Biodiversity in changing environments: An external-driver internal-topology framework to guide intervention.

Accompanying the climate crisis is the more enigmatic biodiversity crisis. Rapid reorganization of biodiversity due to global environmental change has defied prediction and tested the basic tenets of conservation and restoration. Conceptual and practical innovation is needed to support decision making in the face of these unprecedented shifts. Critical questions include: How can we generalize biodiversity change at the community level? When are systems able to reorganize and maintain integrity, and when does abiotic change result in collapse or restructuring? How does this understanding provide a template to guide when and how to intervene in conservation and restoration? To this end, we frame changes in community organization as the modulation of external abiotic drivers on the internal topology of species interactions, using plant-plant interactions in terrestrial communities as a starting point. We then explore how this framing can help translate available data on species abundance and trait distributions to corresponding decisions in management. Given the expectation that community response and reorganization are highly complex, the external-driver internal-topology (EDIT) framework offers a way to capture general patterns of biodiversity that can help guide resilience and adaptation in changing environments.

The soil microbiome affects patterns of local adaptation in an alpine plant under moisture stress.

PREMISE: The soil microbiome plays a role in plant trait expression and fitness, and plants may be locally adapted or maladapted to their soil microbiota. However, few studies of local adaptation in plants have incorporated a microbial treatment separate from manipulations of the abiotic environment, so our understanding of microbes in plant adaptation is limited. METHODS: Here we tested microbial effects on local adaptation in four paired populations of an abundant alpine plant from two community types, dry and moist meadow. In a 5-month greenhouse experiment, we manipulated source population, soil moisture, and soil microbiome and measured plant survival and biomass to assess treatment effects. RESULTS: Dry meadow populations had higher biomass than moist meadow populations at low moisture, demonstrating evidence of local adaptation to soil moisture in the absence of microbes. In the presence of microbes, dry meadow populations had greater survival than moist meadow populations when grown with dry meadow microbes regardless of moisture. Moist meadow populations showed no signs of adaptation or maladaptation. CONCLUSIONS: Our research highlights the importance of microbial mutualists in local adaptation, particularly in dry environments with higher abiotic stress. Plant populations from environments with greater abiotic stress exhibit different patterns of adaptation when grown with soil microbes versus without, while plant populations from less abiotically stressful environments do not. Improving our understanding of the role microbes play in plant adaptation will require further studies incorporating microbial manipulations.

Drivers of bacterial and fungal root endophyte communities: understanding the relative influence of host plant, environment, and space.

Bacterial and fungal root endophytes can impact the fitness of their host plants, but the relative importance of drivers for root endophyte communities is not well known. Host plant species, the composition and density of the surrounding plants, space, and abiotic drivers could significantly affect bacterial and fungal root endophyte communities. We investigated their influence in endophyte communities of alpine plants across a harsh high mountain landscape using high-throughput sequencing. There was less compositional overlap between fungal than bacterial root endophyte communities, with four 'cosmopolitan' bacterial OTUs found in every root sampled, but no fungal OTUs found across all samples. We found that host plant species, which included nine species from three families, explained the greatest variation in root endophyte composition for both bacterial and fungal communities. We detected similar levels of variation explained by plant neighborhood, space, and abiotic drivers on both communities, but the plant neighborhood explained less variation in fungal endophytes than expected. Overall, these findings suggest a more cosmopolitan distribution of bacterial OTUs compared to fungal OTUs, a structuring role of the plant host species for both communities, and largely similar effects of the plant neighborhood, abiotic drivers, and space on both communities.

Saltwater intrusion indirectly intensifies Phragmites australis invasion via alteration of soil microbes.

Although global change clearly influences species invasion, the exact mechanisms by which global change either intensifies or limits invasive spread remain elusive. Global change can affect invasion directly by altering abiotic conditions, as well as indirectly by altering the abundance and composition of interacting species. Here we examine the relative impacts of direct effects of saltwater intrusion and indirect effects via microbial interactions on the expansion of a model invasive plant species, Phragmites australis, in freshwater marshes of coastal Louisiana. Using a mesocosm experiment, we found that overall salinity strongly increases invasion, but the direction and magnitude of direct and indirect effects were context dependent. Indirect effects of salinity, via alterations in soil microbial composition, increased invasive performance when grown in monoculture and decreased native performance in native-only communities. However, when P. australis and natives were grown together, microbial indirect effects were not important; rather the salinity treatment increased P. australis invasion through reduction of native plant growth. Results suggest that salinity-induced alteration of soil microbes will increase susceptibility of native communities to invasion and promote P. australis monoculture expansion in later stages of invasion; whereas non-microbial effects of salinity are more important in early stages of invasion when P. australis is competing with native species. More broadly, these results underscore the importance of considering microbially-mediated indirect effects of global change in investigating the long-term outcomes of plant species interactions.

Does salinity affect lifestyle switching in the plant pathogen Fusarium solani?

Symbiotic microbes that live within plant hosts can exhibit a range in function from mutualistic to pathogenic, but the reason for this lifestyle switching remains largely unknown. Here we tested whether environmental stress, specifically salinity, is a factor that can trigger lifestyle switching in a fungus mainly known as a pathogen, Fusarium solani. F. solani was isolated from roots of Phragmites australis (common reed) in saline coastal marshes of Louisiana, USA, and we used Oryza sativa (rice) as a model organism from wetland environments to test the symbiont lifestyle. We plated rice seeds on control plates or plates with F. solani at three levels of salinity (0, 8 and 16 p.p.t.), then assessed germination and seedling growth after 20 days. Salinity strongly reduced percentage germination, slowed the timing of germination and reduced growth of rice. F. solani slowed germination, and it also caused a minor increase in root growth at medium salinity and a minor decrease in root growth at high salinity. Overall, despite being a common pathogen in other crop species (peas, beans, potatoes and many types of cucurbits), we found little evidence that F. solani has a strong pathogenic lifestyle in rice and we found weak evidence that pathogenicity may increase slightly with elevated salinity. These results have implications for both crops and native plant health in the future as soil salinization increases worldwide.

Soil Microbial Networks Shift Across a High-Elevation Successional Gradient.

While it is well established that microbial composition and diversity shift along environmental gradients, how interactions among microbes change is poorly understood. Here, we tested how community structure and species interactions among diverse groups of soil microbes (bacteria, fungi, non-fungal eukaryotes) change across a fundamental ecological gradient, succession. Our study system is a high-elevation alpine ecosystem that exhibits variability in successional stage due to topography and harsh environmental conditions. We used hierarchical Bayesian joint distribution modeling to remove the influence of environmental covariates on species distributions and generated interaction networks using the residual species-to-species variance-covariance matrix. We hypothesized that as ecological succession proceeds, diversity will increase, species composition will change, and soil microbial networks will become more complex. As expected, we found that diversity of most taxonomic groups increased over succession, and species composition changed considerably. Interestingly, and contrary to our hypothesis, interaction networks became less complex over succession (fewer interactions per taxon). Interactions between photosynthetic microbes and any other organism became less frequent over the gradient, whereas interactions between plants or soil microfauna and any other organism were more abundant in late succession. Results demonstrate that patterns in diversity and composition do not necessarily relate to patterns in network complexity and suggest that network analyses provide new insight into the ecology of highly diverse, microscopic communities.

Tradeoffs in demographic mechanisms underlie differences in species abundance and stability.

Understanding why some species are common and others are rare is a central question in ecology, and is critical for developing conservation strategies under global change. Rare species are typically considered to be more prone to extinction-but the fact they are rare can impede a general understanding of rarity vs. abundance. Here we develop and empirically test a framework to predict species abundances and stability using mechanisms governing population dynamics. Our results demonstrate that coexisting species with similar abundances can be shaped by different mechanisms (specifically, higher growth rates when rare vs. weaker negative density-dependence). Further, these dynamics influence population stability: species with higher intrinsic growth rates but stronger negative density-dependence were more stable and less sensitive to climate variability, regardless of abundance. This suggests that underlying mechanisms governing population dynamics, in addition to population size, may be critical indicators of population stability in an increasingly variable world.

Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem.

Despite decades of interest, few studies have provided evidence supporting theoretical expectations for coupled relationships between aboveground and belowground diversity and ecosystem functioning in non-manipulated natural ecosystems. We characterized plant species richness and density, soil bacterial, fungal and eukaryotic species richness and phylogenetic diversity (using 16S, ITS, and 18S gene sequencing), and ecosystem function (levels of soil C and N, and rates of microbial enzyme activities) along a natural gradient in plant richness and density in high-elevation, C-deficient soils to examine the coupling between above- and belowground systems. Overall, we observed a strong positive relationship between aboveground (plant richness and density) and belowground (bacteria, fungi, and non-fungal eukaryotes) richness. In addition to the correlations between plants and soil communities, C and N pools, and rates of enzyme activities increased as plant and soil communities became richer and more diverse. Our results suggest that the theoretically expected positive correlation between above- and belowground communities does exist in natural systems, but may be undetectable in late successional ecosystems due to the buildup of legacy organic matter that results in extremely complex belowground communities. In contrast, microbial communities in early successional systems, such as the system described here, are more directly dependent on contemporary inputs from plants and therefore are strongly correlated with plant diversity and density.

Teasing apart plant community responses to N enrichment: the roles of resource limitation, competition and soil microbes.

Although ecologists have documented the effects of nitrogen enrichment on productivity, diversity and species composition, we know little about the relative importance of the mechanisms driving these effects. We propose that distinct aspects of environmental change associated with N enrichment (resource limitation, asymmetric competition, and interactions with soil microbes) drive different aspects of plant response. We test this in greenhouse mesocosms, experimentally manipulating each factor across three ecosystems: tallgrass prairie, alpine tundra and desert grassland. We found that resource limitation controlled productivity responses to N enrichment in all systems. Asymmetric competition was responsible for diversity declines in two systems. Plant community composition was impacted by both asymmetric competition and altered soil microbes, with some contributions from resource limitation. Results suggest there may be generality in the mechanisms of plant community change with N enrichment. Understanding these links can help us better predict N response across a wide range of ecosystems.

Assembly of root-associated bacteria communities: interactions between abiotic and biotic factors.

Nitrogen (N) deposition in many areas of the world is over an order of magnitude greater than it would be in absence of human activity. We ask how abiotic (N)and biotic (plant host and neighborhood) effects interact to influence root-associated bacterial (RAB)community assembly. Using 454 pyrosequencing, we examined RAB communities from two dominantal pine tundra plants, Geum rossii and Deschampsia cespitosa, under control, N addition and D. cespitosa removal treatments, implemented in a factorial design. We hypothesized that host would have the strongest effect on RAB assembly, followed by N,then neighbor effects.The most dominant phyla were Proteobacteria (mostly Gammaproteobacteria), Actinobacteria,Bacteroidetes and Acidobacteria. We found RAB communities were host specific, with only 17% overlap in operational taxonomic units. Host effects on composition were over twice as strong as Neffects. D. cespitosa RAB diversity declined with N, while G. rossii RAB did not. D. cespitosa removal did not influence G. rossii RAB community composition, but G. rossii RAB diversity declined with N only when D. cespitosa was absent. We conclude that RAB of both hosts are sensitive to N enrichment, and RAB response to N is influenced by host identity and plant neighborhood.

Biotic mechanisms of community stability shift along a precipitation gradient.

Understanding how biotic mechanisms confer stability in variable environments is a fundamental quest in ecology, and one that is becoming increasingly urgent with global change. Several mechanisms, notably a portfolio effect associated with species richness, compensatory dynamics generated by negative species covariance and selection for stable dominant species populations can increase the stability of the overall community. While the importance of these mechanisms is debated, few studies have contrasted their importance in an environmental context. We analyzed nine long-term data sets of grassland species composition to investigate how two key environmental factors, precipitation amount and variability, may directly influence community stability and how they may indirectly influence stability via biotic mechanisms. We found that the importance of stability mechanisms varied along the environmental gradient: strong negative species covariance occurred in sites characterized by high precipitation variability, whereas portfolio effects increased in sites with high mean annual precipitation. Instead of questioning whether compensatory dynamics are important in nature, our findings suggest that debate should widen to include several stability mechanisms and how these mechanisms vary in importance across environmental gradients.

Separating direct and indirect effects of global change: a population dynamic modeling approach using readily available field data.

Two sources of complexity make predicting plant community response to global change particularly challenging. First, realistic global change scenarios involve multiple drivers of environmental change that can interact with one another to produce non-additive effects. Second, in addition to these direct effects, global change drivers can indirectly affect plants by modifying species interactions. In order to tackle both of these challenges, we propose a novel population modeling approach, requiring only measurements of abundance and climate over time. To demonstrate the applicability of this approach, we model population dynamics of eight abundant plant species in a multifactorial global change experiment in alpine tundra where we manipulated nitrogen, precipitation, and temperature over 7 years. We test whether indirect and interactive effects are important to population dynamics and whether explicitly incorporating species interactions can change predictions when models are forecast under future climate change scenarios. For three of the eight species, population dynamics were best explained by direct effect models, for one species neither direct nor indirect effects were important, and for the other four species indirect effects mattered. Overall, global change had negative effects on species population growth, although species responded to different global change drivers, and single-factor effects were slightly more common than interactive direct effects. When the fitted population dynamic models were extrapolated under changing climatic conditions to the end of the century, forecasts of community dynamics and diversity loss were largely similar using direct effect models that do not explicitly incorporate species interactions or best-fit models; however, inclusion of species interactions was important in refining the predictions for two of the species. The modeling approach proposed here is a powerful way of analyzing readily available datasets which should be added to our toolbox to tease apart complex drivers of global change.

Nitrogen deposition alters plant-fungal relationships: linking belowground dynamics to aboveground vegetation change.

Nitrogen (N) deposition rates are increasing globally due to anthropogenic activities. Plant community responses to N are often attributed to altered competitive interactions between plants, but may also be a result of microbial responses to N, particularly root-associated fungi (RAF), which are known to affect plant fitness. In response to N, Deschampsia cespitosa, a codominant plant in the alpine tundra at Niwot Ridge (CO), increases in abundance, while Geum rossii, its principal competitor, declines. Importantly, G. rossii declines with N even in the absence of its competitor. We examined whether contrasting host responses to N are associated with altered plant-fungal symbioses, and whether the effects of N are distinct from effects of altered plant competition on RAF, using 454 pyrosequencing. Host RAF communities were distinct (only 9.4% of OTUs overlapped). N increased RAF diversity in G. rossii, but decreased it in D. cespitosa. D. cespitosa RAF communities were more responsive to N than G. rossii RAF communities, perhaps indicating a flexible microbial community aids host adaptation to nutrient enrichment. Effects of removing D. cespitosa were distinct from effects of N on G. rossii RAF, and D. cespitosa presence reversed RAF diversity response to N. The most dominant G. rossii RAF order, Helotiales, was the most affected by N, declining from 83% to 60% of sequences, perhaps indicating a loss of mutualists under N enrichment. These results highlight the potential importance of belowground microbial dynamics in plant responses to N deposition.

Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation.

Climate gradients shape spatial variation in the richness and composition of plant communities. Given future predicted changes in climate means and variability, and likely regional variation in the magnitudes of these changes, it is important to determine how temporal variation in climate influences temporal variation in plant community structure. Here, we evaluated how species richness, turnover, and composition of grassland plant communities responded to interannual variation in precipitation by synthesizing long-term data from grasslands across the United States. We found that mean annual precipitation,(MAP) was a positive predictor of species richness across sites, but a positive temporal relationship between annual precipitation and richness was only evident within two sites with low MAP. We also found higher average rates of species turnover in dry sites that in turn had a high proportion of annual species, although interannual rates of species turnover were surprisingly high across all locations. Annual species were less abundant than perennial species at nearly all sites, and our analysis showed that the probability of a species being lost or gained from one year to the next increased with decreasing species abundance. Bray-Curtis dissimilarity from one year to the next, a measure of species composition change that is influenced mainly by abundant species, was insensitive to precipitation at all sites. These results suggest that the richness and turnover patterns we observed were driven primarily by rare species, which comprise the majority of the local species pools at these grassland sites. These findings are consistent with the idea that short-lived and less abundant species are more sensitive to interannual climate variability than longer-lived and more abundant species. We conclude that, among grassland ecosystems, xeric grasslands are likely to exhibit the greatest responsiveness of community composition (richness and turnover) to predicted future increases in interannual precipitation variability. Over the long-term, species composition may shift to reflect spatial patterns of mean precipitation; however, perennial-dominated systems will be buffered against rising interannual variation, while systems that have a large number of rare, annual species will show the greatest temporal variability in species composition in response to rising interannual variability in precipitation.

Erratum: Cooccurrence patterns of plants and soil bacteria in the high-alpine subnival zone track environmental harshness.

[This corrects the article on p. 347 in vol. 3, PMID: 23087675.].

Nitrogen deposition, plant carbon allocation, and soil microbes: changing interactions due to enrichment.

PREMISE OF THE STUDY: Nitrogen (N) inputs to the terrestrial environment have doubled worldwide during the past century. N negatively impacts plant diversity, but it is unknown why some species are more susceptible than others. While it is often assumed that competition drives species decline, N enrichment also strongly affects soil microbial communities. Can these changes affect plant-microbe interactions in ways that differentially influence success of plant species? Furthermore, can altered plant-microbe interactions lead to carbon (C) limitation in plants? METHODS: We focused on a species that increases (Deschampsia cespitosa) and one that decreases (Geum rossii) in abundance in N-fertilized plots in alpine tundra. We measured soil microbes using phospholipid fatty acids, and C limitation and transfer using a (13)C tracer experiment, C:N ratios, nonstructural carbohydrates, and leaf preformation. KEY RESULTS: While N profoundly influenced microbial communities, this change occurred similarly in association with both plant species. N addition did not alter total C allocation to microbes in either species, but it changed patterns of microbial C acquisition more in Geum, specifically in gram-negative bacteria. Geum showed evidence of C limitation: it allocated less C to storage organs, had lower C:N and carbohydrate stores, and fewer preformed leaves in N plots. CONCLUSIONS: Carbon limitation may explain why some species decline with N enrichment, and the decline may be due to physiological responses of plants to N rather than to altered plant-microbe interactions. Global change will alter many processes important in structuring plant communities; noncompetitive mechanisms of species decline may be more widespread than previously thought.

Co-occurrence patterns of plants and soil bacteria in the high-alpine subnival zone track environmental harshness.

Plants and soil microorganisms interact to play a central role in ecosystem functioning. To determine the potential importance of biotic interactions in shaping the distributions of these organisms in a high-alpine subnival landscape, we examine co-occurrence patterns between plant species and bulk soil bacteria abundances. In this context, a co-occurrence relationship reflects a combination of several assembly processes: that both parties can disperse to the site, that they can survive the abiotic environmental conditions, and that interactions between the biota either facilitate survival or allow for coexistence. Across the entire landscape, 31% of the bacterial sequences in this dataset were significantly correlated to the abundance distribution of one or more plant species. These sequences fell into 14 clades, 6 of which are related to bacteria that are known to form symbioses with plants in other systems. Abundant plant species were more likely to have significant as well as stronger correlations with bacteria and these patterns were more prevalent in lower altitude sites. Conversely, correlations between plant species abundances and bacterial relative abundances were less frequent in sites near the snowline. Thus, plant-bacteria associations became more common as environmental conditions became less harsh and plants became more abundant. This pattern in co-occurrence strength and frequency across the subnival landscape suggests that plant-bacteria interactions are important for the success of life, both below- and above-ground, in an extreme environment.

Early development of bacterial community diversity in emergently placed urinary catheters.

BACKGROUND: Approximately 25% of hospitalized patients have a urinary catheter, and catheter associated urinary tract infection is the most common nosocomial infection in the US, causing >1 million cases/year. However, the natural history of the biofilms that rapidly form on urinary catheters and lead to infection is not well described. FINDINGS: We characterized the dynamics of catheter colonization among catheters collected from 3 women and 5 men in a trauma burn unit with different indwelling times using TRFLP and culture. All patients received antibiotic therapy. RESULTS: Colony-forming units increased along the extraluminal catheter surface from the catheter balloon to the urethra, but no trend was apparent for the intraluminal surface. This suggests extraluminal bacteria come from periurethral communities while intraluminal bacteria are introduced via the catheter or already inhabit the urine/bladder. Richness of operational taxonomic units (OTUs) increased over time on the intraluminal surface, but was constant extraluminally. CONCLUSIONS: OTU community composition was explained best by time rather than axial location or surface. Our results suggest that catheter colonization can be very dynamic, and possibly have a predictable succession.

Time lags and the balance of positive and negative interactions in driving grassland community dynamics.

Both facilitative and competitive interactions occur simultaneously among plants, and the net balance between them can vary over time. Despite this, recent model-fitting studies have found that negative interactions predominate. This suggests that more complex models may be necessary to uncover facilitation. Here we fitted models including seasonality, interannual variation, and time lags to survey data to test for patterns in positive and negative interactions among plants in a Michigan dry sand prairie. We hypothesized that interactions would be generally facilitative in this dry environment. Results indicate that most immediate (direct) interactions among dominant species are actually competitive, although interactions were more facilitative over the drier summer season. Interestingly, lagged density dependence was strong for all species in both seasons; it was positive for conspecific interactions and both positive and negative for heterospecific interactions. Observed lagged density dependence is likely due to effects from litter and/or past storage in rhizomes. Conspecific immediate and lagged interactions tended to be stronger than heterospecific interactions, suggesting that population dynamics in this community are driven mostly by conspecifics. Overall, the presence of strong lagged density dependence in this system suggests that it may be more widespread in plants than previously thought.

Litter drives ecosystem and plant community changes in cattail invasion.

Invaded systems are commonly associated with a change in ecosystem processes and a decline in native species diversity; however, many different causal pathways linking invasion, ecosystem change, and native species decline could produce this pattern. The initial driver of environmental change may be anthropogenic, or it may be the invader itself; and the mechanism behind native species decline may be the human-induced environmental change, competition from the invader, or invader-induced environmental change (non-trophic effects). We examined applicability of each of these alternate pathways in Great Lakes coastal marshes invaded by hybrid cattail (Typha x glauca). In a survey including transects in three marshes, we found that T. x glauca was associated with locally high soil nutrients, low light, and large amounts of litter, and that native diversity was highest in areas of shallow litter depth. We tested whether live T. x glauca plants or their litter induced changes in the environment and in diversity with a live plant and litter transplant experiment. After one year, Typha litter increased soil NH4+ and N mineralization twofold, lowered light levels, and decreased the abundance and diversity of native plants, while live Typha plants had no effect on the environment or on native plants. This suggests that T. x glauca, through its litter production, can cause the changes in ecosystem processes that we commonly attribute to anthropogenic nutrient loading and that T. x glauca does not displace native species through competition for resources, but rather affects them non-trophically through its litter. Moreover, because T. x glauca plants were taller when grown with their own litter, we suggest that this invader may produce positive feedbacks and change the environment in ways that benefit itself and may promote its own invasion.