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Mycorrhizal Association As a Primary Control of the CO2 Fertilization Effect César Terrer, Sara Vicca, Bruce A

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Mycorrhizal Association As a Primary Control of the CO2 Fertilization Effect César Terrer, Sara Vicca, Bruce A RESEARCH | REPORTS CARBON CYCLE precipitation (MAP), mean annual temperature (MAT), age of the vegetation at the start of the experiment, vegetation type (such as grassland or forest), CO2 fumigation technology (such as Mycorrhizal association as a primary FACE or growth chamber), length of the study (years), dominant mycorrhizal type (AM or ECM), control of the CO2 fertilization effect and N-status [high or low N availability, consid- ering soil characteristics and occasional fer- César Terrer,1* Sara Vicca,2 Bruce A. Hungate,3,4 Richard P. Phillips,5 I. Colin Prentice1,6 tilizer treatments, following the approach by Vicca et al.(17) and assigning all experiments Plants buffer increasing atmospheric carbon dioxide (CO2) concentrations through enhanced with indications for some degree of N limitation growth, but the question whether nitrogen availability constrains the magnitude of this to the “low N” class and experiments that were ecosystem service remains unresolved. Synthesizing experiments from around the world, we unlikely N limited to the “high N” class] (sup- show that CO2 fertilization is best explained by a simple interaction between nitrogen plementary materials, materials and methods, availability and mycorrhizal association. Plant species that associate with ectomycorrhizal fungi and table S2). show a strong biomass increase (30 ± 3%, P < 0.001) in response to elevated CO2 regardless Model selection analysis, based on corrected of nitrogen availability, whereas low nitrogen availability limits CO2 fertilization (0 ± 5%, P = Akaike Information Criterion (AICc), showed that 0.946) in plants that associate with arbuscular mycorrhizal fungi. The incorporation of the most parsimonious model within two AICc mycorrhizae in global carbon cycle models is feasible, and crucial if we are to accurately project units included N-status, mycorrhizal type, and ecosystem responses and feedbacks to climate change. DCO2 (P <0.001).Therelativeimportanceofthe predictors (Fig. 1) supported the removal of cli- errestrial ecosystems sequester annually observations, none has been found to be general, mate variables, length of the experiment, age of about a quarter of anthropogenic carbon explaining the range of observations globally. the vegetation, fumigation technology, and system dioxide (CO2)emissions(1), slowing climate About 94% of plant species form associations type. Some predictors reduced the CO2 effect on T change. Will this effect persist? Two con- with mycorrhizal fungi, an ancient mutualism biomass (such as age of the vegetation), whereas tradictory hypotheses have been offered: thought to have facilitated the colonization of others were associated with an increased CO2 ef- The first is that CO2 will continue to enhance land by early plants (16). In this mutualism, the fect (such as ECM, DCO2, and high N availability) plant growth, partially mitigating anthropogenic fungus transfers nutrients and water to the plant (fig. S4). on September 28, 2016 CO2 emissions (1, 2), whereas the second is that in exchange for carbohydrates, which are neces- Theresponseoftotalbiomasstoanincrease −1 nitrogen (N) availability will limit the CO2 fertil- sary for fungal growth. Mycorrhizal fungi are of CO2 from 400 to 650 mmol mol was larger ization effect (3, 4), reducing future CO2 uptake critical for terrestrial C cycling (17); are known (P < 0.001) in ECM (30 ± 3%, P < 0.001) than in by the terrestrial biosphere (5–7). Plants exper- to influence plant growth (18), nutrient cycling AM-dominated (7 ± 4%, P = 0.089) ecosystems imentally exposed to elevated levels of CO2 (eCO2) (19, 20), and soil carbon storage (21); and respond (mean ± SE, mixed effects metaregression). The show a range of responses in biomass—from large strongly to elevated CO2 (22, 23). Yet, their impact overall response of total biomass was 20 ± 3% and persistent (8, 9), to transient (6), to nonexistent on the N-dependence of the CO2 fertilization ef- (P < 0.001), which is similar to previous meta- (10)—leaving the question of CO2 fertilization fect has not been tested, despite the increasing analyses (15), with a larger effect under high open. Differences might be driven by different evidence that N limitation constrains the CO2 fer- (27 ± 4%, P < 0.001) than low N availability (15 ± levels of plant N availability across experiments tilization effect (5). Arbuscular mycorrhizae (AM) 4%, P < 0.001), as expected (5, 7, 11). Furthermore, (11), but N availability alone cannot explain con- and ectomycorrhizae (ECM) are by far the most we found a strong interaction between mycor- trasting results based on available evidence (7, 12). widespread types of mycorrhizae (24): AM-plants rhizal type and N-status (P < 0.001); under low N http://science.sciencemag.org/ For instance, among two of the most studied free- predominate in deserts, grasslands, shrublands, availability, eCO2 had no effect on total biomass air CO2 enrichment (FACE) experiments with and tropical forest ecosystems, whereas ECM- of AM-dominated species (0 ± 5%, P = 0.946) trees, eCO2 enhanced biomass production only fungi predominate in boreal and many temperate but increased biomass by 28 ± 5% in ECM- during the first few years at Oak Ridge National forests (for example, those dominated by Pinus). dominated species (P <0.001)(Fig.2A).Under Laboratory (ORNL)–FACE (6), whereas trees in ECM can transfer N to the host plant under eCO2 the Duke University FACE experiment showed a to sustain CO2 fertilization (25), whereas the sym- sustained enhancement during the course of the biotic effects of AM fungi in N-limited systems Downloaded from experiment (8), despite N limitation. In addition can range from beneficial to parasitic (19). Hence, to N limitation, other factors have been suggested the association of Liquidambar styraciflua with as potential drivers of the response of plant bio- AM-fungi at ORNL-FACE, and Pinus taeda with mass to eCO2: age of the vegetation (13), water ECM-fungi at Duke-FACE, might explain why limitation (14), temperature (15), type of vegeta- only trees in the latter could increase N-uptake tion (12), or even the eCO2 fumigation technology and take advantage of eCO2 to grow faster for a used (11). Although these factors may explain some sustained period (20, 25). We tested the hypoth- esis that the differences in the nutrient econo- mies of ECM and AM fungi influence global patterns of the magnitude of plant biomass re- 1AXA Chair Programme in Biosphere and Climate Impacts, Department of Life Sciences, Silwood Park Campus, Ascot, sponses to elevated CO2. Imperial College London, UK. 2Centre of Excellence PLECO We synthesized data (overview is provided (Plant and Vegetation Ecology), Department of Biology, in table S1) on total plant biomass (grams per Fig. 1. Model-averaged importance of the pre- University of Antwerp, 2610 Wilrijk, Belgium. 3Center for square meter) from 83 eCO experiments (fig. dictors of the CO fertilization effect on total Ecosystem Science and Society, Northern Arizona University, 2 2 Flagstaff, AZ 86011, USA. 4Department of Biological S1), separating responses into aboveground bio- biomass. The importance is based on the sum of Sciences, Northern Arizona University, Flagstaff, AZ 86011, mass (n = 83) (fig. S2) and belowground biomass Akaike weights derived from model selection using 5 USA. Department of Biology, Indiana University, (n = 82) (fig. S3) in a mixed-effects meta-analysis. AICc (Akaike’s Information Criteria corrected for Bloomington, IN 47405, USA. 6Department of Biological As potential drivers of the plant biomass re- small samples). Cutoff is set at 0.8 (dashed line) Sciences, Macquarie University, North Ryde, New South Wales 2109, Australia. sponse, we considered the increase in atmos in order to differentiate among the most important *Corresponding author. Email: [email protected] pheric CO2 concentration (DCO2), mean annual predictors. 72 1JULY2016• VOL 353 ISSUE 6294 sciencemag.org SCIENCE RESEARCH | REPORTS high N availability, the CO2 effect on total bio- sponses to eCO2 can thus be used to isolate the ability in the short term, most of the N exists in mass in both AM- and ECM-dominated species influence of mycorrhizal type from that of veg- particulate forms, which should be accessible to was significant: 20 ± 6% (P = 0.002) for AM and etation growth form. These three sensitivity analy- most microbes (including ECM fungi). Therefore, 33 ± 4% (P <0.001)forECM(Fig.2A),withno ses confirmed that the CO2 stimulation of total AM fungi are equipped with less specialized en- significant differences between the two groups andabovegroundplantbiomass was significant zymes for N acquisition than are ECM and occur (P = 0.139). Hence, high N availability signifi- and large in ECM plants regardless of N avail- in soils in which N is more tightly protected. Both cantly increased the CO2 effect in AM [post-hoc, ability, whereas the effect was not significant in factors would presumably limit the enhancement Tukey’s honestly significant difference (HSD): AM plants under low N availability. The trend of AM plant growth in response to eCO2. adj-P = 0.038] but not in ECM-associated species was consistent for belowground biomass in ECM Mycorrhizal symbioses are not accounted for (adj-P =0.999). plants, although with high variance and low in most global vegetation models (24). Thus, the The patterns observed for total biomass were sample size, the effect was not significant (P = projected CO2 fertilization effect by “carbon- reflected in both aboveground and belowground 0.244) under low N when the “medium” class only models” (1) is likely overestimated for AM- biomass. Under low N availability, eCO2 stimu- was included. dominated ecosystems, which cover ~65% of the lated aboveground biomass significantly in ECM Plant N uptake can be enhanced through my- global vegetated area (24), albeit only when N- plants (P < 0.001), with no effect in AM plants corrhizal associations or through associations with limited. On the other hand, global models that (P = 0.584) (Fig. 2B). Similarly, eCO2 enhanced N-fixing microbes.
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