Trophic Position Of Consumers Research Articles

Comparison of δ13C and δ15N of ecologically relevant amino acids among beluga whale tissues

Ecological applications of compound-specific stable isotope analysis (CSIA) of amino acids (AAs) include 1) tracking carbon pathways in food webs using essential AA (AAESS) δ13C values, and 2) estimating consumer trophic position (TP) by comparing relative differences of ‘trophic’ and ‘source’ AA δ15N values. Despite the significance of these applications, few studies have examined AA-specific SI patterns among tissues with different AA compositions and metabolism/turnover rates, which could cause differential drawdown of body AA pools and impart tissue-specific isotopic fractionation. To address this knowledge gap, especially in the absence of controlled diet studies examining this issue in captive marine mammals, we used a paired-sample design to compare δ13C and δ15N values of 11 AAs in commonly sampled tissues (skin, muscle, and dentine) from wild beluga whales (Delphinapterus leucas). δ13C of two AAs, glutamic acid/glutamine (Glx, a non-essential AA) and, notably, threonine (an essential AA), differed between skin and muscle. Furthermore, δ15N of three AAs (alanine, glycine, and proline) differed significantly among the three tissues, with glycine δ15N differences of approximately 10 ‰ among tissues supporting recent findings it is unsuitable as a source AA. Significant δ15N differences in AAs such as proline, a trophic AA used as an alternative to Glx in TP estimation, highlight tissue selection as a potential source of error in ecological applications of CSIA-AA. Amino acids that differed among tissues play key roles in metabolic pathways (e.g., ketogenic and gluconeogenic AAs), pointing to potential physiological applications of CSIA-AA in studies of free-ranging animals. These findings underscore the complexity of isotopic dynamics within tissues and emphasize the need for a nuanced approach when applying CSIA-AA in ecological research.

The influence of dynamic resources and stable isotope incorporation rates on aquatic consumer trophic position estimation

AbstractA key assumption in trophic position (TP) estimation using stable isotope analysis is that consumers are in isotopic equilibrium with their resources. Here, we assess the degree to which time‐varying resource dynamics and isotope incorporation rates of consumers influence consumer TP estimates across multiple trophic levels and aquatic ecosystems. We constructed a first‐order kinetics model to explore consumer stable isotope incorporation rates and modeled the effect on TP calculations using bulk and compound‐specific stable isotope data from previous experimental and observational studies. We found TP estimates of higher trophic level consumers are less accurate than lower trophic level consumers when applying bulk stable isotope analysis (BSIA) and using particulate organic matter as the stable isotope baseline. The accuracy of TP estimates depended on the time‐varying dynamics of the stable isotope baseline. Tertiary consumers had the highest TP estimation error, and this error was not eliminated by sampling tissues with fast incorporation rates (i.e., blood) in the tertiary consumer. Compound‐specific stable isotope analysis (CSIA) of individual amino acids was more accurate in estimating TP for all consumers and ecosystems compared to BSIA. Our analysis confirms that consideration for the dynamic nature of stable isotope ratios is necessary for accurate TP estimates. Finally, we show how first‐order kinetics models can provide a useful framework for integrating prey and consumer incorporation rates in stable isotope studies to improve TP estimates.

Trophic structure and origin of resources of soil macrofauna in the salt marsh of the Wadden Sea: a stable isotope (15N, 13C) study

Salt marshes exist along the gradient of the marine mudflat to the terrestrial dunes, with a gradient of shore height and associated plant zonation. The lower salt marsh (LSM) extends from the mean high tidal level to 35 cm above that level and is followed by the upper salt marsh (USM). Despite changes in the amount of allochthonous marine input and in abiotic conditions, little is known about changes in the trophic structure and used of basal resources by the soil macrofauna along marine—terrestrial boundaries. Natural variations in carbon stable isotope ratios (δ13C signatures) allow insight into basal resources of consumers such as marine algae, terrestrial C3 and C4 photosynthesising plants. Furthermore, variations in nitrogen stable isotope ratios (δ15N signatures) allow insight into the trophic position of consumers. We investigated spatial and temporal changes in stable isotope signatures in salt marsh soil macrofauna of the island of Spiekeroog, German Wadden Sea. The range of δ15N signatures indicated no changes in food chain length across salt marsh zones with consumers in both zones comprising primary decomposers, secondary decomposers and first order predators. However, the trophic position of individual species changed between zones, but in particular with season. Contrasting δ15N signatures, the range in δ13C signatures in the LSM was twice that in the USM indicating a wider range of resources consumed. Bayesian mixing models indicated predominant autochthonous resource use in both the LSM and USM, with the use of marine allochthonous resources never exceeding 29.6%. However, the models also indicate an increase in the use of marine resources in certain species in the LSM with no use in the USM. Overall, the results indicate that the resource use of salt marsh macrofauna varies more in space than in time, with the food web being generally based on autochthonous rather than allochthonous resources. However, there also is trophic plasticity in certain species across both temporal and spatial scales including variations in the use of allochthonous resources. Generally, however, marine input contributes little to the nutrition of salt marsh soil macroinvertebrates.

Trophic Diversity and Food Web Structure of Vegetated Habitats Along a Coastal Topographic Gradient

Land–sea interactions in coastal wetlands create heterogeneous vegetated habitats with regular zonation along a topographic gradient. However, it’s unclear how the trophic diversity of communities and trophic structure of food webs change along the gradient. Here, we investigated the empirically resolved food web structure and trophic diversity across four vegetated habitats (Phragmites australis, Suaeda salsa, Spartina alterniflora, and Zostera japonica seagrass) along a gradient from upland to near-shore waters in the Yellow River Delta wetland. We quantified δ13C and δ15N of carbon sources (detritus, primary producers) and consumers (zooplankton, macroinvertebrates, fish). δ13C and δ15N of the carbon sources and consumers differed significantly among the four habitats. Carbon sources and consumers became more 13C-enriched and 15N-enriched along the gradient, respectively. The consumer trophic position was higher in the S. salsa habitat than in the seagrass habitat, followed by the S. alterniflora and P. australis habitats. The habitat formed by invasive S. alterniflora had the lowest corrected standard ellipse areas in the δ13C vs. δ15N plots for the basal carbon sources and all consumers combined, and the lowest Layman community metrics for the δ13C range, total area, and centroid distance; thus, trophic groups in this habitat had the lowest isotopic trophic diversity. Using a Bayesian isotope mixing model, we found that consumer diet compositions differed greatly among the habitats where the consumer was present, except for shrimps and polychaetes. Food web topological properties (species richness, number of trophic links, linkage density, proportions of intermediate consumers and omnivores) increased along the gradient. Generally, habitat heterogeneity created highly variable food webs. Our results provide insights into the spatial variation in coastal ecosystems along a topographic gradient, and demonstrate the need to protect habitat heterogeneity in coastal wetlands, combined with adaptive management to control invasive species.

Meta‐analysis of primary producer amino acid δ15N values and their influence on trophic position estimation

Abstract Compound‐specific stable isotope analysis of individual amino acids (CSIA‐AA) has emerged as a transformative approach to estimate consumer trophic positions (TPCSIA) that are internally indexed to primary producer nitrogen isotope baselines. Central to accurate TPCSIA estimation is an understanding of beta (β) values—the differences between trophic and source AA δ15N values in the primary producers at the base of a consumers’ food web. Growing evidence suggests higher taxonomic and tissue‐specific β value variability than typically appreciated. This meta‐analysis fulfils a pressing need to comprehensively evaluate relevant sources of β value variability and its contribution to TPCSIA uncertainty. We first synthesized all published primary producer AA δ15N data to investigate ecologically relevant sources of variability (e.g. taxonomy, tissue type, habitat type, mode of photosynthesis). We then reviewed the biogeochemical mechanisms underpinning AA δ15N and β value variability. Lastly, we evaluated the sensitivity of TPCSIA estimates to uncertainty in mean βGlx‐Phe values and Glx‐Phe trophic discrimination factors (TDFGlx‐Phe). We show that variation in βGlx‐Phe values is two times greater than previously considered, with degree of vascularization, not habitat type (terrestrial vs. aquatic), providing the greatest source of variability (vascular autotroph = −6.6 ± 3.4‰; non‐vascular autotroph = +3.3 ± 1.8‰). Within vascular plants, tissue type secondarily contributed to βGlx‐Phe value variability, but we found no clear distinction among C3, C4 and CAM plant βGlx‐Phe values. Notably, we found that vascular plant βGlx‐Lys values (+2.5 ± 1.6‰) are considerably less variable than βGlx‐Phe values, making Lys a useful AA tracer of primary production sources in terrestrial systems. Our multi‐trophic level sensitivity analyses demonstrate that TPCSIA estimates are highly sensitive to changes in both βGlx‐Phe and TDFGlx‐Phe values but that the relative influence of β values dissipates at higher trophic levels. Our results highlight that primary producer β values are integral to accurate trophic position estimation. We outline four key recommendations for identifying, constraining and accounting for β value variability to improve TPCSIA estimation accuracy and precision moving forward. We must ultimately expand libraries of primary producer AA δ15N values to better understand the mechanistic drivers of β value variation.

Shifting baselines: Integrating ecological and isotopic time lags improves trophic position estimates in aquatic consumers

Nitrogen stable isotope ratios (δ15N) are routinely used to estimate consumer trophic positions (TPs). This method is very sensitive to the chosen isotopic baseline, which should incorporate all temporal isotopic variability occurring in the base of the food web sustaining the consumers. However, there is still no consensus on the different methods to represent time intervals for isotopic assimilation. It is uncertain if researchers should compute a single baseline obtained by averaging δ15N source values across all time periods, multiple baselines based on δ15N source values collected concomitantly with consumers, or consider a time lag between sources and consumers. Aiming to provide empirical evidence to help select the best option, we designed 4 methods using different temporal lags between consumers and producers based on a 9 yr time series of carbon and nitrogen stable isotopes in an estuary. The 4 tested baseline methods considered the δ15N average of producers sampled in all years (Global); the same season as consumers (Concomitantly); the season before the collection of consumers (Delayed); and the previous season as well as the same season of consumer sampling (Interpolation). Comparison of results with an expected model (based on stomach content data) showed that the Delayed method is the most appropriate. We conclude that time lags in the incorporation of stable isotope values between sources and consumers must be considered in baseline δ15N calculations to improve TP estimates and provide more reliable modeling results. Additionally, we provide other recommendations to improve sampling designs when using stable isotopes in TP estimations.

Environmental factors drive interannual variation in estuarine food-chain length

Biological communities are strongly affected by environmental factors and their variability. Estuarine biota is driven by abiotic factors such as salinity, rainfall, and river flow, varying at distinct spatial and time scales. The El Niño is a coupled ocean–atmosphere phenomenon occurring at irregular time scales that affects biological communities worldwide, including changes in species composition and diversity patterns. One of the most important attributes in community ecology is the food-chain length (FCL) because affects the ecosystem functioning. Based on the ‘intermediate disturbance’ theory and prior evidences showing effects of El Niño on animal diversity, we hypothesized this phenomenon will increase richness (both at species and trophic guilds levels) and FCL in a shallow-water estuarine community. To evaluate our hypothesis, we analyzed a 9-yr dataset of carbon and nitrogen stable isotope ratios of food web components in a shallow embayment of a subtropical estuary. We estimated consumer's trophic positions (TP) using a recent Bayesian approach that incorporates individual variability and sampling error in isotope fractionation, isotopic baselines and consumers. As expected, both species and trophic guilds richness were higher during El Niño events. FCL ranged from 2.45 to 4.60, but against our prediction showed a slight decreased during higher rainfall periods. These finding suggest FCL in estuaries is resilient to environmental variability and natural climatic perturbations.

Tracing trophic pathways through the marine ecosystem of Rapa Nui (Easter Island)

Abstract The structure of food webs provides important insight into biodiversity, organic matter (OM) pathways, and ecosystem functioning. Stable isotope analysis (δ13C and δ15N) was used to characterize the trophic structure and the main OM pathways supporting food webs in the Rapa Nui coastal marine ecosystem. The trophic position of consumers and isotopic niche metrics were estimated for different assemblages (i.e. mesozooplankton, emergent zooplankton, reef invertebrates, reef fishes, pelagic fishes, and seabirds). Furthermore, the relative importance of different OM sources (i.e. macroalgae, zooxanthellate corals, and particulate OM [POM]) was assessed for heterotrophic consumers using Bayesian mixing model (MixSIAR). Results show a clear pattern of 13C and 15N enrichment from small‐sized pelagic and benthic invertebrates, to reef and pelagic fishes, and seabirds. Most invertebrates were classified as primary consumers, reef fishes as secondary consumers and pelagic predators and seabirds as tertiary and quaternary consumers. Isotopic niche metrics indicate a low trophic diversity for pelagic assemblages (mesozooplankton and pelagic fishes), in contrast to reef fauna (invertebrates and fishes), whose higher trophic diversity suggest the exploitation of a wider range of trophic resources. Overlapping of standard ellipses areas between reef invertebrates and reef fishes indicates that both assemblages could be sharing trophic resources. Mixing models results indicate that POM is the main trophic pathway for mesozooplankton, macroalgae (Rhodophyta) for emergent zooplankton, and a mix of coral‐derived OM and Rhodophyta for coral reef assemblages such as macrobenthos and reef invertebrates. In contrast, POM contribution was notably more important for some pelagic fishes and seabirds from upper trophic levels. This study provides key elements for conservation efforts on coral reefs, management planning and full‐implementation of the recently created Rapa Nui Multiple Use Marine Protected Area.

Amino acid δ15N underestimation of cetacean trophic positions highlights limited understanding of isotopic fractionation in higher marine consumers.

Compound‐specific stable isotope analysis (CSIA) of amino acids (AAs) has been rapidly incorporated in ecological studies to resolve consumer trophic position (TP). Differential 15N fractionation of “trophic” AAs, which undergo trophic 15N enrichment, and “source” AAs, which undergo minimal trophic 15N enrichment and serve as a proxy for primary producer δ15N values, allows for internal calibration of TP. Recent studies, however, have shown the difference between source and trophic AA δ15N values in higher marine consumers is less than predicted from empirical studies of invertebrates and fish. To evaluate CSIA‐AA for estimating TP of cetaceans, we compared source and trophic AA δ15N values of multiple tissues (skin, baleen, and dentine collagen) from five species representing a range of TPs: bowhead whales, beluga whales, short‐beaked common dolphins, sperm whales, and fish‐eating (FE) and marine mammal‐eating (MME) killer whale ecotypes. TP estimates (TPCSIA) using several empirically derived equations and trophic discrimination factors (TDFs) were 1–2.5 trophic steps lower than stomach content‐derived estimates (TPSC) for all species. Although TPCSIA estimates using dual TDF equations were in better agreement with TPSC estimates, our data do not support the application of universal or currently available dual TDFs to estimate cetacean TPs. Discrepancies were not simply due to inaccurate TDFs, however, because the difference between consumer glutamic acid/glutamine (Glx) and phenylalanine (Phe) δ15N values (δ15NGlx‐Phe) did not follow expected TP order. In contrast to pioneering studies on invertebrates and fish, our data suggest trophic 15N enrichment of Phe is not negligible and should be examined among the potential mechanisms driving “compressed” and variable δ15NGlx‐Phe values at high TPs. We emphasize the need for controlled diet studies to understand mechanisms driving AA‐specific isotopic fractionation before widespread application of CSIA‐AA in ecological studies of cetaceans and other marine consumers.

Increased trophic position of black bear (Ursus americanus) at the northern fringe of its distribution range

Studies describing the diet of omnivorous species are abundant, but the drivers affecting the balance between animal and plant resources remain unclear. Among those drivers, latitude has been reported to positively correlate with the trophic position of consumers. Using stable isotope analysis, we tested the hypothesis that trophic position of black bears (Ursus americanus Pallas, 1780) is positively correlated with latitude in eastern North America. We sampled 57 bears over a 15° latitudinal gradient in Quebec, Canada, and used stable isotope analysis to assess individual trophic position and metrics of dietary niches. We found a strong positive correlation between trophic position of bears and latitude (r2= 0.76), which persisted throughout seasons. The width of the dietary niche of bears also appeared to follow a latitudinal pattern, even though bears foraging at the southernmost part of the gradient also showed a wide dietary niche. The impact of latitude on the foraging tactic of omnivores fosters our understanding of their capability to deal with contrasting environmental conditions, especially for species whose distribution ranges are expanding due to climate change. The flexibility of black bear foraging tactic likely allows this species to expand its geographical distribution range toward northern habitats.

Trophic Position of Consumers and Size Structure of Food Webs across Aquatic and Terrestrial Ecosystems.

Do large organisms occupy higher trophic levels? Predators are often larger than their prey in food chains, but empirical evidence for positive body mass-trophic level scaling for entire food webs mostly comes from marine communities on the basis of unicellular producers. Using published data on stable isotope compositions of 1,093 consumer species, we explored how trophic level scales with body size, food web type (green vs. brown), and phylogenetic group across biomes. In contrast to widespread assumptions, the relationship between body size and trophic level of consumers-from protists to large vertebrates-was not significant per se but varied among ecosystem types and animal groups. The correlation between body size and trophic level was strong in marine consumers, weak in freshwater consumers, and absent in terrestrial consumers, which was also observed at the scale of local food webs. Vertebrates occupied higher trophic positions than invertebrates, and green trophic chains were longer than brown ones in aquatic (primarily marine) but not in terrestrial food webs. Variations in body size of top predators suggest that terrestrial and many freshwater food webs are size compartmentalized, implying different trophic dynamics and responses to perturbations than in size-structured marine food webs.

Compound‐specific isotope analysis of amino acids as a new tool to uncover trophic chains in soil food webs

AbstractFood webs in soil differ fundamentally from those aboveground; they are based on inputs from both living plants via root exudates, and from detritus, which is a complex mixture of fungi, bacteria, and dead plant remains. Trophic relationships are difficult to disentangle due to the cryptic lifestyle of soil animals and inevitable microbial contributions to their diet. Compound‐specific isotope analysis of amino acids (AAs) is increasingly used to explore complex food webs. The combined use of AA δ13C and δ15N values is a promising new approach to disentangle trophic relationships since it provides independent but complementary information on basal resources, as well as the trophic position of consumers. We conducted a controlled feeding study in which we reconstructed trophic chains from main basal resources (bacteria, fungi, plants) to primary consumers (springtails, oribatid mites) and predators (gamasid mites, spiders). We analyzed dual compound‐specific isotope AA values of both resources and consumers. By applying an approach termed “stable isotope (13C) fingerprinting” we identified basal resources, and concomitantly calculated trophic positions using 15N values of trophic and source AAs in consumers. In the 13C fingerprinting analysis, consumers in general grouped close to their basal resources. However, higher than usual offsets in AA δ13C between diet and consumers suggest either gut microbial supplementation or the utilization of specific resource fractions. Identification of trophic position crucially depends on correct estimates of the trophic discrimination factor (TDFGlu‐Phe), which was close to the commonly applied value of 7.6‰ in primary consumers feeding on microbial resources, but considerably lower in arachnid predators (~2.4‰), presumably due to higher diet quality, excretion of guanine, and fluid feeding. While our feeding study demonstrates that dual compound‐specific AA analyses hold great promise in delineating trophic linkages among soil‐dwelling consumers and their resources, it also highlights that a “one‐size‐fits‐all” approach to TDFGlu‐Phe does not apply to soil food webs.

Consumer trophic positions respond variably to seasonally fluctuating environments.

The effects of environmental seasonality on food web structure have been notoriously understudied in empirical ecology. Here, we focus on seasonal changes in one key attribute of a food web, consumer trophic position. We ask whether fishes inhabiting tropical river-floodplain ecosystems behave as seasonal omnivores, by shifting their trophic positions in relation to the annual flood pulse, or whether they feed at the same trophic position all year, as much empirical work implicitly assumes. Using dietary data from the Tonle Sap Lake, Cambodia, and a literature review, we find evidence that some fishes, especially small piscivores, increased consumption of invertebrates and/or plant material during the wet season, as predicted. However, nitrogen stable isotope (δ15 N) data for 26 Tonle Sap fishes, spanning a broader range of functional groups, uncovered high variation in seasonal trophic position responses among species (0 to ±0.52 trophic positions). Based on these findings, species respond to the flood pulse differently. Diverse behavioral responses to seasonality, underpinned by spatiotemporal variation at multiple scales, could be central for rerouting matter and energy flow in these dynamic ecosystems. Seasonally flexible foraging behaviors warrant further study given their potential influence on food web dynamics in a range of fluctuating environments.

TRophicPosition, anrpackage for the Bayesian estimation of trophic position from consumer stable isotope ratios

AbstractStable isotope analysis provides a powerful tool to identify the energy sources which fuel consumers, to understand trophic interactions and to infer consumer trophic position (TP), an important concept that describes the ecological role of consumers in food webs. However, current methods for estimating TP using stable isotopes are limited and do not fulfil the complete potential of the isotopic approach. For instance, researchers typically use point estimates for key parameters including trophic discrimination factors and isotopic baselines, and do not explicitly include variance associated with these parameters when calculating TP.We present “tRophicPosition,” anrpackage incorporating a Bayesian model for the calculation of consumer TP at the population level using stable isotopes, with one or two baselines. It combines Markov Chain Monte Carlo simulations through JAGS and statistical and graphical analyses using R. We model consumer and baseline observations using relevant statistical distributions, allowing them to be treated as random variables. The calculation of TP—a random parameter—for one baseline follows standard equations linking15N enrichment per trophic level and the trophic position of the baseline (e.g. a primary producer or primary consumer). In the case of two baselines, a simple mixing model incorporating δ13C allows for the differentiation between two distinct sources of nitrogen, thus including heterogeneity derived from alternatives sources of δ15N.Methods currently implemented in “tRophicPosition” include loading, plotting and summarizing stable isotope data either from multiple sites and/or communities or a local assemblage; loading trophic discrimination factors from an internal database or generating them; defining and initializing a Bayesian model of TP; sampling posterior parameters; analysing, comparing and plotting posterior estimates of TP and other parameters; and calculating a parametric (non‐Bayesian) TP estimate. Additionally, full documentation including examples, multiple vignettes and code are available for download.

Unpacking brown food-webs: Animal trophic identity reflects rampant microbivory.

Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (=“brown”) food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (15N) analyses of amino acids extracted from wild and laboratory‐cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory‐reared and free‐roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild‐collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe‐derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate “up” food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field‐collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis to interpret detritivore trophic identity, and further illuminate the magnitude of microbial contributions to food webs.

Are you what you eat? Effects of trophic discrimination factors on estimates of food assimilation and trophic position with a new estimation method

A key factor for estimates of assimilation of resources and trophic position based on stable isotope data is the trophic discrimination factor (TDF). TDFs are assumed based on literature reviews, but may vary depending on a variety of factors, including the type of diet. We analyzed effects of alternative TDFs on estimates of assimilated resources and trophic positions for an omnivorous fish, Jenynsia multidentata, that reveals dietary variation among locations across a salinity gradient of a coastal lagoon in southern Brazil. We also compared estimates of foods ingested vs. foods assimilated. Food assimilation was estimated using carbon (δ13C) and nitrogen (δ15N) stable isotope ratios of food sources and consumer muscle tissue and an isotopic mixing model (SIAR); consumer trophic position (TP) was estimated from consumer and production source δ15N values. Diet was estimated using an index of relative importance based on frequency of occurrence and volumetric and numeric proportions of food items from stomach contents. The effect of variation in TDF on food assimilation and TP was tested using three alternative TDFs reported in review papers. We then created a new method that used food source-specific TDFs (reported separately for herbivores and carnivores) weighted in proportion to estimated assimilation of resources according to mixing model estimates to estimate TP (hereafter TPWAR). We found that plant material was not assimilated in a proportion similar to its importance in the diet of fish at a freshwater site, and the new method yielded best assimilation estimates. Animal material made greatest contributions to fish biomass irrespective of TDFs used in the mixing model. The new method produced TP estimates consistent with differences in estimated food assimilation along the salinity gradient. Our findings support the idea that food source-specific TDFs should be used in trophic studies of omnivores, since the method improved our ability to estimate trophic position and resource assimilation, two important ecological indicators.

Aphid‐tending ants on introduced fennel: can resources derived from non‐native plants alter the trophic position of higher‐order consumers?

1. Although plant invasions often reduce insect abundance and diversity, non‐native plants that support phytophagous insects can subsidise higher trophic levels via elevated herbivore abundance.2. Here ant–aphid interactions on non‐native fennel on Santa Cruz Island, California are examined. Fennel hosts abundant, honeydew‐producing fennel aphids. The patchiness of fennel and the relative lack of honeydew‐producing insects on other plants at our study sites suggest that assimilation of fennel‐derived honeydew would increase the abundance and decrease the trophic position of the omnivorous, aphid‐tending Argentine ant.3. To assess the strength of the ant–aphid interaction, a comparison of ant abundance on and adjacent to fennel prior to and 3 weeks after experimental aphid removal was performed. Compared with control plants with aphids, ants declined in abundance on and around fennel plants following aphid removal. At the habitat scale, pitfall traps in fennel‐dominated habitats captured more ants than in fennel‐free scrub habitats.4. To determine if assimilation of aphid‐produced honeydew reduces the ant's trophic position, variation in δ15N values among ants, plants and other arthropods was analysed. Unexpectedly, δ15N values for ants in fennel‐dominated habitats were higher than those of arthropod predators from the same sites and also higher than those of ants from fennel‐free habitats.5. Our results illustrate how introduced plants that support phytophagous insects appear to transfer energy to higher trophic levels via elevated herbivore abundance. Although assimilation of fennel‐derived honeydew did not appear to reduce consumer trophic position, spatial variation in alternative food resources might obscure contributions from honeydew.

Microbes are trophic analogs of animals

In most ecosystems, microbes are the dominant consumers, commandeering much of the heterotrophic biomass circulating through food webs. Characterizing functional diversity within the microbiome, therefore, is critical to understanding ecosystem functioning, particularly in an era of global biodiversity loss. Using isotopic fingerprinting, we investigated the trophic positions of a broad diversity of heterotrophic organisms. Specifically, we examined the naturally occurring stable isotopes of nitrogen ((15)N:(14)N) within amino acids extracted from proteobacteria, actinomycetes, ascomycetes, and basidiomycetes, as well as from vertebrate and invertebrate macrofauna (crustaceans, fish, insects, and mammals). Here, we report that patterns of intertrophic (15)N-discrimination were remarkably similar among bacteria, fungi, and animals, which permitted unambiguous measurement of consumer trophic position, independent of phylogeny or ecosystem type. The observed similarities among bacterial, fungal, and animal consumers suggest that within a trophic hierarchy, microbiota are equivalent to, and can be interdigitated with, macrobiota. To further test the universality of this finding, we examined Neotropical fungus gardens, communities in which bacteria, fungi, and animals are entwined in an ancient, quadripartite symbiosis. We reveal that this symbiosis is a discrete four-level food chain, wherein bacteria function as the apex carnivores, animals and fungi are meso-consumers, and the sole herbivores are fungi. Together, our findings demonstrate that bacteria, fungi, and animals can be integrated within a food chain, effectively uniting the macro- and microbiome in food web ecology and facilitating greater inclusion of the microbiome in studies of functional diversity.

Niche‐dependent trophic position distributions among primary, secondary and tertiary consumers

Many consumers display flexible feeding strategies that vary among individuals or populations, through life‐history, or spatiotemporally. Despite the recognized influence of flexible feeding on the structure and dynamics of food webs, the consequences of these feeding strategies on the actual shape and characteristics of trophic position distributions have received less attention. We proposed and tested several a priori hypotheses to predict the likely effect of niche‐dependent (e.g. herbivore, secondary consumer) foraging on the shape and statistical properties of consumer trophic position distributions using natural abundance stable isotope data from a diverse dataset of consumers. We found evidence that the structural characteristics of consumer trophic position distributions varied as a function of trophic niche. Herbivores and tertiary consumers tended to be ‘packed’ closely near their mean trophic position, with few individuals realizing trophic positions markedly higher or lower than the mean. Conversely, secondary consumers often displayed broad trophic position distributions with many individuals dispersed away from the center of the distribution. We examined the effect of applying constant versus dynamic isotope trophic fractionation models and found that both models yielded similar although not identical results. Our findings suggest that trophic level omnivory supports a larger fraction of consumer diet at intermediate trophic positions than at either the lowest or the highest positions in aquatic food webs. These results suggest that vertical trophic niche declines among higher order consumers despite general evidence that the range of potential foraging options (i.e. horizontal trophic niche) tends to increase at higher trophic positions. Although further work is needed to test the generality of these patterns in other ecosystems, proactively examining trophic position distributions and reporting appropriate measures of central tendency (e.g. arithmetic versus geometric means) will increase the accuracy of individual trophic studies as well as the applicability of results for meta‐analytical food web models.

Stable isotope composition in Daphnia is modulated by growth, temperature, and toxic exposure: implications for trophic magnification factor assessment.

The potential for using stable isotope analysis in risk assessment of environmental contaminants is crucially dependent on the predictability of the trophic transfer of isotopes in food webs. The relationship between contaminant levels and trophic position of consumers is widely used to assess biomagnification properties of various pollutants by establishing trophic magnification factors (TMF). However, contaminant-induced variability of the isotopic composition in biota is poorly understood. Here, we investigated effects of toxic exposure on δ(15)N and δ(13)C values in a consumer, with a main hypothesis that these effects would be largely mediated via growth rate and metabolic turnover of the test animals. The cladoceran Daphnia magna was used in two experiments that were conducted to manipulate growth and body condition (assayed as C:N ratio) by food availability and temperature (Experiment 1) and by toxic exposure to the pesticide lindane (Experiment 2). We found a significant negative effect of growth rate and a positive effect of temperature on the consumer-diet discrimination factor for δ(15)N and δ(13)C, with no effects on the C:N ratio (Experiment 1). In lindane-exposed daphnids, a significant growth inhibition was observed, with concomitant increase in metabolic costs and significantly elevated size-specific δ(15)N and δ(13)C values. Moreover, a significantly higher incorporation of carbon relative to nitrogen, yet a concomitant decrease in C:N ratio was observed in the exposed animals. Together, these results have methodological implications for determining trophic positions and TMF in polluted environments, where elevated δ(15)N values would translate into overestimated trophic positions and underestimated TMF. Furthermore, altered δ(13)C values may lead to erroneous food-chain assignment of the consumer in question.