2 Background of the thesis
2.2 Response of vegetation to climate change
The response of vegetation to climate change depends, for example, on the plant species’
abilities to adapt either by modification of their physiology and/or seasonal behaviour or by tracking the shifting climate through migration to new territories (Thuiller 2007). Otherwise, the range size of affected plant species will contract or the species will even become extinct (Parmesan 2006). The speed and global extent of climate change pose additional challenges for plant species survival: shifting the distribution area across short distances might take decades or centuries and evolutionary adaptations will likely require several generations and not all plant species might have the required spatio-temporal abilities to adapt, disperse or migrate (Jentsch & Beierkuhnlein 2003; Visser 2008). According to the climatic variability hypothesis (Dobzhansky 1950; Stevens 1989; Gaston et al. 1998), the probability for plant species to adapt by wide distribution rises with the height of the natural climate variability of the plant species’ site.
In the following, I give examples of observed impact of global climate change on ecosystems in general. I present theories on how climate variability might affect vegetation. Thereby, I focus on ecological thresholds and vegetation shifts as well as on possible factors influencing the stability of ecosystems against perturbation by increased climate variability such as species and functional diversity or biotic interactions.
Evidences of climate change impacts on global ecosystems
The interaction of the multiple drivers of climate change (e.g. global warming, changing precipitation pattern, increased frequency and intensity of extreme weather events, higher concentration of atmospheric CO2, altered nitrogen cycle) together with land cover and land use changes is consequently altering the structure and function of the Earth as a system (Vitousek 1994). Climate change has already wide ranging effects throughout global ecosystems (Parmesan & Yohe 2003; IPCC 2014b). Impacts on vegetation are visible on all scales from genetic (Jump et al. 2008) and elemental level (Gargallo-Garriga et al. 2014;
Urbina et al. 2015), single plant performance (Reyer et al. 2013) and population dynamics (Gornish & Tylianakis 2013) to ecosystem functions (Jentsch et al. 2011). With the continuing global alterations in climate, the loss of biodiversity (Sala et al. 2000; Chapin et al. 2000;
Alkemade et al. 2010), plant species extinctions (Chapin et al. 2000; Thomas et al. 2004;
Thuiller et al. 2005; Smith et al. 2009; Alkemade et al. 2010), higher biological invasions (Dukes & Mooney 1999; Kreyling et al. 2008b; Taylor et al. 2012), shifts in community compositions and species ranges (Parmesan 1996; Walther 2000, 2001; Parmesan & Yohe 2003; Thuiller et al. 2005; Midgley et al. 2006; Murphy et al. 2010; Morueta-Holme et al.
2013, Manuscript 1), as well as alterations in species interactions (Klanderud 2005; Brooker 2006; Suttle et al. 2007; Manuscript 4 & 5), plant phenology (Penuelas & Filella 2001;
Sparks & Menzel 2002; Menzel et al. 2006; Parmesan 2007; Jentsch et al. 2009; Nagy et al.
2013) and primary productivity (Ciais et al. 2005; Kreyling et al. 2008c; Barriopedro et al.
2011, Manuscript 2 & 3) are expected to become more pronounced. The increased climate variability and higher frequency of extreme weather events is now acknowledged in ecological climate change research as they may be biologically more significant than shifts in average conditions and global trends (Easterling et al. 2000b; Jentsch 2006; Jentsch &
Beierkuhnlein 2008; Thompson et al. 2013; Kreyling et al. 2014). However, there is a
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research gap on how exactly altered climate variability affects biodiversity and ecosystem functioning and what kind of processes or mechanisms within the ecosystem are altered.
Phenological and physiological processes in the face of altered climate variability
Changes in climate variability can impact plant’s phenology and physiology: Phenological processes such as onset of leaf unfolding and flowering are mainly driven by changes in mean climatic conditions foremost temperature (Menzel & Fabian 1999; Menzel et al. 2006), i.e. the temperature conditions two months prior to flowering onset determines shifts in flowering phenology. However, there are interactions with changes in climate variability (Reyer et al. 2013). Early warm spells are advantageous for early successional and opportunistic plant species, however, the risk of damages by late frost events rises (Leuzinger et al. 2011b; Kreyling et al. 2012). Extreme warm spells, drought, and heavy rainfall events can, depending on their timing and duration, for example, advance or slow down leaf maturity, and extend or reduce the flowering period (Buxton 1996; Luterbacher et al. 2007; Jentsch et al. 2009; Menzel et al. 2011). Essential for physiological processes, such as photosynthesis and nutrient uptake, is the availability of water for the plant. Changes in plant-water relations are resulting from higher temperatures and more intra-annual precipitation variability expressed as prolonged dry periods and/or heavy rainfalls (Knapp et al. 2008; Reyer et al. 2013). Reduced soil moisture combined with a high atmospheric demand for plant transpiration could lead to drought stress resulting in productivity losses, changes in the carbon cycle or mortality (Fay et al. 2003; Porporato et al. 2004). An excess of soil moisture due to water logging after heavy rainfall events will affect the oxygen supply to the plant roots (Striker et al. 2005; Bartholomeus et al. 2008). Furthermore, flooding may induce stomatal closure and hence limiting gas exchange and plant growth (Bradford 1983;
Chen et al. 2005). The combination of both, wet and dry extremes, are likely harmful for several specialised and endangered plant species, but they may favour generalists (Bartholomeus et al. 2011). Dreesen et al. (2014) showed that repeated water stress in one growing season (two drought events of 25 days or two droughts combined with a heatwave of 10 days) resulted in plant senescence and leaf mortality. These findings suggest that increased precipitation regimes might cause an accumulation of different kinds of water stress for plants and thus may result in the crossing of an ecosystem threshold. Therefore, climate variability, especially the synergistic interaction of weather extremes, may not only change plant performance, vegetation dynamics, and associated ecosystem functions, it may also drive extinctions (Niinemets & Valladares 2006; Reyer et al. 2013).
Ecological thresholds and vegetation shifts
Lloret et al. (2012) introduced a conceptual model of vegetation shifts in response to altered climate variability: increased climate variability and extreme weather events are expected to lead to abrupt vegetation shifts due to induced mortality. In contrast, gradual changes in mean climatic parameters would keep vegetation pattern either stable or would drive successional change in the long term. Furthermore, in some cases vegetation might also remain unaffected under increased climate variability. However, theoretical and empirical evidence exists that also gradual climatic change could lead to abrupt vegetation change when a critical threshold, or so-called tipping point, is crossed (Scheffer & Carpenter 2003;
Lloret et al. 2012). An ecological threshold can be defined as the ‘point at which there is an
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abrupt change in an ecosystem quality, property or phenomenon, or where small changes in an environmental driver produce large responses in the ecosystem’ (Groffman et al. 2006).
Extreme weather events can trigger regime shifts by crossing thresholds, and with the rapid climate change the potential for threshold changes increases (Scheffer et al. 2001; CCSP 2009; Peterson 2009). Extreme events primarily affect individuals or populations in their physiology, growth or fitness which will result in no or small effects on ecosystem processes (Smith 2011; Figure 2). However, the extreme event might cascade to higher hierarchical levels such as shifts in plant species abundance and composition, local extinction or invasion of other species into the ecosystem (Kinzig & Ryan 2006; Smith 2011). Once the ‘extreme response threshold’ is crossed and the function and/or structure of the ecosystem have fundamentally changed, a prolonged return to the previous state is possible but unlikely (CCSP 2009; Smith 2011; Figure 2).
Figure 2 A mechanistic framework for assessing ecosystem response to climate extremes (according to Smith (2011))
According to Lenton et al. (2008) there are indications that some large-scale components of the Earth’s system such as the decay of the Greenland ice sheet, the Atlantic thermohaline circulation, or the dieback of the Amazon rainforest, are close to reaching the threshold to a qualitative altered future state of the system due to the global climate change.
Stability of ecosystem functions
Up to now evidences of species or vegetation shifts due to extreme climatic events are still rare, and there seems to be a certain ‘stability’ of vegetation towards these events (Jentsch et al. 2011; Lloret et al. 2012). Talking about ‘ecological stability’ can be confusing as there are many definitions of and concepts on stable ecosystems (Grimm & Wissel 1997). For example, a stable ecosystem can be defined as a system that persists despite perturbation (Connell & Slatyer 1977). However, ecosystem stability has several aspects e.g. one focussing on the existence of function or, in contrast, one that focus on the efficiency of function (Holling et al. 1997). From 163 reviewed definitions, Grimm & Wissel (1997) were
Climate extreme Species loss/
invasion
Ecosystem response (+/-)
Species re-ordering
Individual/
population
Extreme response threshold
Recovery
Time
State change
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able to condense the term ‘stability’ to three fundamentally different properties: (1) constancy, staying essentially unchanged; (2) resilience, returning to the reference state (or dynamic) after a temporary disturbance; and (3) persistence, continuance through time of an ecological system. According to Isbell et al. (2015), the first property ‘constancy’ can also be called ‘resistance’, which indicates that an ecosystem function (e.g. productivity) remains close to the reference state during a climate event. Grimm & Wissel (1997) also introduced a checklist about ecological stability which could reduce confusion. They point out that the stability properties should be addressed correctly in the statements on stability. Furthermore, they recommend to always classify the ecological situation by giving information on the variable of interest, the level of description, the reference state, disturbance, spatial scale, and temporal scale (Grimm & Wissel 1997). Therefore, when the term “stable” ecosystem is used in this thesis, it refers usually to a grassland ecosystem which provides a resilient and efficient ecosystem function in the face of increased climate variability. Here, ecosystem functions are for example biomass production, high forage quality, or constant plant species composition. The reference state would be the lack of extreme weather events and low intra-annual climate variability. The spatial scale ranges from plot size and the size of a meadow, the temporal scale is between one growing season up to 10 years.
What are the processes and the mechanism that keep ecosystem functions stable in the face of perturbation caused by climatic extremes? Before answering this question, we must confirm that the lack of response in plant performance results from the plant’s resistance and not from a lack of true extremeness (Smith 2011). For example, an extreme drought occurs, but the soil moisture content is not reflecting the same level of extremeness because of buffering effects (compare Glaser et al. 2013). Thus, the plant response would not be extreme itself because the event lay within the natural variability of soil moisture availability and therefore within the ability of the plant to cope (Smith 2011; Lloret et al. 2012, Figure 3a).
This might easily happen if the definition of “extreme climatic event” is not adequate (Smith 2011; Section 2.1.2).
In the following, concepts on species and functional diversity, biotic interactions, demography of plant species population, ecological stress memory, and their role for ecosystem stability under climate variability are shortly presented.
Species and functional diversity
One acknowledged key mechanism for providing a stable ecosystem function (e.g. biomass production) despite perturbation is a high diversity of species and functional groups (Walker 1995; Naeem & Li 1997; Yachi & Loreau 1999; Hooper et al. 2005). Because species differ in their responses to environmental changes such as increased climate variability, higher species richness offers a wider range of species responses to perturbations (Van Ruijven &
Berendse 2010). Thus, more diverse ecosystems have a higher chance to include species that respond with increased performance to the change, compensating the failing performance of other species. This provides a so called ‘insurance’ for maintaining the original ecosystem function (Walker 1995; Folke et al. 1996). Species and functional group richness can also enhance the capacity of the ecosystem to recover from the perturbation;
thus, increasing resilience, and potentially offering an opportunity to deal with changes (Walker 1995; Van Ruijven & Berendse 2010).
17 Biotic interactions
Another possible process for stabilizing ecosystem function in the face of increased climate variability may be the reciprocal feedback between individual species selection and persistence, resulting in alterations in biotic interactions and dominance shifts (see also section 2.3.3 and Manuscripts 1, 4 & 5). According to Walker et al. (1999) and Brooker (2010) an environmental pattern, such as extreme weather events or increased climate variability, could favour a particular suite of species leading to a decline or elimination of the dominant species. Thus, the formerly intense competition between the dominant and minor species would decrease and the minor species might emerge to replace the dominant. If the minor species has similar or congeneric functional attributes as the former dominant, the ecosystem function can be maintained under the changed climate regime (compare with
‘insurance hypothesis’ Folke et al. (1996) and Yachi & Loreau (1999)). Recently, Gellesch et al. (2013) reviewed findings on biotic interaction in the face of climate change. They found that the effect of more than one climatic driver on biotic interactions is especially not yet well understood.
Figure 3 Model of a demographic stabilizing mechanism within populations against extreme climatic events based on compensation by either enhanced survival (b) or increased rate of recruitment (c) after the event caused a higher mortality rate than natural variability; (a) the effect of the climatic extreme does not necessarily cause higher mortality or recruitment rate as alterations fall within the range of natural variability; red lines show rate of mortality, black lines show rate of recruitment (modified from Lloret et al. (2012))
Climate extreme
Time
Recruitment, mortality
(a)
(c) (b)
Natural variability
18 Demography
A further perspective on ecosystem stability in the face of climate variability is a demographic stabilizing mechanism. This mechanism can be based on the balance between the adult mortality of at least one dominant species population induced by an extreme weather event and its enhanced recruitment or adult survival after the event (Lloret et al. 2012). This mechanism could also explain why short-term responses in community composition were found to differ from long-term observations in a warming experiment (Hollister et al. 2005). In the demographic stabilizing mechanism by Lloret et al. (2012), an extreme weather event might cause higher mortality than natural variability (Figure 3b, c). After a certain time, this mortality is compensated by higher survival of the remaining population (Figure 3b) and/or by increased recruitment (Figure 3c). Possible factors which enhance higher survival under or after extreme weather events were named to be site quality, tolerance, plasticity and phenotypic variability as well as reduced competition with plant neighbours. Factors increasing future recruitment could be, for instance, micro-climatic shifts, new suitable sites, better adult reproductive performance, and altered biotic interactions such as less competition, facilitation, and antagonistic release (Lloret et al. 2012). This kind of altered conditions are often brought about by superimposed disturbances (Kröel-Dulay et al. 2015).
Ecological stress-memory
Moreover, there are also evidences that grassland ecosystems show a kind of memory effect to pre-exposure by extreme climatic events such as drought, frost or heat waves (Bruce et al.
2007; Walter et al. 2011, 2013b), which improve the tolerance to further drought stress.
Walter et al. (2011) showed that drought-stressed Arrhenatherum elatius showed improved photoprotection and therefore a more protective response towards recurrent drought.
Together with colleagues, I found that recurrent mild drought stress seemed to improve drought resistance of grassland plant communities and species (Backhaus et al. 2014a). An extreme drought event caused higher tissue die-back of single plant species (Plantago lanceolata) and of grassland communities (consisting of Arrhenatherum elatius, Holcus lanatus, Plantago lanceolata and Geranium pratense), which were regularly watered in the preceding years, compared to plants that were pre-exposed to only mild or severe drought stress. Here, morphological changes such as altered root-shoot ratio did not cause this response. However, epigenetic changes (Bruce et al. 2007), the accumulation of proteins and transcription factors (Baniwal et al. 2004) or protective metabolites (Herms & Mattson 1992) as well as soil biotic legacies (Meisner et al. 2013) could be potential reasons for these findings. Future research, especially on the molecular level, has still to elucidate mechanisms of an ecological stress-memory.
In summary, the multiple drivers of climate change are altering ecosystems worldwide.
Particularly increased climate variability is impacting plant’s phenological and physiological processes e.g. via the higher magnitude and frequency of extreme weather events or via the combined occurrence of both, wet and dry extreme events. As a consequence, abrupt vegetation shifts are expected when ecological thresholds are crossed. Processes and mechanisms that might keep ecosystem functioning stable in the face of perturbations caused by climatic extremes are not yet completely researched and understood. Some evidence suggests that biodiversity, biotic interactions, demographic processes of populations, and an ecological stress-memory are able to influence the resistance and resilience of plant communities. Thus, it is important to close the research gap on how
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altered climate variability affects biodiversity and ecosystem functioning and to empirically and theoretically identify potential ecosystem thresholds before they are actually crossed.
Plant species composition (species and functional diversity) (see Manuscript 1) and plant-plant interactions (e.g. facilitation, role of nitrogen fixing plant-plants) (see Manuscript 4 & 5) in the face of increased climate variability should especially be further studied as they possibly have a mitigating role to climate change effects. Furthermore, land use forms and management strategies might influence the direction of vegetation response. Therefore, land use practices have to be tested for interactions with climate factors (see Manuscript 2 & 3).
In future, the interplay of plant-soil-processes and the influence of biotic interactions across different trophic levels should also be considered. In the following, the focus is placed on the response of mesic temperate grassland as one exemplary ecosystem affected by increased climate variability.
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2.3 Importance of mesic temperate grassland and its response to increased