Heat and desiccation tolerances predict bee abundance under climate change.

Climate change could pose an urgent threat to pollinators, with critical ecological and economic consequences. However, for most insect pollinator species, we lack the long-term data and mechanistic evidence that are necessary to identify climate-driven declines and predict future trends. Here we document 16 years of abundance patterns for a hyper-diverse bee assemblage1 in a warming and drying region2, link bee declines with experimentally determined heat and desiccation tolerances, and use climate sensitivity models to project bee communities into the future. Aridity strongly predicted bee abundance for 71% of 665 bee populations (species × ecosystem combinations). Bee taxa that best tolerated heat and desiccation increased the most over time. Models forecasted declines for 46% of species and predicted more homogeneous communities dominated by drought-tolerant taxa, even while total bee abundance may remain unchanged. Such community reordering could reduce pollination services, because diverse bee assemblages typically maximize pollination for plant communities3. Larger-bodied bees also dominated under intermediate to high aridity, identifying body size as a valuable trait for understanding how climate-driven shifts in bee communities influence pollination4. We provide evidence that climate change directly threatens bee diversity, indicating that bee conservation efforts should account for the stress of aridity on bee physiology.

Dryland sensitivity to climate change and variability using nonlinear dynamics.

Primary productivity response to climatic drivers varies temporally, indicating state-dependent interactions between climate and productivity. Previous studies primarily employed equation-based approaches to clarify this relationship, ignoring the state-dependent nature of ecological dynamics. Here, using 40 y of climate and productivity data from 48 grassland sites across Mongolia, we applied an equation-free, nonlinear time-series analysis to reveal sensitivity patterns of productivity to climate change and variability and clarify underlying mechanisms. We showed that productivity responded positively to annual precipitation in mesic regions but negatively in arid regions, with the opposite pattern observed for annual mean temperature. Furthermore, productivity responded negatively to decreasing annual aridity that integrated precipitation and temperature across Mongolia. Productivity responded negatively to interannual variability in precipitation and aridity in mesic regions but positively in arid regions. Overall, interannual temperature variability enhanced productivity. These response patterns are largely unrecognized; however, two mechanisms are inferable. First, time-delayed climate effects modify annual productivity responses to annual climate conditions. Notably, our results suggest that the sensitivity of annual productivity to increasing annual precipitation and decreasing annual aridity can even be negative when the negative time-delayed effects of annual precipitation and aridity on productivity prevail across time. Second, the proportion of plant species resistant to water and temperature stresses at a site determines the sensitivity of productivity to climate variability. Thus, we highlight the importance of nonlinear, state-dependent sensitivity of productivity to climate change and variability, accurately forecasting potential biosphere feedback to the climate system.

Microbial symbionts buffer hosts from the demographic costs of environmental stochasticity.

Species' persistence in increasingly variable climates will depend on resilience against the fitness costs of environmental stochasticity. Most organisms host microbiota that shield against stressors. Here, we test the hypothesis that, by limiting exposure to temporally variable stressors, microbial symbionts reduce hosts' demographic variance. We parameterized stochastic population models using data from a 14-year symbiont-removal experiment including seven grass species that host Epichloë fungal endophytes. Results provide novel evidence that symbiotic benefits arise not only through improved mean fitness, but also through dampened inter-annual variance. Hosts with "fast" life-history traits benefited most from symbiont-mediated demographic buffering. Under current climate conditions, contributions of demographic buffering were modest compared to benefits to mean fitness. However, simulations of increased stochasticity amplified benefits of demographic buffering and made it the more important pathway of host-symbiont mutualism. Microbial-mediated variance buffering is likely an important, yet cryptic, mechanism of resilience in an increasingly variable world.

Plant-soil microbe feedbacks depend on distance and ploidy in a mixed cytotype population of Larrea tridentata.

PREMISE: Theory predicts that mixed ploidy populations should be short-lived due to strong fitness disadvantages for the rare ploidy. However, mixed ploidy populations are common, suggesting that the fitness costs for rare ploidies are counterbalanced by ecological benefits that emerge when rare. We investigated whether differences in ecological interactions with soil microbes help to maintain a tetraploid-hexaploid population of Larrea tridentata (creosote bush) in the Sonoran Desert, California, United States, where prior work documented ploidy-specific root-associated microbes. METHODS: We used a plant-soil feedback (PSF) experiment to test whether host-specific soil microbes can alter the outcomes of intraploidy vs. interploidy competition. Host-specific soil microbes can build up over time; thus, distance from a host plant can affect the fitness of nearby plants. RESULTS: Seedlings grown in soils from near plants of a different ploidy produced greater biomass relative to seedlings grown in soils from near plants of the same ploidy. Moreover, seedlings grown in soils from near plants of a different ploidy produced more biomass than those grown in soils that were farther from plants of a different ploidy. These results suggest that the ecological consequences of PSF may facilitate the persistence of mixed ploidy populations. CONCLUSIONS: This is the first evidence, to our knowledge, that is consistent with plant-soil microbe feedback as a viable mechanism to maintain the coexistence of multiple ploidy levels in a single population.

Nitrogen addition and fungal symbiosis alter early dune plant succession.

Anthropogenic nitrogen (N) enrichment can have complex effects on plant communities. In low-nutrient, primary successional systems such as sand dunes, N enrichment may alter the trajectory of plant community assembly or the dominance of foundational, ecosystem-engineering plants. Predicting the consequences of N enrichment may be complicated by plant interactions with microbial symbionts because increases in a limiting resource, such as N, could alter the costs and benefits of symbiosis. To evaluate the direct and interactive effects of microbial symbiosis and N addition on plant succession, we established a long-term field experiment in Michigan, USA, manipulating the presence of the symbiotic fungal endophyte Epichloë amarillans in Ammophila breviligulata, a dominant ecosystem-engineering dune grass species. From 2016 to 2020, we implemented N fertilization treatments (control, low, high) in a subset of the long-term experiment. N addition suppressed the accumulation of plant diversity over time mainly by reducing species richness of colonizing plants. However, this suppression occurred only when the endophyte was present in Ammophila. Although Epichloë enhanced Ammophila tiller density over time, N addition did not strongly interact with Epichloë symbiosis to influence vegetative growth of Ammophila. Instead, N addition directly altered plant community composition by increasing the abundance of efficient colonizers, especially C4 grasses. In conclusion, hidden microbial symbionts can alter the consequences of N enrichment on plant primary succession.

Soil nematode assemblages respond to interacting environmental changes.

Multi-factor experiments suggest that interactions among environmental changes commonly influence biodiversity and community composition. However, most field experiments manipulate only single factors. Soil food webs are critical to ecosystem health and may be particularly sensitive to interactions among environmental changes that include soil warming, eutrophication, and altered precipitation. Here, we asked how environmental changes interacted to alter soil nematode communities in a northern Chihuahuan Desert grassland. Factorial manipulations of nitrogen, winter rainfall, and nighttime warming matched predictions for regional environmental change. Warming reduced nematode diversity by 25% and genus-level richness by 32%, but declines dissipated with additional winter rain, suggesting that warming effects occurred via drying. Interactions between precipitation and nitrogen also altered nematode community composition, but only weakly affected total nematode abundance, indicating that most change involved reordering of species abundances. Specifically, under ambient precipitation, nitrogen fertilizer reduced bacterivores by 68% and herbivores by 73%, but did not affect fungivores. In contrast, under winter rain addition, nitrogen fertilization increased bacterivores by 95%, did not affect herbivores, and doubled fungivore abundance. Rain can reduce soil nitrogen availability and increase turnover in the microbial loop, potentially promoting the recovery of nematode populations overwhelmed by nitrogen eutrophication. Nematode communities were not tightly coupled to plant community composition and may instead track microbes, including biocrusts or decomposers. Our results highlight the importance of interactions among environmental change stressors for shaping the composition and function of soil food webs in drylands.

Cross-Site Comparisons of Dryland Ecosystem Response to Climate Change in the US Long-Term Ecological Research Network.

Long-term observations and experiments in diverse drylands reveal how ecosystems and services are responding to climate change. To develop generalities about climate change impacts at dryland sites, we compared broadscale patterns in climate and synthesized primary production responses among the eight terrestrial, nonforested sites of the United States Long-Term Ecological Research (US LTER) Network located in temperate (Southwest and Midwest) and polar (Arctic and Antarctic) regions. All sites experienced warming in recent decades, whereas drought varied regionally with multidecadal phases. Multiple years of wet or dry conditions had larger effects than single years on primary production. Droughts, floods, and wildfires altered resource availability and restructured plant communities, with greater impacts on primary production than warming alone. During severe regional droughts, air pollution from wildfire and dust events peaked. Studies at US LTER drylands over more than 40 years demonstrate reciprocal links and feedbacks among dryland ecosystems, climate-driven disturbance events, and climate change.

Mammalian herbivores restrict the altitudinal range limits of alpine plants.

Although rarely experimentally tested, biotic interactions have long been hypothesised to limit low-elevation range boundaries of species. We tested the effects of herbivory on three alpine-restricted plant species by transplanting plants below (novel), at the edge (limit), or in the centre (core) of their current elevational range and factorially fencing-out above- and belowground mammals. Herbivore damage was greater in range limit and novel habitats than in range cores. Exclosures increased plant biomass and reproduction more in novel habitats than in range cores, suggesting demographic costs of novel interactions with herbivores. We then used demographic models to project population growth rates, which increased 5-20% more under herbivore exclosure at range limit and novel sites than in core habitats. Our results identify mammalian herbivores as key drivers of the low-elevation range limits of alpine plants and indicate that upward encroachment of herbivores could trigger local extinctions by depressing plant population growth.

Divergent responses of primary production to increasing precipitation variability in global drylands.

Interannual variability in precipitation has increased globally as climate warming intensifies. The increased variability impacts both terrestrial plant production and carbon (C) sequestration. However, mechanisms driving these changes are largely unknown. Here, we examined mechanisms underlying the response of aboveground net primary production (ANPP) to interannual precipitation variability in global drylands with mean annual precipitation (MAP) <500 mm year-1 , using a combined approach of data synthesis and process-based modeling. We found a hump-shaped response of ANPP to precipitation variability along the MAP gradient. The response was positive when MAP < ~300 mm year-1 and negative when MAP was higher than this threshold, with a positive peak at 140 mm year-1 . Transpiration and subsoil water content mirrored the response of ANPP to precipitation variability; evaporation responded negatively and water loss through runoff and drainage responded positively to precipitation variability. Mean annual temperature, soil type, and plant physiological traits all altered the magnitude but not the pattern of the response of ANPP to precipitation variability along the MAP gradient. By extrapolating to global drylands (<500 mm year-1  MAP), we estimated that ANPP would increase by 15.2 ± 6.0 Tg C year-1 in arid and hyper-arid lands and decrease by 2.1 ± 0.5 Tg C year-1 in dry sub-humid lands under future changes in interannual precipitation variability. Thus, increases in precipitation variability will enhance primary production in many drylands in the future.

Declines in rodent abundance and diversity track regional climate variability in North American drylands.

Regional long-term monitoring can enhance the detection of biodiversity declines associated with climate change, improving future projections by reducing reliance on space-for-time substitution and increasing scalability. Rodents are diverse and important consumers in drylands, regions defined by the scarcity of water that cover 45% of Earth's land surface and face increasingly drier and more variable climates. We analyzed abundance data for 22 rodent species across grassland, shrubland, ecotone, and woodland ecosystems in the southwestern USA. Two time series (1995-2006 and 2004-2013) coincided with phases of the Pacific Decadal Oscillation (PDO), which influences drought in southwestern North America. Regionally, rodent species diversity declined 20%-35%, with greater losses during the later time period. Abundance also declined regionally, but only during 2004-2013, with losses of 5% of animals captured. During the first time series (wetter climate), plant productivity outranked climate variables as the best regional predictor of rodent abundance for 70% of taxa, whereas during the second period (drier climate), climate best explained variation in abundance for 60% of taxa. Temporal dynamics in diversity and abundance differed spatially among ecosystems, with the largest declines in woodlands and shrublands of central New Mexico and Colorado. Which species were winners or losers under increasing drought and amplified interannual variability in drought depended on ecosystem type and the phase of the PDO. Fewer taxa were significant winners (18%) than losers (30%) under drought, but the identities of winners and losers differed among ecosystems for 70% of taxa. Our results suggest that the sensitivities of rodent species to climate contributed to regional declines in diversity and abundance during 1995-2013. Whether these changes portend future declines in drought-sensitive consumers in the southwestern USA will depend on the climate during the next major PDO cycle.

Improving Instructional Fitness Requires Change.

Transmission of information has benefitted from a breathtaking level of innovation and change over the past 20 years; however, instructional methods within colleges and universities have been slow to change. In the article, we present a novel framework to structure conversations that encourage innovation, change, and improvement in our system of higher education, in general, and our system of biology education, specifically. In particular, we propose that a conceptual model based on evolutionary landscapes in which fitness is replaced by educational effectiveness would encourage educational improvement by helping to visualize the multidimensional nature of education and learning, acknowledge the complexity and dynamism of the educational landscape, encourage collaboration, and stimulate experimental thinking about how new approaches and methodology could take various fields associated with learning, to more universal fitness optima. The framework also would encourage development and implementation of new techniques and persistence through less efficient or effective valleys of death.

Simulated folivory increases vertical transmission of fungal endophytes that deter herbivores and alter tolerance to herbivory in Poa autumnalis.

BACKGROUND AND AIMS: The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission? METHODS: We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission. KEY RESULTS: Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission. CONCLUSIONS: Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.

Correction to: Soil microbes that may accompany climate warming increase alpine plant production.

The DOI link to the data in the Acknowledgments section of the article was incorrect. The proper link to the data is.

Testing for loss of Epichloë and non-epichloid symbionts under altered rainfall regimes.

PREMISE: Microbial symbionts can buffer plant hosts from environmental change. Therefore, understanding how global change factors alter the associations between hosts and their microbial symbionts may improve predictions of future changes in host population dynamics and microbial diversity. Here, we investigated how one global change factor, precipitation, affected the maintenance or loss of symbiotic fungal endophytes in a C3 grass host. Specifically, we examined the distinct responses of Epichloë (vertically transmitted and systemic) and non-epichloid endophytes (typically horizontally transmitted and localized) by considering (1) how precipitation altered associations with Epichloë and non-epichloid endophytic taxa across host ontogeny, and (2) interactive effects of water availability and Epichloë on early seedling life history stages. METHODS: We manipulated the presence of Epichloë amarillans in American beachgrass (Ammophila breviligulata) in a multiyear field experiment that imposed three precipitation regimes (ambient or ±30% rainfall). In laboratory assays, we investigated the interactive effects of water availability and Epichloë on seed viability and germination. RESULTS: Reduced precipitation decreased the incidence of Epichloë in leaves in the final sampling period, but had no effect on associations with non-epichloid taxa. Epichloë reduced the incidence of non-epichloid endophytes, including systemic p-endophytes, in seeds. Laboratory assays suggested that association with Epichloë is likely maintained, in part, due to increased seed viability and germination regardless of water availability. CONCLUSIONS: Our study empirically demonstrates several pathways for plant symbionts to be lost or maintained across host ontogeny and suggests that reductions in precipitation can drive the loss of a plant's microbial symbionts.

Divergence in Diversity and Composition of Root-Associated Fungi Between Greenhouse and Field Studies in a Semiarid Grassland.

Investigations of plant-soil feedbacks (PSF) and plant-microbe interactions often rely exclusively on greenhouse experiments, yet we have little understanding of how, and when, results can be extrapolated to explain phenomena in nature. A systematic comparison of microbial communities using the same host species across study environments can inform the generalizability of such experiments. We used Illumina MiSeq sequencing to characterize the root-associated fungi of two foundation grasses from a greenhouse PSF experiment, a field PSF experiment, field monoculture stands, and naturally occurring resident plants in the field. A core community consisting < 10% of total fungal OTU richness but > 50% of total sequence abundance occurred in plants from all study types, demonstrating the ability of field and greenhouse experiments to capture the dominant component of natural communities. Fungal communities were plant species-specific across the study types, with the core community showing stronger host specificity than peripheral taxa. Roots from the greenhouse and field PSF experiments had lower among sample variability in community composition and higher diversity than those from naturally occurring, or planted monoculture plants from the field. Core and total fungal composition differed substantially across study types, and dissimilarity between fungal communities did not predict plant-soil feedbacks measured in experiments. These results suggest that rhizobiome assembly mechanisms in nature differ from the dynamics of short-term, inoculation studies. Our results validate the efficacy of common PSF experiment designs to test soil inoculum effects, and highlight the challenges of scaling the underlying microbial mechanisms of plant responses from whole-community inoculation experiments to natural ecosystems.

Plant Identity Influences Foliar Fungal Symbionts More Than Elevation in the Colorado Rocky Mountains.

Despite colonizing nearly every plant on Earth, foliar fungal symbionts have received little attention in studies on the biogeography of host-associated microbes. Evidence from regional scale studies suggests that foliar fungal symbiont distributions are influenced both by plant hosts and environmental variation in climate and soil resources. However, previous surveys have focused on either one plant host across an environmental gradient or one gradient and multiple plant hosts, making it difficult to disentangle the influence of host identity from the influence of the environment on foliar endophyte communities. We used a culture-based approach to survey fungal symbiont composition in the leaves of nine C3 grass species along replicated elevation gradients in grasslands of the Colorado Rocky Mountains. In these ecosystems, the taxonomic richness and composition of foliar fungal symbionts were mostly structured by the taxonomic identity of the plant host rather than by variation in climate. Plant traits related to size (height and leaf length) were the best predictors of foliar fungal symbiont composition and diversity, and composition did not vary predictably with plant evolutionary history. The largest plants had the most diverse and distinctive fungal communities. These results suggest that across the ~ 300 m elevation range that we sampled, foliar fungal symbionts may indirectly experience climate change by tracking the shifting distributions of plant hosts rather than tracking climate directly.

Soil microbes that may accompany climate warming increase alpine plant production.

Climate change is causing species with non-overlapping ranges to come in contact, and a key challenge is to predict the consequences of such species re-shuffling. Experiments on plants have focused largely on novel competitive interactions; other species interactions, such as plant-microbe symbioses, while less studied, may also influence plant responses to climate change. In this greenhouse study, we evaluated interactions between soil microbes and alpine-restricted plant species, simulating a warming scenario in which low-elevation microbes migrate upslope into the distribution of alpine plants. We examined three alpine grasses from the Rocky Mountains, CO, USA (Poa alpina, Festuca brachyphylla, and Elymus scribneri). We used soil inocula from within (resident) or below (novel) the plants' current elevation range and examined responses in plant biomass, plant traits, and fungal colonization of roots. Resident soil inocula from the species' home range decreased biomass to a greater extent than novel soil inocula. The depressed growth in resident soils suggested that these soils harbor more carbon-demanding microbes, as plant biomass generally declined with greater fungal colonization of roots, especially in resident soil inocula. Although plant traits did not respond to the provenance of soil inocula, specific leaf area declined and root:shoot ratio increased when soil inocula were sterilized, indicating microbial mediation of plant trait expression. Contrary to current predictions, our findings suggest that if upwardly migrating microbes were to displace current soil microbes, alpine plants may benefit from this warming-induced microbial re-shuffling.

Experimental drought reduces genetic diversity in the grassland foundation species Bouteloua eriopoda.

Understanding the resistance and resilience of foundation plant species to climate change is a critical issue because the loss of these species would fundamentally reshape communities and ecosystem processes. High levels of population genetic diversity may buffer foundation species against climate disruptions, but the strong selective pressures associated with climatic shifts may also rapidly reduce such diversity. We characterized genetic diversity and its responsiveness to experimental drought in the foundation plant, black grama grass (Bouteloua eriopoda), which dominates many western North American grasslands and shrublands. Previous studies suggested that in arid ecosystems, black grama reproduces largely asexually via stolons, and thus is likely to have low genetic variability, which might limit its potential to respond to climate disruptions. Using genotyping-by-sequencing, we demonstrated unexpectedly high genetic variability among black grama plants in a 1 ha site within the Sevilleta National Wildlife Refuge in central New Mexico, suggesting some level of sexual reproduction. Three years of experimental, growing season drought reduced black grama survival and biomass (the latter by 96%), with clear genetic differentiation (higher FST) between plants succumbing to drought and those remaining alive. Reduced genetic variability in the surviving plants in drought plots indicated that the experimental drought had forced black grama populations through selection bottlenecks. These results suggest that foundation grass species, such as black grama, may experience rapid evolutionary change if future climates include more severe droughts.

Testing the roles of vertical transmission and drought stress in the prevalence of heritable fungal endophytes in annual grass populations.

Beneficial inherited symbionts are expected to reach high prevalence in host populations, yet many are observed at intermediate prevalence. Theory predicts that a balance of fitness benefits and efficiency of vertical transmission may interact to stabilize intermediate prevalence. We established populations of grass hosts (Lolium multiflorum) that varied in prevalence of a heritable fungal endophyte (Epichloё occultans), allowing us to infer long-term equilibria by tracking change in prevalence over one generation. We manipulated an environmental stressor (elevated precipitation), which we hypothesized would reduce the fitness benefits of symbiosis, and altered the efficiency of vertical transmission by replacing endophyte-positive seeds with endophyte-free seeds. Endophytes and elevated precipitation both increased host fitness, but symbiont effects were not stronger in the drier treatment, suggesting that benefits of symbiosis were unrelated to drought tolerance. Reduced transmission suppressed the inferred equilibrium prevalence from 42.6% to 11.7%. However, elevated precipitation did not modify prevalence, consistent with the result that it did not modify fitness benefits. Our results demonstrate that failed transmission can influence the prevalence of heritable microbes and that intermediate prevalence can be a stable equilibrium due to forces that allow symbionts to increase (fitness benefits) but prevent them from reaching fixation (failed transmission).

Climate sensitivity functions and net primary production: A framework for incorporating climate mean and variability.

Understanding controls on net primary production (NPP) has been a long-standing goal in ecology. Climate is a well-known control on NPP, although the temporal differences among years within a site are often weaker than the spatial pattern of differences across sites. Climate sensitivity functions describe the relationship between an ecological response (e.g., NPP) and both the mean and variance of its climate driver (e.g., aridity index), providing a novel framework for understanding how climate trends in both mean and variance vary with NPP over time. Nonlinearities in these functions predict whether an increase in climate variance will have a positive effect (convex nonlinearity) or negative effect (concave nonlinearity) on NPP. The influence of climate variance may be particularly intense at ecosystem transition zones, if species reach physiological thresholds that create nonlinearities at these ecotones. Long-term data collected at the confluence of three dryland ecosystems in central New Mexico revealed that each ecosystem exhibited a unique climate sensitivity function that was consistent with long-term vegetation change occurring at their ecotones. Our analysis suggests that rising temperatures in drylands could alter the nonlinearities that determine the relative costs and benefits of variance in precipitation for primary production.