Climate Change Impairs Nitrogen Cycling in European Beech Forests

Abstract

European beech forests growing on marginal calcareous soils have been proposed to be vulnerable to decreased soil water availability. This could result in a large-scale loss of ecological services and economical value in a changing climate. In order to evaluate the potential consequences of this drought-sensitivity, we investigated potential species range shifts for European beech forests on calcareous soil in the 21st century by statistical species range distribution modelling for present day and projected future climate conditions. We found a dramatic decline by 78% until 2080. Still the physiological or biogeochemical mechanisms underlying the drought sensitivity of European beech are largely unknown. Drought sensitivity of beech is commonly attributed to plant physiological constraints. Furthermore, it has also been proposed that reduced soil water availability could promote nitrogen (N) limitation of European beech due to impaired microbial N cycling in soil, but this hypothesis has not yet been tested. Hence we investigated the influence of simulated climate change (increased temperatures, reduced soil water availability) on soil gross microbial N turnover and plant N uptake in the beech-soil interface of a typical mountainous beech forest stocking on calcareous soil in SW Germany. For this purpose, triple 15N isotope labelling of intact beech seedling-soil-microbe systems was combined with a space-for-time climate change experiment. We found that nitrate was the dominant N source for beech natural regeneration. Reduced soil water content caused a persistent decline of ammonia oxidizing bacteria and therefore, a massive attenuation of gross nitrification rates and nitrate availability in the soil. Consequently, nitrate and total N uptake of beech seedlings were strongly reduced so that impaired growth of beech seedlings was observed already after one year of exposure to simulated climatic change. We conclude that the N cycle in this ecosystem and here specifically nitrification is vulnerable to reduced water availability, which can directly lead to nutritional limitations of beech seedlings. This tight link between reduced water availability, drought stress for nitrifiers, decreased gross nitrification rates and nitrate availability and finally nitrate uptake by beech seedlings could represent the Achilles' heel for beech under climate change stresses.

Fig 1. Experimental design.

The figure illustrates coring of beech-soil-mesocosms by use of stainless steel cylinders with subsequent pre-incubation for one year either under cool-moist microclimate at the coring site (NW exposure, control) or warm-dry microclimate (SW-exposure, climate change). After pre-incubation and equilibration, homogeneous labelling of the intact beech seedling-soil-microbe systems with either ¹⁵N/¹³C-enriched glutamine, ¹⁵N-ammonium (NH₄⁺) or ¹⁵N-nitrate (NO₃^-) and subsequent double harvests (6 and 48 hours after labelling) were conducted for determination of gross N turnover rates in the beech seedling-soil-microbe system in June (comparison of ambient NW vs. SW climatic conditions) and August (ambient NW conditions vs. roof-intensified drought at SW). A final sampling of mesocosms labelled in June allowed investigating long-term isotope recovery in September (three months after labelling). All three sampling dates were accompanied by determination of supporting soil and plant parameters such as abuncance of microbial genes related to ammonia oxidation, mycorrhization, and plant metabolites.

Fig 2. Modelled potential distribution of beech forests on calcareous soils in Europe (green colour) under current climatic conditions (left panel).

I.e., For the SRES A2 scenario, we computed a potential distribution of 7.2 million ha in the year 2080 (right panel), i.e., a reduction to 22% of the current distribution. Made with Natural Earth under CC0 license.

Fig 3. Soil temperature differences (5 cm depth) between beech-soil-mesocosms incubated at SW exposure (warm-dry microclimate, climate change treatment) and at NW exposure (cool-moist microclimate, control treatment).

Data represent mean values of five temperature probes per treatment directly installed horizontally in soil of transferred beech-soil-mesocosms. Arrows indicate the three sampling campaigns. The period between the sampling in June and August equals the roof period of 39 days.

Fig 4. Dynamics of volumetric soil moisture in 5 cm depth (mean values of n = 5 measurements) in intact beech-soil-mesocosms of the control treatment (NW exposure, cool-moist microclimate) and climate change treatment (SW exposure, warm-dry microclimate) in the growing season 2011, i.e., 1 year after implementation of treatments by transferring beech seedling-soil-mesocosms within NW exposure or to SW exposure in summer 2010.

Arrows indicate sampling campaigns (see Fig 1).

Fig 5. Gravimetric soil moisture related to water holding capacity (WHC) as determined from labelled (n = 48) and unlabelled (n = 4 to 8) beech-soil-mesocosms in June (ambient conditions at both exposures), August (intensified drought at SW exposure due to roof) and September (final harvest).

Asterisks indicate significant differences (p<0.05) between NW and SW exposure at the respective harvest. Different indices indicate significant differences between different sampling dates and labelled and unlabelled beech-soil-mesocosms.

Fig 6. Gross N turnover rates (mg N m^-2 day^-1) (n = 8) and N pool sizes (mg N m^-2) (N = 48) in intact beech seedling-soil-mesocosms.

Blue: NW exposure (control treatment); Red: SW exposure (climate change treatment). The June sampling represents the onset of the growing season after full development of leaves, while the August sampling was conducted in the middle of the growing season after 39 days of rainfall exclusion at SW. Gross rates of N turnover were calculated based on ¹⁵N tracing and pool dilution approaches following homogeneous labelling of the intact soil with double-labelled ¹⁵N/¹³C-glutamine, ¹⁵NH₄⁺, or ¹⁵NO₃^-. Thickness of process arrows and nitrogen pool signatures is representative for respective turnover rates and pool sizes. Processes and pools significantly affected by the climate change treatment are indicated by bold letters with asterisks. Different indices show significant differences between June and August for a given treatment/exposure.

Fig 7. Ammonia oxidizing bacteria and nitrification rates.

Abundance of genes encoding for ammonia monooxygenase of ammonia oxidizing bacteria in bulk soil (AOB, left panel) and relationships between AOB gene abundance and gross rates of nitrification (right panel). Blue colour: control treatment (NW exposure). Red colour: climate change treatment (SW exposure).

Fig 8. ¹⁵N recovery (n = 8) in beech seedlings (sum of fine roots, coarse roots, stem and leaves).

Data were collected in September, i.e., three months after isotope labelling with glutamine, NH₄⁺ or NO₃^- and indicate recovered % of isotopic excess, i.e., after subtracting ¹⁵N natural abundance. Blue: NW exposure (control treatment); red: SW exposure (climate change treatment). ¹⁵N recovery was highest after nitrate labelling both for SW and NW as indicated by different indices. The climate change treatment always reduced ¹⁵N recovery, as indicated by p<0.05.

Fig 9. Metabolites (total amino acids, total soluble proteins, NO₃^-) extracted from fine roots of beech seedlings in June.

Blue colour represents the control treatment (NW exposure), red colour represents the climate change treatment (SW exposure). Error bars denote standard errors of the mean (n = 4 per time and treatment). Amino acid and NO₃^- metabolite levels were significantly lower in beech seedlings of the climate change treatment.