Applying stable isotopes to examine food‐web structure: an overview of analytical tools

Stable isotope analysis has emerged as one of the primary means for examining the structure and dynamics of food webs, and numerous analytical approaches are now commonly used in the field. Techniques range from simple, qualitative inferences based on the isotopic niche, to Bayesian mixing models that can be used to characterize food‐web structure at multiple hierarchical levels. We provide a comprehensive review of these techniques, and thus a single reference source to help identify the most useful approaches to apply to a given data set. We structure the review around four general questions: (1) what is the trophic position of an organism in a food web?; (2) which resource pools support consumers?; (3) what additional information does relative position of consumers in isotopic space reveal about food‐web structure?; and (4) what is the degree of trophic variability at the intrapopulation level? For each general question, we detail different approaches that have been applied, discussing the strengths and weaknesses of each. We conclude with a set of suggestions that transcend individual analytical approaches, and provide guidance for future applications in the field.     

Linking Water Quality and Quantity in Environmental Flow Assessment in Deteriorated Ecosystems: A Food Web View

Most rivers worldwide are highly regulated by anthropogenic activities through flow regulation and water pollution. Environmental flow regulation is used to reduce the effects of anthropogenic activities on aquatic ecosystems. Formulating flow alteration–ecological response relationships is a key factor in environmental flow assessment. Traditional environmental flow models are characterized by natural relationships between flow regimes and ecosystem factors. However, food webs are often altered from natural states, which disturb environmental flow assessment in such ecosystems. In ecosystems deteriorated by heavy anthropogenic activities, the effects of environmental flow regulation on species are difficult to assess with current modeling approaches. Environmental flow management compels the development of tools that link flow regimes and food webs in an ecosystem. Food web approaches are more suitable for the task because they are more adaptive for disordered multiple species in a food web deteriorated by anthropogenic activities. This paper presents a global method of environmental flow assessment in deteriorated aquatic ecosystems. Linkages between flow regimes and food web dynamics are modeled by incorporating multiple species into an ecosystem to explore ecosystem-based environmental flow management. The approach allows scientists and water resources managers to analyze environmental flows in deteriorated ecosystems in an ecosystem-based way.     

农田土壤食物网管理的原理与方法

土壤食物网在维持生态系统生产力和健康等方面起着重要作用,但现代农业中,化肥农药等外部投入已经改变或部分替代了土壤食物网的功能,由此也造成一系列的环境问题。为了协调作物高产与环境保护的利益,需要对土壤食物网进行管理,使土壤食物网符合作物生长的需要,即建立健康土壤食物网。管理土壤食物网有两种方式:(1)直接方式,即通过调节食物网各个功能群的组成来管理土壤食物网;(2)间接方式,即根据农田土壤食物网以自下而上调控方式为主、强调低营养阶层的资源限制的原理,通过调节碎屑的数量和质量来管理食物网。在这两种调控方式中,都需要对被管理的食物网进行监测,监测的方式也分两种,一种是直接测定食物网各功能群的数量和生物量,另外一种方式即以线虫为工具来反应土壤食物网的结构。     

Adaptive foraging does not always lead to more complex food webs

Recent modeling studies exploring the effect of consumers’ adaptivity in diet composition on food web complexity invariably suggest that adaptivity in foraging decisions of consumers makes food webs more complex. That is, it allows for survival of a higher number of species when compared with non-adaptive food webs. Population-dynamical models in these studies share two features: parameters are chosen uniformly for all species, i.e. they are species-independent, and adaptive foraging is described by the search image model. In this article, we relax both these assumptions. Specifically, we allow parameters to vary among the species and consider the diet choice model as an alternative model of adaptive foraging. Our analysis leads to three important predictions. First, for species-independent parameter values for which the search image model demonstrates a significant effect of adaptive foraging on food web complexity, the diet choice model produces no such effect. Second, the effect of adaptive foraging through the search image model attenuates when parameter values cease to be species-independent. Finally, for the diet choice model we observe no (significant) effect of adaptive foraging on food web complexity. All these observations suggest that adaptive foraging does not always lead to more complex food webs. As a corollary, future studies of food web dynamics should pay careful attention to the choice of type of adaptive foraging model as well as of parameter values.     

食物网结构与功能: 理论进展与展望

食物网刻画了物种间通过捕食而形成的复杂网络关系。阐明食物网结构与功能之间的关系, 既是生态学的基本理论问题, 也是预测全球变化背景下生态系统响应的重要依据。早期关于食物网结构与功能的研究往往是分离的, 或是基于食物链等的简单网络模型, 而近期研究基于复杂食物网模型取得了重要理论进展。本文综述了食物网研究的理论方法和近期进展, 特别介绍了复杂食物网中的结构、多样性和功能的度量指标、结构-多样性-功能之间的关系以及全球变化对食物网结构与功能的影响。本文最后对未来的一些研究方向进行了展望, 包括与功能性状和化学计量学的整合、食物网与其他网络类型的整合以及拓展食物网研究的空间和时间尺度。     

Quantifying the relative importance of variation in predation and the environment for species coexistence

Coexistence and food web theory are two cornerstones of the long‐standing effort to understand how species coexist. Although competition and predation are known to act simultaneously in communities, theory and empirical study of these processes continue to be developed largely independently. Here, we integrate modern coexistence theory and food web theory to simultaneously quantify the relative importance of predation and environmental fluctuations for species coexistence. We first examine coexistence in a theoretical, multitrophic model, adding complexity to the food web using machine learning approaches. We then apply our framework to a stochastic model of the rocky intertidal food web, partitioning empirical coexistence dynamics. We find the main effects of both environmental fluctuations and variation in predator abundances contribute substantially to species coexistence. Unexpectedly, their interaction tends to destabilise coexistence, leading to new insights about the role of bottom‐up vs. top‐down forces in both theory and the rocky intertidal ecosystem.     

全球变化对食物网结构影响机制的研究进展

食物网主要依靠基于不同营养级间物种互作形成的上行与下行调控维持其结构。全球变化能够改变种间关系, 威胁生物多样性的维持, 然而目前对全球变化改变食物网结构的机制仍处于探索阶段。近年来通过大时空格局与多营养级食物网研究, 发现全球变化的作用机制主要可归结为3种: 物候错配、关键种丧失与生物入侵。该文聚焦于这3种机制, 综述各种机制造成的食物网结构变化并探讨相关的进化与生态驱动因素。三种干扰机制均通过改变原有种间关系, 影响食物网调控, 改变食物网结构。不同的是, 物候错配造成的种间关系变化是由于不同物种的物候对全球变化产生非同步响应所致; 关键种丧失则使营养级间取食/捕食关系发生变化甚至缺失; 而入侵物种通过竞争排除同营养级物种改变种间关系。最后, 该文提出食物网结构变化的实质是物种是否能够适应快速变化的生态环境, 并据此展望未来研究方向。随着全球变化影响日益加剧, 急需继续深入探索导致全球变化下食物网结构改变的机制, 为制定合理的生物多样性保护与生态修复规划提供重要理论支撑。     

Exogenous carbon turnover within the soil food web strengthens soil carbon sequestration through microbial necromass accumulation

Exogenous carbon turnover within soil food web is important in determining the trade-offs between soil organic carbon (SOC) storage and carbon emission. However, it remains largely unknown how soil food web influences carbon sequestration through mediating the dual roles of microbes as decomposers and contributors, hindering our ability to develop policies for soil carbon management. Here, we conducted a ¹³C-labeled straw experiment to demonstrate how soil food web regulated the residing microbes to influence the soil carbon transformation and stabilization process after 11 years of no-tillage. Our work demonstrated that soil fauna, as a “temporary storage container,” indirectly influenced the SOC transformation processes and mediated the SOC sequestration through feeding on soil microbes. Soil biota communities acted as both drivers of and contributors to SOC cycling, with 32.0% of exogenous carbon being stabilizing in the form of microbial necromass as “new” carbon. Additionally, the proportion of mineral-associated organic carbon and particulate organic carbon showed that the “renewal effect” driven by the soil food web promoted the SOC to be more stable. Our study clearly illustrated that soil food web regulated the turnover of exogenous carbon inputs by and mediated soil carbon sequestration through microbial necromass accumulation.     

Exploring the temporal variability of a food web using long‐term biomonitoring data

Ecological communities are constantly being reshaped in the face of environmental change and anthropogenic pressures. Yet, how food webs change over time remains poorly understood. Food web science is characterized by a trade‐off between complexity (in terms of the number of species and feeding links) and dynamics. Topological analysis can use complex, highly resolved empirical food web models to explore the architecture of feeding interactions but is limited to a static view, whereas ecosystem models can be dynamic but use highly aggregated food webs. Here, we explore the temporal dynamics of a highly resolved empirical food web over a time period of 18 years, using the German Bight fish and benthic epifauna community as our case study. We relied on long‐term monitoring ecosystem surveys (from 1998 to 2015) to build a metaweb, i.e. the meta food web containing all species recorded over the time span of our study. We then combined time series of species abundances with topological network analysis to construct annual food web snapshots. We developed a new approach, ‘node‐weighted’ food web metrics by including species abundances to represent the temporal dynamics of food web structure, focusing on generality and vulnerability. Our results suggest that structural food web properties change through time; however, binary food web structural properties may not be as temporally variable as the underlying changes in species composition. Further, the node‐weighted metrics enabled us to detect that food web structure was influenced by changes in species composition during the first half of the time series and more strongly by changes in species dominance during the second half. Our results demonstrate how ecosystem surveys can be used to monitor temporal changes in food web structure, which are important ecosystem indicators for building marine management and conservation plans.     

Complexity and structural properties of food webs in the Barents Sea

A food web topology describes the diversity of species and their trophic interactions, i.e. who eats whom, and structural analysis of food web topologies can provide insight into ecosystem structure and function. It appears simple, at first sight, to list all species and their trophic interactions. However, the very large number of species at low trophic levels and the impossibility to monitor all trophic interactions in the ocean makes it impossible to construct complete food web topologies. In practice, food web topologies are simplified by aggregating species into groups termed trophospecies. It is not clear though, how much simplified versions of food webs retain the structural properties of more detailed networks. Using the most comprehensive Barents Sea food web to date, we investigate the performance of methods to construct simplified food webs using three approaches: taxonomic, structural and regular clustering. We then evaluate how topological properties vary with the level of network simplification. Results show that alteration of food web structural properties due to aggregation are highly sensitive to the methodology used for grouping species and trophic links. In the specific case of the Barents Sea, we show that it is possible to preserve key structural properties of the original complex food web in simplified versions when using taxonomic or structural clustering combined with intermediate 25% linkage for trophic aggregation.     

Genetic variation, predator-prey interactions and food web structure

Food webs are networks of species that feed on each other. The role that within-population phenotypic and genetic variation plays in food web structure is largely unknown. Here, I show via simulation how variation in two key traits, growth rates and phenology, by influencing the variability of body sizes present through time, can potentially affect several structural parameters in the direction of enhancing food web persistence: increased connectance, decreased interaction strengths, increased variation among interaction strengths and increased degree of omnivory. I discuss other relevant traits whose variation could affect the structure of food webs, such as morphological and additional life-history traits, as well as animal personalities. Furthermore, trait variation could also contribute to the stability of food web modules through metacommunity dynamics. I propose future research to help establish a link between within-population variation and food web structure. If appropriately established, such a link could have important consequences for biological conservation, as it would imply that preserving (functional) genetic variation within populations could ensure the preservation of entire communities.     

Patterns in intraspecific interaction strengths and the stability of food webs

A common approach to analyse stability of biological communities is to calculate the interaction strength matrix. Problematic in this approach is defining intraspecific interaction strengths, represented by diagonal elements in the matrix, due to a lack of empirical data for these strengths. Theoretical studies have shown that an overall increase in these strengths enhances stability. However, the way in which the pattern in intraspecific interaction strengths, i.e. the variation in these strengths between species, influences stability has received little attention. We constructed interaction strength matrices for 11 real soil food webs in which four patterns for intraspecific interaction strengths were chosen, based on the ecological literature. These patterns included strengths that were (1) similar for all species, (2) trophic level dependent, (3) biomass dependent, or (4) death rate dependent. These four patterns were analysed for their influence on (1) ranking food webs by their stability and (2) the response in stability to variation of single interspecific interaction strengths. The first analysis showed that ranking the 11 food webs by their stability was not strongly influenced by the choice of diagonal pattern. In contrast, the second analysis showed that the response of food web stability to variation in single interspecific interaction strengths was sensitive to the choice of diagonal pattern. Notably, stability could increase using one pattern and decrease using another. This result asks for deliberate approaches to choose diagonal element values in order to make predictions on how particular species, interactions, or other food web parameters affect food web stability.     

Climate change and multitrophic interactions in soil: the primacy of plants and functional domains

Soil multitrophic interactions transfer energy from plants as the predominant primary producer to communities of organisms that occupy different positions in the food chain and are linked by multiple ecological networks, which is the soil food web. Soil food web sequesters carbon, cycles nutrients, maintains soil health to suppress pathogens, helps plants tolerate abiotic and biotic stress, and maintains ecosystem resilience and sustainability. Understanding the influence of climate change on soil multitrophic interactions is necessary to maintain these essential ecosystem services. But summarising this influence is a daunting task due to a paucity of knowledge and a lack of clarity on the ecological networks that constitute these interactions. The scant literature is fragmented along disciplinary lines, often reporting inconsistent findings that are context and scale‐dependent. We argue for the differentiation of soil multitrophic interactions along functional and spatial domains to capture cross‐disciplinary knowledge and mechanistically link all ecological networks to reproduce full functionalities of the soil food web. Distinct from litter mediated interactions in detritosphere or elsewhere in the soil, the proposed ‘pathogen suppression’ and ‘stress tolerance’ interactions operate in the rhizosphere. A review of the literature suggests that climate change will influence the relative importance, frequency and composition of functional groups, their trophic interactions and processes controlling these interactions. Specific climate change factors generally have a beneficial influence on pathogen suppression and stress tolerance, but findings on the overall soil food web are inconsistent due to a high level of uncertainty. In addition to an overall improvement in the understanding of soil multitrophic interactions using empirical and modelling approaches, we recommend linking biodiversity to function, understanding influence of combinations of climatic factors on multitrophic interactions and the evolutionary ecology of multitrophic interactions in a changing climate as areas that deserve most attention.     

重金属污染土壤中生物间相互作用及其协同修复应用

土壤是人类赖以生存的物质基础。我国土壤重金属污染状况不容乐观,给人类健康构成严重威胁。生物修复重金属污染土壤被广泛认为是可持续的修复技术,但当前仍存在修复效率不高的科学瓶颈问题。土壤中生活着丰富的微生物、植物和动物,且这些生物之间存在着复杂的相互作用,并且通过物质循环和能量传递形成了错综复杂的食物网联系。土壤生物间的相互作用能深刻影响土壤中污染物的迁移转化和生物修复的效率,多元生物协同的修复技术集合了单一生物修复方法的优势,具有强化生物修复效果的巨大潜力。文中综述了土壤中微生物-植物-动物之间的相互作用,及其对土壤重金属迁移转化和生物修复效果的影响,并对定向调控土壤食物网结构、提高重金属污染土壤的生物修复效果、建立基于食物网的多元生物协同修复技术进行了展望。     

Phytoplankton food quality control of planktonic food web processes

We developed a mechanistic model of nutrient, phytoplankton, zooplankton and fish interactions to test the effects of phytoplankton food quality for herbivorous zooplankton on planktonic food web processes. When phytoplankton food quality is high strong trophic cascades suppress phytoplankton biomass, the zooplankton can withstand intense zooplanktivory, and energy is efficiently transferred through the food web sustaining higher trophic level production. Low food quality results in trophic decoupling at the plant-animal interface, with phytoplankton biomass determined primarily by nutrient availability, zooplankton easily eliminated by fish predation, and poor energy transfer through the food web. At a given nutrient availability, food quality and zooplanktivory interact to determine zooplankton biomass which in turn determines algal biomass. High food quality resulted in intense zooplankton grazing which favored fast-growing phytoplankton taxa, whereas fish predation favored slow-growing phytoplankton. These results suggest algal food quality for herbivorous zooplankton can strongly influence the nature of aquatic food web dynamics, and can have profound effects on water quality and fisheries production. Handling editor: D. Hamilton     

The Serengeti food web: empirical quantification and analysis of topological changes under increasing human impact

1.?To address effects of land use and human overexploitation on wildlife populations, it is essential to better understand how human activities have changed species composition, diversity and functioning. Theoretical studies modelled how network properties change under human-induced, non-random species loss. However, we lack data on realistic species-loss sequences in threatened, real-world food webs to parameterize these models. 2.?Here, we present a first size-structured topological food web of one of the most pristine terrestrial ecosystems in the world, the Serengeti ecosystem (Tanzania). The food web consists of 95 grouped nodes and includes both invertebrates and vertebrates ranging from body masses between 10(-7) and 10(4) kg. 3.?We study the topological changes in this food web that result from the simulated IUCN-based species-loss sequence representing current species vulnerability to human disturbances in and around this savanna ecosystem. We then compare this realistic extinction scenario with other extinction sequences based on body size and connectance and perform an analysis of robustness of this savanna food web. 4.?We demonstrate that real-world species loss in this case starts with the biggest (mega) herbivores and top predators, causing higher predator-prey mass ratios. However, unlike theoretically modelled linear species deletion sequences, this causes poor-connected species to be lost first, while more highly connected species become lost as human impact progresses. This food web shows high robustness to decreasing body size and increasing connectance deletion sequences compared with a high sensitivity to the decreasing connectance deletion scenario. 5.?Furthermore, based on the current knowledge of the Serengeti ecosystem, we discuss how the focus on food web topology alone, disregarding nontrophic interactions, may lead to an underestimation of human impacts on wildlife communities, with the number of trophic links affected by a factor of two. 6.?This study underlines the importance of integrative efforts between the development of food web theory and basic field work approaches in the quantification of the structure of interaction networks to sustain natural ecosystems in a changing world.     

Review Behaviour and indirect interactions in food webs of plant-inhabiting arthropods

With the increased use of biological control agents, artificial food webs are created in agricultural crops and the interactions between plants, herbivores and natural enemies change from simple tritrophic interactions to more complex food web interactions. Therefore, herbivore densities will not only be determined by direct predator–prey interactions and direct and indirect defence of plants against herbivores, but also by other direct and indirect interactions such as apparent competition, intraguild predation, resource competition, etc. Although these interactions have received considerable attention in theory and experiments, little is known about their impact on biological control. In this paper, we first present a review of indirect food web interactions in biological control systems. We propose to distinguish between numerical indirect interactions, which are interactions where one species affects densities of another species through an effect on the numbers of an intermediate species and functional indirect interactions, defined as changes in the way that two species interact through the presence of a third species. It is argued that functional indirect interactions are important in food webs and deserve more attention. Subsequently, we discuss experimental results on interactions in an artificial food web consisting of pests and natural enemies on greenhouse cucumber. The two pest species are the two-spotted spider mite Tetranychus urticae and the western flower thrips, Frankliniella occidentalis. Their natural enemies are the predatory mite Phytoseiulus persimilis, which is commonly used for spider mite control and the predatory mites Neoseiulus cucumeris and Iphiseius degenerans and the predatory bug Orius laevigatus, all natural enemies of thrips. First, we analyse the possible interactions between these seven species and we continue by discussing how functional indirect interactions, particularly the behaviour of arthropods, may change the significance and impact of direct interactions and numerical indirect interactions. It was found that a simple food web of only four species already gives rise to some quite complicated combinations of interactions. Spider mites and thrips interact indirectly through resource competition, but thrips larvae are intraguild predators of spider mites. Some of the natural enemies used for control of the two herbivore species are also intraguild predators. Moreover, spider mites produce a web that is subsequently used by thrips to hide from their predators. We discuss these and other results obtained so far and we conclude with a discussion of the potential impact of functional indirect and direct interactions on food webs and their significance for biological control.     

线虫区系分析指示土壤食物网结构和功能研究进展

土壤食物网结构复杂,功能众多,直接测定土壤食物网各功能群生物量并结合数学模型来推断土壤食物网结构和功能,工作量大且分析过程繁琐。线虫生态学的发展为土壤食物网的研究开辟了一条新的思路,即利用线虫区系分析来定性推断食物网的结构和功能。线虫作为土壤中数量最丰富的后生动物,占据着土壤食物网的中心位置,其物种多样性、食性多样性、生活史策略多样性、功能团多样性奠定了其作为土壤食物网结构和功能指示生物的生态学基础。线虫区系分析根据发展历史可以分为个体分类、生活史策略分类、功能团分类和代谢足迹分类四个时期,其中后两个时期主要用于推断土壤食物网结构和功能。基于功能团的线虫区系分析将线虫的食性和生活史策略结合起来,发展出一系列指数来判断土壤食物网的连通性、食物网链长度、外界养分投入情况、分解途径及对外界干扰的响应等。基于代谢足迹的线虫区系分析在功能团分析基础上,加入线虫能流分析,从而定性反映了土壤食物网功能的大小。两者在指示土壤食物网自下而上调节及对植物线虫控制等方面起着重要的作用。     

Tracing Consumer-Derived Nitrogen in Riverine Food Webs

The flux of consumer-derived nutrients is recognized as an important ecosystem process, yet few studies have quantified the impact of these fluxes on freshwater ecosystems. The high abundance of bivalves in both marine and freshwater suggests that bivalves can exert large effects on aquatic food webs. The objective of our study was to determine the importance of unionid mussel-derived nitrogen (MDN) to the food web. We used a stable isotope tracer approach in conjunction with nutrient uptake and excretion experiments. We fed mussels (Lampsilis siliquiodea, n = 249) a ¹⁵N-enriched algal diet and placed them into a N-limited stream for 63 days. Mussel hemolymph was non-lethally sampled over the course of the experiment to measure tissue turnover of δ¹⁵N and excretion experiments were done to model the amount of N mussels provided in comparison to stream N uptake demand. Multiple food web pools were sampled twice prior and five times following the mussel addition to trace the ¹⁵N through the food web. Our mussel excretion rates in comparison to areal uptake demand suggested that mussel excretion can account for 40% of the total N demand in this stream. Our enrichment showed that MDN was entering the food web and supplied up to 19% of the N in specific compartments of the food web near the mussel bed. When scaled to a natural mussel aggregation, our results suggest up to 74% of N in the food web may be mussel-derived. Our results show that N supplied by mussels can be an important nutrient subsidy that provides food web support.