Impact of changing climate on bryophyte contributions to terrestrial water, carbon, and nitrogen cycles.

Bryophytes, including the lineages of mosses, liverworts, and hornworts, are the second-largest photoautotroph group on Earth. Recent work across terrestrial ecosystems has highlighted how bryophytes retain and control water, fix substantial amounts of carbon (C), and contribute to nitrogen (N) cycles in forests (boreal, temperate, and tropical), tundra, peatlands, grasslands, and deserts. Understanding how changing climate affects bryophyte contributions to global cycles in different ecosystems is of primary importance. However, because of their small physical size, bryophytes have been largely ignored in research on water, C, and N cycles at global scales. Here, we review the literature on how bryophytes influence global biogeochemical cycles, and we highlight that while some aspects of global change represent critical tipping points for survival, bryophytes may also buffer many ecosystems from change due to their capacity for water, C, and N uptake and storage. However, as the thresholds of resistance of bryophytes to temperature and precipitation regime changes are mostly unknown, it is challenging to predict how long this buffering capacity will remain functional. Furthermore, as ecosystems shift their global distribution in response to changing climate, the size of different bryophyte-influenced biomes will change, resulting in shifts in the magnitude of bryophyte impacts on global ecosystem functions.

Moss functional trait ecology: Trends, gaps, and biases in the current literature.

Functional traits are critical tools in plant ecology for capturing organism-environment interactions based on trade-offs and making links between organismal and ecosystem processes. While broad frameworks for functional traits have been developed for vascular plants, we lack the same for bryophytes, despite an escalation in the number of studies on bryophyte functional trait in the last 45 years and an increased recognition of the ecological roles bryophytes play across ecosystems. In this review, we compiled data from 282 published articles (10,005 records) that focused on functional traits measured in mosses and sought to examine trends in types of traits measured, capture taxonomic and geographic breadth of trait coverage, reveal biases in coverage in the current literature, and develop a bryophyte-function index (BFI) to describe the completeness of current trait coverage and identify global gaps to focus research efforts. The most commonly measured response traits (those related to growth/reproduction in individual organisms) and effect traits (those that directly affect community/ecosystem scale processes) fell into the categories of morphology (e.g., leaf area, shoot height) and nutrient storage/cycling, and our BFI revealed that these data were most commonly collected from temperate and boreal regions of Europe, North America, and East Asia. However, fewer than 10% of known moss species have available functional trait information. Our synthesis revealed a need for research on traits related to ontogeny, sex, and intraspecific plasticity and on co-measurement of traits related to water relations and bryophyte-mediated soil processes.

Responses of Biocrust and Associated Soil Bacteria to Novel Climates Are Not Tightly Coupled.

Climate change is expanding drylands even as land use practices degrade them. Representing ∼40% of Earth's terrestrial surface, drylands rely on biological soil crusts (biocrusts) for key ecosystem functions including soil stability, biogeochemical cycling, and water capture. Understanding how biocrusts adapt to climate change is critical to understanding how dryland ecosystems will function with altered climate. We investigated the sensitivity of biocrusts to experimentally imposed novel climates to track changes in productivity and stability under both warming and cooling scenarios. We established three common gardens along an elevational-climate gradient on the Colorado Plateau. Mature biocrusts were collected from each site and reciprocally transplanted intact. Over 20 months we monitored visible species composition and cover, chlorophyll a, and the composition of soil bacterial communities using high throughput sequencing. We hypothesized that biocrusts replanted at their home site would show local preference, and biocrusts transplanted to novel environments would maintain higher cover and stability at elevations higher than their origin, compared to at elevations lower than their origin. We expected responses of the visible biocrust cover and soil bacterial components of the biocrust community to be coupled, with later successional taxa showing higher sensitivity to novel environments. Only high elevation sourced biocrusts maintained higher biocrust cover and community stability at their site of origin. Biocrusts from all sources had higher cover and stability in the high elevation garden. Later successional taxa decreased cover in low elevation gardens, suggesting successional reversal with warming. Visible community composition was influenced by both source and transplant environment. In contrast, soil bacterial community composition was not influenced by transplant environments but retained fidelity to the source. Thus, responses of the visible and soil bacterial components of the biocrust community were not coupled. Synthesis: Our results suggest biocrust communities are sensitive to climate change, and loss of species and function can be expected, while associated soil bacteria may be buffered against rapid change.

Strategies of desiccation tolerance vary across life phases in the moss Syntrichia caninervis.

PREMISE: Desiccation tolerance (DT) is a widespread phenomenon among land plants, and variable ecological strategies for DT are likely to exist. Using Syntrichia caninervis, a dryland moss and model system used in DT studies, we hypothesized that DT is lowest in juvenile (protonemal) tissues, highest in asexual reproductive propagules (gemmae), and intermediate in adults (shoots). We tested the long-standing hypothesis of an inherent constitutive strategy of DT in this species. METHODS: Plants were rapidly dried to levels of equilibrating relative humidity (RHeq) ranging from 0 to 93%. Postrehydration recovery was assessed using chlorophyll fluorescence, regeneration rates, and visual tissue damage. For each life phase, we estimated the minimum rate of drying (RoDmin ) at RHeq = 42% that did not elicit damage 24 h postrehydration. RESULTS: DT strategy varied with life phase, with adult shoots having the lowest RoDmin (10-25 min), followed by gemmae (3-10 h) and protonema (14-20 h). Adult shoots exhibited no detectable damage 24 h postrehydration following a rapid-dry only at the highest RHeq used (93%), but when dried to lower RHs the response declined to <50% of control fluorescence values. Notably, immediately following rehydration (0 h postrehydration), shoots were damaged below control levels of fluorescence regardless of the RHeq, thus implicating damage. CONCLUSIONS: Life phases of the moss S. caninervis had a range of strategies from near constitutive (adult shoots) to demonstrably inducible (protonema). A new response variable for assessing degree of DT is introduced as the minimum rate of drying from which full recovery occurs.

To dry perchance to live: Insights from the genome of the desiccation-tolerant biocrust moss Syntrichia caninervis.

With global climate change, water scarcity threatens whole agro/ecosystems. The desert moss Syntrichia caninervis, an extremophile, offers novel insights into surviving desiccation and heat. The sequenced S. caninervis genome consists of 13 chromosomes containing 16 545 protein-coding genes and 2666 unplaced scaffolds. Syntenic relationships within the S. caninervis and Physcomitrella patens genomes indicate the S. caninervis genome has undergone a single whole genome duplication event (compared to two for P. patens) and evidence suggests chromosomal or segmental losses in the evolutionary history of S. caninervis. The genome contains a large sex chromosome composed primarily of repetitive sequences with a large number of Copia and Gypsy elements. Orthogroup analyses revealed an expansion of ELIP genes encoding proteins important in photoprotection. The transcriptomic response to desiccation identified four structural clusters of novel genes. The genomic resources established for this extremophile offer new perspectives for understanding the evolution of desiccation tolerance in plants.

Morphological and physiological traits in relation to carbon balance in a diverse clade of dryland mosses.

Plant functional trait analyses have focused almost exclusively on vascular plants, but bryophytes comprise ancient and diverse plant lineages that have widespread global distributions and important ecological functions in terrestrial ecosystems. We examined a diverse clade of dryland mosses, Syntrichia, and studied carbon balance during a precipitation event (C-balance), a functional trait related to physiological functioning, desiccation tolerance, survival, and ecosystem carbon and nitrogen cycling. We examined variability in C-balance among 14 genotypes of Syntrichia and measured an additional 10 physiological and 13 morphological traits at the cell, leaf, shoot, and clump level. C-balance varied 20-fold among genotypes, and highest C-balances were associated with long, narrow leaves with awns, and small cells with thick cell walls, traits that may influence water uptake and retention during a precipitation event. Ordination analyses revealed that the axis most strongly correlated with C-balance included the maximum chlorophyll fluorescence, Fm , indicating the importance of photosystem II health for C exchange. C-balance represents a key functional trait in bryophytes, but its measurement is time intensive and not feasible to measure on large scales. We propose two models (using physiological and morphological traits) to predict C-balance, whereby identifying simpler to measure traits for trait databases.

Student Performance along Axes of Scenario Novelty and Complexity in Introductory Biology: Lessons from a Unique Factorial Approach to Assessment.

In an undergraduate introductory biology laboratory course, we used a summative assessment to directly test the learning objective that students will be able to apply course material to increasingly novel and complex situations. Using a factorial framework, we developed multiple true-false questions to fall along axes of novelty and complexity, which resulted in four categories of questions: familiar content and low complexity (category A); novel content and low complexity (category B); familiar content and high complexity (category C); and novel content and high complexity (category D). On average, students scored more than 70% on all questions, indicating that the course largely met this learning objective. However, students scored highest on questions in category A, likely because they were most similar to course content, and lowest on questions in categories C and D. While we anticipated students would score equally on questions for which either novelty or complexity was altered (but not both), we observed that student scores in category C were lower than in category B. Furthermore, students performed equally poorly on all questions for which complexity was higher (categories C and D), even those containing familiar content, suggesting that application of course material to increasingly complex situations is particularly challenging to students.

Physiology-based prognostic modeling of the influence of changes in precipitation on a keystone dryland plant species.

Fluctuations in mean annual precipitation (MAP) will strongly influence the ecology of dryland ecosystems in the future, yet, because individual precipitation events drive growth and resource availability for many dryland organisms, changes in intra-annual precipitation may disproportionately influence future dryland processes. This work examines the hypothesis that intra-annual precipitation changes will drive dryland productivity to a greater extent than changes to MAP. To test this hypothesis, we created a physiology-based model to predict the effects of precipitation change on a widespread biocrust moss that regulates soil structure, water retention, and nutrient cycling in drylands. First, we used the model to examine moss productivity over the next 100 years driven by alterations in MAP by ± 10, 20 and 30%, and changes in intra-annual precipitation (event size and frequency). Productivity increased as a function of MAP, but differed among simulations where intra-annual precipitation was manipulated under constant MAP. Supporting our hypothesis, this demonstrates that, even if MAP does not change, changes in the features of individual precipitation events can strongly influence long-term performance. Second, we used the model to examine 100-year productivity based on projected dryland precipitation from published global and regional models. These simulations predicted 25-63% reductions in productivity and increased moss mortality rates, declines that will likely alter water and nutrient cycling in dryland ecosystems. Intra-annual precipitation in model-based simulations was a stronger predictor of productivity compared to MAP, further supporting our hypothesis, and illustrating that intra-annual precipitation patterns may dominate dryland responses to altered precipitation in a future climate.

Precipitation-driven carbon balance controls survivorship of desert biocrust mosses.

Precipitation patterns including the magnitude, timing, and seasonality of rainfall are predicted to undergo substantial alterations in arid regions in the future, and desert organisms may be more responsive to such changes than to shifts in only mean annual rainfall. Soil biocrust communities (consisting of cyanobacteria, lichen, and mosses) are ubiquitous to desert ecosystems, play an array of ecological roles, and display a strong sensitivity to environmental changes. Crust mosses are particularly responsive to changes in precipitation and exhibit rapid declines in biomass and mortality following the addition of small rainfall events. Further, loss of the moss component in biocrusts leads to declines in crust structure and function. In this study, we sought to understand the physiological responses of the widespread and often dominant biocrust moss Syntrichia caninervis to alterations in rainfall. Moss samples were collected during all four seasons and exposed to two rainfall event sizes and three desiccation period (DP) lengths. A carbon balance approach based on single precipitation events was used to define the carbon gain or loss during a particular hydration period. Rainfall event size was the strongest predictor of carbon balance, and the largest carbon gains were associated with the largest precipitation events. In contrast, small precipitation events resulted in carbon deficits for S. caninervis. Increasing the length of the DP prior to an event resulted in reductions in carbon balance, probably because of the increased energetic cost of hydration following more intense bouts of desiccation. The season of collection (i.e., physiological status of the moss) modulated these responses, and the effects of DP and rainfall on carbon balance were different in magnitude (and often in sign) for different seasons. In particular, S. caninervis displayed higher carbon balances in the winter than in the summer, even for events of identical size. Overall, our results suggest that annual carbon balance and survivorship in biocrust mosses are largely driven by precipitation, and because of the role mosses play in biocrusts, changes in intra-annual precipitation patterns can have implications for hydrology, soil stability, and nutrient cycling in dryland systems.

Physiological ecology of desert biocrust moss following 10 years exposure to elevated CO2: evidence for enhanced photosynthetic thermotolerance.

In arid regions, biomes particularly responsive to climate change, mosses play an important biogeochemical role as key components of biocrusts. Using the biocrust moss Syntrichia caninervis collected from the Nevada Desert Free Air CO2 Enrichment Facility, we examined the physiological effects of 10 years of exposure to elevated CO2, and the effect of high temperature events on the photosynthetic performance of moss grown in CO2-enriched air. Moss exposed to elevated CO2 exhibited a 46% decrease in chlorophyll, a 20% increase in carbon and no difference in either nitrogen content or photosynthetic performance. However, when subjected to high temperatures (35-40°C), mosses from the elevated CO2 environment showed higher photosynthetic performance and photosystem II (PSII) efficiency compared to those grown in ambient conditions, potentially reflective of a shift in nitrogen allocation to components that offer a higher resistance of PSII to heat stress. This result suggests that mosses may respond to climate change in markedly different ways than vascular plants, and observed CO2-induced photosynthetic thermotolerance in S. caninervis will likely have consequences for future desert biogeochemistry.