When microbes and consumers determine the limiting nutrient of autotrophs: a theoretical analysis

Ecological stoichiometry postulates that differential nutrient recycling of elements such as nitrogen and phosphorus by consumers can shift the element that limits plant growth. However, this hypothesis has so far considered the effect of consumers, mostly herbivores, out of their food-web context. Microbial decomposers are important components of food webs, and might prove as important as consumers in changing the availability of elements for plants. In this theoretical study, we investigate how decomposers determine the nutrient that limits plants, both by feeding on nutrients and organic carbon released by plants and consumers, and by being fed upon by omnivorous consumers. We show that decomposers can greatly alter the relative availability of nutrients for plants. The type of limiting nutrient promoted by decomposers depends on their own elemental composition and, when applicable, on their ingestion by consumers. Our results highlight the limitations of previous stoichiometric theories of plant nutrient limitation control, which often ignored trophic levels other than plants and herbivores. They also suggest that detrital chains play an important role in determining plant nutrient limitation in many ecosystems.     

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.     

浮游动物化学计量学稳态性特征研究进展

稳态性是有机体的基本属性,也是生态化学计量学理论成立的前提和基础。一般来讲,浮游植物的元素组成变化较大,而浮游动物具有明显的稳态性特征。浮游动物稳态性特征的研究不仅有助于了解水生生态系统的能量流动和物质循环,同时也对研究营养元素如何调节生物生长、繁殖和代谢起到促进作用。在综述生态化学计量学研究的基础上,主要介绍了稳态性的概念和浮游动物稳态性特征的基本框架及变化规律,以期为促进国内相关研究工作的开展提供参考。     

Consequences of inferring diet from feeding guilds when estimating and interpreting consumer–resource stoichiometry

相似文献   

Elemental composition and degree of homeostasis of fungi: are aquatic hyphomycetes more like metazoans,bacteria or plants?

Ecological stoichiometry generally assumes that heterotrophs have a higher degree of elemental homeostasis than autotrophs. Differences between fixed consumer nutrient requirements and nutrients available in resources allow prediction of the intensity of nutrient recycling ensured by heterotrophs. Despite their fundamental role in detritus decomposition, extremely few data are currently available on fungal elemental composition. In this study, we quantified the degree of elemental homeostasis of aquatic hyphomycetes used as model organisms. Contrary to metazoans, but similar to plants, aquatic hyphomycetes exhibited highly plastic elemental compositions. Mycelium also reached far higher C/nutrient ratios than reported for bacteria. Our results suggest that non-homeostasis of fungi should be explicitly included in stoichiometric models dealing with nutrient recycling, and that the discrepancy in homeostasis between some bacterial strains and fungi should certainly be considered when investigating interactions between both groups of decomposers.     

Spatial stoichiometry: cross‐ecosystem material flows and their impact on recipient ecosystems and organisms

Cross‐ecosystem material flows, in the form of inorganic nutrients, detritus and organisms, spatially connect ecosystems and impact food web dynamics. To date research on material flows has focused on the impact of the quantity of these flows and largely ignored their elemental composition, or quality. However, the ratios of elements like carbon, nitrogen and phosphorus can influence the impact material flows have on food web interactions through stoichiometric mismatches between resources and consumers. The type and movement of materials likely vary in their ability to change stoichiometric constraints within the recipient ecosystem and materials may undergo changes in their own stoichiometry during transport. In this literature review we evaluate the importance of cross‐ecosystem material flows within the framework of ecological stoichiometry. We explore how movement in space and time impacts the stoichiometry of material flow, as these transformations are essential to consider when assessing the ability of these flows to impact food web productivity and ecosystem functioning. Our review suggests that stoichiometry of cross‐ecosystem material flows are highly dynamic and undergo changes during transport across the landscape or from human influence. These material flows can impact recipient organisms if they change stoichiometry of the abiotic medium, or provide resources that have a different stoichiometry to in situ resources. They might also alter consumer excretion rates, in turn altering the availability of nutrients in the recipient ecosystem. These alterations in stoichiometric constraints of recipient organisms can have cascading trophic effects and shape food web dynamics. We highlight significant gaps in the literature and suggest new avenues for research that explore how cross‐ecosystem material flows impact recipient ecosystems when considering differences in stoichiometric quality, their movement through the landscape and across ecosystem boundaries, and the nutritional constraints of the recipient organisms.     

Correlates of elemental‐isotopic composition of stream fishes: the importance of land‐use,species identity and body size

The isotopic (δ¹³C and δ¹⁵N) and stoichiometric (C:N:P) compositions of four fish species (Family Centrarchidae: Lepomis auritus, Lepomis cyanellus; Family Cyprinidae: Nocomis leptocephalus, Semotilus atromaculatus) were examined across four North Carolina Piedmont streams arrayed along an urbanization gradient. Both isotopic and stoichiometric composition of fishes appeared to track changes occurring in basal resource availability. Values of δ¹³C of basal resources and consumers were more enriched at the most urbanized streams. Similarly, basal resources and consumers were δ¹⁵N–enriched at more urbanized streams. Basal resource stoichiometry varied across streams, with periphyton being the most variable. Primary consumers stoichiometry also differed across streams. Intraspecific variation in fish stoichiometry correlated with the degree of urbanization, as the two cyprinids had higher N content and L. cyanellus had higher P content in more urbanized streams, probably due to enrichment of basal resources. Intrinsic factors, specifically species identity and body size also affected stoichiometric variation. Phosphorus (P) content increased significantly with body size in centrarchids, but not in cyprinids. These results suggest that although species identity and body size are important predictors of elemental stoichiometry, the complex nature of altered urban streams may yield imbalances in the elemental composition of consumers via their food resources.     

Testing the ecological consequences of evolutionary change using elements

Understanding the ecological consequences of evolutionary change is a central challenge in contemporary biology. We propose a framework based on the ~25 elements represented in biology, which can serve as a conduit for a general exploration of poorly understood evolution‐to‐ecology links. In this framework, known as ecological stoichiometry, the quantity of elements in the inorganic realm is a fundamental environment, while the flow of elements from the abiotic to the biotic realm is due to the action of genomes, with the unused elements excreted back into the inorganic realm affecting ecological processes at higher levels of organization. Ecological stoichiometry purposefully assumes distinct elemental composition of species, enabling powerful predictions about the ecological functions of species. However, this assumption results in a simplified view of the evolutionary mechanisms underlying diversification in the elemental composition of species. Recent research indicates substantial intraspecific variation in elemental composition and associated ecological functions such as nutrient excretion. We posit that attention to intraspecific variation in elemental composition will facilitate a synthesis of stoichiometric information in light of population genetics theory for a rigorous exploration of the ecological consequences of evolutionary change.     

Variation in Detrital Resource Stoichiometry Signals Differential Carbon to Nutrient Limitation for Stream Consumers Across Biomes

Stoichiometric ratios of resources and consumers have been used to predict nutrient limitation across diverse terrestrial and aquatic ecosystems. In forested headwater streams, coarse and fine benthic organic matter (CBOM, FBOM) are primary basal resources for the food web, and the distribution and quality of these organic matter resources may therefore influence patterns of secondary production and nutrient cycling within stream networks or among biomes. We measured carbon (C), nitrogen (N), and phosphorus (P) content of CBOM and FBOM and calculated their stoichiometric ratios (C/N, C/P, N/P) from first- to fourth-order streams from tropical montane, temperate deciduous, and boreal forests, and tallgrass prairie, to compare the magnitude and variability of these resource types among biomes. We then used the ratios to predict nutritional limitations for consumers of each resource type. Across biomes, CBOM had consistently higher %C and %N, and higher and more variable C/N and C/P than FBOM, suggesting that microbial processing results in more tightly constrained elemental composition in FBOM than in CBOM. Biome-specific differences were observed in %P and N/P between the two resource pools; CBOM was lower in %P but higher in N/P than FBOM in the tropical montane and temperate deciduous forest biomes, while CBOM was higher in %P but similar in N/P than FBOM in the grassland and boreal forest biomes. Stable ¹³C isotopes suggest that FBOM likely derives from CBOM in tropical and temperate deciduous forest, but that additional non-detrital components may contribute to FBOM in boreal forests and grasslands. Comparisons of stoichiometric ratios of CBOM and FBOM to estimated needs of aquatic detritivores suggest that shredders feeding on CBOM are more likely to experience nutrient (N and/or P) than C limitation, whereas collector–gatherers consuming FBOM are more likely to experience C than N and/or P limitation. Our results suggest that differences in basal resource elemental content and stoichiometric ratios have the potential to affect consumer production and ecosystem rates of C, N, and P cycling in relatively consistent ways across diverse biomes.     

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.     

Genotypic differences in phosphorus use physiology in producers (<Emphasis Type="Italic">Chlamydomonas reinhardtii</Emphasis>) and consumers (<Emphasis Type="Italic">Daphnia pulex</Emphasis>) interact to alter primary and secondary production

By considering the relative abundance of elements in trophic interactions, ecological stoichiometry makes predictions about key ecological processes such as biomass production and consumer-driven nutrient recycling. Theoretical and empirical work has focused on interspecific variation in elemental composition, and stoichiometric imbalances between resources and consumers in determining productivity, particularly at the base of foodwebs. Recent work has found considerable intraspecific variation in elemental composition. We know little about the ecological relevance of such variation, and whether predictions of stoichiometric theory hold at the intraspecific level. Here, we used two genotypes of a primary producer Chlamydomonas reinhardtii, and two genotypes of a primary consumer Daphnia pulex, which are already known to vary considerably in their phosphorus (P) use physiology, under conditions of P abundance and limitation, to explore whether such intraspecific differences alter primary as well as secondary production. Specifically, we tested whether there are intraspecific differences in the carbon: phosphorus (C:P) stoichiometry of Chlamydomonas genotypes, whether such differences affect growth and abundance of the two Daphnia genotypes, and whether the two Daphnia genotypes had distinct effects on primary production and growth of the two Chlamydomonas genotypes. We found significant differences in C:P stoichiometry between the two Chlamydomonas genotypes in both P supply conditions. Such intraspecific differences altered the growth of Daphnia genotypes, and affected the outcome of genotypic competition. Finally, Daphnia genotype affected primary production, and interacted with P supply to distinctly affect the growth of the two Chlamydomonas genotypes. Together, our results highlight the potential ecological relevance of intraspecific differences in nutrient use physiology and elemental composition, and the utility of ecological stoichiometry in understanding such consequences.     

Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil

A soil community food web model was used to improve the understanding of what factors govern the mineralisation of nutrients and carbon and the decay of dead organic matter. The model derives the rates of C and N mineralisation by organisms by splitting their uptake rate of food resources into a rate at which faeces or prey remains are added to detritus, a rate at which elements are incorporated into biomass, and a rate at which elements are released by organisms as inorganic compounds. The functioning of soil organisms in the mineralisation of C and N was modelled in the soil horizon of a Scots pine forest. The organic horizon was divided into three distinct layers, representing successive stages of decay, i.e. litter, fragmented litter, and humus. Each of the layers had a different, quantitative, biota composition. For each layer the annual C and N mineralisation rates were simulated and compared to observed C and N mineralisation rates from organic matter in stratified litterbags. Simulated C and N mineralisation was relatively close to measured losses of C and N, but the fit was not perfect. Discrepancies between the observed and predicted mineralisation rates are discussed in terms of variation in model parameter values of those organisms that showed the highest contribution to mineralisation rates. The measured, and by the model predicted, significant decrease in mineralisation rates down the profile was not explained by the biomass of the primary decomposers and only partly by the total food web biomass. Modelling results indicated that indirect effects of soil fauna, due to trophic interactions with their resources, are an important explanatory factor. In addition, the analyses suggest that community food web structure is an important factor in the regulation of nutrient mineralisation. The model provided the means to evaluate the contribution of functionally defined groups of organisms, structured in a detrital food web, to losses of C and N from successive decay stages.     

Coexistence and community structure in a consumer resource model with implicit stoichiometry

We combine stoichiometry theory and optimal foraging theory into the MacArthur consumer-resource model. This generates predictions for diet choice, coexistence, and community structure of heterotroph communities. Tradeoffs in consumer resource-garnering traits influence community outcomes. With scarce resources, consumers forage opportunistically for complementary resources and may coexist via tradeoffs in resource encounter rates. In contrast to single currency models, stoichiometry permits multiple equilibria. These alternative stable states occur when tradeoffs in resource encounter rates are stronger than tradeoffs in elemental conversion efficiencies. With abundant resources consumers exhibit partially selective diets for essential resources and may coexist via tradeoffs in elemental conversion efficiencies. These results differ from single currency models, where adaptive diet selection is either opportunistic or selective. Interestingly, communities composed of efficient consumers share many of the same properties as communities based on substitutable resources. However, communities composed of relatively inefficient consumers behave similarly to plant communities as characterized by Tilman’s consumer resource theory. The results of our model indicate that the effects of stoichiometry theory on community ecology are dependent upon both consumer foraging behavior and the nature of resource garnering tradeoffs.     

Ecological Stoichiometry and Density Responses of Plant-Arthropod Communities on Cormorant Nesting Islands

Seabirds deposit large amounts of nutrient rich guano on their nesting islands. The increased nutrient availability strongly affects plants and consumers. Consumer response differs among taxonomic groups, but mechanisms causing these differences are poorly understood. Ecological stoichiometry might provide tools to understand these mechanisms. ES suggests that nutrient rich taxa are more likely to be nutrient limited than nutrient poorer taxa and are more favored under nutrient enrichment. Here, we quantified differences in the elemental composition of soil, plants, and consumers between islands with and without nesting cormorant colonies and tested predictions made based on ES by relating the elemental composition and the eventual mismatch between consumer and resource stoichiometry to observed density differences among the island categories. We found that nesting cormorants radically changed the soil nutrient content and thereby indirectly plant nutrient content and resource quality to herbivores. In contrast, consumers showed only small differences in their elemental composition among the island categories. While we cannot evaluate the cause of the apparent homeostasis of invertebrates without additional data, we can conclude that from the perspective of the next trophic level, there is no difference in diet quality (in terms of N and P content) between island categories. Thus, bottom-up effects seemed mainly be mediated via changes in resource quantity not quality. Despite a large potential trophic mismatch we were unable to observe any relation between the invertebrate stoichiometry and their density response to nesting cormorant colonies. We conclude that in our system stoichiometry is not a useful predictor of arthropod responses to variation in resource nutrient content. Furthermore, we found no strong evidence that resource quality was a prime determinant of invertebrate densities. Other factors like resource quantity, habitat structure and species interactions might be more important or masked stoichiometric effects.     

Intermediate-consumer identity and resources alter a food web with omnivory

1. Omnivory is an important interaction that has been the centre of numerous theoretical and empirical studies in recent years. Most of these studies examine the conditions necessary for coexistence between an omnivore and an intermediate consumer. Trait variation in ecological interactions (competition and predator tolerance) among intermediate consumers has not been considered in previous empirical studies despite the evidence that variation in species-specific traits can have important community-level effects. 2. I conducted a multifactorial microcosm experiment using species from the Sarracenia purpurea phytotelmata community, organisms that inhabit the water collected within its modified leaves. The basal trophic level consisted of bacterial decomposers, the second trophic level (intermediate consumers) consisted of protozoa and rotifers, and the third trophic level (omnivore) were larvae of the pitcher plant mosquito Wyeomyia smithii. Trophic level number (1, 2 and 3), resources (low and high), omnivore density (low and high) and intermediate consumer (monoculture of five protozoa and rotifers) identity were manipulated. Abundance of the basal trophic level, intermediate consumers, and growth of the omnivore were measured, as well as time to extinction (intermediate consumers) and time to pupation (mosquito larvae). 3. The presence of different intermediate consumers affected both bacteria abundance and omnivore growth. At high resource levels, Poteriochromonas, Colpidium and Habrotrocha rosa reduced bacteria densities greater than omnivore reduction of bacteria. Mosquito larvae did not pupate at low resource levels except when Poteriochromonas and Colopoda were present as intermediate consumers. Communities with H. rosa were the only ones consistent with the prediction that omnivores should exclude intermediate consumers at high resources. 4. These results had mixed support for predictions from omnivory food web theory. Intermediate consumers responded and affected this community differently under different community structures and resource levels. Consequently, variation in species-specific traits can have important population- and community-level effects and needs to be considered in food webs with omnivory.     

Stoichiometric distribution models: ecological stoichiometry at the landscape extent

Human activities are altering the fundamental geography of biogeochemicals. Yet we lack an understanding of how the spatial patterns in organismal stoichiometry affect biogeochemical processes and the tools to predict the impacts of global changes on biogeochemical processes. In this contribution we develop stoichiometric distribution models (StDMs), which allow us to map spatial structure in resource elemental composition across a landscape and evaluate spatial responses of consumers. We parameterise StDMs for a consumer‐resource (moose‐white birch) system and demonstrate that we can develop predictive models of resource stoichiometry across a landscape and that such models could improve our predictions of consumer space use. With results from our study system application, we argue that explicit consideration of the spatial patterns in organismal elemental composition may uncover emergent individual, population, community and ecosystem properties that are not revealed at the local extents routinely used in ecological stoichiometry. We discuss perspectives for further developments and application of StDMs to advance three emerging frameworks for spatial ecosystem ecology in an era of global change; meta‐ecosystem theory, macroecological stoichiometry and remotely sensed biogeochemistry. Progress on these emerging frameworks will allow for the integration of ecological stoichiometry and individual space use and fitness.     

To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs

Homeostasis of element composition is one of the central concepts of ecological stoichiometry. In this context, homeostasis is the resistance to change of consumer body composition in response to the chemical composition of consumer's food. To simplify theoretical analysis, it has generally been assumed that autotrophs exhibit flexibility in their composition, while heterotrophs are confined to a constant (strictly homeostatic) body composition. Yet, recent studies suggest that heterotrophs are not universally strictly homeostatic. We examined the degree to which autotrophs and heterotrophs regulate stoichiometric homeostasis (P:C, N:C, N:P, or %P and %N). We conducted a quantitative review and meta‐analysis using 132 datasets extracted from 57 literature sources which examined the dependence of organismal stoichiometry on resource stoichiometry. Among individual datasets, there was a wide range of responses from strictly homeostatic to non‐homeostatic. Even within heterotrophic organisms, varying levels of homeostasis were observed. Comparing the degree of homeostasis between organisms based on large‐scale habitat types using meta‐analysis indicated some significant differences between groups. For example, aquatic macroinvertebrates were significantly more homeostatic in terms of P:C than terrestrial invertebrates. Our meta‐analysis also confirmed that, with regard to N:P, heterotrophs are significantly more homeostatic than autotrophs. Furthermore, our analysis indicated that the homeostasis parameter 1/H, despite being a potentially useful predictive metric, has to be utilized with caution since it oversimplifies some important aspects of the responses of organisms to elemental imbalances. This critical evaluation of stoichiometric homeostasis contributes to a better understanding of many food‐web interactions, which are commonly driven by elemental imbalances between consumers and their resources.     

Light-induced mass turnover in a mono-species community of mixotrophs.

We formulate a simple model for growth of a facultative photoautotroph with chemoheterotrophic capabilities. The organism is described by zero, one or three reserve components, and one structural component, all taken to be generalized compounds. The rules of synthesizing units are used for interactions among the uptake processes of the various nutrients and light (parallel processing), and for the merging of autotrophic and heterotrophic activities (sequential processing). For simplicity, we focus on the assimilation of inorganic carbon, inorganic nitrogen and light, and of two organic compounds (dead reserves and dead structure) that originate from aging. The process of resource recycling in a closed environment, as driven by light, and its links with community's structure (amount of biomass) is analysed in this simplest of all communities. Explicit analytical expressions for the steady states show how structure and function depend on the system parameters light, total carbon and total nitrogen. The behaviour resembles the Monod model for the Canonical Community, a three-species ecosystem consisting of producers, consumers and decomposers. If trophic preferences of a mixotroph are allowed to follow a random walk across generations, a trophic structure evolves where mixotrophs coexist with auto- and heterotrophs. Depth profiles are presented for the implied steady-state concentrations of dissolved inorganic carbon and nitrogen.     

Predicting availability to consumers of spatially and temporally variable resources

Ecological dynamics in many aquatic communities are strongly influenced by spatial and temporal variability of key limiting resources, and the extent to which consumers can locate and exploit concentrations of those resources. Intuitively, resource concentrations that are `close' and `long-lived' should typically be more available to consumers than `distant' and `ephemeral' resource concentrations. The speed and accuracy with which consumers can locate concentrations of their resources is in part determined by their movement characteristics and sensory constraints, which vary with taxon, life-history stage, physiological state, environmental conditions, and other factors. This has motivated detailed observation and modelling of individual-level foraging behaviors in a wide variety of taxa. However, our abilities to develop this intuitive concept of availability into empirically-based, quantitative predictions for consumer–resource interactions remain limited, largely due to the complexities of formulating and simulating spatially explicit models of consumer–resource interactions, and the difficulty of understanding how specific simulation results relate to broader ecological situations. This paper presents a non-dimensional index, the Frost number, that provides a simple prediction of availability to consumers of spatially and temporally varying resource concentrations. This index incorporates characteristics of both resource distributions and consumer movement behaviors. When Frost numbers characterizing consumer–resource interactions are much less than unity, resource concentrations are typically unavailable to consumers because travel time to reach them exceeds the longevity of the resource. Conversely, when Frost numbers are much greater than unity, resource longevity exceeds travel time so that resource concentrations are available. The Frost number may provide a preliminary identification of the length and time scales at which resources are available to consumers in complex ecological systems, even when detailed spatial observations and simulations are not available.