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.     

Growth rate–stoichiometry couplings in diverse biota

Biological stoichiometry provides a mechanistic theory linking cellular and biochemical features of co‐evolving biota with constraints imposed by ecosystem energy and nutrient inputs. Thus, understanding variation in biomass carbon : nitrogen : phosphorus (C : N : P) stoichiometry is a major priority for integrative biology. Among various factors affecting organism stoichiometry, differences in C : P and N : P stoichiometry have been hypothesized to reflect organismal P‐content because of altered allocation to P‐rich ribosomal RNA at different growth rates (the growth rate hypothesis, GRH). We tested the GRH using data for microbes, insects, and crustaceans and we show here that growth, RNA content, and biomass P content are tightly coupled across species, during ontogeny, and under physiological P limitation. We also show, however, that this coupling is relaxed when P is not limiting for growth. The close relationship between P and RNA contents indicates that ribosomes themselves represent a biogeochemically significant repository of P in ecosystems and that allocation of P to ribosome generation is a central process in biological production in ecological systems.     

The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives

C, N and P are three of the most important elements used to build living beings, and their uptake from the environment is consequently essential for all organisms. We have reviewed the available studies on water, soils and organism elemental content ratios (stoichiometry) with the aim of identifying the general links between stoichiometry and the structure and function of organisms and ecosystems, in both aquatic and terrestrial contexts. Oceans have variable C:N:P ratios in coastal areas and a narrow range approximating the Redfield ratio in deep water and inner oceanic areas. Terrestrial ecosystems have a general trend towards an increase in soil and plant N:P ratios from cool and temperate to tropical ecosystems, but with great variation within each climatic area. The C:N:P content ratio (from now on C:N:P ratio) is more constrained in organisms than in the water and soil environments they inhabit. The capacity to adjust this ratio involves several mechanisms, from leaf re-absorption in plants to the control of excretion in animals. Several differences in C:N:P ratios are observed when comparing different taxa and ecosystems. For freshwater ecosystems, the growth rate hypothesis (GRH), which has consistent experimental support, states that low N:P supply determines trophic web structures by favoring organisms with a high growth rate. For terrestrial organisms, however, evidence not yet conclusive on the relevance of the GRH. Recent studies suggest that the N:P ratio could play a role, even in the evolution of the genomes of organisms. Further research is warranted to study the stoichiometry of different trophic levels under different C:N:P environment ratios in long-term ecosystem-scale studies. Other nutrients such as K or Fe should also be taken into account. Further assessment of the GRH requires more studies on the effects of C:N:P ratios on anabolic (growth), catabolic (respiration), storage and/or defensive allocation. Combining elemental stoichiometry with metabolomics and/or genomics should improve our understanding of the coupling of different levels of biological organization, from elemental composition to the structure and evolution of ecosystems, via cellular metabolism and nutrient cycling.     

Optimization of biomass composition explains microbial growth-stoichiometry relationships

Integrating microbial physiology and biomass stoichiometry opens far-reaching possibilities for linking microbial dynamics to ecosystem processes. For example, the growth-rate hypothesis (GRH) predicts positive correlations among growth rate, RNA content, and biomass phosphorus (P) content. Such relationships have been used to infer patterns of microbial activity, resource availability, and nutrient recycling in ecosystems. However, for microorganisms it is unclear under which resource conditions the GRH applies. We developed a model to test whether the response of microbial biomass stoichiometry to variable resource stoichiometry can be explained by a trade-off among cellular components that maximizes growth. The results show mechanistically why the GRH is valid under P limitation but not under N limitation. We also show why variability of growth rate-biomass stoichiometry relationships is lower under P limitation than under N or C limitation. These theoretical results are supported by experimental data on macromolecular composition (RNA, DNA, and protein) and biomass stoichiometry from two different bacteria. In addition, compared to a model with strictly homeostatic biomass, the optimization mechanism we suggest results in increased microbial N and P mineralization during organic-matter decomposition. Therefore, this mechanism may also have important implications for our understanding of nutrient cycling in ecosystems.     

刨花楠不同相对生长速率下林木叶片碳氮磷的适应特征

分别对9年生与13年生刨花楠林木叶片氮磷养分之间关系及林木生物量相对生长速率与叶片碳氮磷化学计量比关系进行分析,探讨不同相对生长速率下的林木叶片N、P养分适应特征,并检验相对生长速率假说理论对刨花楠树种的适应性。结果表明:两种年龄刨花楠林木生物量相对生长速率、叶片C、N、P含量及其计量比值均存在显著差异;同一年龄的林木叶片N、P之间存在显著相关性,二者具有协同相关性;9年生林木叶片P含量及C∶P、N∶P与生物量相对生长速率呈二次曲线相关,而13年生林木叶片N、P含量及C∶N、C∶P、N∶P则与生物量相对生长速率均呈线性相关。研究表明,在能满足植物生长所需养分供给的土壤环境中,叶片N、P含量与林木相对生长速率间呈线性正相关,但当土壤中养分供应满足不了植物高速生长时,植物则会对有限的养分资源进行适应性调整。     

Growth rate hypothesis and efficiency of protein synthesis under different sulphate concentrations in two green algae

The growth rate hypothesis (GRH) predicts a positive correlation between growth rate and RNA content because growth depends upon the protein synthesis machinery. The application of this hypothesis to photoautotrophic organisms has been questioned. We tested the GRH on one prasinophycean, Tetraselmis suecica, and one chlorophycean, Dunaliella salina, grown at three sulphate concentrations. Sulphate was chosen because its concentration in the oceans increased through geological time and apparently had a role in the evolutionary trajectories of phytoplankton. Cell protein content and P quota were positively related to the RNA content (r = 0.62 and r = 0.74, respectively). The correlation of the RNA content with growth rates (r = 0.95) indicates that the GRH was valid for these species when growth rates were below 0.82 d^?1.     

IS THE GROWTH RATE HYPOTHESIS APPLICABLE TO MICROALGAE?1

The growth rate hypothesis (GRH) asserts, from known biochemistry, that maintaining high growth rates requires high concentrations of ribosomes. Since ribosomes are rich in phosphorus (P), the GRH predicts a positive correlation between growth rate and P content; this correlation is observed in some organisms. We consider the application of the GRH to phytoplankton and identify several key problems that require further research before the hypothesis can be accepted for these organisms. There are severe methodological problems that confound interpretation of data for testing the GRH. These problems include the measurement of protein and nucleic acids (such that ratio of these components carries a high level of uncertainty), studies of steady‐state versus dynamic systems, and the presentation of data per cell (especially as cell size varies with growth rate limitations) and the calculation of growth rates. In addition, because of the short generation times and rapid responses of these organisms to perturbations, ribosome and RNA content is expected to vary in response to (de)repression of various systems; content may increase on application of growth‐limiting stress. Finally, that most phytoplankton accumulate P when not P stressed conflicts with the GRH. In consequence, the value of the GRH for any sort of predictive role in nature appears to be severely limited. We conclude that the GRH cannot be assumed to apply to phytoplankton taxa without first performing experimental tests under transient conditions.     

Phenotypic plasticity and biogeographic variation in physiology of habitat‐forming seaweed: response to temperature and nitrate

Southeastern Australian waters are warming at nearly four times the global average rate (~0.7°C · century^?1) driven by strengthening incursions of the warm oligotrophic East Australian Current. The growth rate hypothesis (GRH) predicts that nutrient depletion will impact more severely on seaweeds at high latitudes with compressed growth seasons. This study investigates the effects of temperature and nutrients on the ecophysiology of the habitat‐forming seaweed Phyllospora comosa in a laboratory experiment using temperature (12°C, 17°C, 22°C) and nutrient (0.5, 1.0, 3.0 μM NO₃^?) scenarios representative of observed variation among geographic regions. Changes in growth, photosynthetic characteristics (via chlorophyll fluorescence), pigment content, tissue chemistry (δ¹³C, % C, % N, C:N) and nucleic acid characteristics (absolute RNA and DNA, RNA:DNA ratios) were determined in seaweeds derived from cool, high‐latitude and warm, low‐latitude portions of the species’ range. Performance of P. comosa was unaffected by nitrate availability but was strongly temperature‐dependent, with photosynthetic efficiency, growth, and survival significantly impaired at 22°C. While some physiological processes (photosynthesis, nucleic acid, and accessory pigment synthesis) responded rapidly to temperature, others (C/N dynamics, carbon concentrating processes) were largely invariant and biogeographic variation in these characteristics may only occur through genetic adaptation. No link was detected between nutrient availability, RNA synthesis and growth, and the GRH was not supported in this species. While P. comosa at high latitudes may be less susceptible to oligotrophy than predicted by the GRH, warming water temperatures will have deleterious effects on this species across its range unless rapid adaptation is possible.     

C: N: P stoichiometry and specific growth rate of clover colonized by arbuscular mycorrhizal fungi

Ecological stoichiometry has been widely applied in aquatic ecosystems, but has limited implications in terrestrial ecosystems. The pot experiments with Trifolium repens L. were conducted to demonstrate the relations between C: N: P, biological components and growth rate of clover colonized by arbuscular mycorrhizal (AM) fungi. The results showed that for mycorrhizal clover, N, P concentrations increased with increasing growth rate, in support of the Growth Rate Hypothesis (GRH). Mycorrhizal clover had higher P and RNA concentrations than non-mycorrhizal clover, indicating that the increase in P concentration would invest more RNA to meet the synthesis of protein. Results also indicated that the increase in N concentration with rapid growth rate may be attributed to the increase in the concentration of protein N. Underlying mechanisms driving the association of C: N: P with growth rate for symbiotic partners should help elucidate the allocation of major nutrients to cellular organs and trophic dynamics in terrestrial ecosystems.     

Testing the growth rate hypothesis in vascular plants with above- and below-ground biomass

The growth rate hypothesis (GRH) proposes that higher growth rate (the rate of change in biomass per unit biomass, μ) is associated with higher P concentration and lower C:P and N:P ratios. However, the applicability of the GRH to vascular plants is not well-studied and few studies have been done on belowground biomass. Here we showed that, for aboveground, belowground and total biomass of three study species, μ was positively correlated with N:C under N limitation and positively correlated with P:C under P limitation. However, the N:P ratio was a unimodal function of μ, increasing for small values of μ, reaching a maximum, and then decreasing. The range of variations in μ was positively correlated with variation in C:N:P stoichiometry. Furthermore, μ and C:N:P ranges for aboveground biomass were negatively correlated with those for belowground. Our results confirm the well-known association of growth rate with tissue concentration of the limiting nutrient and provide empirical support for recent theoretical formulations.     

N、P施肥对塔里木河上游绿洲棉花C、N、P生态化学计量特征的影响

施肥通过外源物质的添加直接干预了农田生态系统中作物元素的运移循环过程。通过野外N、P施肥试验,测定棉花各生育期碳(C)、氮(N)、磷(P)元素含量及其生物量,分析棉株C、N、P元素的分配规律,探讨棉株对生长速率调控的内在机制,获得棉株体内N、P元素的内稳性指数,并判断其限制性元素类型。结果表明:棉花C、N、P元素平均含量分别为388.7、20.97、3.43 g/kg;棉花比生长速率与N∶P、C∶P间均存在负相关关系,棉花生长符合生长速率假说;N、P元素内稳性指数H分别在1.02—5.28、1.01—4.55范围内。叶片N∶P可表征植物限制性元素类型,棉花最大生长速率所对应的叶片N∶P为13,是判断限制元素的标准;综合棉花生长速率和内稳性指数研究可知研究区棉花生长受到N、P元素的共同限制,同时,在生长前期更易受P元素的限制,生长后期更易受N元素的限制。     

氮磷施肥对拟南芥叶片碳氮磷化学计量特征的影响

研究植物碳(C)氮(N)磷(P)化学计量特征, 有助于了解C、N、P元素的分配规律和确定限制植物生长的元素类型, 理解生长速率调控的内在机制。该研究基于盆栽施肥试验, 测定不同N、P供应水平下拟南芥(Arabidopsis thaliana)叶片的生物量和C、N、P含量, 分析拟南芥的限制元素类型、验证生长速率假说、探讨N、P的内稳性差异和C、N、P元素间的异速生长关系。主要结果如下: 盆栽试验基质中限制元素是P, 施N过多可能引起毒害作用; 拟南芥的生长符合生长速率假说, 即随着叶片N:P和C:P的增加, 比生长速率显著减小; 叶片P含量存在显著的调整系数(3.5), 但叶片N含量与基质N含量之间无显著相关; 叶片N和P含量具有显著的异速生长关系, 但不符合N-P^3/4关系, 施P肥导致表征N、P异速生长关系的幂指数(0.209)显著低于施N肥处理(0.466)。该研究首次基于温室培养实验分析了拟南芥C、N、P的化学计量特征及其对N、P添加的响应, 研究结果将为野外研究不同物种、群落或生态系统的化学计量特征提供参考。     

温度对4种大型海藻氮磷吸收效率及光合生理特性的影响

研究以裂片石莼(Ulva fasciata)、肠浒苔(Ulva intestinalis)、龙须菜(Gracilaria lemaneaformis)、坛紫菜(Pyropia haitanensis)为实验材料, 分析了不同温度(15、20、25、30℃)下4种大型海藻对海水中N、P元素的吸收效率和光合特性的特点。结果显示: (1)4种大型海藻对水体N、P均有明显的吸收效果, 吸收能力高低依次为肠浒苔>裂片石莼>坛紫菜>龙须菜; (2)温度过高或过低都会限制藻类对N、P的吸收和正常生长, 同时降低4种藻的相对电子传递速率及光化学效率; (3)裂片石莼与肠浒苔的N、P吸收能力强, 且光合系统对温度耐受性高, 是实施养殖污水生物净化的良好材料; (4)4种海藻对水体中N、P营养盐的吸收在48h内基本完成, 实地应用中可考虑24—48h周期换水或采用流通循环式的培养模式, 以达到既促进藻类的生长又提高营养盐吸收效率的目的, 以避免藻体因营养缺乏引起负生长而造成二次污染。     

Seasonal changes in situ grazing of the mesoherbivores Idotea baltica and Gammarus oceanicus on the brown algae Fucus vesiculosus and Pylaiella littoralis in the central Gulf of Finland, Baltic Sea

The in situ grazing experiments were performed in the shallow water rocky habitat of the northern Baltic Sea during ice-free season 2002. In the experiments the effects of algal species and choice on the grazing of the mesoherbivores Idotea baltica (Pallas) and Gammarus oceanicus Segerstråle were tested. Salinity, temperature, concentration of nutrients in water and macroalgae and net production of macroalgae were considered as random effects in the analysis. The invertebrate feeding rate was mainly a function of the net photosynthetic activity of Pylaiella littoralis (L.) Kjellman and Fucus vesiculosus L. Feeding rate increased significantly with decreasing algal photosynthetic activity. When the two algal species were incubated together invertebrates fed primarily on P. littoralis. Low selectivity towards P. littoralis coincided with its high photosynthetic activity. The presence of F. vesiculosus did not modify the invertebrate feeding on P. littoralis. The results indicated that (1) the grazing on F. vesiculosus depended on the availability of P. littoralis, (2) the photosynthetic activity of algae explained the best the variation in grazing rate and (3) the grazers are not likely to control the early outbreak of filamentous algae in the northern Baltic Sea by avoiding young and photosynthetically active algae. The likely mechanism behind the relationship is that the increased photosynthetic activity of macroalgae coincides with their higher resistance to herbivory.     

Extending the growth rate hypothesis to species development: Can stoichiometric traits help to explain the composition of macroinvertebrate communities?

Ecological stoichiometry seeks to understand the ecological consequences of elemental imbalances between consumers and their resources. Therein, the well-accepted growth rate hypothesis (GRH) states that organisms exhibiting rapid growth have higher phosphorus (P) demand – and thus lower C:P and N:P ratios – than slow growing ones, due to a higher allocation to P-rich rRNA. However, GRH has rarely been extended to other biological traits than growth, especially at the community level. In this study, we investigated whether macroinvertebrate stoichiometric traits (e.g. C:P and N:P ratios) can be linked to their development traits, and whether these stoichiometric traits are related to macroinvertebrate community assemblage under different nutrient conditions. We allocated more than 400 European taxa to different groups, defined using available information about three development-related traits: ‘life span', ‘voltinism' and ‘number of reproductive cycles per individual'. We sampled 18 invertebrate taxa in six streams exhibiting different levels of nutrient concentration and measured their stoichiometric traits. Further, we quantified invertebrate taxon abundances in these streams during an annual survey. Based on these data, we tested whether community composition regarding the developmental groups differs, depending on nutrient concentration. We found significant differences in the proportions of the developmental groups along a gradient of water N:P, in relation to their stoichiometric traits. Taxa with low C:P and N:P ratios were generally associated with faster development groups, and these taxa tended to occur at higher proportions in streams exhibiting low dissolved N:P ratios. In contrast, communities from P-poor, high dissolved N:P streams, were dominated by slowly developing taxa with high N:P ratios. Our results highlight that extending the GRH to species development rate might give some insights about the mechanisms by which nutrient concentrations in ecosystems influence consumers' community composition.     

N : P stoichiometry and protein : RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis

The growth-rate hypothesis states that fast-growing organisms need relatively more phosphorus-rich RNA to support rapid rates of protein synthesis, and therefore predicts, within and among taxa, increases in RNA and phosphorus content (relative to protein and nitrogen content) with increased growth rate. Here, we present a test of this hypothesis in vascular plants. We determined nitrogen : phosphorus ratios and protein : RNA ratios in pines growing at different rates due to nutrient conditions. In general, when comparing leaves of the same species at low and high growth rates, the faster-growing plants had higher RNA content, higher %N and %P, and lower protein : RNA ratios, but not consistently lower N : P ratios. We found no link between growth rate and foliar N : P or protein : RNA when comparing multiple species of different inherent growth rates. We conclude that plants adjust the balance of protein and RNA to favour either speed or efficiency of protein synthesis, but this balance does not alone dictate leaf stoichiometry.     

Testing the growth rate and translation compensation hypotheses in marine bacterioplankton

Two different hypotheses have been raised as to how temperature affects resource allocation in microorganisms. The translation-compensation hypothesis (TCH) predicts that the increase in enzymatic efficiency with temperature results in fewer required ribosomes per cell and lower RNA:protein ratio. In contrast, the growth rate hypothesis (GRH) predicts that increasing the growth rate with temperature requires more ribosomes and hence a higher cellular RNA:protein. We tested these two hypotheses in laboratory cultures of Prochlorococcus and Alteromonas as well as over an annual cycle in the Eastern Mediterranean Sea. The RNA:protein of Alteromonas mostly decreased with temperature in accordance with the TCH, while that of Prochlorococcus increased with temperature, as predicted by the GRH. No support was found for either hypothesis in surface waters from the Eastern Mediterranean, whereas the fraction of phosphorus in RNA was positively correlated with per-cell bacterial production in the deep chlorophyll maximum, supporting the GRH in this niche. A considerable part of the cellular phosphorus was not allocated to RNA, DNA, phospholipids or polyphosphate, raising the question which cellular molecules contain these P reserves. While macromolecular quotas differed significantly between laboratory cultures and field samples, these were connected through a power law, suggesting common rules of resource allocation.     

Responses of leaf C:N:P stoichiometry to water supply in the desert shrub Zygophyllum xanthoxylum

• Based on the elemental composition of major biochemical molecules associated with different biological functions, the ‘growth rate hypothesis’ proposed that organisms with a higher growth rate would be coupled to lower C:N, especially lower C:P and N:P ratios. However, the applicability of the growth rate hypothesis for plants is unclear, especially for shrubs growing under different water supply.
• We performed an experiment with eight soil moisture levels (soil water content: 4%, 6%, 8%, 13%, 18%, 23%, 26% and 28%) to evaluate the effects of water availability on leaf C:N:P stoichiometry in the shrub Zygophyllum xanthoxylum.
• We found that leaves grew slowly and favored accumulation of P over C and N under both high and low water supply. Thus, leaf C:P and N:P ratios were unimodally related to soil water content, in parallel with individual leaf area and mass. As a result, there were significant positive correlations between leaf C:P and N:P with leaf growth (u).
• Our result that slower‐growing leaves had lower C:P and N:P ratios does not support the growth rate hypothesis, which predicted a negative association of N:P ratio with growth rate, but it is consistent with recent theoretical derivations of growth–stoichiometry relations in plants, where N:P ratio is predicted to increase with increasing growth for very low growth rates, suggesting leaf growth limitation by C and N rather than P for drought and water saturation.

     

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.