Herbivory changes soil microbial communities and greenhouse gas fluxes in a high-latitude wetland.

Herbivory can have strong impacts on greenhouse gas fluxes in high-latitude ecosystems. For example, in the Yukon-Kuskokwim (Y-K) Delta in western Alaska, migratory goose grazing affects the magnitude of soil carbon dioxide (CO2) and methane (CH4) fluxes. However, the underlying drivers of this relationship are unclear, as few studies systematically tease apart the processes by which herbivores influences soil biogeochemistry. To examine these mechanisms in detail, we conducted a laboratory incubation experiment to quantify changes in greenhouse gas fluxes in response to three parameters altered by herbivores in situ: temperature, soil moisture content, and nutrient inputs. These treatments were applied to soils collected in grazing lawns and nearby ungrazed habitat, allowing us to assess how variation in microbial community structure influenced observed responses. We found pronounced differences in both fungal and prokaryotic community composition between grazed and ungrazed areas. In the laboratory incubation experiment, CO2 and CH4 fluxes increased with temperature, soil moisture, and goose fecal addition, suggesting that grazing-related changes in the soil abiotic environment may enhance soil C losses. Yet, these abiotic drivers were insufficient to explain variation in fluxes between soils with and without prior grazing. Differences in trace gas fluxes between grazed and ungrazed areas may result both from herbivore-induced shifts in abiotic parameters and grazing-related alterations in microbial community structure. Our findings suggest that relationships among herbivores and soil microbial communities could mediate carbon-climate feedbacks in rapidly changing high-latitude ecosystems.

Beyond leaf habit: generalities in plant function across 97 tropical dry forest tree species.

Leaf habit has been hypothesized to define a linkage between the slow-fast plant economic spectrum and the drought resistance-avoidance trade-off in tropical forests ('slow-safe vs fast-risky'). However, variation in hydraulic traits as a function of leaf habit has rarely been explored for a large number of species. We sampled leaf and branch functional traits of 97 tropical dry forest tree species from four sites to investigate whether patterns of trait variation varied consistently in relation to leaf habit along the 'slow-safe vs fast-risky' trade-off. Leaf habit explained from 0% to 43.69% of individual trait variation. We found that evergreen and semi-deciduous species differed in their location along the multivariate trait ordination when compared to deciduous species. While deciduous species showed consistent trait values, evergreen species trait values varied as a function of the site. Last, trait values varied in relation to the proportion of deciduous species in the plant community. We found that leaf habit describes the strategies that define drought avoidance and plant economics in tropical trees. However, leaf habit alone does not explain patterns of trait variation, which suggests quantifying site-specific or species-specific uncertainty in trait variation as the way forward.

From pools to flow: The PROMISE framework for new insights on soil carbon cycling in a changing world.

Soils represent the largest terrestrial reservoir of organic carbon, and the balance between soil organic carbon (SOC) formation and loss will drive powerful carbon-climate feedbacks over the coming century. To date, efforts to predict SOC dynamics have rested on pool-based models, which assume classes of SOC with internally homogenous physicochemical properties. However, emerging evidence suggests that soil carbon turnover is not dominantly controlled by the chemistry of carbon inputs, but rather by restrictions on microbial access to organic matter in the spatially heterogeneous soil environment. The dynamic processes that control the physicochemical protection of carbon translate poorly to pool-based SOC models; as a result, we are challenged to mechanistically predict how environmental change will impact movement of carbon between soils and the atmosphere. Here, we propose a novel conceptual framework to explore controls on belowground carbon cycling: Probabilistic Representation of Organic Matter Interactions within the Soil Environment (PROMISE). In contrast to traditional model frameworks, PROMISE does not attempt to define carbon pools united by common thermodynamic or functional attributes. Rather, the PROMISE concept considers how SOC cycling rates are governed by the stochastic processes that influence the proximity between microbial decomposers and organic matter, with emphasis on their physical location in the soil matrix. We illustrate the applications of this framework with a new biogeochemical simulation model that traces the fate of individual carbon atoms as they interact with their environment, undergoing biochemical transformations and moving through the soil pore space. We also discuss how the PROMISE framework reshapes dialogue around issues related to SOC management in a changing world. We intend the PROMISE framework to spur the development of new hypotheses, analytical tools, and model structures across disciplines that will illuminate mechanistic controls on the flow of carbon between plant, soil, and atmospheric pools.

Trait-based signatures of cloud base height in a tropical cloud forest.

PREMISE: Clouds have profound consequences for ecosystem structure and function. Yet, the direct monitoring of clouds and their effects on biota is challenging especially in remote and topographically complex tropical cloud forests. We argue that known relationships between climate and the taxonomic and functional composition of plant communities may provide a fingerprint of cloud base height, thus providing a rapid and cost-effective assessment in remote tropical cloud forests. METHODS: To detect cloud base height, we compared species turnover and functional trait values among herbaceous and woody plant communities in an ecosystem dominated by cloud formation. We measured soil and air temperature, soil nutrient concentrations, and extracellular enzyme activity. We hypothesized that woody and herbaceous plants would provide signatures of cloud base height, as evidenced by abrupt shifts in both taxonomic composition and plant function. RESULTS: We demonstrated abrupt changes in taxonomic composition and the community- weighted mean of a key functional trait, specific leaf area, across elevation for both woody and herbaceous species, consistent with our predictions. However, abrupt taxonomic and functional changes occurred 100 m higher in elevation for herbaceous plants compared to woody ones. Soil temperature abruptly decreased where herbaceous taxonomic and functional turnover was high. Other environmental variables including soil biogeochemistry did not explain the abrupt change observed for woody plant communities. CONCLUSIONS: We provide evidence that a trait-based approach can be used to estimate cloud base height. We outline how rises in cloud base height and differential environmental requirements between growth forms can be distinguished using this approach.

Observed variation in soil properties can drive large variation in modelled forest functioning and composition during tropical forest secondary succession.

Censuses of tropical forest plots reveal large variation in biomass and plant composition. This paper evaluates whether such variation can emerge solely from realistic variation in a set of commonly measured soil chemical and physical properties. Controlled simulations were performed using a mechanistic model that includes forest dynamics, microbe-mediated biogeochemistry, and competition for nitrogen and phosphorus. Observations from 18 forest inventory plots in Guanacaste, Costa Rica were used to determine realistic variation in soil properties. In simulations of secondary succession, the across-plot range in plant biomass reached 30% of the mean and was attributable primarily to nutrient limitation and secondarily to soil texture differences that affected water availability. The contributions of different plant functional types to total biomass varied widely across plots and depended on soil nutrient status. In Central America, soil-induced variation in plant biomass increased with mean annual precipitation because of changes in nutrient limitation. In Central America, large variation in plant biomass and ecosystem composition arises mechanistically from realistic variation in soil properties. The degree of biomass and compositional variation is climate sensitive. In general, model predictions can be improved through better representation of soil nutrient processes, including their spatial variation.

Plant community responses to stand-level nutrient fertilization in a secondary tropical dry forest.

The size of the terrestrial carbon (C) sink is mediated by the availability of nutrients that limit plant growth. However, nutrient controls on primary productivity are poorly understood in the geographically extensive yet understudied tropical dry forest biome. To examine how nutrients influence above- and belowground biomass production in a secondary, seasonally dry tropical forest, we conducted a replicated, fully factorial nitrogen (N) and phosphorus (P) fertilization experiment at the stand scale in Guanacaste, Costa Rica. The production of leaves, wood, and fine roots was monitored through time; root colonization by mycorrhizal fungi and the abundance of N-fixing root nodules were also quantified. In this seasonal forest, interannual variation in rainfall had the largest influence on stand-level productivity, with lower biomass growth under drought. By contrast, aboveground productivity was generally not increased by nutrient addition, although fertilization enhanced growth of individual tree stems in a wet year. However, root growth increased markedly and consistently under P addition, significantly altering patterns of stand-level biomass allocation to above- vs. belowground compartments. Although nutrients did not stimulate total biomass production at the community scale, N-fixing legumes exhibited a twofold increase in woody growth in response to added P, accompanied by a dramatic increase in the abundance of root nodules. These data suggest that the relationship between nutrient availability and primary production in tropical dry forest is contingent on both water availability and plant functional diversity.

Tropical dry forest trees and lianas differ in leaf economic spectrum traits but have overlapping water-use strategies.

Tree species in tropical dry forests employ a wide range of strategies to cope with seasonal drought, including regulation of hydraulic function. However, it is uncertain if co-occurring lianas also possess a diversity of strategies. For a taxonomically diverse group of 14 tree and 7 liana species, we measured morphological and hydraulic functional traits during an unusual drought and under non-drought conditions to determine (i) if trees have different water-use strategies than lianas and (ii) if relationships among these traits can be used to better understand how tree and liana species regulate diurnal leaf water potential (Ψdiurnal). In this Costa Rican tropical dry forest, lianas and trees had overlapping water-use strategies, but differed in many leaf economic spectrum traits. Specifically, we found that both lianas and trees employed a diversity of Ψdiurnal regulation strategies, which did not differ statistically. However, lianas and trees did significantly differ in terms of certain traits including leaf area, specific leaf area, petiole length, wood vessel diameter and xylem vessel density. All liana and tree species we measured fell along a continuum of isohydric (partial) to anisohydric (strict or extreme) Ψdiurnal regulation strategies, and leaf area, petiole length, stomatal conductance and wood vessel diameter correlated with these strategies. These findings contribute to a trait-based understanding of how plants regulate Ψdiurnal under both drought stress and sufficient water availability, and underscore that lianas and trees employ a similarly wide range of Ψdiurnal regulation strategies, despite having vastly different growth forms.

Historical climate controls soil respiration responses to current soil moisture.

Ecosystem carbon losses from soil microbial respiration are a key component of global carbon cycling, resulting in the transfer of 40-70 Pg carbon from soil to the atmosphere each year. Because these microbial processes can feed back to climate change, understanding respiration responses to environmental factors is necessary for improved projections. We focus on respiration responses to soil moisture, which remain unresolved in ecosystem models. A common assumption of large-scale models is that soil microorganisms respond to moisture in the same way, regardless of location or climate. Here, we show that soil respiration is constrained by historical climate. We find that historical rainfall controls both the moisture dependence and sensitivity of respiration. Moisture sensitivity, defined as the slope of respiration vs. moisture, increased fourfold across a 480-mm rainfall gradient, resulting in twofold greater carbon loss on average in historically wetter soils compared with historically drier soils. The respiration-moisture relationship was resistant to environmental change in field common gardens and field rainfall manipulations, supporting a persistent effect of historical climate on microbial respiration. Based on these results, predicting future carbon cycling with climate change will require an understanding of the spatial variation and temporal lags in microbial responses created by historical rainfall.

Effects of soil type and light on height growth, biomass partitioning, and nitrogen dynamics on 22 species of tropical dry forest tree seedlings: Comparisons between legumes and nonlegumes.

PREMISE OF THE STUDY: The seedling stage is particularly vulnerable to resource limitation, with potential consequences for community composition. We investigated how light and soil variation affected early growth, biomass partitioning, morphology, and physiology of 22 tree species common in tropical dry forest, including eight legumes. Our hypothesis was that legume seedlings are better at taking advantage of increased resource availability, which contributes to their successful regeneration in tropical dry forests. METHODS: We grew seedlings in a full-factorial design under two light levels in two soil types that differed in nutrient concentrations and soil moisture. We measured height biweekly and, at final harvest, biomass partitioning, internode segments, leaf carbon, nitrogen, δ13C, and δ15N. KEY RESULTS: Legumes initially grew taller and maintained that height advantage over time under all experimental conditions. Legumes also had the highest final total biomass and water-use efficiency in the high-light and high-resource soil. For nitrogen-fixing legumes, the amount of nitrogen derived from fixation was highest in the richer soil. Although seed mass tended to be larger in legumes, seed size alone did not account for all the differences between legumes and nonlegumes. Both belowground and aboveground resources were limiting to early seedling growth and function. CONCLUSIONS: Legumes may have a different regeneration niche, in that they germinate rapidly and grow taller than other species immediately after germination, maximizing their performance when light and belowground resources are readily available, and potentially permitting them to take advantage of high light, nutrient, and water availability at the beginning of the wet season.

Forest composition modifies litter dynamics and decomposition in regenerating tropical dry forest.

We investigated how forest composition, litter quality, and rainfall interact to affect leaf litter decomposition across three successional tropical dry forests in Costa Rica. We monitored litter stocks and bulk litter turnover in 18 plots that exhibit substantial variation in soil characteristics, tree community structure, fungal communities (including forests dominated by ecto- or arbuscular mycorrhizal host trees), and forest age. Simultaneously, we decomposed three standard litter substrates over a 6-month period spanning an unusually intense drought. Decay rates of standard substrates depended on the interaction between litter identity and forest type. Decomposition rates were correlated with tree and soil fungal community composition as well as soil fertility, but these relationships differed among litter types. In low fertility soils dominated by ectomycorrhizal oak trees, bulk litter turnover rates were low, regardless of soil moisture. By contrast, in higher fertility soils that supported mostly arbuscular mycorrhizal trees, bulk litter decay rates were strongly dependent on seasonal water availability. Both measures of decomposition increased with forest age, as did the frequency of termite-mediated wood decay. Taken together, our results demonstrate that soils and forest age exert strong control over decomposition dynamics in these tropical dry forests, either directly through effects on microclimate and nutrients, or indirectly by affecting tree and microbial community composition and traits, such as litter quality.

Historical precipitation predictably alters the shape and magnitude of microbial functional response to soil moisture.

Soil moisture constrains the activity of decomposer soil microorganisms, and in turn the rate at which soil carbon returns to the atmosphere. While increases in soil moisture are generally associated with increased microbial activity, historical climate may constrain current microbial responses to moisture. However, it is not known if variation in the shape and magnitude of microbial functional responses to soil moisture can be predicted from historical climate at regional scales. To address this problem, we measured soil enzyme activity at 12 sites across a broad climate gradient spanning 442-887 mm mean annual precipitation. Measurements were made eight times over 21 months to maximize sampling during different moisture conditions. We then fit saturating functions of enzyme activity to soil moisture and extracted half saturation and maximum activity parameter values from model fits. We found that 50% of the variation in maximum activity parameters across sites could be predicted by 30-year mean annual precipitation, an indicator of historical climate, and that the effect is independent of variation in temperature, soil texture, or soil carbon concentration. Based on this finding, we suggest that variation in the shape and magnitude of soil microbial response to soil moisture due to historical climate may be remarkably predictable at regional scales, and this approach may extend to other systems. If historical contingencies on microbial activities prove to be persistent in the face of environmental change, this approach also provides a framework for incorporating historical climate effects into biogeochemical models simulating future global change scenarios.

Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests.

Rates of ecosystem nitrogen (N) cycling may be mediated by the presence of ectomycorrhizal fungi, which compete directly with free-living microbes for N. In the regenerating tropical dry forests of Central America, the distribution of ectomycorrhizal trees is affected by succession and soil parent material, both of which may exert independent influence over soil N fluxes. In order to quantify these interacting controls, we used a scale-explicit sampling strategy to examine soil N cycling at scales ranging from the microsite to ecosystem level. We measured fungal community composition, total and inorganic N pools, gross proteolytic rate, net N mineralization and microbial extracellular enzyme activity at multiple locations within 18 permanent plots that span dramatic gradients of soil N concentration, stand age and forest composition. The ratio of inorganic to organic N cycling was correlated with variation in fungal community structure, consistent with a strong influence of ectomycorrhiza on ecosystem-scale N cycling. However, on average, > 61% of the variation in soil biogeochemistry occurred within plots, and the effects of forest composition were mediated by this local-scale heterogeneity in total soil N concentrations. These cross-scale interactions demonstrate the importance of a spatially explicit approach towards an understanding of controls on element cycling.

Pervasive and strong effects of plants on soil chemistry: a meta-analysis of individual plant 'Zinke' effects.

Plant species leave a chemical signature in the soils below them, generating fine-scale spatial variation that drives ecological processes. Since the publication of a seminal paper on plant-mediated soil heterogeneity by Paul Zinke in 1962, a robust literature has developed examining effects of individual plants on their local environments (individual plant effects). Here, we synthesize this work using meta-analysis to show that plant effects are strong and pervasive across ecosystems on six continents. Overall, soil properties beneath individual plants differ from those of neighbours by an average of 41%. Although the magnitudes of individual plant effects exhibit weak relationships with climate and latitude, they are significantly stronger in deserts and tundra than forests, and weaker in intensively managed ecosystems. The ubiquitous effects of plant individuals and species on local soil properties imply that individual plant effects have a role in plant-soil feedbacks, linking individual plants with biogeochemical processes at the ecosystem scale.

Nitrogen, phosphorus, and cation use efficiency in stands of regenerating tropical dry forest.

Plants on infertile soils exhibit physiological and morphological traits that support conservative internal nutrient cycling. However, potential trade-offs among use efficiencies for N, P, and cations are not well explored in species-rich habitats where multiple elements may limit plant production. We examined uptake efficiency and use efficiency of N, P, K, Ca, Mg, Al, and Na in plots of regenerating tropical dry forests spanning a gradient of soil fertility. Our aim was to determine whether plant responses to multiple elements are correlated, or whether there are trade-offs among exploitation strategies across stands varying in community composition, soil quality, and successional stage. For all elements, both uptake efficiency and use efficiency decreased as availability of the corresponding element increased. Plant responses to N, Na, and Al were uncoupled from uptake and use efficiencies for P and essential base cations, which were tightly correlated. N and P use efficiencies were associated with shifts in plant species composition along the soil fertility gradient, and there was also a trend towards increasing N use efficiency with stand age. N uptake efficiency was positively correlated with the abundance of tree species that associate with ectomycorrhizal fungi. Taken together, our results suggest that successional processes and local species composition interact to regulate plant responses to availability of multiple resources. Successional tropical dry forests appear to employ different strategies to maximize response to N vs. P and K.

Short-term precipitation exclusion alters microbial responses to soil moisture in a wet tropical forest.

Many wet tropical forests, which contain a quarter of global terrestrial biomass carbon stocks, will experience changes in precipitation regime over the next century. Soil microbial responses to altered rainfall are likely to be an important feedback on ecosystem carbon cycling, but the ecological mechanisms underpinning these responses are poorly understood. We examined how reduced rainfall affected soil microbial abundance, activity, and community composition using a 6-month precipitation exclusion experiment at La Selva Biological Station, Costa Rica. Thereafter, we addressed the persistent effects of field moisture treatments by exposing soils to a controlled soil moisture gradient in the lab for 4 weeks. In the field, compositional and functional responses to reduced rainfall were dependent on initial conditions, consistent with a large degree of spatial heterogeneity in tropical forests. However, the precipitation manipulation significantly altered microbial functional responses to soil moisture. Communities with prior drought exposure exhibited higher respiration rates per unit microbial biomass under all conditions and respired significantly more CO2 than control soils at low soil moisture. These functional patterns suggest that changes in microbial physiology may drive positive feedbacks to rising atmospheric CO2 concentrations if wet tropical forests experience longer or more intense dry seasons in the future.

Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models.

Since fungi and bacteria are the dominant decomposers in soil, their distinct physiologies are likely to differentially influence rates of ecosystem carbon (C) and nitrogen (N) cycling. We used meta-analysis and an enzyme-driven biogeochemical model to explore the drivers and biogeochemical consequences of changes in the fungal-to-bacterial ratio (F : B). In our meta-analysis data set, F : B increased with soil C : N ratio (R(2) = 0.224, P < 0.001), a relationship predicted by our model. We found that differences in biomass turnover rates influenced F : B under conditions of C limitation, while differences in biomass stoichiometry set the upper bounds on F : B once a nutrient limitation threshold was reached. Ecological interactions between the two groups shifted along a gradient of resource stoichiometry. At intermediate substrate C : N, fungal N mineralisation fuelled bacterial growth, increasing total microbial biomass and decreasing net N mineralisation. Therefore, we conclude that differences in bacterial and fungal physiology may have large consequences for ecosystem-scale C and N cycling.