Increasing plant group productivity through latent genetic variation for cooperation.

Historic yield advances in the major crops have, to a large extent, been achieved by selection for improved productivity of groups of plant individuals such as high-density stands. Research suggests that such improved group productivity depends on "cooperative" traits (e.g., erect leaves, short stems) that-while beneficial to the group-decrease individual fitness under competition. This poses a problem for some traditional breeding approaches, especially when selection occurs at the level of individuals, because "selfish" traits will be selected for and reduce yield in high-density monocultures. One approach, therefore, has been to select individuals based on ideotypes with traits expected to promote group productivity. However, this approach is limited to architectural and physiological traits whose effects on growth and competition are relatively easy to anticipate. Here, we developed a general and simple method for the discovery of alleles promoting cooperation in plant stands. Our method is based on the game-theoretical premise that alleles increasing cooperation benefit the monoculture group but are disadvantageous to the individual when facing noncooperative neighbors. Testing the approach using the model plant Arabidopsis thaliana, we found a major effect locus where the rarer allele was associated with increased cooperation and productivity in high-density stands. The allele likely affects a pleiotropic gene, since we find that it is also associated with reduced root competition but higher resistance against disease. Thus, even though cooperation is considered evolutionarily unstable except under special circumstances, conflicting selective forces acting on a pleiotropic gene might maintain latent genetic variation for cooperation in nature. Such variation, once identified in a crop, could rapidly be leveraged in modern breeding programs and provide efficient routes to increase yields.

Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia.

Late-spring frosts (LSFs) affect the performance of plants and animals across the world's temperate and boreal zones, but despite their ecological and economic impact on agriculture and forestry, the geographic distribution and evolutionary impact of these frost events are poorly understood. Here, we analyze LSFs between 1959 and 2017 and the resistance strategies of Northern Hemisphere woody species to infer trees' adaptations for minimizing frost damage to their leaves and to forecast forest vulnerability under the ongoing changes in frost frequencies. Trait values on leaf-out and leaf-freezing resistance come from up to 1,500 temperate and boreal woody species cultivated in common gardens. We find that areas in which LSFs are common, such as eastern North America, harbor tree species with cautious (late-leafing) leaf-out strategies. Areas in which LSFs used to be unlikely, such as broad-leaved forests and shrublands in Europe and Asia, instead harbor opportunistic tree species (quickly reacting to warming air temperatures). LSFs in the latter regions are currently increasing, and given species' innate resistance strategies, we estimate that ∼35% of the European and ∼26% of the Asian temperate forest area, but only ∼10% of the North American, will experience increasing late-frost damage in the future. Our findings reveal region-specific changes in the spring-frost risk that can inform decision-making in land management, forestry, agriculture, and insurance policy.

Biodiversity increases the resistance of ecosystem productivity to climate extremes.

It remains unclear whether biodiversity buffers ecosystems against climate extremes, which are becoming increasingly frequent worldwide. Early results suggested that the ecosystem productivity of diverse grassland plant communities was more resistant, changing less during drought, and more resilient, recovering more quickly after drought, than that of depauperate communities. However, subsequent experimental tests produced mixed results. Here we use data from 46 experiments that manipulated grassland plant diversity to test whether biodiversity provides resistance during and resilience after climate events. We show that biodiversity increased ecosystem resistance for a broad range of climate events, including wet or dry, moderate or extreme, and brief or prolonged events. Across all studies and climate events, the productivity of low-diversity communities with one or two species changed by approximately 50% during climate events, whereas that of high-diversity communities with 16-32 species was more resistant, changing by only approximately 25%. By a year after each climate event, ecosystem productivity had often fully recovered, or overshot, normal levels of productivity in both high- and low-diversity communities, leading to no detectable dependence of ecosystem resilience on biodiversity. Our results suggest that biodiversity mainly stabilizes ecosystem productivity, and productivity-dependent ecosystem services, by increasing resistance to climate events. Anthropogenic environmental changes that drive biodiversity loss thus seem likely to decrease ecosystem stability, and restoration of biodiversity to increase it, mainly by changing the resistance of ecosystem productivity to climate events.

Biodiversity promotes primary productivity and growing season lengthening at the landscape scale.

Experiments have shown positive biodiversity-ecosystem functioning (BEF) relationships in small plots with model communities established from species pools typically comprising few dozen species. Whether patterns found can be extrapolated to complex, nonexperimental, real-world landscapes that provide ecosystem services to humans remains unclear. Here, we combine species inventories from a large-scale network of 447 1-km2 plots with remotely sensed indices of primary productivity (years 2000-2015). We show that landscape-scale productivity and its temporal stability increase with the diversity of plants and other taxa. Effects of biodiversity indicators on productivity were comparable in size to effects of other important drivers related to climate, topography, and land cover. These effects occurred in plots that integrated different ecosystem types (i.e., metaecosystems) and were consistent over vast environmental and altitudinal gradients. The BEF relations we report are as strong or even exceed the ones found in small-scale experiments, despite different community assembly processes and a species pool comprising nearly 2,000 vascular plant species. Growing season length increased progressively over the observation period, and this shift was accelerated in more diverse plots, suggesting that a large species pool is important for adaption to climate change. Our study further implies that abiotic global-change drivers may mediate ecosystem functioning through biodiversity changes.

Tree-species interactions increase light absorption and growth in Chinese subtropical mixed-species plantations.

Light-related interactions can increase productivity in tree-species mixtures compared with monocultures due to higher stand-level absorption of photosynthetically active radiation (APAR) or light-use efficiency (LUE). However, the effects of different light-related interactions, and their relative importance, have rarely been quantified. Here, measurements of vertical leaf-area distributions, tree sizes, and stand density were combined with a tree-level light model (Maestra) to examine how crown architecture and vertical or horizontal canopy structure influence the APAR of 16 monocultures and eight different two-species mixtures with 16 different species in a Chinese subtropical tree diversity experiment. A higher proportion of crown leaf area occurred in the upper crowns of species with higher specific leaf areas. Tree-level APAR depended largely on tree leaf area and also, but to a lesser extent, on relative height (i.e., tree dominance) and leaf-area index (LAI). Stand-level APAR depended on LAI and canopy volume, but not on the vertical stratification or canopy leaf-area density. The mixing effects, in terms of relative differences between mixtures and monocultures, on stand-level APAR were correlated with the mixing effects on basal area growth, indicating that light-related interactions may have been responsible for part of the mixing effects on basal area growth. While species identity influences the vertical distributions of leaf area within tree crowns, this can have a relatively small effect on tree and stand APAR compared with the size and vertical positioning of the crowns, or the LAI and canopy volume.

Tree species richness increases ecosystem carbon storage in subtropical forests.

Forest ecosystems are an integral component of the global carbon cycle as they take up and release large amounts of C over short time periods (C flux) or accumulate it over longer time periods (C stock). However, there remains uncertainty about whether and in which direction C fluxes and in particular C stocks may differ between forests of high versus low species richness. Based on a comprehensive dataset derived from field-based measurements, we tested the effect of species richness (3-20 tree species) and stand age (22-116 years) on six compartments of above- and below-ground C stocks and four components of C fluxes in subtropical forests in southeast China. Across forest stands, total C stock was 149 ± 12 Mg ha-1 with richness explaining 28.5% and age explaining 29.4% of variation in this measure. Species-rich stands had higher C stocks and fluxes than stands with low richness; and, in addition, old stands had higher C stocks than young ones. Overall, for each additional tree species, the total C stock increased by 6.4%. Our results provide comprehensive evidence for diversity-mediated above- and below-ground C sequestration in species-rich subtropical forests in southeast China. Therefore, afforestation policies in this region and elsewhere should consider a change from the current focus on monocultures to multi-species plantations to increase C fixation and thus slow increasing atmospheric CO2 concentrations and global warming.

Positive diversity-functioning relationships in model communities of methanotrophic bacteria.

Biodiversity enhances ecosystem functions such as biomass production and nutrient cycling. Although the majority of the terrestrial biodiversity is hidden in soils, very little is known about the importance of the diversity of microbial communities for soil functioning. Here, we tested effects of biodiversity on the functioning of methanotrophs, a specialized group of soil bacteria that plays a key role in mediating greenhouse gas emissions from soils. Using pure strains of methanotrophic bacteria, we assembled artificial communities of different diversity levels, with which we inoculated sterile soil microcosms. To assess the functioning of these communities, we measured methane oxidation by gas chromatography throughout the experiment and determined changes in community composition and community size at several time points by quantitative PCR and sequencing. We demonstrate that microbial diversity had a positive overyielding effect on methane oxidation, in particular at the beginning of the experiment. This higher assimilation of CH4 at high diversity translated into increased growth and significantly larger communities towards the end of the study. The overyielding of mixtures with respect to CH4 consumption and community size were positively correlated. The temporal CH4 consumption profiles of strain monocultures differed, raising the possibility that temporal complementarity of component strains drove the observed community-level strain richness effects; however, the community niche metric we derived from the temporal activity profiles did not explain the observed strain richness effect. The strain richness effect also was unrelated to both the phylogenetic and functional trait diversity of mixed communities. Overall, our results suggest that positive biodiversity-ecosystem-function relationships show similar patterns across different scales and may be widespread in nature. Additionally, biodiversity is probably also important in natural methanotrophic communities for the ecosystem function methane oxidation. Therefore, maintaining soil conditions that support a high diversity of methanotrophs may help to reduce the emission of the greenhouse gas methane.

Can niche plasticity promote biodiversity-productivity relationships through increased complementarity?

Most experimental biodiversity-ecosystem functioning research to date has addressed herbaceous plant communities. Comparably little is known about how forest communities will respond to species losses, despite their importance for global biogeochemical cycling. We studied tree species interactions in experimental subtropical tree communities with 33 distinct tree species mixtures and one, two, or four species. Plots were either exposed to natural light levels or shaded. Trees grew rapidly and were intensely competing above ground after 1.5 growing seasons when plots were thinned and the vertical distribution of leaves and wood determined by separating the biomass of harvested trees into 50 cm height increments. Our aim was to analyze effects of species richness in relation to the vertical allocation of leaf biomass and wood, with an emphasis on bipartite competitive interactions among species. Aboveground productivity increased with species richness. The community-level vertical leaf and wood distribution depended on the species composition of communities. Mean height and breadth of species-level vertical leaf and wood distributions did not change with species richness. However, the extra biomass produced by mixtures compared to monocultures of the component species increased when vertical leaf distributions of monocultures were more different. Decomposition of biodiversity effects with the additive partitioning scheme indicated positive complementarity effects that were higher in light than in shade. Selection effects did not deviate from zero, irrespective of light levels. Vertical leaf distributions shifted apart in mixed stands as consequence of competition-driven phenotypic plasticity, promoting realized complementarity. Structural equation models showed that this effect was larger for species that differed more in growth strategies that were characterized by functional traits. In 13 of the 18 investigated two-species mixtures, both species benefitted relative to intraspecific competition in monoculture. In the remaining five pairwise mixtures, the relative yield gain of one species exceeded the relative yield loss of the other species, resulting in a relative yield total (RYT) exceeding 1. Overall, our analysis indicates that richness-productivity relationships are promoted by interspecific niche complementarity at early stages of stand development, and that this effect is enhanced by architectural plasticity.

Options of partners improve carbon for phosphorus trade in the arbuscular mycorrhizal mutualism.

The mutualism between plants and arbuscular mycorrhizal fungi (AMF) is widespread and has persisted for over 400 million years. Although this mutualism depends on fair resource exchange between plants and fungi, inequality exists among partners despite mechanisms that regulate trade. Here, we use (33) P and (14) C isotopes and a split-root system to test for preferential allocation and reciprocal rewards in the plant-AMF symbiosis by presenting a plant with two AMF that differ in cooperativeness. We found that plants received more (33) P from less cooperative AMF in the presence of another AMF species. This increase in (33) P resulted in a reduced (14) C cost per unit of (33) P from less cooperative AMF when alternative options were available. Our results indicate that AMF diversity promotes cooperation between plants and AMF, which may be an important mechanism maintaining the evolutionary persistence of and diversity within the plant-AMF mutualism.

Plant species diversity affects soil-atmosphere fluxes of methane and nitrous oxide.

Plant diversity effects on ecosystem functioning can potentially interact with global climate by altering fluxes of the radiatively active trace gases nitrous oxide (N2O) and methane (CH4). We studied the effects of grassland species richness (1-16) in combination with application of fertilizer (nitrogen:phosphorus:potassium = 100:43.6:83 kg ha(-1) a(-1)) on N2O and CH4 fluxes in a long-term field experiment. Soil N2O emissions, measured over 2 years using static chambers, decreased with species richness unless fertilizer was added. N2O emissions increased with fertilization and the fraction of legumes in plant communities. Soil CH4 uptake, a process driven by methanotrophic bacteria, decreased with plant species numbers, irrespective of fertilization. Using structural equation models, we related trace gas fluxes to soil moisture, soil inorganic N concentrations, nitrifying and denitrifying enzyme activity, and the abundance of ammonia oxidizers, nitrite oxidizers, and denitrifiers (quantified by real-time PCR of gene fragments amplified from microbial DNA in soil). These analyses indicated that plant species richness increased soil moisture, which in turn increased N cycling-related activities. Enhanced N cycling increased N2O emission and soil CH4 uptake, with the latter possibly caused by removal of inhibitory ammonium by nitrification. The moisture-related indirect effects were surpassed by direct, moisture-independent effects opposite in direction. Microbial gene abundances responded positively to fertilizer but not to plant species richness. The response patterns we found were statistically robust and highlight the potential of plant biodiversity to interact with climatic change through mechanisms unrelated to carbon storage and associated carbon dioxide removal.