Taxonomic and regional patterns in benthic macroinvertebrate elemental composition in streams

1. Ecological stoichiometry has been used to better understand dynamics in consumer growth and the role of consumer‐recycled nutrients because it focuses on more than one element. Most research has focused on pelagic rather than benthic consumers. Variation in elemental composition among benthic consumer taxa would suggest that taxa differ in their susceptibility to nutrient limitation or in their role in recycling nutrients. 2. We collected benthic macroinvertebrates from streams in two regions (Indiana–Michigan and Wisconsin, U.S.A.) to examine taxonomic and regional variation in benthic macroinvertebrate body carbon (C), nitrogen (N), and phosphorus (P) concentrations and ratios. 3. Elemental composition varied little within taxa common to both regions. In contrast, elemental composition differed greatly among taxa and appeared to be related to phylogeny. The elemental composition of macroinvertebrates clustered into three distinct groups: insects, mollusks, and crustaceans. To a lesser extent, insects and mollusks also differed in elemental composition among genera. 4. Functional feeding groups (FFGs) differed in elemental composition, with predators having a higher N content than other groups. Substantial elemental imbalances between C and N were found between most primary consumers and their likely food sources, and the magnitude of the imbalance depended in part on the FFG. 5. Our results support an assumption of most ecological stoichiometry models that, within a species, the elemental composition of aquatic invertebrates is relatively constant. Variation in elemental composition among taxa at various higher taxonomic levels suggests that susceptibility of stream invertebrates to nutrient limitation and their role in nutrient cycling will strongly depend on phylogeny.     

Resource quality and stoichiometric constraints on stream ecosystem functioning

1. Resource quality and stoichiometric imbalances in carbon : nutrient ratios between consumers and resources can influence key ecosystem processes. In many streams, this has important implications for food webs that are based largely upon the utilization of terrestrial leaf‐litter, which varies widely among litter types in its value as a food source for detritivores and as a substrate for microbial decomposers. 2. We measured breakdown rates and macroinvertebrate colonization of leaf‐litter from a range of native and exotic plants of differing resource quality and palatability to consumers [e.g. carbon : nitrogen : phosphorus (C : N : P) ratios, lignin and cellulose content], in a field experiment. We also measured C : N : P ratios of the principal leaf‐shredding invertebrates, which revealed strong stoichiometric imbalances across trophic levels: C : N and C : P ratios typically differed by at least one order of magnitude between consumers and resources, whereas N : P imbalances were less marked. Application of the threshold elemental ratio approach, which integrates animal bioenergetics and body elemental composition in examining nutrient deficiency between consumers and resources, revealed less marked C : P imbalances than those based on the simpler arithmetic differences described above. 3. Litter breakdown rates declined as nutrient imbalances widened and resource quality fell, but they were independent of whether resources were exotic or native. The principal drivers of total, microbial and invertebrate‐mediated breakdown rates were lignin : N, lignin : P and fungal biomass, respectively. However, multiple regression using orthogonal predictors yielded even more efficient models of litter breakdown, as consumers responded to more than one aspect of resource quality. For example, fungal biomass and litter C : N both influenced invertebrate‐mediated breakdown. 4. Large stoichiometric imbalances and changes in resource quality are likely to have serious consequences for stream ecosystem functioning, especially when riparian zones have been invaded by exotic plant species whose chemical composition differs markedly from that of the native flora. Consequently, the magnitude and direction of change in breakdown rates and, thus, resource depletion, will be driven to a large extent by the biochemical traits (rather than taxonomic identity per se) of the resident and invading flora.     

Microbial community dynamics alleviate stoichiometric constraints during litter decay

Under the current paradigm, organic matter decomposition and nutrient cycling rates are a function of the imbalance between substrate and microbial biomass stoichiometry. Challenging this view, we demonstrate that in an individual‐based model, microbial community dynamics alter relative C and N limitation during litter decomposition, leading to a system behaviour not predictable from stoichiometric theory alone. Rather, the dynamics of interacting functional groups lead to an adaptation at the community level, which accelerates nitrogen recycling in litter with high initial C : N ratios and thus alleviates microbial N limitation. This mechanism allows microbial decomposers to overcome large imbalances between resource and biomass stoichiometry without the need to decrease carbon use efficiency (CUE), which is in contrast to predictions of traditional stoichiometric mass balance equations. We conclude that identifying and implementing microbial community‐driven mechanisms in biogeochemical models are necessary for accurately predicting terrestrial C fluxes in response to changing environmental conditions.     

Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen

Spence, R. and Smith, C. 2011. Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen. —Acta Zoologica (Stockholm) 00 : 1–6. Understanding how parasites inflict fitness costs on their hosts is a key question in host–parasite biology. Rose bitterling (Rhodeus ocellatus) are small cyprinid fish that place their eggs in the gills of living freshwater mussels. The embryos complete their development inside the mussel gill and emerge as free‐swimming larvae after approximately 4 weeks. Bitterling show a range of specialized adaptations for using mussels as a spawning substrate, and the presence of bitterling embryos has been shown to retard the growth of mussels. We compared the development and survival of embryos incubated in either mussels or Petri dishes and exposed to either nutrient‐rich or nutrient‐poor pond water. Embryonic development rate was significantly faster in Petri dishes, probably as a result of oxygen limitation in mussel gills. Embryo survival rate was significantly higher in nutrient‐rich than filtered water, suggesting that the embryos obtained a nutritional benefit prior to emergence from the host. The results imply that bitterling embryos compete for oxygen and nutrients with their host mussel, as well as each other, and in this way, impose a growth cost on mussels.     

Growth and survival of the superorganism: Ant colony macronutrient intake and investment

In this study, we used two common ant species (Lasius niger and Lasius neoniger) to assay how they translate variation in the diet (both in composition and frequency) into growth. We measured colony development for over 8 months and measured several phenotypic traits of the worker caste, and examined whether forager preference corresponded with diet quality. Optimal colony growth was a balance between survival and growth, and each of these was maximized with different nutrient regimes. Interestingly, forager preference was not totally aligned with the diet that maximized colony growth. Our results highlight that: (a) organism and superorganism size are controlled by the same nutrients, and this may reflect a common molecular basis for size across life's organizational levels, (b) there are nutrient trade‐offs that are associated with life‐history trade‐offs, likely leading to selection for a balanced diet, and (c) the connection between the preference of foragers for different nutrients and how nutrient combinations affect colony success and demographics are complex and only beginning to be understood.     

Elemental composition of strawberry plants inoculated with the plant growth‐promoting bacterium Azospirillum brasilense REC3, assessed with scanning electron microscopy and energy dispersive X‐ray analysis

The elemental composition of strawberry plants (Fragaria ananassa cv. Macarena) inoculated with the plant growth‐promoting bacterium Azospirillum brasilense REC3, and non‐inoculated controls, was studied using scanning electron microscopy (SEM) and energy dispersive X‐ray (EDS) analysis. This allowed simultaneous semi‐quantification of different elements in a small, solid sample. Plants were inoculated and grown hydroponically in 50% or 100% Hoagland solution, corresponding to limited or optimum nutrient medium, respectively. Bacteria‐inoculated plants increased the growth index 45% and 80% compared to controls when grown in 100% and 50% Hoagland solution, respectively. Thus, inoculation with A. brasilense REC3 in a nutrient‐limited medium had the strongest effect in terms of increasing both shoot and root biomass and growth index, as already described for Azospirillum inoculated into nutrient‐poor soils. SEM‐EDS spectra and maps showed the elemental composition and relative distribution of nutrients in strawberry tissues. Leaves contained C, O, N, Na, P, K, Ca and Cu, while roots also had Si and Cl. The organic fraction (C, O and N) accounted for over 96.3% of the total chemical composition; of the mineral fraction, Na had higher accumulation in both leaves and roots. Azospirillum‐inoculated and control plants had similar elemental quantities; however, in bacteria‐inoculated roots, P was significantly increased (34.33%), which constitutes a major benefit for plant nutrition, while Cu content decreased (35.16%).     

Environmental and stoichiometric controls on microbial carbon-use efficiency in soils

Carbon (C) metabolism is at the core of ecosystem function. Decomposers play a critical role in this metabolism as they drive soil C cycle by mineralizing organic matter to CO(2) . Their growth depends on the carbon-use efficiency (CUE), defined as the ratio of growth over C uptake. By definition, high CUE promotes growth and possibly C stabilization in soils, while low CUE favors respiration. Despite the importance of this variable, flexibility in CUE for terrestrial decomposers is still poorly characterized and is not represented in most biogeochemical models. Here, we synthesize the theoretical and empirical basis of changes in CUE across aquatic and terrestrial ecosystems, highlighting common patterns and hypothesizing changes in CUE under future climates. Both theoretical considerations and empirical evidence from aquatic organisms indicate that CUE decreases as temperature increases and nutrient availability decreases. More limited evidence shows a similar sensitivity of CUE to temperature and nutrient availability in terrestrial decomposers. Increasing CUE with improved nutrient availability might explain observed declines in respiration from fertilized stands, while decreased CUE with increasing temperature and plant C?:?N ratios might decrease soil C storage. Current biogeochemical models could be improved by accounting for these CUE responses along environmental and stoichiometric gradients.     

Bromeliad growth and stoichiometry: responses to atmospheric nutrient supply in fog-dependent ecosystems of the hyper-arid Atacama Desert, Chile

Carbon, nitrogen, and phosphorus (C, N, P) stoichiometry influences the growth of plants and nutrient cycling within ecosystems. Indeed, elemental ratios are used as an index for functional differences between plants and their responses to natural or anthropogenic variations in nutrient supply. We investigated the variation in growth and elemental content of the rootless terrestrial bromeliad Tillandsia landbeckii, which obtains its moisture, and likely its nutrients, from coastal fogs in the Atacama Desert. We assessed (1) how fog nutrient supply influences plant growth and stoichiometry and (2) the response of plant growth and stoichiometry to variations in nutrient supply by using reciprocal transplants. We hypothesized that T. landbeckii should exhibit physiological and biochemical plastic responses commensurate with nutrient supply from atmospheric deposition. In the case of the Atacama Desert, nutrient supply from fog is variable over space and time, which suggests a relatively high variation in the growth and elemental content of atmospheric bromeliads. We found that the nutrient content of T. landbeckii showed high spatio-temporal variability, driven partially by fog nutrient deposition but also by plant growth rates. Reciprocal transplant experiments showed that transplanted individuals converged to similar nutrient content, growth rates, and leaf production of resident plants at each site, reflecting local nutrient availability. Although plant nutrient content did not exactly match the relative supply of N and P, our results suggest that atmospheric nutrient supply is a dominant driver of plant growth and stoichiometry. In fact, our results indicate that N uptake by T. landbeckii plants depends more on N supplied by fog, whereas P uptake is mainly regulated by within-plant nutrient demand for growth. Overall, these findings indicate that variation in fog nutrient supply exerts a strong control over growth and nutrient dynamics of atmospheric plants, which are ubiquitous across fog-dominated ecosystems.     

Energy use efficiency of soil microorganisms: Driven by carbon recycling and reduction

Carbon use efficiency (CUE) is being intensively applied to quantify carbon (C) cycling processes from microbial cell to global scales. Energy use efficiency (EUE) is at least as important as the CUE because (i) microorganisms use organic C mainly as an energy source and not as elemental C per se, and (ii) microbial growth and maintenance are limited by energy, but not by C as a structural element. We conceptualize and review the importance of EUE by soil microorganisms and focus on (i) the energy content in organic compounds depending on the nominal oxidation state of carbon (NOSC), (ii) approaches to assess EUE, (iii) similarities and differences between CUE and EUE, and (iv) discuss mechanisms responsible for lower EUE compared to CUE. The energy content per C atom (enthalpy of combustion, the total energy stored in a compound) in organic compounds is very closely (R² = 0.98) positively related to NOSC and increases by 108 kJ mol⁻¹ C per one NOSC unit. For the first time we assessed the NOSC of microbial biomass in soil (−0.52) and calculated the corresponding energy content of −510 kJ mol⁻¹ C. We linked CUE and EUE considering the NOSC of microbial biomass and element compositions of substrates utilized by microorganisms. The mean microbial EUE (0.32–0.35) is 18% lower than CUE (0.41) using glucose as a substrate. This definitely indicates that microbial growth is limited by energy relative to C. Based on the comparison of a broad range of processes of C and energy utilization for cell growth and maintenance, as well as database of experimental CUE from various compounds, we clearly explained five mechanisms and main factors why EUE is lower than CUE. The two main mechanisms behind lower EUE versus CUE are: (i) microbial recycling: C can be microbially recycled, whereas energy is always utilized only once, and (ii) chemical reduction of organic and inorganic compounds: Energy is used for reduction, which is ongoing without C utilization.     

Microbial Growth and Carbon Use Efficiency in the Rhizosphere and Root-Free Soil

Plant-microbial interactions alter C and N balance in the rhizosphere and affect the microbial carbon use efficiency (CUE)–the fundamental characteristic of microbial metabolism. Estimation of CUE in microbial hotspots with high dynamics of activity and changes of microbial physiological state from dormancy to activity is a challenge in soil microbiology. We analyzed respiratory activity, microbial DNA content and CUE by manipulation the C and nutrients availability in the soil under Beta vulgaris. All measurements were done in root-free and rhizosphere soil under steady-state conditions and during microbial growth induced by addition of glucose. Microorganisms in the rhizosphere and root-free soil differed in their CUE dynamics due to varying time delays between respiration burst and DNA increase. Constant CUE in an exponentially-growing microbial community in rhizosphere demonstrated the balanced growth. In contrast, the CUE in the root-free soil increased more than three times at the end of exponential growth and was 1.5 times higher than in the rhizosphere. Plants alter the dynamics of microbial CUE by balancing the catabolic and anabolic processes, which were decoupled in the root-free soil. The effects of N and C availability on CUE in rhizosphere and root-free soil are discussed.     

Microbial carbon use efficiency in different ecosystems: A meta-analysis based on a biogeochemical equilibrium model

Soil microbial carbon use efficiency (CUE) is a crucial parameter that can be used to evaluate the partitioning of soil carbon (C) between microbial growth and respiration. However, general patterns of microbial CUE among terrestrial ecosystems (e.g., farmland, grassland, and forest) remain controversial. To address this knowledge gap, data from 41 study sites (n = 197 soil samples) including 58 farmlands, 95 forests, and 44 grasslands were collected and analyzed to estimate microbial CUEs using a biogeochemical equilibrium model. We also evaluated the metabolic limitations of microbial growth using an enzyme vector model and the drivers of CUE across different ecosystems. The CUEs obtained from soils of farmland, forest, and grassland ecosystems were significantly different with means of 0.39, 0.33, and 0.42, respectively, illustrating that grassland soils exhibited higher microbial C sequestration potentials (p < .05). Microbial metabolic limitations were also distinct in these ecosystems, and carbon limitation was dominant exhibiting strong negative effects on CUE. Exoenzyme stoichiometry played a greater role in impacting CUE values than soil elemental stoichiometry within each ecosystem. Specifically, soil exoenzymatic ratios of C:phosphorus (P) acquisition activities (EEA_C:P) and the exoenzymatic ratio of C:nitrogen (N) acquisition activities (EEA_C:N) imparted strong negative effects on soil microbial CUE in grassland and forest ecosystems, respectively. But in farmland soils, EEA_C:P exhibited greater positive effects, showing that resource constraints could regulate microbial resource allocation with discriminating patterns across terrestrial ecosystems. Furthermore, mean annual temperature (MAT) rather than mean annual precipitation (MAP) was a critical climate factor affecting CUE, and soil pH as a major factor remained positive to drive the changes in microbial CUE within ecosystems. This research illustrates a conceptual framework of microbial CUEs in terrestrial ecosystems and provides the theoretical evidence to improve soil microbial C sequestration capacity in response to global change.     

An investigation of non-steady-state algal growth. I. An experimental model ecosystem

In order to test rigorously the transient behaviour of mathematical models of algal growth, detailed laboratory data sets with good temporal resolution are required. A series of algal growth experiments was conducted in transient conditions. Monoculture growth of, and competition for nutrients between, three contrasting species of phytoplankton (the diatom Thalassiosira pseudonana, the harmful flagellate Heterosigma carterae and the toxic dinoflagellate Alexandrium minutum) were investigated in different temperature, light and nutrient regimes. Although growth dynamics were qualitatively similar in batch culture, quantitative differences were evident in the growth response of the different species when grown in single yield-limiting nutrient conditions in identical physical conditions. Quantities such as the carbon:nitrogen (C:N) ratio and C and N per cell varied between species and within species under different growth conditions. Such results have particular significance to the development of mathematical models, which commonly represent algal populations as a single homogeneous group using a single currency such as numbers, C or N. Changes in light and temperature regime influenced algal growth: Alexandrium failed to grow at low temperatures, while specific growth rates of Thalassiosira were more sensitive to changes in temperature than those of Heterosigma. Changes in the dominant organism(s) and/or its size or nutrient status may influence the transfer of nutrients within the food web. Commonly, mathematical models make cell growth a function of a single yield-limiting nutrient. Decreased growth rates and high residual nutrient concentrations in competition experiments indicate that this approach is unlikely to be successful in conditions of limited supply of more than one nutrient, where multiple nutrient stresses will be significant.      

土壤微生物碳素利用效率研究进展

土壤微生物碳素利用效率(CUE)是指微生物将吸收的碳(C)转化为自身生物量C的效率,也称为微生物的生长效率。土壤微生物CUE是生态系统C循环中的重要生理生态学参数,影响着生态系统的C固持、周转、土壤矿化以及温室气体排放等过程。在全球环境变化背景下,认识土壤微生物CUE的变异及其影响机制,对于更好的认识生态系统C循环过程及其对全球变化的响应具有重要意义。概述了CUE的定义及其测定方法,重点综述和分析土壤微生物CUE的变异及影响因素取得的研究进展。基于现有研究的分析得出,土壤微生物CUE通常表示为微生物的生长与吸收的比值,分为基于微生物生长速率、微生物生物量、底物吸收速率和底物浓度变化等方法进行测定。土壤微生物CUE在0.2-0.8的范围内变化,这种变异主要受到来自热力学、生态环境因子、底物养分质量和有效性、化学计量平衡以及微生物群落组成的影响。今后土壤微生物CUE的研究应加强对微量代谢组分的定量分析,生物和环境要素交互影响的调控机理解析,以及微生物动态生理响应过程的碳循环模型优化。     

Carbon use efficiency of microbial communities: stoichiometry,methodology and modelling

Carbon use efficiency (CUE) is a fundamental parameter for ecological models based on the physiology of microorganisms. CUE determines energy and material flows to higher trophic levels, conversion of plant‐produced carbon into microbial products and rates of ecosystem carbon storage. Thermodynamic calculations support a maximum CUE value of ~ 0.60 (CUE _max). Kinetic and stoichiometric constraints on microbial growth suggest that CUE in multi‐resource limited natural systems should approach ~ 0.3 (CUE _max/2). However, the mean CUE values reported for aquatic and terrestrial ecosystems differ by twofold (~ 0.26 vs. ~ 0.55) because the methods used to estimate CUE in aquatic and terrestrial systems generally differ and soil estimates are less likely to capture the full maintenance costs of community metabolism given the difficulty of measurements in water‐limited environments. Moreover, many simulation models lack adequate representation of energy spilling pathways and stoichiometric constraints on metabolism, which can also lead to overestimates of CUE. We recommend that broad‐scale models use a CUE value of 0.30, unless there is evidence for lower values as a result of pervasive nutrient limitations. Ecosystem models operating at finer scales should consider resource composition, stoichiometric constraints and biomass composition, as well as environmental drivers, to predict the CUE of microbial communities.     

Growth and composition of Escherichia coli subjected to square-wave perturbations in nutrient supply: Effect of varying frequencies

The effect of regularly varying the input nutrient concentration on the growth and composition (elemental and macromolecular) of Escherichia coli ML30 grown in chemostat culture is reported. After each change in substrate concentration a lag between the stimulus and organism response occurred, the magnitude of which was dependent upon the frequency of the perturbations. Both the growth yield and macromolecular composition of the cells were found to vary with the frequency of nutrient cycling: the yield decreased by some 10% as the cycle-times decreased from 6.0 to 0.25 hr. It is suggested that maintaining microorganisms under controlled transient conditions might be useful in increasing yields of specific microbial products (e.g., single-cell protein).     

Emergence of robust growth laws from optimal regulation of ribosome synthesis

Bacteria must constantly adapt their growth to changes in nutrient availability; yet despite large‐scale changes in protein expression associated with sensing, adaptation, and processing different environmental nutrients, simple growth laws connect the ribosome abundance and the growth rate. Here, we investigate the origin of these growth laws by analyzing the features of ribosomal regulation that coordinate proteome‐wide expression changes with cell growth in a variety of nutrient conditions in the model organism Escherichia coli. We identify supply‐driven feedforward activation of ribosomal protein synthesis as the key regulatory motif maximizing amino acid flux, and autonomously guiding a cell to achieve optimal growth in different environments. The growth laws emerge naturally from the robust regulatory strategy underlying growth rate control, irrespective of the details of the molecular implementation. The study highlights the interplay between phenomenological modeling and molecular mechanisms in uncovering fundamental operating constraints, with implications for endogenous and synthetic design of microorganisms.     

Atmospheric CO2 mole fraction affects stand‐scale carbon use efficiency of sunflower by stimulating respiration in light

Plant carbon‐use‐efficiency (CUE), a key parameter in carbon cycle and plant growth models, quantifies the fraction of fixed carbon that is converted into net primary production rather than respired. CUE has not been directly measured, partly because of the difficulty of measuring respiration in light. Here, we explore if CUE is affected by atmospheric CO₂. Sunflower stands were grown at low (200 μmol mol^?1) or high CO₂ (1000 μmol mol^?1) in controlled environment mesocosms. CUE of stands was measured by dynamic stand‐scale ¹³C labelling and partitioning of photosynthesis and respiration. At the same plant age, growth at high CO₂ (compared with low CO₂) led to 91% higher rates of apparent photosynthesis, 97% higher respiration in the dark, yet 143% higher respiration in light. Thus, CUE was significantly lower at high (0.65) than at low CO₂ (0.71). Compartmental analysis of isotopic tracer kinetics demonstrated a greater commitment of carbon reserves in stand‐scale respiratory metabolism at high CO₂. Two main processes contributed to the reduction of CUE at high CO₂: a reduced inhibition of leaf respiration by light and a diminished leaf mass ratio. This work highlights the relevance of measuring respiration in light and assessment of the CUE response to environment conditions.     

Parasite and host elemental content and parasite effects on host nutrient excretion and metabolic rate

Ecological stoichiometry uses the mass balance of elements to predict energy and elemental fluxes across different levels of ecological organization. A specific prediction of ecological stoichiometry is the growth rate hypothesis (GRH), which states that organisms with faster growth or reproductive rates will require higher phosphorus content for nucleic acid and protein synthesis. Although parasites are found ubiquitously throughout ecosystems, little is understood about how they affect nutrient imbalances in ecosystems. We (1) tested the GRH by determining the carbon (C), nitrogen (N), and phosphorus (P) content of parasitic trematodes and their intermediate host, the freshwater snail Elimia livescens, and (2) used this framework to determine the trematode effects on host nutrient excretion and metabolism. Snail and parasite tissues were analyzed for elemental content using a CHN analyzer and soluble reactive phosphorus (SRP) methods. Ammonium and SRP assays were used to estimate N and P excretion rates. A respirometer was used to calculate individual snail metabolism. Trematode tissues contained lower C:P and N:P (more P per unit C and N) than the snail tissues. Snail gonadal tissues more closely resembled the elemental content of parasite tissues, although P content was 13% higher in the gonad than the trematode tissues. Despite differences in elemental content, N and P excretion rates of snails were not affected by the presence of parasites. Parasitized snails maintained faster metabolic rates than nonparasitized snails. However, the species of parasite did not affect metabolic rate. Together, this elemental imbalance between parasite and host, and the altered metabolic rate of infected snails may lead to broader parasite effects in stream ecosystems.