Effects of climate change on native plant communities in semiarid gypsum ecosystem

Laburpena

ABSTRACT Anthropogenic greenhouse gas emissions are expected to increase global mean temperature by 2-6ºC by the end of the XXI century. The Mediterranean region will be one of the most responsive to global climate change (Giorgi, 2006), and current climatic models predict drastic changes including temperature increases and reduced amount and frequency of rainfall relative to current climate conditions. Semiarid Mediterranean ecosystems might be particularly vulnerable to climate change, since both increased temperature and decreased precipitation will tend to reduce soil moisture availability, which is already the major limiting factor for primary productivity under current climate conditions. These ecosystems have a high conservation value as one of the most important biodiversity hotspots of the Earth and provide multiple ecosystem goods and services to society, but they could be at increased risk of vegetation cover loss, land degradation and desertification under the forecasted climate change scenario. Moreover, semiarid shrubland communities growing on gypsum soils are very rich in rare and endemic species (several of our target shrub species are considered vulnerable in the IUCN Red List of Spanish Vascular Flora). In this thesis, we have simulated the climate conditions projected for the second half of XXI century, by using open top chambers (1-2ºC temperature increase in the wintertime and 4-6ºC in the summertime; W treatment), rainout shelters (-30% rainfall exclusion; RR treatment) and their combination (W+RR treatment) in order to assess the effects of forecasted climate change conditions on the performance of three semiarid Mediterranean shrubland communities located in central (Aranjuez) and southeastern Spain (Sorbas and Sax) throughout 4 hydrological years (2011-2015). Our target species are Helianthemum squamatum (present at the three study sites), Helianthemum syriacum, Gypsohila struthium, Santolina viscosa, Teucrium turredanum and Coris hispanica, which are native shrub species with different sizes/biovolumes, life history traits, phenology, stoichiometry, water use strategies and mycorrhizal association types (ectomycorrhizal or arbuscular mycorrhizal). For this purpose, we measured leaf gas exchange parameters (photosynthesis rate, stomatal conductance, transpiration, maximum efficiency of photosystem II under light conditions, the quantum efficiency of photosystem II and water use efficiency), carbon isotope ratio (δ13C), foliar nutrient status, leaf mass per unit area, shoot dry biomass production, shoot elongation, shoot growth phenology and survival rate at the end of the 4-year study period, as well as mycorrhizal fungal community composition and relative abundances. We hypothesized that warming, rainfall reduction and their combination would reduce soil water availability to an extent that would significantly impair plant nutrient uptake and status, while at the same time increasing stomatal limitation of photosynthesis, thus negatively affecting photosynthesis, productivity and survival across coexisting plant species in these three semiarid ecosystems. Moreover, we predicted that the climate manipulation treatments would impair the performance of both mycorrhizal fungi and their host plants due to the adverse effects of increased heat and drought stress on fungal and plant physiology. Warming sharply reduced the net photosynthesis rate and water use efficiency of the target plants across the three experimental sites throughout the 4-year study period, without any evidence of photosynthetic acclimation to warming. The target plants also showed a significant downregulation of photosystem II, likely to match a reduced carboxylation capacity linked to decreased leaf nutrient (N, P) status. Stomatal conductance was unaffected by warming in the experimental site of Sax, likely due to the presence of a Pinus halepensis overstory that provides shade to understory H. squamatum shrubs and thus moderates temperature and vapor pressure deficit extremes. In the sites of Aranjuez and Sorbas, stomatal conductance was generally increased by warming, probably as an adaptive mechanism to prevent leaf overheating and photosynthetic machinery damage through enhanced evaporative leaf cooling. The leaf δ13C values of the target shrub species were consistently lower in plants exposed to warming across the three study sites, indicating decreased time-integrated water use efficiency under warming and demonstrating the validity of stable isotope techniques as a useful tool in ecophysiological studies evaluating the impacts of climate manipulation on vegetation. Warming also consistently reduced leaf N and P concentrations relative to control plants across study sites over the 4-years study period, which could be the result of a hindered soil nutrient mineralization, solubilization, diffusion and/or uptake by roots under warming, owing to a more rapid and severe drying of the upper soil layers where the majority of nutrients available for plants are located. In the site of Sorbas, we found that the foliar concentrations of other important nutrients for photosynthesis such as K, Fe, Cu and Zn were also strongly decreased by warming and moderately decreased by rainfall reduction. Warming strongly reduced shoot dry biomass production relative to control plants in all the target species across study sites. Warmed plants showed an advanced shoot growth phenology, concentrating vegetative growth in the earlier part of spring. Simulated climate change sharply reduced the diversity and relative abundance of EMF communities in the rhizosphere of H. squamatum in the site of Aranjuez, likely due to detrimental effects of soil warming and drying on mycorrhizal fungi and to reductions in belowground carbon allocation by host plants. The deeply interdependent responses of plants and their EMF partners to experimental climate change had mutually amplifying effects that strongly reduced plant nutrient status, photosynthesis, water use efficiency, shoot biomass production and drought survival. The post-summer survival rate of H. squamatum was not affected by warming at the Sax site, likely due to the buffering effects of the pine overstory on microclimatic conditions for understory plants. In the coolest and wettest site, Aranjuez, the post-summer survival rate of H. squamatum shrubs remained high and similar across treatments in years with above- or near-average rainfall, likely due to the wide range of adaptive phenotypic plasticity mechanisms that enable plants to adjust their physiology to warmer and/or drier conditions. However, in a dry year, warming exceeded plant phenotypic plasticity capacity, leading to sharp declines in post-summer survival rate, probably due to plant hydraulic impairment caused by xylem embolism, carbon starvation, or the combination of both factors. In the warmest and driest site (Sorbas), plant survival rate at the end of the 4 year study period was sharply reduced by experimental warming across target species (especially when in combination with rainfall reduction). Across species and experimental sites, the detrimental effects of warming on plant performance were generally stronger than those of rainfall reduction, likely because native plant species are well preadapted to nearly chronic drought stress. The detrimental effects of the combination of warming and rainfall reduction on plant performance tended to be additive (or not even that) rather than synergistic across species and sites. Overall, the results of this thesis highlight the potential vulnerability of Mediterranean-type native semiarid shrublands (and their ectomycorrhizal fungal partners in the case of H. squamatum) to forecasted climate change, which will likely cause multiple detrimental feedback loops that could lead to an alternative state of decreased vegetation productivity and push these ecosystems to a degradation and desertification pathway. Therefore, the findings reported in thesis will hopefully contribute to a better understanding and anticipation of the detrimental impacts of ongoing climate warming and aridification on the structure and functioning of plant and mycorrhizal fungal communities in semiarid gypsum ecosystems, which will ultimately aid the long-term management and conservation of biodiversity in these vulnerable habitats.