Trophic Shifts of a Generalist Consumer in Response to Resource Pulses

Acute resource pulses can have dramatic legacies for organismal growth, but the legacy effects of resource pulses on broader aspects of community structure and ecosystem processes are less understood. Mass emergence of periodical cicadas (Magicicada spp.) provides an excellent opportunity to shed light on the influence of resource pulses on community and ecosystem dynamics: the adults emerge every 13 or 17 years in vast numbers over much of eastern North America, with a smaller but still significant number becoming incorporated into forest food webs. To study the potential effects of such arthropod resource pulse on primary production and belowground food webs, we added adult cicada bodies to the soil surface surrounding sycamore trees and assessed soil carbon and nitrogen concentrations, plant-available nutrients, abundance and community composition of soil fauna occupying various trophic levels, decomposition rate of plant litter after 50 and 100 days, and tree performance for 4 years. Contrary to previous studies, we did not find significant cicada effects on tree performance despite observing higher plant-available nutrient levels on cicada addition plots. Cicada addition did change the community composition of soil nematodes and increased the abundance of bacterial- and fungal-feeding nematodes, while plant feeders, omnivores, and predators were not influenced. Altogether, acute resource pulses from decomposing cicadas propagated belowground to soil microbial-feeding invertebrates and stimulated nutrient mineralization in the soil, but these effects did not transfer up to affect tree performance. We conclude that, despite their influence on soil food web and processes they carry out, even massive resource pulses from arthropods do not necessarily translate to NPP, supporting the view that ephemeral nutrient pulses can be attenuated relatively quickly despite being relatively large in magnitude.

Pulsed fluxes of organisms across ecosystem boundaries can exert top-down and bottom-up effects in recipient food webs, through both direct effects on the subsidized trophic levels and indirect effects on other components of the system. While previous theoretical and empirical studies demonstrate the influence of allochthonous subsidies on bottom-up and top-down processes, understanding how these forces act in conjunction is still limited, particularly when an allochthonous resource can simultaneously subsidize multiple trophic levels. Using the Lake Mývatn region in Iceland as an example system of allochthony and its potential effects on multiple trophic levels, we analyzed a mathematical model to evaluate how pulsed subsidies of aquatic insects affect the dynamics of a soil-plant-arthropod food web. We found that the relative balance of top-down and bottom-up effects on a given food web compartment was determined by trophic position, subsidy magnitude, and top predators' ability to exploit the subsidy. For intermediate trophic levels (e.g., detritivores and herbivores), we found that the subsidy could either alleviate or intensify top-down pressure from the predator. For some parameter combinations, alleviation and intensification occurred sequentially during and after the resource pulse. The total effect of the subsidy on detritivores and herbivores, including top-down and bottom-up processes, was determined by the rate at which predator consumption saturated with increasing size of the allochthonous subsidy, with greater saturation leading to increased bottom-up effects. Our findings illustrate how resource pulses to multiple trophic levels can influence food web dynamics by changing the relative strength of bottom-up and top-down effects, with bottom-up predominating top-down effects in most scenarios in this subarctic system.

Ontogenetic niche shifts are widespread. However, individual differences in size at birth, morphology, sex, and personalities can cause variability in behavior. As such, inherent inter-individual differences within populations may lead to context-dependent changes in behavior with animal body size, which is of concern for understanding population dynamics and optimizing ecological monitoring. Using stable carbon and nitrogen isotope values from concurrently sampled tissues, we quantified the direction and magnitude of intraspecific variation in trophic shifts among three shark species, and how these changed with body size: spurdogs (Squalus spp.) in deep-sea habitats off La Réunion, bull sharks (Carcharhinus leucas) in estuarine habitats of the Florida Everglades, and blacktip reef sharks (Carcharhinus melanopterus) in coral reef ecosystems of Moorea, French Polynesia. Intraspecific variation in trophic shifts was limited among spurdogs, and decreased with body size, while bull sharks exhibited greater individual differences in trophic shifts, but also decreased in variability through ontogeny. In contrast, blacktip reef sharks exhibited increased intraspecific variation in trophic interactions with body size. Variability in trophic interactions and ontogenetic shifts are known to be associated with changes in energetic requirements, but can vary with ecological context. Our results suggest that environmental stability may affect variability within populations, and ecosystems with greater spatial and/or temporal variability in environmental conditions, and those with more diverse food webs may facilitate greater individual differences in trophic interactions, and thus ontogenetic trophic shifts. In light of concerns over environmental disturbance, elucidating the contexts that promote or dampen phenotypic variability is invaluable for predicting population- and community-level responses to environmental changes.

Resource pulses can have cascading effects on the dynamics of multiple trophic levels. Acorn mast is a pulsed resource in oak-dominated forests that has significant direct effects on acorn predators and indirect effects on their predators, prey, and pathogens. We evaluated changes in acorn mast, rodent abundance, raptor abundance, and reproductive success of a ground-nesting songbird over a 24-year period (1980-2004) in the southern Appalachian Mountains in an effort to determine the relationships among the four trophic levels. In particular, we examined the following: acorn mast from red oaks (Quercus rubra) and white oaks (Q. alba), abundance of white-footed mice (Peromyscus leucopus) and deer mice (P. maniculatus), population estimates of seven raptor species from three feeding guilds, and nest failure and number of juveniles of dark-eyed juncos (Junco hyemalis). Finally, we recorded seasonal temperature and precipitation to determine the effects of weather on each trophic level. We found that weather patterns had delayed effects of up to 3 years on these trophic interactions. Variation in acorn mast, the keystone resource in this community, was explained by weather conditions as far back as 2 years before the mast event. Acorn mast, in turn, was a strongly positive predictor of rodent abundance the following year, whereas spring and summer temperature and raptor abundance negatively affected rodent abundance. Dark-eyed junco nests were more likely to fail in years in which there were more rodents and raptors. Nest failure rate was a strong predictor of the number of juvenile juncos caught at the end of the summer. Our results improve our understanding of the complex ecological interactions in oak-dominated forests by illustrating the importance of abiotic and biotic factors at different trophic levels.

The degree of shift in stable isotope ratios between trophic levels, known as trophic shift, can help elucidate trophic interactions in systems not amenable to conventional analyses. Gall wasp communities have long been a model system for community ecologists, yet much remains to be explored concerning trophic interactions between hosts, herbivores, and natural enemies. Before stable isotopes can be successfully applied to trophic interactions within gall communities, quality estimates of trophic shift between community members are required. In this study, we document the degree of trophic shift in carbon (&dgr;13C) and nitrogen (&dgr;15N) isotopes within a simple cynipid gall wasp community, Neuroterus sp. (Cynipidae), in Quercus turbinella Greene (Fagaceae). The trophic shift in &dgr;15N between Neuroterus sp. and Q. turbinella was much lower than values reported for Cecidomyiid gallers, whereas the shift in &dgr;15N between Neuroterus sp. and its parasitoid, Omyrus sp., was similar to that reported for parasitoids. The trophic shift in &dgr;13C was considerably greater in Neuroterus sp. than previous estimates from other types of herbivores, whereas Omyrus sp. exhibited a trophic shift in &dgr;13C similar to other biological systems. The unusual trophic shift in &dgr;13C in Neuroterus sp. is likely a result of metabolic differences between host and gall tissues. We discuss commonalities in the observed trophic shift of &dgr;13C and &dgr;15N in the Neuroterus sp. community to other biological systems and postulate physiological mechanisms for deviations from reported estimates of trophic shift.

Resource pulses affect productivity and dynamics in a diversity of ecosystems, including islands, forests, streams, and lakes. Terrestrial and aquatic systems differ in food web structure and biogeochemistry; thus they may also differ in their responses to resource pulses. However, there has been a limited attempt to compare responses across ecosystem types. Here, we identify similarities and differences in the causes and consequences of resource pulses in terrestrial and aquatic systems. We propose that different patterns of food web and ecosystem structure in terrestrial and aquatic systems lead to different responses to resource pulses. Two predictions emerge from a comparison of resource pulses in the literature: (1) the bottom-up effects of resource pulses should transmit through aquatic food webs faster because of differences in the growth rates, life history, and stoichiometry of organisms in aquatic vs. terrestrial systems, and (2) the impacts of resource pulses should also persist longer in terrestrial systems because of longer generation times, the long-lived nature of many terrestrial resource pulses, and reduced top-down effects of consumers in terrestrial systems compared to aquatic systems. To examine these predictions, we use a case study of a resource pulse that affects both terrestrial and aquatic systems: the synchronous emergence of periodical cicadas (Magicicada spp.) in eastern North American forests. In general, studies that have examined the effects of periodical cicadas on terrestrial and aquatic systems support the prediction that resource pulses transmit more rapidly in aquatic systems; however, support for the prediction that resource pulse effects persist longer in terrestrial systems is equivocal. We conclude that there is a need to elucidate the indirect effects and long-term implications of resource pulses in both terrestrial and aquatic ecosystems.

Soil food webs are complex networks that consist of several trophic levels and taxonomic groups including soil microorganisms, protists, nematodes, annelids and soil arthropods. Interactions between and within trophic levels and taxonomic groups regulate important ecosystem functions such as the cycling of carbon (C) and nutrients, with soil microorganisms channeling resources from the base of the food web to higher trophic levels of meso- and macrofauna decomposers and predators. Root exudates and decomposing plant residues are the major basal resources of C, and recent research highlighted the dominant role of root C for forest soil food webs. However, despite the large importance of agroecosystems for the global energy budget, channeling of C and nutrients in arable systems still is little understood. The present thesis focused on the flux of shoot residue- and root-derived C within arable soil food webs. In three field experiments I investigated soil animal community responses and the incorporation of shoot residue- and root-derived C into soil meso- and macrofauna at the species level. In the experiment presented in Chapter 2 I investigated the effects of aboveground resources on abundances and community composition of the soil animal food web of two arable fields planted with wheat and maize, respectively, by adding hackled maize shoot residues to the fields. Addition of shoot residue-derived resources did not affect the soil animal food web, suggesting that aboveground resources are of minor importance for soil animal communities. However, independent of shoot residue addition, the abundance and diversity were much higher and more fluctuating in wheat as compared to maize fields, due to more favourable habitat conditions and more pronounced pulses of root-derived resources in form of root exudates and decomposing root residues in wheat. Taking advantage of the differences in natural 13C/12C signatures of wheat and maize I tracked the incorporation of shoot residue- and root-derived resources into the body tissue of soil animals (Chapter 3). In general, one year after the start of the experiment incorporation of root-derived resources exceeded that of shoot residue-derived resources by a factor of two, highlighting the importance of root-derived resources for arable soil food webs. Furthermore, at higher taxonomic resolution only few soil animal taxa predominantly relied on shoot residue-derived resources, while approximately 30% preferred root-derived resources, and half of the taxa were generalist feeders incorporating both shoot residue- and root-derived resources. In a pulse labelling experiment (Chapter 4) I investigated the short-term incorporation of root-derived C and fertilizer N into the soil animal food web using 13CO2 and K15NO3. Ratios of 13C/12C and 15N/14N were measured in bulk soil, maize shoots, roots and meso- and macrofauna, plus 13C/12C in nematodes and microbial phospholipid fatty acids over a period of 25 days. Both 13C and 15N were incorporated into all compartments of the soil food web, with saprotrophic fungi incorporating by far the highest amounts of 13C, while higher trophic levels, i.e. nematodes and meso- and macrofauna, were less enriched. This suggests a prominent role of saprotrophic fungi in C and nutrient cycling in arable fields, but also that the majority of root-derived C remains locked up at the base of the food web. Further, higher amounts of 13C in predators than decomposers of meso- and macrofauna indicate a prominent role of nematodes for transferring resources to higher trophic levels. Overall, the present thesis highlights the importance of root-derived as compared to shoot residue-derived resources for arable soil food webs, thereby contributing to a better understanding of C and nutrient fluxes in agroecosystems.

Natural and anthropogenic disturbances commonly alter patterns of biodiversity and ecosystem functioning. However, how networks of interacting species respond to these changes remains poorly understood. We described aquatic food webs using invertebrate and fish community composition, functional traits and stable isotopes from twelve agricultural streams along a landscape disturbance gradient. We predicted that excessive deposition of fine inorganic sediment (sedimentation) associated with agricultural activities would negatively influence aquatic trophic diversity (e.g. reduced vertical and horizontal trophic niche breadths). We hypothesized that multiple mechanisms might cause trophic niche 'compression', as indicated by changes in realized trophic roles. Food-web properties based on consumer stable isotope data (δ13 C and δ15 N) showed that increasing sediment disturbance was associated with reduced trophic diversity. In particular, the aquatic invertebrate community occupied a smaller area in isotopic niche space along the sedimentation gradient that was best explained by a narrowing of the invertebrate community δ13 C range. Decreased niche partitioning, driven by increasing habitat homogeneity, environmental filtering and resource scarcity all seemingly lead to greater trophic equivalency caused by the collapse of the autochthonous food-web channel. Bayesian mixing-model analyses supported this contention with invertebrate consumers increasingly reliant on detritus along the sedimentation gradient, and predatory invertebrates relying more on the prey using these basal resources. The narrowing of the fish community δ13 C range along the sedimentation gradient contributed to an apparent 'trophic shift' towards terrestrial carbon, further indicating the loss of the autochthonous food-web channel. On the vertical trophic niche axis, fish became increasingly separated from aquatic invertebrates with an increase in their estimated trophic position. In combination, these responses were most likely mediated through reduced fish densities and a diminished reliance on aquatic prey. Although species losses remain a major threat to ecosystem integrity, the functional roles of biota that persist dictate how food webs and ecosystem functioning respond to environmental change. Sedimentation was associated with nonlinear reductions in trophic diversity which could affect the functioning and stability of aquatic ecosystems. Our study helps explain how multiple mechanisms may radically reshape food-web properties in response to this type of disturbance.

Food webs

Resource pulses provide short-duration, large-magnitude resources that influence ecosystem productivity, structure, and function. However, little empirical evidence is available evaluating how lake ecosystems respond to varying resource pulse magnitudes. We used mesocosms inoculated with primary producers and consumers to compare resource pulses of 0, 25, 50, 100, and 250 kg/ha of common carp Cyprinus carpio to simulate post-winterkill fish biomass in shallow lakes. Ecosystem responses to a gradient of resource pulse magnitudes typically had the greatest effects on nutrient availability and primary producers with fewer detectable effects for consumers. Total phosphorus, total Kjeldahl nitrogen, nitrate, phytoplankton, and periphyton productions increased as a result of the resource pulse, whereas copepods were the only consumer observed to elicit a positive response. In contrast, pulse magnitude had little effect on ecosystem stability, trophic position, or energy flow, potentially due to the low biomass of pulse magnitudes introduced. Resource pulses of moderate or large size generally increased nutrient availability and primary productivity while decreasing water clarity, suggesting that resource pulses can be an important factor influencing shallow eutrophic lakes but that effects may not be proportional to pulse size.

Nearly all ecosystems are contaminated with highly toxic methylmercury (MeHg), but the specific sources and pathways leading to the uptake of MeHg within and among food webs are not well understood. In this study, we report stable mercury (Hg) isotope compositions in food webs in a river and an adjacent forest in northern California and demonstrate the utility of Hg isotopes for studying MeHg sources and cross-habitat transfers. We observed large differences in both δ(202)Hg (mass-dependent fractionation) and Δ(199)Hg (mass-independent fractionation) within both food webs. The majority of isotopic variation within each food web could be accounted for by differing proportions of inorganic Hg [Hg(II)] and MeHg along food chains. We estimated mean isotope values of Hg(II) and MeHg in each habitat and found a large difference in δ(202)Hg between Hg(II) and MeHg (∼2.7‰) in the forest but not in the river (∼0.25‰). This is consistent with in situ Hg(II) methylation in the study river but suggests Hg(II) methylation may not be important in the forest. In fact, the similarity in δ(202)Hg between MeHg in forest food webs and Hg(II) in precipitation suggests that MeHg in forest food webs may be derived from atmospheric sources (e.g., rainfall, fog). Utilizing contrasting δ(202)Hg values between MeHg in river food webs (-1.0‰) and MeHg in forest food webs (+0.7‰), we estimate with a two-source mixing model that ∼55% of MeHg in two riparian spiders is derived from riverine sources while ∼45% of MeHg originates from terrestrial sources. Thus, stable Hg isotopes can provide new information on subtle differences in sources of MeHg and trace MeHg transfers within and among food webs in natural ecosystems.

Although belowground food webs have received much attention, studies concerning microarthropods in nondetrital food webs are scarce. Because adult oribatid mites often number between 250,000–500,000/m2 in coniferous forests, microarthropods are a potential food resource for macroarthropod and vertebrate predators of the forest floor. Although the contribution of microarthropods to aboveground food webs has received little attention, sufficient data concerning macroarthropods and vertebrate predators were available at the Savannah River Site (SRS, Aiken, South Carolina) to construct a food web model of the various trophic interactions. To supplement this analysis, literature of microarthropod predation by arthropods and vertebrates was reviewed. This information was incorporated with the existing data to produce a model for taxa occurring in coniferous forests at the SRS. Because of the diversity and natural history of microarthropod predators, both vertebrate and invertebrate, the resulting web is quite connected and includes transfers to many trophic levels. The diets of arthropods and vertebrates are variable; yet feeding patterns reflect the relative abundance of prey at a place and time. Also, many predators feed on members of their own group. These factors suggest that belowground transfers are deserved of more attention in these and other forest food webs where substantial numbers of detritus feeding invertebrates inhabit the soil/litter interface and are available as prey items. Moreover, this model can be generalized to describe the dynamics of arthropod and vertebrate communities in other coniferous forests. The functioning of terrestrial ecosystems is dependent upon the interrelationships between aboveground and belowground food webs, and transfers of biotic components of the decomposer subsystem to aboveground consumers connect the two subsystems. It is hoped that those consumers traditionally associated with foliage-based food webs be reconsidered, as they may be gaining a proportion of their nutrition from organisms in the detrital pathway.

Habitat loss poses the greatest threat to the survival of a species, and often precipitates the demise of top predators and wide-ranging animals, like the Siberian tiger and the orangutan. Any hope of recovering such critically endangered species depends on understanding what drives changes in population size following habitat contraction. The key question is whether population change is driven directly by changes in habitat volume, or indirectly, through responses to other species of potential predators, prey, and competitors. Ecologists rely on two types of models to predict potential responses to habitat alterations. In single-factor models, population size is controlled by one factor, such as changes in habitat size (as large blocks of forest are fragmented by clear-cutting and development, for example). This is the classic ecological model, in which habitat size drives changes in the abundance of individual species. These models also include “keystone species effects,” which look at how populations respond to the loss of a single top predator, like the tiger. In food-web models, species abundance depends on complex interactions across multiple trophic levels, including energy transfer through the food chain. In a new study, Nicholas Gotelli and Aaron Ellison test the relative contributions of habitat contraction, keystone species effects, and food-web interactions on species abundance, and provide experimental evidence that trophic interactions exert a dominant effect. Until now, direct evidence that trophic interactions play such an important role has been lacking, in part because manipulating an intact food web has proven experimentally intractable, and in part because these different modeling frameworks have not been explicitly compared. Gotelli and Ellison overcame such technical limitations by using the carnivorous pitcher plant (Sarracenia purpurea) and its associated food web as a model for studying what regulates abundance in shrinking habitats. Every year, the pitcher plant, found in bogs and swamps throughout southern Canada and the eastern United States, grows six to 12 tubular leaves that collect enough water to support an entire aquatic food web. The pitcher plant food web starts with ants, flies, and other arthropods unlucky enough to fall into its trap. Midges and sarcophagid fly larvae “shred” and chew on the hapless insect. This shredded detritus is further broken down by bacteria, which in turn are consumed by protozoa, rotifers, and mites. Pitcher plant mosquito larvae feed on bacteria, protozoa, and rotifers. Older, larger sarcophagid fly larvae also feed on rotifers as well as on younger, smaller mosquito larvae. Working with 50 pitcher plants in a bog in Vermont, Gotelli and Ellison subjected the plants to one of five experimental treatments, in which they manipulated habitat size (by changing the volume of water in the leaves), simplified the trophic structure (by removing the top trophic level—larvae of the dipterans fly, midge, and mosquito), did some combination of the two, or none of the above (the control condition). Dipteran larvae and water were measured as each treatment was maintained; both were replaced in the control condition and more water was added in the habitat expansion treatment. These treatments mimic the kinds of changes that occur in nature as habitat area shrinks and top predators disappear from communities. Gotelli and Ellison counted all the pitcher plant residents through the course of an entire field season in which the treatments were applied to the plants. They next evaluated how well the different models—incorporating different assumptions about habitat, keystone species, and food-web interactions—predicted the observed abundances. Overall, food-web models provided more-accurate indicators of species abundance than simple single-factor models, in which the abundance of each species depends on only one variable. The model based on habitat size alone (that is, the water volume), for example, did not do a good job of predicting individual species’ abundances, undercutting the traditional notion that habitat contraction leads to a simple decline in abundance across the board. The best predictors of abundance were models that incorporated trophic structure—including the mosquito keystone model. This model accurately reflected the pitcher plant food web, with mosquito larvae preying on rotifers, and sarcophagid flies preying on mosquito larvae. “Bottom-up” food-web models (in which links flow from prey to predator) predicted that changes in bacteria population size influence protozoa abundances, which in turn affect mosquito numbers, and that changes in bacteria abundance also affect mite numbers, which impact rotifer abundance. This scenario lends support to the model of a Sarracenia food web in which each link in the chain performs a specialized service in breaking down the arthropod prey that is used by the next species in the processing chain. With over 200 million acres of the world’s forestlands destroyed in the 1990s alone, and an estimated 40% increase in the human population by 2050, a growing number of species will be forced to cope with shrinking habitat. Instead of trying to determine how individual species might respond to habitat loss, Gotelli and Ellison argue that incorporating trophic structure into ecological models may yield more-accurate predictions of species abundance—a critical component of species restoration strategies.

Studies of trophodynamics and contaminant bioaccumulation in tropical marine ecosystems are limited. The present study employed stable isotope and trace contaminant analysis to assess sources of primary productivity, trophic interactions, and chemical bioaccumulation behavior in 2 mangrove food webs and 1 offshore coastal marine food web in Singapore. Samples of sediment, phytoplankton, mangrove leaves, clams, snails, crabs, worms, prawns, and fishes were analyzed for stable carbon and nitrogen isotope values, as well as concentrations of persistent organic pollutants. In the mangrove food webs, consumers exhibited similar δ13 C values, probably because of the well-mixed nature of these systems. However, the 2 primary consumers (common nerite and rodong snail) exhibited distinct δ13 C values (-21.6‰ vs -17.7‰), indicating different carbon sources. Fish from Singapore Strait exhibited similar δ13 C values, indicating common carbon sources in this offshore marine food web. The highest trophic level was found in glass perchlet (trophic level = 3.3) and tilapia (trophic level = 3.4) in the 2 mangrove food webs and grunter (trophic level = 3.7) in the Singapore Strait food web. Concentrations of polychlorinated biphenyl (PCB 153) and p,p'-dichlorodiphenyldichloroethylene (p,p'-DDE) concentrations ranged from 0.9 to 84.6 ng/g lipid weight and from <0.2 to 267.4 ng/g lipid weight, respectively. The trophic magnification factors of PCB 153 and p,p'-DDE ranged between 1.63 and 4.62, indicating biomagnification in these tropical marine food webs. The findings provide important information that will aid future chemical bioaccumulation assessment initiatives. Environ Toxicol Chem 2017;36:2521-2532. © 2017 SETAC.

Summary Energy and material flows from dead organic matter, or detritus, to generalist predators have a potential impact on the food web dynamics. However, little is known about how commonly generalist predators depend on detritivorous prey, or the detritus on which the detritivores have fed in terrestrial food webs. To examine this, we measured the diet ages of terrestrial invertebrate and vertebrate consumers (&gt;30 species) at multiple trophic levels in a tropical rain forest, with a particular focus on ants and termites by using radiocarbon (14C). Here, we defined diet age as the lag time between the primary production and the utilization by consumer organisms. The diet ages varied from 0 to &gt;50 years and corresponded to known feeding habits of the consumers. Herbivores such as bees, butterflies, a frugivorous bird and bat, and nectar‐feeding ants had young diet ages (0–3 years). Meanwhile, detritivores such as termites had old diet ages, which increased according to the food resources in the order of litter (6 years), soil (10 years) and wood (≥19 years). The diet ages of predators such as wolf spiders, hunting wasps, army ants, tree shrews and an insectivorous bat were intermediate (2–8 years), indicating the dependence of many predators on detritivores. Because known dietary components of the predators include herbivores and detritivores, the intermediate ages likely indicate the coupling of energy and material flows between plant‐based and detritus‐based food webs. Diet ages of soil‐feeding termite and army ant differed significantly, although a previous study reported that their nitrogen isotope ratios were indistinguishable despite the differing feeding habits. This indicates that radiocarbon can distinguish the two factors, trophic enrichment and the below‐ground processes (humification), both of which could influence the nitrogen isotopic signatures of the terrestrial consumers. Our results show that radiocarbon would provide insights into structures of terrestrial food webs as well as time frame of energy and material flows through the webs.