Bonnie G. Waring

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.

Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils

The relative activities of soil enzymes involved in mineralizing organic carbon (C), nitrogen (N), and phosphorus (P) reveal stoichiometric and energetic constraints on microbial biomass growth. Although tropical forests and grasslands are a major component of the global C cycle, the effects of soil nutrient availability on microbial activity and C dynamics in these ecosystems are poorly understood. To explore potential microbial nutrient limitation in relation to enzyme allocation in low latitude ecosystems, we performed a meta-analysis of acid/alkaline phosphatase (AP), β-1,4-glucosidase (BG), and β-1,4-N-acetyl-glucosaminidase (NAG) activities in tropical soils. We found that BG:AP and NAG:AP ratios in tropical soils are significantly lower than those of temperate ecosystems overall. The lowest BG:AP and NAG:AP ratios were associated with old or acid soils, consistent with greater biological phosphorus demand relative to P availability. Additionally, correlations between enzyme activities and mean annual temperature and precipitation suggest some climatic regulation of microbial enzyme allocation in tropical soils. We used the results of our analysis in conjunction with previously published data on soil and biomass C:N:P stoichiometry to parameterize a biogeochemical equilibrium model that relates microbial growth efficiency to extracellular enzyme activity. The model predicts low microbial growth efficiencies in P-limited soils, indicating that P availability may influence C cycling in the highly weathered soils that underlie many tropical ecosystems. Therefore, we suggest that P availability be included in models that simulate microbial enzyme allocation, biomass growth, and C mineralization.

A Meta-analysis of Climatic and Chemical Controls on Leaf Litter Decay Rates in Tropical Forests

Although tropical forests occupy a small fraction of the earth’s total land area, they play a disproportionately large role in regulating the global carbon cycle. Yet controls on both primary productivity and decomposition in tropical forests are not well-studied in comparison with temperate forests and grasslands, despite their extreme biogeochemical heterogeneity. To evaluate the relative importance of climate and foliar chemical variables in driving decomposition in tropical forests, I performed a meta-analysis of reported leaf litter decay rates throughout tropical forest ecosystems. Using a model selection procedure based on Akaike’s Information Criterion, I found that temperature and precipitation played little direct role in regulating decomposition rates, except in montane forests where cool temperatures slowed decay. Foliar concentrations of calcium, magnesium, nitrogen, phosphorus, and potassium were important predictors of mass loss rates, although each of these factors explained a very small amount of variance when considered in isolation. The large amount of unexplained variation in decomposition rates observed both within and across tropical forest sites may be due to other factors not explored here, such as soil biota or complex plant secondary chemistry. Carbon cycling in tropical forests seems to be modulated by the availability of multiple nutrients, underscoring the need for additional manipulative experiments to explore patterns of belowground nutrient limitation across the biome. Because models of decomposition developed in temperate ecosystems do not appear to be generalizable to wet tropical forests, new biogeochemical paradigms should be developed to accommodate their unique combination of climatic, edaphic, and biotic factors.

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.

White-tailed deer (Odocoileus virginianus) positively affect the growth of mature northern red oak (Quercus rubra) trees.

Understanding and predicting the effects of deer (Cervidae) on forest ecosystems present significant challenges in ecosystem ecology. Deer herbivory can cause large changes in the biomass and species composition of forest understory plant communities, including early life-cycle trees (i.e., seedlings and saplings). Such changes can impact juvenile to adult transitions and the future age structure and species composition of mature forests. Changes to understory vegetation also impact flow of energy and nutrients in forest ecosystems. Studies examining the influence of deer on mature trees, however, are rare and rely on extrapolating effects from early life cycle stages of trees. We tested the hypothesis that the absence of deer would result in an increase in the growth rate of mature trees by examining the impact of white-tailed deer (Odocoileus virginianus) on mature canopy trees. We examined incremental growth in individuals of Quercus rubra, an important component of temperate deciduous forests in North America, inside and outside 16-year deer exclosures in eastern U.S. deciduous forests. We found that adult trees inside exclosures grew less than those directly exposed to deer. Our findings highlight the indirect effects of white-tailed deer on the growth of adult individuals of Q. rubra in a way opposite of what would be expected from previous studies based on immature or understory tree populations. We suggest the increased growth of adult trees in the presence of deer may be explained by increased nutrient inputs through deer fecal and urine deposits and the alteration of the competitive environment belowground through the reduction of understory vegetation by browsing. Underscoring the ecological and demographic importance of adult trees in forest ecosystems, results from this study suggest the direct and indirect effects of deer on mature trees should not be overlooked.

Nitrogen limitation of decomposition and decay: how can it occur?

The availability of nitrogen (N) is a critical control on the cycling and storage of soil carbon (C). Yet, there are conflicting conceptual models to explain how N availability influences the decomposition of organic matter by soil microbial communities. Several lines of evidence suggest that N availability limits decomposition; the earliest stages of leaf litter decay are associated with a net import of N from the soil environment, and both observations and models show that high N organic matter decomposes more rapidly. In direct contrast to these findings, experimental additions of inorganic N to soils broadly show a suppression of microbial activity, which is inconsistent with N limitation of decomposition. Resolving this apparent contradiction is critical to representing nutrient dynamics in predictive ecosystem models under a multitude of global change factors that alter soil N availability. Here, we propose a new conceptual framework, the Carbon, Acidity, and Mineral Protection hypothesis, to understand the effects of N availability on soil C cycling and storage and explore the predictions of this framework with a mathematical model. Our model simulations demonstrate that N addition can have opposing effects on separate soil C pools (particulate and mineral-protected carbon) because they are differentially affected by microbial biomass growth. Moreover, changes in N availability are frequently linked to shifts in soil pH or osmotic stress, which can independently affect microbial biomass dynamics and mask N stimulation of microbial activity. Thus, the net effect of N addition on soil C is dependent upon interactions among microbial physiology, soil mineralogy, and soil acidity. We believe that our synthesis provides a broadly applicable conceptual framework to understand and predict the effect of changes in soil N availability on ecosystem C cycling under global change.

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.

Historical climate controls soil respiration responses to current soil moisture

Significance Ecosystems’ feedback to climate change remains a source of uncertainty in global models that project future climate conditions. That uncertainty rests largely on how much soil carbon will be lost as microbial respiration and how that loss varies across ecosystems. Although there has been a large emphasis on microbial temperature responses, how soil microorganisms respond to changes in moisture remains poorly understood. Here we show that historical rainfall controls soil respiration responses to current moisture. This finding was robust, with historical climate repeatedly limiting current respiration regardless of alterations to soil moisture, rainfall, or the arrival of new taxa. This study highlights the importance that legacies in microbial responses to climate change can have in future ecosystem responses. 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.

Nutrient addition effects on tropical dry forests: a mini-review from microbial to ecosystem scales

Humans have more than doubled inputs of reactive nitrogen globally and greatly accelerated the biogeochemical cycles of phosphorus and metals. However, the impacts of increased element mobility on tropical ecosystems remain poorly quantified, particularly for the vast tropical dry forest biome. Tropical dry forests are characterized by marked seasonality, relatively little precipitation, and high heterogeneity in plant functional diversity and soil chemistry. For these reasons, increased nutrient deposition may affect tropical dry forests differently than wet tropical or temperate forests. Here we review studies that investigated how nutrient availability affects ecosystem and community processes from the microsite to ecosystem scales in tropical dry forests. The effects of N and P addition on ecosystem carbon cycling and plant and microbial dynamics depend on forest successional stage, soil parent material and rainfall regime. Responses may depend on whether overall productivity is N- versus P-limited, although data to test this hypothesis are limited. These results highlight the many important gaps in our understanding of tropical dry forest responses to global change. Large-scale experiments are required to resolve these uncertainties.

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.