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Exposure to warming and CO2 enrichment promotes greater above-ground biomass, nitrogen, phosphorus and arbuscular mycorrhizal colonization in newly ...

Plant Soil (2012) 359:121–136 DOI 10.1007/s11104-012-1190-y

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Exposure to warming and CO2 enrichment promotes greater above-ground biomass, nitrogen, phosphorus and arbuscular mycorrhizal colonization in newly established grasslands Costanza Zavalloni & Sara Vicca & Manu Büscher & Ivan E. de la Providencia & Hervé Dupré de Boulois & Stéphane Declerck & Ivan Nijs & Reinhart Ceulemans

Received: 14 April 2011 / Accepted: 21 February 2012 / Published online: 8 March 2012 # Springer Science+Business Media B.V. 2012

Abstract Aims In view of the projected increase in global air temperature and CO2 concentration, the effects of climatic changes on biomass production, CO2 fluxes and arbuscular mycorrhizal fungi (AMF) colonization in newly established grassland communities were investigated. We hypothesized that above- and belowground biomass, gross primary productivity (GPP), AMF root colonization and nutrient acquisition would increase in response to the future climate conditions. Furthermore, we expected that increased belowground C allocation would enhance soil respiration (Rsoil).

Methods Grassland communities were grown either at ambient temperatures with 375 ppm CO2 (Amb) or at ambient temperatures +3°C with 620 ppm CO2 (T+CO2). Results Total biomass production and GPP were stimulated under T+CO2. Above-ground biomass was increased under T+CO2 while belowground biomass was similar under both climates. The significant increase in root colonization intensity under T+CO2, and therefore the better contact between roots and AMF, probably determined the higher above-ground P and N content. Rsoil was not significantly affected by the future climate conditions, only showing a tendency to increase under future climate at the end of the season.

Responsible Editor: Katja Klumpp. Electronic supplementary material The online version of this article (doi:10.1007/s11104-012-1190-y) contains supplementary material, which is available to authorized users. C. Zavalloni : S. Vicca : M. Büscher : I. Nijs : R. Ceulemans Research Group of Plant and Vegetation Ecology, Department of Biology, University of Antwerp (Campus Drie Eiken), Universiteitsplein 1, B-2610 Wilrijk, Belgium C. Zavalloni (*) Department of Agricultural and Environmental Sciences, University of Udine, via delle Scienze, 208, 33100 Udine, Italy e-mail: [email protected]

I. E. de la Providencia : H. Dupré de Boulois : S. Declerck Université catholique de Louvain, Unité de Microbiologie, Croix du Sud 3, 1348 Louvain-la-Neuve, Belgium I. E. de la Providencia Biodiversity Centre, Université de Montreal, 4201 Rue Sherbrooke Est, Montreal H1X 2B2, Canada I. Nijs King Saud University, Riyadh, Saudi Arabia

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Conclusions Newly established grasslands benefited from the exposure to elevated CO2 and temperature in terms of total biomass production; higher root AMF colonization may partly provide the nutrients required to sustain this growth response. Keywords Climate warming . Elevated CO2 . Arbuscular mycorrhizal fungi . Soil respiration . GPP . Roots . Nitrogen . Phosphorus

Introduction Grasslands are important agricultural ecosystems worldwide and in Europe represent one of the dominant forms of land use (approximately 22% of the European Union land area, EEA, 2005). The amount of CO2 that these ecosystems sequester from, or release to the atmosphere depends on the magnitude of the photosynthetic and respiratory processes, which are regulated by climatic factors such as atmospheric CO2 concentration, temperature and water availability. Although rising temperature and CO2 concentration are known to affect the global carbon (C) balance, the uncertainties surrounding their combined effects on CO2 fluxes in grasslands are still large. Warming was reported to increase evapotranspiration and lower soil water availability in perennial grassland communities (Saleska et al. 1999) significantly reducing ecosystem biomass (De Boeck et al. 2008) and gross primary productivity (GPP, De Boeck et al. 2007). De Boeck et al. (2007) observed the largest decrease in GPP during the summer months, when warming-associated drought was most prominent compared to other periods. Similarly, during the 2003 summer heat wave, C fluxes were greatly reduced by drought stress in grasslands of the Central Swiss Plateau (Ammann et al. 2007) and of the Hungarian Plains (Nagy et al. 2007). On the other hand, elevated CO2 may directly stimulate plant productivity (Ainsworth and Long 2005), especially in the presence of high nutrient supply (Luo et al. 2006; Nowak et al. 2004; Poorter 1998), shifting the annual C balance toward a higher influx or a lower efflux (e.g., observed in Mediterranean grasslands, Nijs et al. 2000). In several studies, elevated CO2 also enhanced below-ground C allocation due to CO2-induced increase in carbon supply (Rogers and Runion 1994; Rillig et al. 1999b, 2002a), although such increase was not observed in all studies (e.g., Arnone et al. 2000). Temperature, on the other

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hand, had either no effect (Gavito et al. 2003; Kandeler et al. 1998; Volder et al. 2007) or decreased root biomass (De Boeck et al. 2008; Hartley et al. 2007a; Wan et al. 2004). Important indirect effects of elevated CO2 include an increase of plant water-use efficiency, achieved by high CO2-induced stomatal closure (Morgan et al. 2004). Therefore, when combined with warming, elevated CO2 could alleviate the negative effects of climate warming on soil water content. Nutrient dynamics in plants are also often modulated by changing climate. For example, in winter wheat N and P uptake were driven by plant growth and stimulated by increasing soil temperature but reduced by elevated CO2 (Gavito et al. 2001). In Pisum sativum L., P-use efficiency increased both in plant exposed to either elevated temperatures or elevated CO2 (Gavito et al. 2003). However, downregulation of photosynthesis and respiration to warming and elevated CO2 could mediate the effects of climatic changes on the ecosystem C balance. Several studies reported acclimation of photosynthesis and respiration to elevated temperatures (Atkin et al. 2006; Loveys et al. 2003; Vicca et al. 2007; Wythers et al. 2005), to elevated CO2 (Ainsworth and Long 2005; Ellsworth et al. 2004), or to the combination of both (Tjoelker et al. 1998). The C sequestration of newly established grasslands mainly depends on the potential to increase belowground C. Therefore, soil respiration (Rsoil) is a crucial component of the C balance of these ecosystems. Under elevated CO2, Rsoil may increase due to enhanced root biomass (Rogers and Runion 1994), higher specific root respiration (Edwards and Norby 1999), and/or through higher heterotrophic respiration resulting from an increased supply of labile organic substrates from plants (Zak et al. 2000). Elevated temperature also can increase Rsoil (Rustad et al. 2001), but this response is often limited to the initial period of exposure, after which Rsoil usually returns to its original level (Hyvönen et al. 2007). Such down-regulation is probably due to depletion of the labile soil organic C pools (Hartley et al. 2007b). Available studies on the combined effects of elevated CO2 and temperature on Rsoil are currently not conclusive as they report an increase, a decrease or no change in Rsoil (Comstedt et al. 2006; Edwards and Norby 1999; Garten et al. 2009; Pajari 1995; Pendall et al. 2008, 2011; Tingey et al. 2006; Wan et al. 2007). Due to their key position at the soil-root interface, it is important to consider arbuscular mycorrhizal fungi (AMF) when studying the impact of climatic factors on C fluxes in terrestrial ecosystems. AMF are obligate

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root symbionts that depend on the host plant for C acquisition. In exchange, the AMF transfer inorganic nutrients such as phosphorus (e.g., Jakobsen et al. 2002) and nitrogen (e.g., Ames et al. 1983) to their host, which often results in higher plant biomass production. Any climatic change affecting plants is likely to affect AMF, and vice versa. Elevated temperature or changes in soil water availability may have a direct impact on both the host plant and AMF (Rillig et al. 2002b). Review by Augé (2001) highlighted that under water limited conditions plants inoculated with AMF compared to non-inoculated ones had greater drought tolerance, stomatal conductance and transpiration, and a better supply of diffusion-limited nutrients. In some cases drought-stressed AMF plants absorbed more P, even when the non-inoculated plants had adequate P nutrition (Neumann and George 2004). Hawkes et al. (2008) observed a warming-induced increase in photosynthates translocated to the fungus, independent of plant size and rates of photosynthesis. Temperature significantly altered the structure and allocation of the AMF which switched from more vesicles in cooled soils to more extraradical hyphal networks in warmed soils (Hawkes et al. 2008). An increase in the size of the extraradical hyphal matrix with warming was also observed in a culture study (Gavito et al. 2005) and in pots with sand/clay mixtures (Heinemeyer and Fitter 2004; Heinemeyer et al. 2006). Elevated CO2 can only affect AMF indirectly via increased C transfer from host plant to fungus (Sanders et al. 1998). As reviewed by Díaz (1996), exposure of AMF-colonized plants to elevated CO2 may induce an additional increase in dry weight and/or a better nutritional status. However, some studies reported no AMF-related increase in plant growth or nutrient uptake under elevated CO2 (Gavito et al. 2000; Staddon et al. 1999). Prediction of the outcome of plant competition based on the responses of individual plants to AMF colonization has been only partially successful (Zabinski et al. 2002). Competition between plants is mostly influenced by abiotic factors such as nutrient availability and climate. Since AMF have a significant influence on nutrient uptake, they are likely to influence plant competition and therefore community structure (Grime et al. 1987; Van der Heijden et al. 1998). Moreover, AMF are able to interconnect different species and transfer nutrients between plants (Grime et al. 1987; Newman 1988; Simard et al. 2002) which in turn leads to changes in the competitive ability of plants. However different plant species

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do not profit equally from AMF and some plants acquire more nutrients from AMF than others (Smith and Read 1997). Scheublin et al. (2007) found that the leguminous Lotus corniculatus was favoured in communities with AMF compared to non-AMF communities. Also the competition between the leguminous and the grass Festuca ovina was strongly affected: both the grass and the leguminous benefited from AMF when grown in monoculture but when in competition AMF favoured the leguminous. The influence of AMF on the competition between species will be even more critical during the establishment of grassland communities having possibly a greater impact on the community structure. In this study we investigated the effects of combined warming (ambient +3°C) and elevated atmospheric CO2 concentration (620 ppm CO2) on biomass production, CO2 fluxes and AMF root colonization in newly established grassland communities. Communities were grown on soil from a Belgian grassland field. We hypothesize that in communities exposed to elevated temperature and CO2: a) GPP, above- and below-ground biomass will increase due to the higher C availability; b) AMF root colonization at the community level will be promoted; c) the higher AMF colonization will coincide with greater nutrients acquisition, and d) Rsoil will be enhanced due the higher below-ground C allocation.

Materials and methods Experimental set-up The study was conducted on newly established grassland communities at the Drie Eiken Campus, University of Antwerp, Wilrijk, Belgium (51° 09′ N, 04° 24′ E, 10 m elevation). Average annual precipitation is 776 mm (evenly distributed throughout the year) and average annual air temperature (Tair) is 10.1°C (average period 1971–2000). The grassland communities were grown in ten sunlit, climate-controlled chambers, facing south. Each chamber had an interior surface area of 2.25 m2 and was covered with UV transparent polycarbonate plate on the top and polyethylene film on the sides. Communities in five chambers were exposed to ambient Tair and 375 ppm CO2 (Amb), while in the other five chambers the plant communities were exposed to ambient Tair +3°C and 620 ppm CO2 (future climate, T+CO2). Each T+CO2 chamber had its individual CO2 control group, where air CO2 concentration was measured with

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a CO2 analyzer (WMA-4, PP-Systems, Hitchin, UK) and adjusted to 620 ppm. Each chamber had an individual air-control group with an electrical heating battery, and was linked to a central refrigeration unit by isolated pipes. The conditioned air was distributed evenly throughout the chambers by means of aerators with regulated flow. Tair in each chamber was controlled separately and measured together with relative humidity with a humidity-temperature sensor (Siemens, type QFA66, Berlin, Germany). Inside each chamber photosynthetically active radiation was also measured with a quantum sensor (SDEC, type JYP1000, Reignacsur-Indre, France). All the microclimate parameters from inside each chamber and outside were automatically logged on a computer. For the full duration of the experiment communities in the two climate scenarios received the same irrigation regime based on the last 10-year average monthly precipitation recorded in the nearby station of Deurne, Antwerp, Belgium (51° 12′ N, 04° 28′ E, 14 m elevation). Communities were watered three times per week with a drip irrigation system. Total monthly irrigation was equal to 61.5, 64.4, 85.1, 80.2, 80.9 and 69.7 mm in May, June, July, August, September and October, respectively. Water could freely drain from the plastic containers where communities were established, while capillary rise was prevented by a drainage system placed below the chambers. The containers (24 cm inner diameter, 40 cm height) were buried into the soil to obtain realistic soil temperatures. Profile probe tubes for the soil moisture sensor (PR2 probe, Delta-T Devices Ltd., UK) were installed in each community and soil water content (SWC) was monitored every 10 days during the experiment. Throughout the experiment plants were healthy and free of pests and diseases. Leaf fungal infections were treated only once in August (COMPO Geyser®, active ingredient, difenoconazole) while pests control was done twice in August (KB Polysect 3P, active ingredient, acetamiprid). Studies on degradation of difenoconazole in soils after leaf spray reported either no influence on AMF growth and colonization ability (Hilber et al. 1998) or small negative effects (Meenakshi et al. 2007). Communities were all equally sprayed. During the experiment, no fertilizer was added and weeding was done manually. Each chamber contained 30 randomly placed grassland communities. The experiment in this study used a subset of 30 communities (15 communities per climate scenario) evenly distributed over the ten chambers (three communities per chamber, Fig. 7 and 8 supplementary

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material). Communities were established at the beginning of May 2007 by transplanting 5-week old seedlings into the plastic containers filled with soil from a relatively species-rich, extensively managed grassland site in Berlaar (province of Antwerp, Belgium). The soil was classified as sandy (89.2% sand, 8.7% silt, 2.1% clay), with a pH05.3, 1.5% total C, 117 mg of total nitrogen (N) and 45 mg of total phosphorus (P) per 100 g of air dry soil, cation exchange capacity 0 7.73 meq/100 g of soil. All plant communities were assembled using an identical scheme with six perennial species selected from three functional groups, equally represented in each community: two grass species (Poa pratensis L., Lolium perenne L.), two N-fixing dicots (Medicago lupulina L., Lotus corniculatus L.), and two non-N-fixing dicots (Rumex acetosa L., Plantago lanceolata L.). Each community contained 18 individuals (three individuals per species) planted in a hexagonal grid with a 4.5 cm interspace between plants, with interspecific interactions maximized by avoiding clumping. Community CO2 fluxes Community CO2 fluxes were measured in three periods, lasting approximately five consecutive days, starting from 16 July (day of the year, DOY 197), 13 August (DOY 225), and 17 September (DOY 260) 2007. Flux measurements were made using a closed gas exchange system with a transparent polycarbonate cuvette (25 cm diameter, 60 cm height), sealing the entire container surface. The cuvette was coupled to an EGM-4 infrared gas analyzer (PP Systems, Hitchin, UK). Inside the cuvette, a quantum sensor (JYP 1000, SDEC, Reignacsur-Indre, France) measured photosynthetic photon flux density (PPFD) above the vegetation. After placing the cuvette on the community, net ecosystem CO2 exchange (NEE) was recorded. Immediately after NEE was recorded for a given plant community, the cuvette was darkened with a black cloth to determine total ecosystem respiration (TER). GPP was estimated as GPP 0 NEE – TER. Measurements in the compared treatments were randomized during each period. To collect measurements at different light intensities within a short time frame and limit the influence of varying outside weather conditions, measurements were performed on seven communities per climate scenario, four of which measured in each period and three harvested after recording the CO2 fluxes. To obtain sufficient measurements with varying PPFD, all 14 communities were measured twice

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during each week-period. Measurements were made between 9 h and 18 h. Below-ground respiration (Rsoil) was measured in small PVC chambers (12 cm2 basal area, 5 cm height) installed permanently when plant were transplanted on a strip of bare soil in each container. Each soil respiration chamber had an aerating hole to ensure mixing of air with the outside air between measurements. During measurements, the chambers were sealed with an impermeable material (Terostat, Henkel KGaA, Düsseldorf, Germany). Measurements of Rsoil were used to derive above-ground respiration (Rabove) as Rabove 0 TER – Rsoil. Immediately following the Rsoil measurements, soil temperature (Tsoil) at 5 cm depth was recorded with a soil thermometer (Hanna Instruments, Woonsocket, RI, USA). As photosynthesis is mainly driven by PPFD, GPP – PPFD curves were obtained for each measurement period by fitting a rectangular hyperbola model (De Boeck et al. 2007; Gilmanov et al. 2007; Tamiya 1951): GPP ¼ ðQE  GPPmax  PPFDÞ=ðQE  PPFD þ GPPmax Þ

ð1Þ where QE is the quantum efficiency and GPPmax is the maximum gross primary productivity. Both Rabove and Rsoil depend mainly on temperature. In order to compare respiratory rates between the treatments the following function was fitted (Luo and Zhou 2006): ðTTref Þ=10

Rabove or Rsoil ¼ BR  Q10

ð2Þ

potential down-regulation, with full homeostasis occurring if BR is equal in both climates. During 5 days between 15 and 22 October 2007, Rsoil was measured in five communities for each climate. In order to obtain a sufficiently large temperature range, with an overlap between both climates, air temperatures in the chambers were altered (within the range of −1 to +7°C relative to outside Tair) for approximately 24 h prior to measuring Rsoil. Average soil temperatures (at 5 cm depth) during Rsoil measurements for the 5 days were 12.0, 14.0, 11.4, 10.1 and 8.7°C in Amb and 13.0, 14.3, 11.3, 9.2 and 7.9°C in T+CO2. Each of these 5 days, Rsoil in each community was measured three times within 10 min, using the same procedure as during seasonal measurements. In order to avoid confounding effects through changes in plant photosynthesis (Heinemeyer et al. 2006; Moyano et al. 2007), Rsoil was measured in the morning between 8 and 12 h. Both BR and Q10 of Rsoil were computed using Eq. 2, with T 0 soil temperature at 5 cm depth and Tref 0 10°C for Amb or Tref 0 13°C for T+CO2. These Tref were selected in the range of measured soil temperatures, considering a 3°C difference between both climate scenarios to obtain BR at growth conditions. To illustrate the goodness of fit, the regressions for Rsoil for each community are shown in Fig. 6 in the supplementary material. For each treatment, the weighted mean BR at growth temperature and the weighted mean Q10 were computed using 1/SE of the parameters as weight factor (SE of BR and Q10 of each fitted regression was considered). Biomass and leaf C, N and P concentration

where BR is the basal respiration rate (BRabove and BRsoil for above-ground and soil respiration, respectively) computed at a reference temperature (Tref), Q10 is the temperature sensitivity of Rabove or Rsoil, and T is the recorded air or soil temperature at the time of measurement. In order to compare respiration rates at growth conditions, the 3°C difference between the climate scenarios was taken into account by computing BR at 20°C and 23°C for Amb and T+CO2, respectively. For Rsoil, regression analyses were performed for each climate, combining the measurements obtained in the three periods (within one period, the temperature range was too small to properly fit temperature response curves). An additional set of Rsoil measurements was collected at the end of the season to test whether Rsoil had acclimated to the combined elevated temperature and CO2. Basal respiration at growth conditions may indicate

Above- and below-ground biomass were collected immediately after each CO2 flux measurement period and additionally on 6 November (DOY 310) 2007. At each harvest, three different communities per climate scenario were destructively harvested (five at the end), after recording the number of remaining individuals per species. Above-ground biomass was subdivided by species while total below-ground biomass was estimated from roots collected in 12 soil cores (2 cm diameter) per community divided into four soil depths: 0–9, 10–18, 19–27 and 28–36 cm. To avoid misrepresentation of root biomass of individual species and allow comparison of root biomass collected in the different harvests, each pot was sampled using the same spatial scheme: six soil cores were collected in close proximity of each species and the other six cores

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were collected in the middle of a triangle between three plants. Biomass was dried for 48 h at 70°C and afterwards the dry weight was recorded. During the last harvest roots were washed and stored in the fridge (4°C) in Ringer’s solution. Within 2 weeks, these roots were analyzed to determine root length and diameter, using WinRHIZO image analysis software (Regent Instruments Inc., Quebec, Canada). Analyses of leaf and root (from the top 9 cm soil layer) C and N concentrations and analysis of leaf P concentration were carried out only at the last harvest (November). C and N were determined on 5 to 7 mg of dried sample with a CN element analyser (NC-2100, Carlo Erba Instruments, Milano, Italy). Total leaf P concentration was determined by colorimetrical analysis (Scheel 1936) after acid digestion of 0.2 g of dried leaf sample. Since root samples were also used for AMF determination, the remaining part of the root samples was not sufficient for the determination of P concentration in roots. AMF root colonization Dried roots sampled from the four soil depths (0–9, 10– 18, 19–27 and 28–36 cm) were cleared in 10% KOH (90°C for 30 min) and stained with a blue ink solution (90°C for 10 min, 1% HCl with 1% Parker blue ink, Vierheilig et al. 1998). Thirty randomly selected root pieces (10 mm length) per soil layer and community were observed under a bright-field microscope at 50× or 125× magnification and the frequency and intensity of AMF root colonization was estimated according to the method described by Plenchette and Morel (1996). Frequency of AMF root colonization was calculated as the percentage of root segments that contained either hyphae, arbuscules or vesicles, while the abundance of hyphae, arbuscules and vesicles in each root segment (intensity of colonization) was estimated using intensity classes: 1– 20, 21–40, 41–60, 61–80, 81–100% (Plenchette and Morel 1996). To properly compare treatments, weighted means of frequency and intensity of colonization were calculated using the root biomass per soil layer as weighing factor. Only for the last harvest, after determining root length, the root length density (RLD) colonized by AMF was also calculated considering the RLD and the average % of frequency of AMF root colonization for that harvest.

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Statistical analysis Regression analyses of CO2 fluxes were performed in Matlab 7 (The Math-Works, Inc., Natick, USA). Analyses of variance (ANOVA) of biomass and nutrients contents were performed in SAS 9.1 (SAS Institute Inc., Cary, NC, USA) using the mixed procedure described in Littell et al. (2006). The ANOVAs included climate (Amb and T+CO2) and time period (when appropriate) as fixed factors and their interaction. Variables were transformed (either squared root or logarithm) when the assumption of normal distribution was violated (ShapiroWilk test). Differences in seasonal CO2 fluxes between climates were evaluated with ANCOVA analyses after data were log-transformed. The ANCOVA analysis for GPP included PPFD as covariate and climate scenario and time period as fixed factors. Values of GPP at PPFDs below 100 μmol photons m−2 s−1 were excluded from the analysis because they caused a nonlinear distribution after the log transformation. The ANCOVA analyses for Rabove and seasonal Rsoil included air or soil temperature as covariate, respectively. Climate was a fixed factor. For Rabove, the time period was also included as a fixed factor. Effects of climate on Rsoil measured at the end of the season were tested via a weighted ANOVA analysis on BR at growth temperature and Q10, with climate as fixed factor and 1/SE of the specific parameter as weight factor. Frequency and intensity of AMF root colonization were arcsin √(x/100) transformed to obtain normal distribution. Significant (P

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