Hans J. De Boeck

Precipitation manipulation experiments: challenges and recommendations for the future

Climatic changes, including altered precipitation regimes, will affect key ecosystem processes, such as plant productivity and biodiversity for many terrestrial ecosystems. Past and ongoing precipitation experiments have been conducted to quantify these potential changes. An analysis of these experiments indicates that they have provided important information on how water regulates ecosystem processes. However, they do not adequately represent global biomes nor forecasted precipitation scenarios and their potential contribution to advance our understanding of ecosystem responses to precipitation changes is therefore limited, as is their potential value for the development and testing of ecosystem models. This highlights the need for new precipitation experiments in biomes and ambient climatic conditions hitherto poorly studied applying relevant complex scenarios including changes in precipitation frequency and amplitude, seasonality, extremity and interactions with other global change drivers. A systematic and holistic approach to investigate how soil and plant community characteristics change with altered precipitation regimes and the consequent effects on ecosystem processes and functioning within these experiments will greatly increase their value to the climate change and ecosystem research communities. Experiments should specifically test how changes in precipitation leading to exceedance of biological thresholds affect ecosystem resilience and acclimation.

Whole‐system responses of experimental plant communities to climate extremes imposed in different seasons

• Discrete climate events such as heat waves and droughts can have a disproportionate impact on ecosystems relative to the temporal scale over which they occur. Research oriented towards (extreme) events rather than (gradual) trends is therefore urgently needed. • Here, we imposed heat waves and droughts (50-yr return time) in a full factorial design on experimental plant communities in spring, summer or autumn. Droughts were created by removing the controlled water table (rainout shelters prevented precipitation), while heat waves were imposed with infrared heaters. • Measurements of whole-system CO(2) exchange, growth and biomass production revealed multiple interactions between treatments and the season in which they occurred. Heat waves had only small and transient effects, with infrared imaging showing little heat stress because of transpirational cooling. If heat waves were combined with drought, negative effects observed in single factor drought treatments were exacerbated through intensified soil drying, and heat stress in summer. Plant recovery from stress differed, affecting the biomass yield. • In conclusion, the timing of extreme events is critical regarding their impact, and synergisms between heat waves and drought aggravate the negative effects of these extremes on plant growth and functioning.

Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species

Significance Leaf phenology of temperate ecosystems is shifting in response to global warming. This affects surface albedo, ecosystem carbon balance, and evapotranspiration, and the response of leaf phenology to climatic drivers has therefore received particular interest. However, despite considerable effort, models have failed to accurately reproduce phenology patterns, likely because mechanistic understanding is incomplete. Here, we show that earlier leaf flushing in response to a warm winter translated into earlier leaf senescence and even earlier leaf flushing in the following year. This legacy effect of winter warming on leaf phenology has important implications for understanding and modelling leaf phenology and its impact on ecosystem functioning, especially in relation to global warming, and is likely to open new research lines. Recent temperature increases have elicited strong phenological shifts in temperate tree species, with subsequent effects on photosynthesis. Here, we assess the impact of advanced leaf flushing in a winter warming experiment on the current year’s senescence and next year’s leaf flushing dates in two common tree species: Quercus robur L. and Fagus sylvatica L. Results suggest that earlier leaf flushing translated into earlier senescence, thereby partially offsetting the lengthening of the growing season. Moreover, saplings that were warmed in winter–spring 2009–2010 still exhibited earlier leaf flushing in 2011, even though the saplings had been exposed to similar ambient conditions for almost 1 y. Interestingly, for both species similar trends were found in mature trees using a long-term series of phenological records gathered from various locations in Europe. We hypothesize that this long-term legacy effect is related to an advancement of the endormancy phase (chilling phase) in response to the earlier autumnal senescence. Given the importance of phenology in plant and ecosystem functioning, and the prediction of more frequent extremely warm winters, our observations and postulated underlying mechanisms should be tested in other species.

Increased heat requirement for leaf flushing in temperate woody species over 1980–2012: effects of chilling, precipitation and insolation

Recent studies have revealed large unexplained variation in heat requirement-based phenology models, resulting in large uncertainty when predicting ecosystem carbon and water balance responses to climate variability. Improving our understanding of the heat requirement for spring phenology is thus urgently needed. In this study, we estimated the species-specific heat requirement for leaf flushing of 13 temperate woody species using long-term phenological observations from Europe and North America. The species were defined as early and late flushing species according to the mean date of leaf flushing across all sites. Partial correlation analyses were applied to determine the temporal correlations between heat requirement and chilling accumulation, precipitation and insolation sum during dormancy. We found that the heat requirement for leaf flushing increased by almost 50% over the study period 1980-2012, with an average of 30 heat units per decade. This temporal increase in heat requirement was observed in all species, but was much larger for late than for early flushing species. Consistent with previous studies, we found that the heat requirement negatively correlates with chilling accumulation. Interestingly, after removing the variation induced by chilling accumulation, a predominantly positive partial correlation exists between heat requirement and precipitation sum, and a predominantly negative correlation between heat requirement and insolation sum. This suggests that besides the well-known effect of chilling, the heat requirement for leaf flushing is also influenced by precipitation and insolation sum during dormancy. However, we hypothesize that the observed precipitation and insolation effects might be artefacts attributable to the inappropriate use of air temperature in the heat requirement quantification. Rather than air temperature, meristem temperature is probably the prominent driver of the leaf flushing process, but these data are not available. Further experimental research is thus needed to verify whether insolation and precipitation sums directly affect the heat requirement for leaf flushing.

Experiments to confront the environmental extremes of climate change

Extreme climate conditions can dramatically alter ecosystems and are expected to become more common in the future; however, our understanding of species and ecosystem responses to extreme conditions is limited. We must meet this challenge by designing experiments that cover broad ranges of environmental stress, extending to levels well beyond those observed currently. Such experiments are important because they can identify physiological, community, and biogeochemical thresholds, and improve our understanding of mechanistic ecological responses to climate extremes. Although natural environmental gradients can be used to observe a range of ecological responses, manipulation experiments – including those that impose drought and heat gradients – are necessary to induce variation beyond common limits. Importantly, manipulation experiments allow for determination of the cause and effect of species and ecosystem threshold responses. We present a rationale and recommendations for conducting extreme experiments that extend beyond the historical and even the predicted ranges of environmental conditions.

Simulated heat waves affected alpine grassland only in combination with drought

The Alpine region is warming fast, and concurrently, the frequency and intensity of climate extremes are increasing. It is currently unclear whether alpine ecosystems are sensitive or resistant to such extremes. We subjected Swiss alpine grassland communities to heat waves with varying intensity by transplanting monoliths to four different elevations (2440-660 m above sea level) for 17 d. Half of these were regularly irrigated while the other half were deprived of irrigation to additionally induce a drought at each site. Heat waves had no significant impacts on fluorescence (Fv /Fm , a stress indicator), senescence and aboveground productivity if irrigation was provided. However, when heat waves coincided with drought, the plants showed clear signs of stress, resulting in vegetation browning and reduced phytomass production. This likely resulted from direct drought effects, but also, as measurements of stomatal conductance and canopy temperatures suggest, from increased high-temperature stress as water scarcity decreased heat mitigation through transpiration. The immediate responses to heat waves (with or without droughts) recorded in these alpine grasslands were similar to those observed in the more extensively studied grasslands from temperate climates. Responses following climate extremes may differ in alpine environments, however, because the short growing season likely constrains recovery.

Increased Turnover but Little Change in the Carbon Balance of High-Arctic Tundra Exposed to Whole Growing Season Warming

Abstract Tundra ecosystems constitute large stocks of carbon and might therefore, if climate warming releases CO2, induce positive feedback and amplify temperature increase. We studied the effect of a 2.5°C temperature increment, induced by controlled infrared irradiation, on various components of the carbon balance of a High Arctic tundra ecosystem at Zackenberg in Northeast Greenland (74°N, 21°W) over the 1999 growing season. Gross photosynthesis (Pgross), belowground respiration (Rsoil), and canopy respiration (Rcanopy) were regularly determined with closed dynamic CO2 exchange systems, and the whole-growing season C-balance was reconstructed by relating these components to potentially controlling factors (green cover, soil moisture, radiation, soil and canopy temperature, and thawing depth). Thawing depth and green cover increased in heated plots, while soil moisture was not significantly affected. Pgross increased 24.2%, owing to both a green cover and a physiological influence of warming. Belowground respiration was enhanced 33.3%, mainly through direct warming impact and in spite of lower Q10 in the heated plots; the factors controlling Rsoil were day of the year and soil moisture. Rcanopy did not differ significantly between treatments, although green cover was higher in the heated plots. This tundra ecosystem acted as a relatively small net sink both under current (0.86 mol CO2 m−2) and heated (1.24 mol CO2 m−2) conditions. Nevertheless, turnover increased, which was best explained by a combination of direct and indirect temperature effects, and delayed senescence.

Effects of climate warming and species richness on photochemistry of grasslands

In view of the projected climatic changes and the global decrease in plant species diversity, it is critical to understand the effects of elevated air temperature (T(air)) and species richness (S) on physiological processes in plant communities. Therefore, an experiment of artificially assembled grassland ecosystems, with different S (one, three or nine species), growing in sunlit climate-controlled chambers at ambient T(air) and ambient T(air) + 3 degrees C was established. We investigated whether grassland species would be more affected by midday high-temperature stress during summer in a warmer climate scenario. The effect of elevated T(air) was expected to differ with S. This was tested in the second and third experimental years by means of chlorophyll a fluorescence. Because acclimation to elevated T(air) would affect the plants stress response, the hypothesis of photosynthetic acclimation to elevated T(air) was tested in the third year by gas exchange measurements in the monocultures. Plants in the elevated T(air) chambers suffered more from midday stress on warm summer days than those in ambient chambers. In absence of severe drought, the quantum yield of PSII was not affected by elevated T(air). Our results further indicate that species had not photosynthetically acclimated to a temperature increase of 3 degrees C after 3 years exposure to a warmer climate. Although effects of S and T(air) x S interactions were mostly not significant in our study, we expect that combined effects of T(air) and S would be important in conditions of severe drought events.

Greater impact of extreme drought on photosynthesis of grasslands exposed to a warmer climate in spite of acclimation

In view of the projected increase in the frequency of extreme events during this century, we investigated the impact of a drought extreme on leaf ecophysiological parameters and carbon isotope composition (delta(13)C) of grassland communities with species richness (S) of one, three or nine species. The communities, grown for 3 years at either ambient air temperatures (ambient T(air)) or ambient T(air) + 3 degrees C (elevated T(air)), were additionally subjected to an imposed drought by withholding water for 24 days. During the previous 3 years equal precipitation was applied in both temperature treatments, thus communities at elevated T(air) had experienced more frequent, mild droughts. However, it was unknown whether this resulted in a higher resistance for facing extreme droughts. At similar soil matric potentials stomatal conductance (g(s)) and transpiration (Tr) were higher at elevated than ambient T(air), indicating acclimation to lower soil water content. Despite the stomatal acclimation observed, plants in elevated T(air) showed a lower resistance to the drought extreme as indicated by their lower photosynthetic rate (A(max)), g(s) and Tr during the entire duration of the drought extreme. Lower values for A(max), Tr and g(s) were also recorded in species at S = 3 as compared with species at S = 1 for both temperature treatments, but no further differences with S = 9 suggesting that stress was not alleviated at higher S-levels. The discrimination of (13)C was poorly correlated with measurements of instantaneous leaf water-use efficiency (A(max)/Tr) and, with this time scale and sampling method, it was not possible to detect any potential change in plant water-use efficiency using leaf delta(13)C.

Mean annual precipitation predicts primary production resistance and resilience to extreme drought

Extreme drought is increasing in frequency and intensity in many regions globally, with uncertain consequences for the resistance and resilience of ecosystem functions, including primary production. Primary production resistance, the capacity to withstand change during extreme drought, and resilience, the degree to which production recovers, vary among and within ecosystem types, obscuring generalized patterns of ecological stability. Theory and many observations suggest forest production is more resistant but less resilient than grassland production to extreme drought; however, studies of production sensitivity to precipitation variability indicate that the processes controlling resistance and resilience may be influenced more by mean annual precipitation (MAP) than ecosystem type. Here, we conducted a global meta-analysis to investigate primary production resistance and resilience to extreme drought in 64 forests and grasslands across a broad MAP gradient. We found resistance to extreme drought was predicted by MAP; however, grasslands (positive) and forests (negative) exhibited opposing resilience relationships with MAP. Our findings indicate that common plant physiological mechanisms may determine grassland and forest resistance to extreme drought, whereas differences among plant residents in turnover time, plant architecture, and drought adaptive strategies likely underlie divergent resilience patterns. The low resistance and resilience of dry grasslands suggests that these ecosystems are the most vulnerable to extreme drought - a vulnerability that is expected to compound as extreme drought frequency increases in the future.