is such a broad term, involving many different processes, factors and phenomena, every outcome of their individual and combined influence is difficult to anticipate. The differences and similarities within the result will be discussed in further detail below.

Temperature changes can lead to frost damage - but also more light The establishment of P. tremuloides ramets depends on temperature and moisture (Shinneman, 2019). This could be expected since historically, aspen has been shown to benefit from cool climate and frequent fires, whereas warmth is inhibiting for regeneration (Carter et al., 2017). High temperature lead to high mortality in seedlings when they are subjected to frost treatment. Although P. tremula therefore may suffer from warming, some seedlings survived the treatment. This competition within the population might provide an adaptive response towards frost damage (Zeps, 2017). Furthermore, if frost damage increases, the amount of damage may prove important to survival. Freezing teamed with complete defoliation leads to diminished growth whereas a smaller degree of defoliation does not significantly affect the growth in both P. tremuloides and P. balsamifiera (Man, 2013). How defoliation affects growth and regeneration is especially necessary to consider as defoliation is one of the main symptoms of Sudden Aspen Decline (SAD) in the United States (Singer, 2019). Defoliation however, leads to increased light conditions which also favour regeneration (Zhao, 2018), thus the mortality caused by climate change could be dampened by providing good conditions for seedlings to grow in, as stands thin out. On the same topic, aspen mortality was compensated by an increased regeneration in P. davidiana in China. Measurements in wild stands revealed that although large individuals had died due to warming and drought, the increased light conditions facilitated the regeneration of seedlings, which increased significantly in number during the study period (Zhao, 2018).

Moreover on the topic of SAD, Worrall et al. showed that large individuals were affected more severely by the decline than those belonging to a younger regeneration (J. J. Worrall, Marchetti, S. B., Egeland, L., Mask, R. A., Eager, T. & Howell, B., 2010). This could be due to size, since as 11

they are larger than younger individuals, they have a greater water uptake and therefore are more affected by drought. Fewer root suckers were observed in SAD-affected stands (J. J. Worrall et al., 2015) which suggests that although already established young regeneration was not as strongly affected as adult ones, a long and untreated exposure to SAD may cause a severe decrease in the number of new young trees. Although many studies have been made on SAD in the U.S., this phenomenon seems to be absent in Europe, or at least poorly investigated. This is crucial to study further, since Quaking and European aspen are closely related and therefore could be expected to have a similar response towards drought. This is especially important since it was found that seedlings of European aspen lost leaves when subjected to drought (Pliura, 2018), which is similar to what was observed in Quaking aspen (Singer, 2019). If SAD is found in Europe, an early discovery and response might lessen the consequences before mortality advances too far. Such a response might be in the form of clearcutting of certain areas, which was suggested in a field study made in 2015. This study observed improved regeneration in SAD-affected areas that had been clearcut (Shepperd, 2015). This might be because the lessened density of the stand drastically increases the available water for the remaining trees and leads to better health of these individuals.

Severe fire is better than mild fire As mentioned in the introduction, fire has a positive effect on aspen regeneration. Additionally, severe fire facilitates seedling recruitment and establishment better than non-severe fire (Gill, 2017; Latva-Karjanmaa, 2006; H. Y. Wan, Olson, A. C., Muncey, K. D. & St. Clair, S. B. , 2014; Whitman, 2018). With this in mind, in a future scenario where wildfire is expected to occur more often (Handmer, 2012) aspen regeneration is likely to experience a surge. Provided that fires are severe enough, that is. In the case of more, but relatively mild fire events, regeneration could remain unaltered or even decrease. This would be consistent with the findings of Whitman et al. who observed fewer seedlings in areas where fire had been mild (Whitman, 2018).

Phenotypic plasticity and climate changes Genetic variation may cause a variation of the response towards climate change, within a species since many boreal trees, Populus included, cover large areas of land (Hänninen, 2011). But also, phenotypic plasticity may be important in the warming climate since it could enable individual trees to respond to changing conditions. In balsam poplar (P. balsamifiera) genetic heritability of bud flush and bud set was investigated in trees growing in a northern region to trees in a southern region. The result showed that there was a difference in when bud set and bud flush occurred due to different requirements of photoperiod and heat accumulation. The variability in genes controlling these processes suggest that balsam poplar can over time adapt to a changing growing season. The authors proposed that this could influence future distribution of different genotypes since in a warming climate, southern trees could utilize the growth period more efficiently than northern ones. This was due to the fact that they are genetically bound to set bud later, thus allowing for more growth, than its northern counterpart (Olson, 2013). This makes it even more difficult to anticipate a global response of aspen towards climate change. Since climate change already affects different regions in different ways (Seneviratne, 2012), and if the response of aspen varies due to phenotypic plasticity, this is a further call to more regional research.

Conservation and management As CO₂ uptake through trees is a very efficient system for mitigating climate change on a global scale (Bastin, 2019), the future of aspen stands is relevant to tree restoration projects. Bastin et al. performed global mapping of the potential area that could be covered by trees and how it could increase the carbon sink. There is according to the article 0.9 billion hectares of potential canopy 12

cover which would be able store 205 gigatons of carbon. This would substantially reduce the concentration of carbon dioxide in the atmosphere. However, the amount of available area is shrinking as climate change proceeds which is why this restoration process has an expiration date (Bastin, 2019). Successfully evaluating the health of current aspen stands, which cover many hectares in both North America and Europe (Jansson, 2010), and managing them with appropriate measures, can thus increase the amount of stored carbon in those regions. On the same topic, management of declining forests can be further useful on a regional scale. Due to the positive effect that severe fire has on aspen regeneration (Gill, 2017; H. Y. Wan, Olson, A. C., Muncey, K. D. & St. Clair, S. B. , 2014; H. Y. Wan, Rhodes, A. C. & St. Clair, S. B., 2014; Whitman, 2018) fire could be used as a restoration method., as mentioned earlier. Fire was also prescribed by Singer et al. along with the use of coppicing to improve aspen health (Singer, 2019). As mentioned earlier, in 2015 a field experiment on SAD-affected aspen showed that clearcutting had a positive impact on regeneration. However, the result depended on the magnitude of the current mortality in the stand. Therefore, the authors concluded that treatment should be performed before mortality was too severe (Shepperd, 2015). The impact of widespread clearcutting on other wildlife however, is something that should be taken into consideration. Since the response may vary between different species with some reacting to a changed habitat and others mainly are affected by fragmentation, it is important to study them independently (St-Laurent, 2009). Perhaps the practice of clearcutting could be sparingly used, and then only at the stands which are most affected by SAD, to limit unwanted effects on other flora and fauna. When looking at stands affected by drought, forest management can either intensify the negative effect of drought or alleviate drought stress depending on how it is structured and implemented. Thus it is important to address the need of each stand on an individual basis (Clark, 2016). This approach is similar to that which was mentioned earlier concerning phenotypic plasticity, and could thus be beneficial from several standpoints.

Further studies Further studies on aspen regeneration is needed in several areas. For example, what is the effect of several stressors combined? As already discussed, warming combined with drought is detrimental to growth whereas warmth combined with good water availability increases growth (Carroll, 2019; Paudel, 2015). Perhaps there are unknown disadvantages of the combination of say, fire disturbance followed by high or low summer temperature. More information is also needed on pollen production and dispersal, specifically how they are affected by changing spring temperatures or moisture conditions. Most experimental studies included in this review were performed on seedlings, which shows that further studies also could be undertaken on features of asexual regeneration such as root suckers and ramets.

Conclusions There seems to have been an increase in the amount of research made in the area concerning climate change and forestry. Precise predictions are impossible, when it comes to exactly how the regeneration of Populus will be affected by future climate changes. In short terms, higher temperatures and drought is negative for both Quaking and European aspen, whereas fire, especially severe fire events, is positive. Based on the result in this review drought seems to be the single biggest threat to regeneration of aspen since normal or good growth has been observed in the presence of high temperature and good water availability although only high temperature has been detrimental to the health of the plant. In conclusion, in view of our current knowledge, the regeneration of Populus tremuloides and Populus tremula is affected both negatively and positively by climate change.

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Acknowledgements The author would like to thank the supervisor of the project, Åslög Dahl. Other thanks go out to the course leader, Mats Andersson, and Nicolina Andersson.

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