Plant Biology ISSN 1435-8603
RESEARCH PAPER
Effects of temperature and drought manipulations on seedlings of Scots pine provenances S. Taeger1,2, T. H. Sparks3,4,5,6 & A. Menzel1,3 1 2 3 4 5 6
€nchen, Freising, Germany Technische Universit€ at Mu Bavarian State Institute of Forestry, Freising, Germany €nchen, Garching, Germany Institute for Advanced Study, Technische Universit€ at Mu University of Life Sciences, Poznan , Poland Institute of Zoology, Poznan Department of Zoology, University of Cambridge, Cambridge, UK Sigma, Coventry University, Coventry, UK
Keywords Climate change; extremes; manipulation experiment; Pinus sylvestris; plasticity. Correspondence Steffen Taeger, Bavarian State Institute of Forestry, Hans-Carl-von-Carlowitz Platz 1, 85354 Freising, Germany. E-mail: [email protected] Editor H. Rennenberg Received: 11 April 2014; Accepted: 1 August 2014 doi:10.1111/plb.12245
ABSTRACT Rising temperatures and more frequent and severe climatic extremes as a consequence of climate change are expected to affect growth and distribution of tree species that are adapted to current local conditions. Species distribution models predict a considerable loss of habitats for Pinus sylvestris. These models do not consider possible intraspecific differences in response to drought and warming that could buffer those impacts. We tested 10 European provenances of P. sylvestris, from the southwestern to the central European part of the species distribution, for their response to warming and to drought using a factorial design. In this common-garden experiment the air surrounding plants was heated directly to prevent excessive soil heating, and drought manipulation, using a rain-out shelter, permitted almost natural radiation, including high light stress. Plant responses were assessed as changes in phenology, growth increment and biomass allocation. Seedlings of P. sylvestris revealed a plastic response to drought by increased taproot length and root–shoot ratios. Strongest phenotypic plasticity of root growth was found for southwestern provenances, indicating a specific drought adaptation at the cost of overall low growth of aboveground structures even under non-drought conditions. Warming had a minor effect on growth but advanced phenological development and had a contrasting effect on bud biomass and diameter increment, depending on water availability. The intraspecific variation of P. sylvestris provenances could buffer climate change impacts, although additional factors such as the adaptation to other climatic extremes have to be considered before assisted migration could become a management option.
INTRODUCTION Climate change will have a major impact on European forests, including the goods and services they provide (Lindner et al. 2010). In addition to a rise of mean temperatures, an increase of extreme climatic events is expected (Salinger 2005; Beniston et al. 2007; IPCC 2012, 2013). Due to the particular importance of extreme events in shaping forest ecosystems (Fuhrer et al. 2006) and their possible consequences (Reichstein et al. 2013; Reyer et al. 2013), the adaptedness and adaptability of forest trees to increased climate variability is a prerequisite for survival under future conditions. A changing climate has now been shown to contribute to dieback of forest trees (Allen et al. 2010). The numerous reports on Pinus sylvestris mortality (Dobbertin et al. 2005; Galiano et al. 2010; Giuggiola et al. 2010) could therefore suggest a gradual decline of its southernmost distribution in the future, accompanied by an expansion to higher latitudes (Matıas & Jump 2012). As a consequence, for many regions, such as Germany, the future fitness of this species is questioned, as for other tree species, e.g. Picea abies (K€ olling et al.
2009). However, due to its huge distribution range (Euforgen 2009), P. sylvestris inhabits contrasting environments and has evolved wide genotypic variation and phenotypic plasticity (Lang et al. 2007). This has resulted in considerable differences in phenology, morphology and growth traits among different P. sylvestris provenances described in various provenance tests of this species (Giertych 1979; Matyas 1996). Pinus sylvestris provenances reveal latitudinal and longitudinal clines, and differ in bud burst, growth cessation and bud set (Andersson & Fedorkov 2004; Chmura et al. 2012). Growth rates and overall growth traits vary among provenances even at the seedling stage (Chmura et al. 2012) and continue to maturity (Giertych 1979). This was also demonstrated in a greenhouse experiment using the same provenances as in this study (Taeger et al. 2013a). In the context of climate change, populations at the rear edge of the distribution are of special interest because they could store special genetic diversity or adaptations to heat or drought (Nielsen & Jørgensen 2003; Hampe & Petit 2005). However, those populations have often been neglected in established provenance trials, which have focused mainly on quality and maximum growth under optimum conditions.
Plant Biology 17 (2015) 361–372 © 2014 German Botanical Society and The Royal Botanical Society of the Netherlands
361
Provenance manipulation
Taeger, Sparks & Menzel
In spite of high within-population variability and low genetic differentiation of P. sylvestris populations (Prus-Glowacki & Stephan 1994; Robledo-Arnuncio et al. 2005), investigations of European populations reveal differences in genetic variation, particularly between populations of the continuous distribution range and marginal populations. Spanish provenances are distinguished by characteristic patterns of rare alleles (Prus-Głowacki et al. 2012). Scalfi et al. (2009) showed the distinctiveness of Italian provenances derived from the Apennine region. Provenances with different genetic composition are also expected to exhibit different responses to extreme events (Thiel et al. 2012). Thus, the characterisation of their genetic composition, as well as investigation of their response patterns, is of utmost importance to predict the future performance of P. sylvestris provenances in response to increased climatic variability (Martınez-Vilalta et al. 2012). Identification of pre-adapted provenances could then enable assisted migration to be used as a tool to stabilise forest stands for the future (Kreyling et al. 2011). The response of tree growth to temperature is not uniform. In some experiments warming did not impact growth performance of P. sylvestris (Richter et al. 2012), Pinus nigra (Thiel et al. 2012) or oak species (Kuster et al. 2013). Pumpanen et al. (2012) describe a positive effect of temperature on root biomass, photosynthetic rate and respiration of P. sylvestris, Picea abies and Betula pendula. A rise in temperature can increase P. sylvestris growth as long as water availability is sufficient (Martınez-Vilalta et al. 2008). In contrast, high temperatures accompanied by strong radiation input can boost evaporation rates and negatively affect growth conditions (Pichler & Oberhuber 2007). Therefore an increase in temperatures due to climate change is expected to reduce growth and survival of P. sylvestris trees in warm and dry regions, whereas it will stimulate growth in temperature-limited areas of higher altitudes or northern latitudes (Reich & Oleksyn 2008). In addition, extreme high temperatures are a serious threat since they affect plant metabolism directly (Rennenberg et al. 2006) and have to be taken into consideration. Clearly, the impact of drought leads to growth reduction and plays a major role in the discussion of mortality and dieback of P. sylvestris (Dobbertin et al. 2007; Eilmann et al. 2011; Vacchiano et al. 2012). Growth reductions due to limited water availability are associated with allocation changes in trees (Delucia et al. 2000; Breda et al. 2006). Differences in the response to drought stress among provenances are expected, although Thiel et al. (2012) could not prove this for P. nigra provenances. Similar to the results of Czajkowski & Bolte (2006) for Fagus sylvatica, the studies of Cregg & Zhang (2001) and Alia et al. (2001) provide evidence for differences in drought adaptation among P. sylvestris provenances. In order to obtain a mechanistic understanding of tree responses to extreme events, experiments are indispensable (Jentsch et al. 2007; Reyer et al. 2013). The relevance of results depends on the design of the experiment. Pot experiments easily allow the control of important factors affecting plant responses, but encompass a number of artefacts at the same time (Ray & Sinclair 1998; Passioura 2006). Most importantly, natural root development is hindered, being a trait of major interest in terms of drought response. Root growth is also affected by planting, which has to be taken into account in investigations focusing on seedlings and young plants (Gross362
nickle 2005; Struve 2009). Furthermore, microclimatic artefacts have to be minimised to simulate climatic extremes as realistically as possible. The manipulation of precipitation using permanent shelters causes various artefacts such as shading or passive warming (Beier et al. 2012). In particular, radiation, as a potential additional stress factor, is often neglected. However, high light stress is one component of stress affecting plants during heatwaves, accompanying a precipitation deficit and maximum temperatures (De Boeck et al. 2010). In addition, atmospheric feedback in terms of altered potential evapotranspiration is absent under permanent shelters, which could be alleviated by simultaneous heating. Open-top chambers are a viable method for increasing daytime temperature, but their heating capacity is usually limited (Godfree et al. 2011). Active heating via infrared lamps to imitate climate change has been controversial (Aronson & McNulty 2009; Amthor et al. 2010). Experiments using soil heating via heating cables are another approach (Richter et al. 2012), but this method affects belowground parts of plants to a larger extent than aboveground parts. It would be more realistic to directly warm the air enveloping the plants (Amthor et al. 2010). In this study, we investigated the response of P. sylvestris seedlings to predicted future climate conditions. We tested 10 provenances from the southwestern border of its distribution range up to more central European origins in the field using a factorial combination of warming and drought. Warming was achieved using a novel advanced air heating system preventing excessive soil warming, whereas drought was simulated using an automatic rain-out shelter allowing for high light stress and almost natural radiation throughout the experiment. We assessed plant responses as changes in phenology, growth increment, allocation and overall growth performance. We focused on the following questions: (i) are there differences in growth traits between the treatments and populations; (ii) are there differences between the provenances in their response to drought and warming; (iii) does warming enhance drought stress; (iv) is there a trade-off between performance of provenances under control conditions and under drought; and (v) are we able to identify a provenance better adapted to extreme conditions? MATERIAL AND METHODS Provenances and treatment of seeds and seedlings We used seeds of P. sylvestris from 10 different regions for this experiment (Table 1). Except for the German progeny, Alpenkiefer, which was obtained from a seed orchard in Germany (parent trees originate from the Bavarian Alps, above 900 m a.s.l.), all seeds were derived from autochthonous populations. For more details about the origin of seeds as well as genetic information, see Taeger et al. (2013a). Throughout the study we will refer to all progeny simply as ‘provenances’ or ‘populations’. Five days before sowing, seeds were soaked in water for 12 h. Seeds were sown in a split-plot design on 25 May 2011. Seedling locations within the plots were defined following a regular grid. We sowed 10 seeds at each seedling location, reduced the germinated seedlings at each location to three individuals on 30 July 2011 and further to one individual on 1 March 2012. During the germination period, all plots were covered with a
Plant Biology 17 (2015) 361–372 © 2014 German Botanical Society and The Royal Botanical Society of the Netherlands
Provenance manipulation
Taeger, Sparks & Menzel
Table 2. Results of the split plot ANOVA of whole-plot factors drought, warming and the subplot factor provenance on stem length increment and diameter increment in the period from July to October 2012. stem length increment (July–October)
drought warming drought 9 warming whole-plot error provenance provenance 9 drought provenance 9 warming provenance 9 drought 9 warming subplot Error total
diameter increment (July–October)
df
F
P
df
F
P
1 1 1 8 9 9 9 9 72 119
141.76 0.97 3.17
RESEARCH PAPER
Effects of temperature and drought manipulations on seedlings of Scots pine provenances S. Taeger1,2, T. H. Sparks3,4,5,6 & A. Menzel1,3 1 2 3 4 5 6
€nchen, Freising, Germany Technische Universit€ at Mu Bavarian State Institute of Forestry, Freising, Germany €nchen, Garching, Germany Institute for Advanced Study, Technische Universit€ at Mu University of Life Sciences, Poznan , Poland Institute of Zoology, Poznan Department of Zoology, University of Cambridge, Cambridge, UK Sigma, Coventry University, Coventry, UK
Keywords Climate change; extremes; manipulation experiment; Pinus sylvestris; plasticity. Correspondence Steffen Taeger, Bavarian State Institute of Forestry, Hans-Carl-von-Carlowitz Platz 1, 85354 Freising, Germany. E-mail: [email protected] Editor H. Rennenberg Received: 11 April 2014; Accepted: 1 August 2014 doi:10.1111/plb.12245
ABSTRACT Rising temperatures and more frequent and severe climatic extremes as a consequence of climate change are expected to affect growth and distribution of tree species that are adapted to current local conditions. Species distribution models predict a considerable loss of habitats for Pinus sylvestris. These models do not consider possible intraspecific differences in response to drought and warming that could buffer those impacts. We tested 10 European provenances of P. sylvestris, from the southwestern to the central European part of the species distribution, for their response to warming and to drought using a factorial design. In this common-garden experiment the air surrounding plants was heated directly to prevent excessive soil heating, and drought manipulation, using a rain-out shelter, permitted almost natural radiation, including high light stress. Plant responses were assessed as changes in phenology, growth increment and biomass allocation. Seedlings of P. sylvestris revealed a plastic response to drought by increased taproot length and root–shoot ratios. Strongest phenotypic plasticity of root growth was found for southwestern provenances, indicating a specific drought adaptation at the cost of overall low growth of aboveground structures even under non-drought conditions. Warming had a minor effect on growth but advanced phenological development and had a contrasting effect on bud biomass and diameter increment, depending on water availability. The intraspecific variation of P. sylvestris provenances could buffer climate change impacts, although additional factors such as the adaptation to other climatic extremes have to be considered before assisted migration could become a management option.
INTRODUCTION Climate change will have a major impact on European forests, including the goods and services they provide (Lindner et al. 2010). In addition to a rise of mean temperatures, an increase of extreme climatic events is expected (Salinger 2005; Beniston et al. 2007; IPCC 2012, 2013). Due to the particular importance of extreme events in shaping forest ecosystems (Fuhrer et al. 2006) and their possible consequences (Reichstein et al. 2013; Reyer et al. 2013), the adaptedness and adaptability of forest trees to increased climate variability is a prerequisite for survival under future conditions. A changing climate has now been shown to contribute to dieback of forest trees (Allen et al. 2010). The numerous reports on Pinus sylvestris mortality (Dobbertin et al. 2005; Galiano et al. 2010; Giuggiola et al. 2010) could therefore suggest a gradual decline of its southernmost distribution in the future, accompanied by an expansion to higher latitudes (Matıas & Jump 2012). As a consequence, for many regions, such as Germany, the future fitness of this species is questioned, as for other tree species, e.g. Picea abies (K€ olling et al.
2009). However, due to its huge distribution range (Euforgen 2009), P. sylvestris inhabits contrasting environments and has evolved wide genotypic variation and phenotypic plasticity (Lang et al. 2007). This has resulted in considerable differences in phenology, morphology and growth traits among different P. sylvestris provenances described in various provenance tests of this species (Giertych 1979; Matyas 1996). Pinus sylvestris provenances reveal latitudinal and longitudinal clines, and differ in bud burst, growth cessation and bud set (Andersson & Fedorkov 2004; Chmura et al. 2012). Growth rates and overall growth traits vary among provenances even at the seedling stage (Chmura et al. 2012) and continue to maturity (Giertych 1979). This was also demonstrated in a greenhouse experiment using the same provenances as in this study (Taeger et al. 2013a). In the context of climate change, populations at the rear edge of the distribution are of special interest because they could store special genetic diversity or adaptations to heat or drought (Nielsen & Jørgensen 2003; Hampe & Petit 2005). However, those populations have often been neglected in established provenance trials, which have focused mainly on quality and maximum growth under optimum conditions.
Plant Biology 17 (2015) 361–372 © 2014 German Botanical Society and The Royal Botanical Society of the Netherlands
361
Provenance manipulation
Taeger, Sparks & Menzel
In spite of high within-population variability and low genetic differentiation of P. sylvestris populations (Prus-Glowacki & Stephan 1994; Robledo-Arnuncio et al. 2005), investigations of European populations reveal differences in genetic variation, particularly between populations of the continuous distribution range and marginal populations. Spanish provenances are distinguished by characteristic patterns of rare alleles (Prus-Głowacki et al. 2012). Scalfi et al. (2009) showed the distinctiveness of Italian provenances derived from the Apennine region. Provenances with different genetic composition are also expected to exhibit different responses to extreme events (Thiel et al. 2012). Thus, the characterisation of their genetic composition, as well as investigation of their response patterns, is of utmost importance to predict the future performance of P. sylvestris provenances in response to increased climatic variability (Martınez-Vilalta et al. 2012). Identification of pre-adapted provenances could then enable assisted migration to be used as a tool to stabilise forest stands for the future (Kreyling et al. 2011). The response of tree growth to temperature is not uniform. In some experiments warming did not impact growth performance of P. sylvestris (Richter et al. 2012), Pinus nigra (Thiel et al. 2012) or oak species (Kuster et al. 2013). Pumpanen et al. (2012) describe a positive effect of temperature on root biomass, photosynthetic rate and respiration of P. sylvestris, Picea abies and Betula pendula. A rise in temperature can increase P. sylvestris growth as long as water availability is sufficient (Martınez-Vilalta et al. 2008). In contrast, high temperatures accompanied by strong radiation input can boost evaporation rates and negatively affect growth conditions (Pichler & Oberhuber 2007). Therefore an increase in temperatures due to climate change is expected to reduce growth and survival of P. sylvestris trees in warm and dry regions, whereas it will stimulate growth in temperature-limited areas of higher altitudes or northern latitudes (Reich & Oleksyn 2008). In addition, extreme high temperatures are a serious threat since they affect plant metabolism directly (Rennenberg et al. 2006) and have to be taken into consideration. Clearly, the impact of drought leads to growth reduction and plays a major role in the discussion of mortality and dieback of P. sylvestris (Dobbertin et al. 2007; Eilmann et al. 2011; Vacchiano et al. 2012). Growth reductions due to limited water availability are associated with allocation changes in trees (Delucia et al. 2000; Breda et al. 2006). Differences in the response to drought stress among provenances are expected, although Thiel et al. (2012) could not prove this for P. nigra provenances. Similar to the results of Czajkowski & Bolte (2006) for Fagus sylvatica, the studies of Cregg & Zhang (2001) and Alia et al. (2001) provide evidence for differences in drought adaptation among P. sylvestris provenances. In order to obtain a mechanistic understanding of tree responses to extreme events, experiments are indispensable (Jentsch et al. 2007; Reyer et al. 2013). The relevance of results depends on the design of the experiment. Pot experiments easily allow the control of important factors affecting plant responses, but encompass a number of artefacts at the same time (Ray & Sinclair 1998; Passioura 2006). Most importantly, natural root development is hindered, being a trait of major interest in terms of drought response. Root growth is also affected by planting, which has to be taken into account in investigations focusing on seedlings and young plants (Gross362
nickle 2005; Struve 2009). Furthermore, microclimatic artefacts have to be minimised to simulate climatic extremes as realistically as possible. The manipulation of precipitation using permanent shelters causes various artefacts such as shading or passive warming (Beier et al. 2012). In particular, radiation, as a potential additional stress factor, is often neglected. However, high light stress is one component of stress affecting plants during heatwaves, accompanying a precipitation deficit and maximum temperatures (De Boeck et al. 2010). In addition, atmospheric feedback in terms of altered potential evapotranspiration is absent under permanent shelters, which could be alleviated by simultaneous heating. Open-top chambers are a viable method for increasing daytime temperature, but their heating capacity is usually limited (Godfree et al. 2011). Active heating via infrared lamps to imitate climate change has been controversial (Aronson & McNulty 2009; Amthor et al. 2010). Experiments using soil heating via heating cables are another approach (Richter et al. 2012), but this method affects belowground parts of plants to a larger extent than aboveground parts. It would be more realistic to directly warm the air enveloping the plants (Amthor et al. 2010). In this study, we investigated the response of P. sylvestris seedlings to predicted future climate conditions. We tested 10 provenances from the southwestern border of its distribution range up to more central European origins in the field using a factorial combination of warming and drought. Warming was achieved using a novel advanced air heating system preventing excessive soil warming, whereas drought was simulated using an automatic rain-out shelter allowing for high light stress and almost natural radiation throughout the experiment. We assessed plant responses as changes in phenology, growth increment, allocation and overall growth performance. We focused on the following questions: (i) are there differences in growth traits between the treatments and populations; (ii) are there differences between the provenances in their response to drought and warming; (iii) does warming enhance drought stress; (iv) is there a trade-off between performance of provenances under control conditions and under drought; and (v) are we able to identify a provenance better adapted to extreme conditions? MATERIAL AND METHODS Provenances and treatment of seeds and seedlings We used seeds of P. sylvestris from 10 different regions for this experiment (Table 1). Except for the German progeny, Alpenkiefer, which was obtained from a seed orchard in Germany (parent trees originate from the Bavarian Alps, above 900 m a.s.l.), all seeds were derived from autochthonous populations. For more details about the origin of seeds as well as genetic information, see Taeger et al. (2013a). Throughout the study we will refer to all progeny simply as ‘provenances’ or ‘populations’. Five days before sowing, seeds were soaked in water for 12 h. Seeds were sown in a split-plot design on 25 May 2011. Seedling locations within the plots were defined following a regular grid. We sowed 10 seeds at each seedling location, reduced the germinated seedlings at each location to three individuals on 30 July 2011 and further to one individual on 1 March 2012. During the germination period, all plots were covered with a
Plant Biology 17 (2015) 361–372 © 2014 German Botanical Society and The Royal Botanical Society of the Netherlands
Provenance manipulation
Taeger, Sparks & Menzel
Table 2. Results of the split plot ANOVA of whole-plot factors drought, warming and the subplot factor provenance on stem length increment and diameter increment in the period from July to October 2012. stem length increment (July–October)
drought warming drought 9 warming whole-plot error provenance provenance 9 drought provenance 9 warming provenance 9 drought 9 warming subplot Error total
diameter increment (July–October)
df
F
P
df
F
P
1 1 1 8 9 9 9 9 72 119
141.76 0.97 3.17
