Species-specific growth responses to simulated atmospheric and climate change
In this study of three dominant ericaceous dwarf shrub species growing at the treeline in the Swiss Alps, V. myrtillus growth was stimulated by both CO2 enrichment and soil warming and generally showed a stronger response than V. gaultherioides or E. hermaphroditum.
The CO2 effect on each dwarf shrub species was relatively consistent over several years of enrichment, providing a clear indication that these species differ in their responsiveness, irrespective of annual variations in climatic conditions. In contrast to our first hypothesis, the shoot growth response of V. myrtillus to elevated CO2 was sustained over the full experimental period. This result suggests that any increase in competition for nutrients or light that occurred over time with enhanced plant growth and microbial activity did not constrain the longer term above-ground growth response of this species. CO2 enrichment did not lead to a significant decline in the soil inorganic N pool or in leaf N concentration, providing evidence that the treatment did not cause N to become limiting.
The relatively strong response of V. myrtillus to CO2 enrichment compared with the other two dwarf shrub species might be related to different leaf traits. For example, higher SLA in V. myrtillus compared with V. gaultherioides (20–30% in all years measured) and E. hermaphroditum (> 50%; Zumbrunn, 2004) means that there is a larger amount of leaf area displayed per unit mass invested (Poorter et al., 2009) in V. myrtillus than in the other two species. Efficient light capture and high photosynthetic capacity associated with higher SLA could have led to larger assimilation gains under elevated CO2 (Roumet & Roy, 1996) in V. myrtillus compared with the other two species. For V. gaultherioides, the CO2 effect on annual shoot growth and total ramet height depended on which tree species grew in the experimental plot. This response could not be explained by differences in light conditions (canopy shading), snowmelt date, plot topography, soil moisture, leaf N concentration (slightly higher in plots with larch than in those with pine) or soil inorganic N pool size (Tables S1, S4). Reasons for the shoot growth response of V. gaultherioides remain unclear, but differences in litter production and quality or in below-ground competition, for example the availability of nutrients other than N, might have played a role. In general, lower V. gaultherioides ramet height in plots with larch than in those with pine could indicate less favourable growth conditions for this species in the understorey of larch trees.
Consistent with our findings, species-specific responses were observed in a 3-yr mesocosm CO2 enrichment study at the Abisko research station in northern Sweden that included the same three dwarf shrub species as in our experiment (Gwynn-Jones et al., 1997). Similar to our results, V. myrtillus was the only species in this subarctic experiment to show a positive growth response to CO2 enrichment. However, whereas we observed a tree species-specific CO2 response in V. gaultherioides (group V. uliginosum agg.) and no effect in E. hermaphroditum, at the Abisko site V. uliginosum showed no CO2 response and there was a significant negative effect for E. hermaphroditum in one treatment year (Gwynn-Jones et al., 1997). Enhanced growth was also observed for V. myrtillus exposed to elevated CO2 for a single season in a glasshouse study in low-elevation heathlands of the Netherlands (Arp et al., 1998). The consistent growth responses to CO2 enrichment observed for V. myrtillus across multiple studies under various growth conditions indicates an inherent CO2 responsiveness of this species and suggests that V. myrtillus growth and abundance might increase in a future CO2-enriched atmosphere.
Deciduous V. myrtillus was also the only species to show a significant positive shoot growth response to the warming treatment, with an average stimulation over twice the size of the mean CO2 effect. Vaccinium gaultherioides, which is also deciduous, showed no response to warming, suggesting that factors other than leaf type had a greater influence on the responses of individual species. In the Alps, V. myrtillus has a lower elevational distribution compared with V. gaultherioides and E. hermaphroditum, both of which extend to > 3000 m asl (Landolt et al., 2010). Vaccinium myrtillus might therefore be better adapted and more responsive to warmer temperatures. As in our study, V. myrtillus had a more pronounced shoot growth response to soil warming than E. hermaphroditum (stimulation only with additional air warming) or V. uliginosum (no growth response) in a 5-yr study in Abisko, Sweden (Hartley et al., 1999). Positive shoot growth responses were similarly observed for dwarf shrubs after the second and third seasons of warming by OTCs in the Swedish subarctic heath (Parsons et al., 1994), although there all three species that also occur in our experiment responded positively. Finally, warming by OTCs at a temperate alpine site in northern Japan had no effect on vegetative growth of V. uliginosum (Kudo & Suzuki, 2003), whereas Empetrum nigrum var. japonicum shoot elongation was strongly stimulated.
Different responses to warming for the same species might be attributable to genetic differences between regions, especially for E. nigrum and V. uliginosum, which are highly heterogeneous species complexes (Bell & Tallis, 1973; Jacquemart, 1996). Lower atmospheric pressure (and therefore lower CO2 partial pressure), contrasting day–night solar radiation and temperatures during summer, and generally higher precipitation in temperate alpine environments compared with arctic regions might also have contributed to the different findings (Körner, 2003). Finally, different heating techniques might have played a role in the divergent results: passive warming by OTCs generally results in smaller increases in air and soil temperature than warming by heating cables on the ground surface (Rustad et al., 2001). Further, warming by OTCs is confounded to some extent with shelter effects, that is, increased humidity and reduced wind speed and night-time radiative cooling, whereas the heating cables in our study slightly reduced air humidity near the ground surface and did not affect the latter two parameters (Hagedorn et al., 2010).
Soil warming led to a strong increase in soil mineral N content that was still evident after three growing seasons. This result supports our prediction that warming would at least initially accelerate N cycling and lead to an enhanced N supply (Melillo et al., 2002). In a study in open birch (Betula pubescens ssp. tortuosa) forest in northern Sweden including the same dwarf shrub species as our study, N mineralization rates were doubled compared with controls in plots with 5°C soil warming in the second year of treatment, although no effect was observed in the fifth year (Hartley et al., 1999). Corresponding to the larger inorganic N pool in the soil, the leaf N concentration of both Vaccinium species showed a short-term increase in warmed plots in our study. Warming effects on V. myrtillus leaf N concentration were only apparent in the first year of treatment when the growth response was smallest. It is possible that greater stimulation of shoot growth in 2008 and 2009 diluted the soil warming-induced increase in total N uptake, yielding an overall larger N pool in leaf biomass but no effect on concentrations (Weih & Karlsson, 2001). Hartley et al. (1999) observed no effect of soil warming on foliar N concentrations in V. myrtillus or V. uliginosum in any year of their study, despite increased N mineralization rates. By contrast, 8 yr of warming by tents and then OTCs in another experiment in northern Sweden had a large positive effect on leaf and shoot N concentration of V. myrtillus (73%) but a negative effect on that of V. uliginosum (19%) (Richardson et al., 2002). We observed weak but positive correlations between V. myrtillus shoot increment length and soil/leaf N, suggesting that increased N availability might have been partially responsible for stimulation of shoot growth but that other mechanisms (i.e. direct effects of temperature on photosynthesis) were probably also important.
In contrast to our third hypothesis, we found no evidence of a positive CO2 × warming interactive effect on dwarf shrub growth, suggesting that responses to CO2 enrichment were not constrained by low N availability or low temperature. This result is in contrast to the positive CO2 × warming interactive effect on NPP observed for tussock tundra vegetation in Alaska (Oechel et al., 1994). Although no other combined warming and CO2 enrichment studies have been conducted at high elevation, an alpine grassland community showed no effect of CO2 enrichment on biomass production even when combined with 40 kg ha−1 a−1 of NPK fertilization, indicating that nutrient limitation was not the reason for no biomass response to elevated CO2 (Körner et al., 1997). Similarly, a FACE × N addition experiment on glacier forefield vegetation showed strong stimulation by fertilization over 3 yr but no positive CO2 effect or interaction between treatments (N. Inauen, pers. comm.).
Independent growth responses of V. myrtillus to elevated CO2 and soil warming suggest that this species will have a competitive advantage over the co-occurring dwarf shrub species in the future. However, at our research site both treatments increased the sensitivity of V. myrtillus to damage from early growing season freezing events, whereas neither V. gaultherioides nor E. hermaphroditum was affected (Martin et al., 2010). Further, V. myrtillus was found to be more susceptible than the other two species to negative effects of early snow ablation (Wipf et al., 2009). Therefore, stochastic climate events that consistently impact V. myrtillus more severely than the other dwarf shrub species could counteract increases in its dominance.
Decline in species richness with elevated CO2 concentrations and soil warming
The experimental treatments led to changes in vegetation composition at the plot scale during the final 4 yr of the 9-yr study, with a decline in the number of vascular and nonvascular species in the plots. The observed trend of greater species loss in plots with taller V. myrtillus ramets, although not in those with greater canopy shading, suggests that increased shading within the understorey canopy and/or increased below-ground competition played a role in the decline. The opposite pattern in plots with pine was surprising because the height of V. myrtillus was also enhanced in elevated CO2 plots shared with this tree species. Three years of experimental warming had no detectable effect on vascular plant composition, consistent with results from a 5-yr soil warming treatment in Abisko, Sweden (Hartley et al., 1999). By contrast, 9 yr of warming in glasshouses near Toolik Lake, Alaska led to a decline in species richness (Chapin et al., 1995). Given that the response of V. myrtillus shoot growth to warming was more pronounced than that to CO2 enrichment, sustained shoot growth enhancement of this abundant species could lead to changes in vegetation composition and species richness over the longer term. The warming treatment in our study did result in a loss of moss and lichen species. Increased vascular plant productivity with warming has been associated with reduced abundance of mosses and lichens in several (sub)arctic studies (meta-analysis by Walker et al., 2006). This relationship has previously been attributed to increased shading by vascular plants (Chapin et al., 1995; Cornelissen et al., 2001), although the observed correlation with soil moisture in our study suggests that drying associated with the warming treatment was at least partially responsible for the loss of these species. Overall, negative effects of CO2 enrichment and soil warming on species richness indicate that the ongoing environmental change could lead to less diverse plant communities at the studied alpine treeline.