A stable carbon and nitrogen isotope study of lake food webs in Canada's Boreal Plain

1.  Stable carbon and nitrogen isotope and fish stomach content analyses were used to investigate food webs in five relatively undisturbed lakes on the Boreal Plain of Canada. Stable isotope analysis was also used to determine the importance of external and internal carbon sources.
2.  Overlap in the carbon and nitrogen signatures of primary producers made it difficult to determine unambiguously the feeding habits of many invertebrates. However, isotope analysis suggested that external carbon inputs were detectable in the aquatic food chains of the one lake with a short water residence time («1 year). In the other four lakes, with water residence times ≥1 year, autochthonous carbon was the only detectable carbon source in the food webs.
3.  Food webs in these lakes spanned a range of four to five trophic levels. Both invertebrates and fish appeared to eat a variety of food, often feeding at more than one trophic level.
4.  With the exception of one lake (SPH20), top predators in these lakes, northern pike ( Esox lucius ) and fathead minnows ( Pimephales promelas ), occupied similar trophic positions despite large differences in body size and trophic morphology. In SPH20, where there were two additional fish species, pike occupied a higher trophic position. However, all the top predators in each lake appeared to be omnivores and generalists.
5.  The prevalence of omnivory and the apparent generalist feeding habits of fish in these lakes suggest that organisms are flexible in their feeding habits and that these food webs will be resilient to disturbance.     

Invertebrate food webs along a stream resource gradient

1. The flow of energy through food webs with similar species can vary with both space and time. The river continuum concept (RCC) provides a useful framework for predicting variability in the biota and food availability along streams. We estimated the flow of organic matter (g m^?2 year^?1) through food webs, arrayed along a stream, that had different resource inputs. Four sites were sampled along the Little Tennessee River, North Carolina, U.S.A.: two fifth order sites, one sixth and one seventh order site. The dominant resource is leaf detritus in the upstream reach (the upstream fifth order site), algae in the mid‐reaches (the downstream fifth and sixth order sites), and suspended material downstream (seventh order site). 2. Eleven genera, contributing from 50 to 66% of the total macroinvertebrate secondary production of each site, were studied. We estimated organic matter flow from resource to consumer by combining previously measured rates of invertebrate secondary production with gut content analyses and assimilation efficiencies. 3. Organic matter flow through food webs increased in a downstream direction, while the structure of the food webs remained constant. The total food consumed by the taxa analysed increased from 34 g m^?2 year^?1 at the upstream site to 730 g m^?2 year^?1 at the most downstream site. We estimate that the organic matter consumed by the entire macroinvertebrate community ranged from 66 to 1164 g m^?2 year^?1. These results indicate that there is variation in the magnitude of organic matter flow through the food webs along this river continuum. 4. The dominant food resource consumed also changed along the gradient. Leaf detritus consumption decreased from 58% of the total consumption upstream to 6% downstream, whereas consumption of amorphous detritus increased from 18 to 64%. The proportion of animal material consumed also increased from 3 to 27%. The total consumption of autochthonous resources (diatoms and filamentous algae) increased along the continuum (from 6.41 to 34.05 g m^?2 year^?1). We conclude that these results are related to variation in resource availability, dietary shifts and invertebrate secondary production. These results link resource availability to energy flow, a relationship originally suggested by the RCC.     

Sulphur stable isotopes can distinguish trophic dependence on sediments and plankton in boreal lakes

1. Stable isotopes of carbon are useful for differentiating between freshwater food chains based on planktonic algae or benthic algae, but are reported to be of limited use for identifying food chains based on sedimentary detritus. Because data from marine systems suggest that stable isotopes of sulphur (δ³⁴S values) have potential in this regard, we tested their utility in freshwater lakes.
2. We found that sulphate in the water column of four boreal lakes was enriched in ³⁴S compared to the sulphur in bulk sediments from these lakes. Furthermore, within a given lake, insects known to feed on sediment (directly or via predation) had δ³⁴S values similar to those of sediment, whereas planktonic and benthic invertebrates known to feed on suspended particles had δ³⁴S values similar to those of sulphate in the water column.
3. Using the stable S isotope values of invertebrates that obtain their S from either the sediment or the water column as end members in a two-source mixing model, we show that two fish species obtain their food from both planktonic and sedimentary sources. Furthermore, model results suggest that, as expected, the more benthic-feeding fish species obtains more of its S from the sediment compartment than does the species that feeds in the water-column.
4. Our results suggest that measurements of stable sulphur isotopes provide a means of distinguishing between members of food chains that are based in the water column from those based on sedimentary detritus. As such, they would be a useful complement to stable C isotopes that are used to distinguish between food chains based on planktonic or benthic algae.     

Trophic fractionation of carbon and nitrogen stable isotopes in Chironomus riparius reared on food of aquatic and terrestrial origin

1. Trophic fractionation was studied in short‐term laboratory feeding experiments with larvae of the deposit‐feeding midge Chironomus riparius. Larvae were fed food of terrestrial (oats, peat) and aquatic origin (Spirulina, Tetraphyll^®). 2. By analysing both whole larvae and isolated gut contents we were able to distinguish between the isotopic signature of recently ingested food and that of assimilated carbon and nitrogen in body tissue. Additionally we studied the effects of microbial conditioning, i.e. the colonisation and growth on food particles of microbes, on the isotopic signal of food resources. 3. Nitrogen fractionation for the different food types ranged from 0.67‰ to 2.68‰ between consumer and diet and showed that isotopic fractionation can be much lower than the value of 3.4‰ that is commonly assumed. 4. Microbial degradation of food particles resulted in an approximate doubling of the δ¹⁵N in 8 days, from 6.24 ± 0.05‰ to 11.36 ± 0.56‰. Values for δ¹³C increased only marginally, from ?20.66 ± 0.11‰ to ?20.34 ± 0.12‰. These results show that microbial conditioning of food may affect dietary isotope signatures (in particular N) and, unless accounted for, could introduce an error in measures of trophic fractionation. Microbial conditioning could well account for some of the variation in fractionation reported in the literature.     

Characterization of riparian species and stream detritus using multiple stable isotopes

Multiple stable isotopes were used to determine the effectiveness of distinguishing among several dominant riparian species and aquatic macrophytes both spatially (three sites) and temporally (three seasons) along an 8-km reach of a blackwater stream. The differences in isotopic composition were used to assess contributions of various organic matter sources to the detrital pool of the stream. Samples of riparian and aquatic macrophyte vegetation and detritus were collected at three times to represent early leaf-out (April), mid-summer (August), and just prior to abscission (October). Each sample was analyzed for stable isotopes of carbon ¹³C, nitrogen ¹⁵N, and sulfur ³⁴S Within a site and sampling date, ¹³C-values were significantly different among certain riparian species and detritus samples. Species differences persisted between seasons. ³⁴S values were the most variable of the three elements examined although they remained fairly constant through time within each species and site. The results suggest that temporal changes in isotopic compositions of riparian species and aquatic macrophytes are site-specific. Discriminant analysis dissimilarity plots (based on all three isotopes) demonstrated that the contribution of species to the detrital pool depended on the site and season. At the upper site, detritus was isotopically most similar to Quercus laurifolia and Sparganium americanum in April, and the aquatic macrophytes (S. americanum and Potamogeton spp.) in August and October. At the middle site, detritus was most similar to Carpinus caroliniana and Q. nigra in April but no single source was similar to detritus in August or October. At the lower site, detritus was most similar to Taxodium distichum for all three seasons.     

The impact of climate change on the structure of Pleistocene food webs across the mammoth steppe

Species interactions form food webs, impacting community structure and, potentially, ecological dynamics. It is likely that global climatic perturbations that occur over long periods of time have a significant influence on species interaction patterns. Here, we integrate stable isotope analysis and network theory to reconstruct patterns of trophic interactions for six independent mammalian communities that inhabited mammoth steppe environments spanning western Europe to eastern Alaska (Beringia) during the Late Pleistocene. We use a Bayesian mixing model to quantify the contribution of prey to the diets of local predators, and assess how the structure of trophic interactions changed across space and the Last Glacial Maximum (LGM), a global climatic event that severely impacted mammoth steppe communities. We find that large felids had diets that were more constrained than those of co-occurring predators, and largely influenced by an increase in Rangifer abundance after the LGM. Moreover, the structural organization of Beringian and European communities strongly differed: compared with Europe, species interactions in Beringian communities before—and possibly after—the LGM were highly modular. We suggest that this difference in modularity may have been driven by the geographical insularity of Beringian communities.     

Detecting trophic‐level variation in consumer assemblages

1. Stable isotopes of nitrogen are useful for quantifying the trophic structure of food webs, but only if the variation in trophic enrichment (Δ_N), which is the difference in δ¹⁵N between a consumer and its food, is small relative to the value of Δ_N itself. 2. We examined the sources of variation in zooplankton Δ_N by measuring the trophic enrichment (Δ_N) of seven species of freshwater cladocerans, and by testing for an effect of age and temperature on the Δ_N of Daphnia pulicaria. 3. We found that Δ_N was similar among Cladocera and was not correlated with body size. Overall, the Δ_N for D. pulicaria was 1.4‰ (SE = 0.69, n = 57), as was expected for the detritus diet that we used in our experiments. We found no effect of temperature (15–25 °C) on Δ_N, but found that Δ_N of D. pulicaria increased with increasing age (10–30 days). 4. We developed a new method to test for trophic‐level variation in a group of consumers that explicitly accounts for the uncertainty in Δ_N. Using this approach, we confirmed that natural assemblages of zooplankton feed at several trophic levels in lake food webs.     

Effects of an invasive crayfish on trophic relationships in north‐temperate lake food webs

1. The introduction of invasive species is one of the main threats to global biodiversity, ecosystem structure and ecosystem processes. In freshwaters, invasive crayfish alter macroinvertebrate community structure and destroy macrophyte beds. There is limited knowledge on how such invasive species‐driven changes affect consumers at higher trophic levels. 2. In this study, we explore how the invasive rusty crayfish Orconectes rusticus, a benthic omnivore, affects benthic macroinvertebrates, as well as the broader consequences for ecosystem‐level trophic flows in terms of fish benthivory and trophic position (TP). We expected crayfish to decrease abundance of benthic macroinvertebrates, making most fish species less reliant on benthic resources. We expected crayfish specialists (e.g. Lepomis sp. and Micropterus sp.) to increase their benthic dependence. 3. In 10 northern Wisconsin lakes, we measured rusty crayfish relative abundance (catch per unit effort, CPUE), macroinvertebrate abundance, and C and N stable isotope ratios of 11 littoral fish species. We used stable isotope data and mixing models to characterise the trophic pathways supporting each fish species, and related trophic structure to crayfish relative abundance, fish body size and abiotic predictors using hierarchical Bayesian models. 4. Benthic invertebrate abundance was negatively correlated with rusty crayfish relative abundance. Fish benthivory increased with crayfish CPUE for all 11 fish species; posterior probabilities of a positive effect were >95%. TP also increased slightly with crayfish CPUE for some species, particularly smallmouth bass, largemouth bass, rock bass and Johnny darter. Moreover, both fish body size and lake abiotic variables explained variation in TP, while their effects on benthivory were small. 5. Rusty crayfish abundance explained relatively little of the overall variation in fish benthivory and TP. Although rusty crayfish appear to have strong effects on abundances of benthic macroinvertebrates, energy flow pathways and trophic niches of lentic fishes were not strongly influenced by invasive rusty crayfish.     

Trophic relationships in a tropical stream food web assessed by stable isotope analysis

1. Stable isotope analysis, coupled with dietary data from the literature, was used to investigate trophic patterns of freshwater fauna in a tropical stream food web (Guadeloupe, French West Indies).
2. Primary producers (biofilm, algae and plant detritus of terrestrial origin) showed distinct δ¹³C signatures, which allowed for a powerful discrimination of carbon sources. Both autochthonous (¹³C-enriched signatures) and allochthonous (¹³C-depleted signatures) resources enter the food web. The migrating behaviour of fishes and shrimps between marine and freshwater during their life cycles can be followed by carbon isotopes. Here, shrimp δ¹³C signatures were shown to shift from −16‰ (for juveniles under marine influence) to −24.7‰ (for adults in freshwater habitats). For resident species, δ¹³C values partly reflected the species' habitat preferences along the river continuum : species living in river mouths were ¹³C-enriched in comparison with those collected upstream.
3. Nitrogen isotopic ratios were also discriminating and defined three main trophic guilds among consumers. The δ¹⁵N values of herbivores/detritivores were 5.0–8.4‰, omnivores 8.8–10.2‰ and carnivores 11–12.7‰.
4. Mixing model equations were employed to calculate the possible range of contribution made by respective food sources to the diet of each species. The results revealed the importance of omnivorous species and the dependence of riverine biota on terrestrial subsidies, such as leaf detritus and fruits. Finally, the abundance of shrimps and their feeding habits placed in relief their key role in tropical freshwater food webs. Isotopic analysis provides a useful tool for assessing animal feeding patterns.     

Tracing Mississippi River influences in estuarine food webs of coastal Louisiana

The Breton Sound estuary in southern Louisiana receives large amounts of Mississippi River water via a controlled diversion structure at the upstream end of the estuary. We used stable isotopes to trace spatial and seasonal responses of the downstream food web to winter and spring introductions of river water. Analysis of δ¹³C, δ¹⁵N, and δ³⁴S in the common local consumers such as grass shrimp (Palaemonetes sp.), barnacles (Balanus sp.), and small plankton-feeding fish (bay anchovies, Anchoa mitchilli) showed that the diversion was associated with two of the five major source regimes that were supporting food webs: a river regime near the diversion and a river-influenced productive marsh regime farther away from the diversion. Mixing models identified a third river-influenced source regime at the marine end of the estuary where major natural discharge from the Bird’s Foot Delta wraps around into estuarine waters. The remaining two source regimes represented typical estuarine conditions: local freshwater sources especially from precipitation and a brackish source regime representing higher salinity marine influences. Overall, the Mississippi River diversion accounted for 75% of food web support in the upper estuary and 25% in the middle estuary, with influence strongest along known flow pathways and closest to the diversion. Isotopes also traced seasonal changes in river contributions, and indicated increased plant community productivity along the major flow path of diversion water. In the Breton Sound estuary, bottom–up forcing of food webs is strongly linked to river introductions and discharge, occurring in spatial and temporal patterns predictable from known river input regimes and known hydrologic circulation patterns.     

Alteration of trophic interactions between periphyton and invertebrates in an acidified stream: a stable carbon isotope study

The hypothesis according to which proliferation of periphytic algae under acid conditions results from a release of grazing pressure is tested. Stable carbon isotope analysis is used to investigate the autochthonous/allochthonous balance of invertebrate feeding in streamside artificial channels that were experimentally acidified. We find that the relative contribution of autochthonous food sources (epilithon) to total invertebrate biomass was slightly lower (after 1 mo of acidification) or not altered (after 2 mo) under acidified conditions when compared with a control. Feeding shifts were exhibited by some invertebrate taxa and provided evidence that acidification modifies trophic interactions between attached algae and primary consumers. Cross-treatment calculations showed that reduction of grazing pressure after the first month of acidification was an effect rather than the cause of periphyton proliferation. Our approach using stable carbon isotope analysis and biomass measurements of macroinvertebrates allows the quantification of the trophic base of lotic secondary producer communities under both experimental and natural conditions.     

Incorporation of marine-derived nutrients from petrel breeding colonies into stream food webs

1. Stable isotope ratios of aquatic invertebrates, aquatic mosses and leaves of riparian plants were used to determine whether marine‐derived nutrients from breeding colonies of the Westland petrel (Procellaria westlandica) were incorporated into the food webs of small streams in New Zealand. 2. The δ¹⁵N signatures of all plants and animals examined were higher by 3.6–4.6‰ in small streams draining catchments with petrel colonies than in nearby streams where petrels were absent. δ¹³C values of leaves from terrestrial plants were also enriched by about 2‰ where petrels were present, but the carbon ratios of aquatic species were depleted in ¹³C, rather than enriched, suggesting that any marine signal was over‐ridden by isotopic shifts related to photosynthetic fractionation. 3. A high marine‐nitrogen signal was maintained along the 3 km length of Scotchman Creek with the δ¹⁵N values of leptophlebiid mayflies and predatory insects ranging from 7.4–9.5 and 9.2–11.9‰, respectively. 4. Most nutrients derived from petrels are likely to be translocated to streams via the soil, which they enter in the form of excreta, spilled food, feathers, dead chicks, and abandoned eggs. However, because changes in δ¹⁵N values are brought about by soil processes such as volatilisation of ammonia, nitrification and denitrification, it is difficult to predict the exact isotope signature of nitrogen entering a stream. Tentative estimates of the proportion of marine‐derived nitrogen in stream biota, calculated using a mass‐balance approach, ranged from 28–38%. 5. Our findings indicate that marine nutrients transported inland by seabirds can be incorporated into the food webs of streams. In pre‐human times when there were many more seabird colonies on mainland New Zealand than exist today, marine‐derived nutrients introduced by birds may have had significant effects on nitrogen cycling and the productivity of New Zealand streams.     

Establishing pathways of energy flow for insect predators using stable isotope ratios: field and laboratory evidence

 Quantifying pathways of energy transfer between plants, pests, and beneficial insects is a necessary step toward maintaining pest stable agroecosystems in the absence of chemical subsidies. A diet switching experiment utilizing a predatory ladybird beetle, Hippodamia variegata (Goeze), evaluated the use of naturally occurring stable C and N isotopes as an economically feasible and safe method for quantifying pathways of energy flow within agroecosystems. Stable isotope values of the ladybird beetle Coleomegilla maculata lengi (Timberlake) collected from an agroecosystem were used to estimate the relative amount of C and N derived from agricultural plants and incorporated by ladybird beetles based on mass balance equations. At the beginning of the diet-switching experiment δ¹³C and δ¹⁵N values of H. variegata (–12.0‰ and 6.3‰, respectively) differed by –0.2‰ and 2.9‰ from the aphids that were provided exclusively as their diet. These data are consistent with previous estimates of trophic level isotope effects. After switching the diet of H. variegata to an alternative food, isotope values of H. variegata gradually shifted toward expected values for individuals fed this diet (–22.9‰ and 8.8‰ for δ¹³C and δ¹⁵N values, respectively). Isotope values of another ladybird beetle, C. maculata, collected from the field indicated that in May, alfalfa and maize (pollen) obtained in the previous year contributed 32% and 68% of the C or N to the diets of these individuals and in August, 52%, 6%, and 42% of the C or N assimilated by these insects was derived from alfalfa, wheat, and maize, respectively. These data are consistent with expectations based on the relative abundance of C. maculata in various crops during the season. The field and laboratory data are a clear indication that isotope values are sensitive to dietary changes on a relatively short time scale (days) and provide a strong basis for the use stable C and N isotope to trace energy flow patterns of these beneficial organisms within agroecosystems. Received: 17 November 1995 / Accepted: 20 June 1996     

Linking aquatic and terrestrial food webs – Odonata in boreal systems

1. It is increasingly realised that aquatic and terrestrial systems are closely linked. We investigated stable isotope variations in Odonata species, putative prey and basal resources of aquatic and terrestrial systems of northern Mongolia during summer. 2. In permanent ponds, δ¹³C values of Odonata larvae were distinctly lower than those of putative prey, suggesting that body tissue comprised largely of carbon originating from isotopically light carbon sources. Presumably, prey consumed during autumn and winter when carbon is internally recycled and/or methanotrophic bacteria form an important basal resource of the food web. In contrast, in a temporary pond, δ¹³C values of Odonata larvae were similar to those of putative prey, indicating that their body carbon originated mainly from prey species present. 3. Changes in δ¹⁵N and δ¹³C values between larvae and adults were species specific and reflected differential replacement of the larval isotopic signature by the terrestrial diet of adult Odonata. The replacement was more pronounced in Odonata species of permanent ponds than in those of the temporary pond, where larvae hatched later in the year. Replacement of larval carbon varied between tissues, with wings representing the larval isotopic signature whereas thoracic muscles and eggs reflected the δ¹⁵N and δ¹³C values of the terrestrial diet of adults. 4. The results suggest that because of their long larval development, Odonata species of permanent ponds carry the larval signature, which is partly replaced during their terrestrial life. Terrestrial prey forms the basis for egg production and thus the next generation of aquatic larvae. In temporary ponds, in contrast, Odonata species rely on prey from a single season, engage in a prolonged aquatic phase and hatch later, leaving less time to acquire terrestrial prey resources for offspring production. Stable isotope analysis provided important insights into the food webs of the waterbodies and their relationship to the terrestrial system.     

Tracing origins and migration of wildlife using stable isotopes: a review

To understand the ecology of migratory animals it is important to link geographic regions used by individuals including breeding, wintering, and intermediate stopover sites. Previous conventional approaches used to track animal movements have relied on extrinsic markers and typically the subsequent recovery of individuals. This approach has generally been inappropriate for most small, or non-game animals. The use of intrinsic markers such as fatty acid profiles, molecular DNA analyses, and the measurement of naturally occurring stable isotopes in animal tissues offer alternative approaches. This paper reviews the use of stable isotope analyses (primarily δ¹³C, δ¹⁵N, δ³⁴S, δD, δ⁸⁷Sr) to trace nutritional origin and migration in animals. This approach relies on the fact that foodweb isotopic signatures are reflected in the tissues of organisms and that such signatures can vary spatially based on a variety of biogeochemical processes. Organisms moving between isotopically distinct foodwebs can carry with them information on the location of previous feeding. Such an approach has been used to track animal use of inshore versus offshore, marine versus freshwater, terrestrial C₃ versus marine, terrestrial mesic versus xeric, and C₃ versus C₄ or Crassulacean acid metabolism foodwebs. More recently, the use of stable hydrogen isotope analyses (δD) to link organisms to broad geographic origin in North America is based on large-scale isotopic contours of growing-season average δD values in precipitation. This technique, especially when combined with the assay of other stable isotopes, will be extremely useful in helping to track migration and movement of a wide range of animals from insects to birds and mammals. Future research to refine our understanding of natural and anthropogenic-induced isotopic gradients in nature, and to explore the use of stable isotopes of other elements, is recommended. Received: 1 July 1998 / Accepted: 9 December 1998     

应用稳定同位素测定贵州凤冈麻湾洞洞穴陆生动物的食物来源及营养级

以贵州凤冈麻湾洞洞穴生态系统为研究对象,运用δ¹³C、δ¹⁵N测定了洞穴动物及其有机碳源的同位素比值,分析了洞穴生态系统的营养级关系及洞穴动物食源。结果表明:洞内植物δ¹³C范围为-41. 78‰～-38. 80‰,较洞外植物低;δ¹⁵N范围为-1. 31‰～1.23‰,在洞外陆源有机质δ¹⁵N范围内;洞穴土壤有机质的δ¹³C范围为-31. 09‰～-24.95‰,δ¹⁵N范围为-1.08‰～7.72‰;洞穴动物δ¹³C范围为-30.41‰～-12.02‰,δ¹⁵N范围为2.07‰～8.94‰;洞穴土壤有机质对动物的食源贡献率超过72%,远高于植物对动物的食源贡献率,即洞穴土壤有机质是洞穴动物的主要食物来源。麻湾洞生态系统主要由4个营养层次组成:植物为第一营养层次;闪夜蛾、螺类、马陆类处于第二营养层次;裸灶螽、长头地蜈蚣处于第三营养层次;蜘蛛类处于第三或第四营养层次。即大部分同种(或同类群)...