Dual‐tracer‐based isotope turnover rates in a highly invasive mysid Limnomysis benedeni from Lake Constance

Understanding the ecological patterns of invasive species and their habitats require an understanding of the species’ foraging ecology. Stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values provide useful information into the study of animal ecology and evolution, since the isotope ratios of consumers reflect consumer's dietary patterns. Nevertheless, the lack of species‐ and element‐specific laboratory‐derived turnover rates could limit their application. Using a laboratory‐based dual stable isotope tracer approach (Na¹⁵NO₃ and NaH¹³CO₃), we evaluated the δ¹⁵N and δ¹³C isotope turnover rates in full‐grown adult invasive Limnomysis benedeni from Lake Constance. We provide δ¹⁵N and δ¹³C turnover rates based on nonlinear least‐squares regression and posterior linear regression models. Model precisions and fit were evaluated using Akaike's information criterion. Within a couple of days, the δ¹⁵N and δ¹³C of mysids began to change. Nevertheless, after about 14 days, L. benedeni did not reach equilibrium with their new isotope values. Since the experiment was conducted on adult subjects, it is evident that turnover was mainly influenced by metabolism (in contrast to growth). Unlike traditional dietary shifts, our laboratory‐based dual stable isotope tracer approach does not shift the experimental organisms into a new diet and avoids dietary effects on isotope values. Results confirm the application of isotopic tracers to label mysid subpopulations and could be used to reflect assimilation and turnover from the labeled dietary sources. Field‐based stable isotope studies often use isotopic mixing models commonly assuming diet‐tissue steady state. Unfortunately, in cases where the isotopic composition of the animal is not in equilibrium with its diet, this can lead to highly misleading conclusions. Thus, our laboratory‐based isotopic incorporation rates assist interpretation of the isotopic values from the field and provide a foundation for future research into using isotopic tracers to investigate invasion ecology.     

Factors controlling the stable isotope composition and C:N ratio of seston and periphyton in shallow lake mesocosms with contrasting nutrient loadings and temperatures

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Importance of multi-dimensional analyses of resource partitioning in highly mobile species assemblages

Resource partitioning is an essential mechanism enabling species coexistence. The resources that are used by an animal are linked to its morphology and ecology. Therefore, similar species should use similar resources. The ecological niche of an individual summarizes all used resources and is therefore composed of several dimensions. Many methods are established to study different dimensions of an animal's niche. The aim of this study was to demonstrate that a combination of suitable methods is needed to study spatial and dietary resource partitioning of sympatric species in detail. We hypothesized that, while each individual method might identify differences between species, the combined results of several methods will lead to a more complete picture of spatial and dietary resource partitioning. As model organisms we chose the sympatric insectivorous bat species Myotis bechsteinii, M. nattereri, and P. auritus. We examined horizontal habitat use by telemetry, vertical habitat use by measuring δ¹³C, trophic position by measuring δ¹⁵N in wing membrane, and diet composition by molecular fecal analysis. Our results show that each method is able to provide information about spatial/dietary resource partitioning. However, considering further dimensions by combining several methods allows a more comprehensive assessment of dietary and spatial resource partitioning in bats.     

Terrestrialization alters organic matter dynamics and habitat quality for freshwater mussels (Unionoida) in floodplain backwaters

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Resource partitioning of sympatric small mammals in an African forest‐grassland vegetation mosaic

It is often hypothesized that two species competing for the same resource cannot stably coexist unless they partition their resources in space and time. More recently stable isotope analyses have complemented traditional, observation‐based niche research by conceptualizing many of the characteristics of communities, for example, trophic niche width and the partitioning of resources. Here we quantify resource partitioning of sympatric small mammal species in an African ecosystem by analysing stable isotope ratios of hair collected from a South African forest‐grassland vegetation mosaic, and combine this with known spatial and temporal behavioural data to interpret community competition and resource partitioning. We observe niche separation to different degrees across the entire community, with different species displaying either unique isotopic dietary preferences, or partitioning resources in space and/or time. δ¹³C values were more enriched in species that inhabited afromontane grassland compared with those that inhabited afromontane forest, a reflection of the dominant vegetation in each habitat. Contrary to expectations, arboreal rodents occupied higher trophic positions than terrestrial rodents and approaching δ¹⁵N values similar to insectivorous shrews, suggesting that arboreal rodents feed on items such as arthropods enriched in ¹⁵N. While grassland species display phenotypic plasticity in terms of dietary preferences, small mammals that occurred in forests display narrow niche preferences, suggesting these species may be particularly sensitive to habitat modifications. Our results illustrate that the use of stable isotopes can be used in conjunction with spatial and temporal behavioural knowledge to elucidate resource partitioning in small African mammal communities.     

Sulfur stable isotope signature identifies the source of reduced sulfur in benthic communities in macrophyte zones of Lake Biwa, Japan

Carbon, nitrogen and sulfur stable isotope ratios (δ¹³C, δ¹⁵N and δ³⁴S) were measured from water column sulfate, sediments, particulate organic matter (POM), macrophytes, periphyton, macroinvertebrates and fish, sampled from the littoral, open water and macrophyte zones of Lake Biwa. In most of the littoral zones, the δ¹³C and δ¹⁵N values of organisms indicated that POM and periphyton support the consumers. However, in the dysoxic interior macrophyte (IM) zone, the δ¹³C values of Sinotaia quadrata histrica, Propsilocerus akamusi and Anodonta woodiana were lower than that of all resources. The δ¹⁵N values of S. quadrata histrica were lower than those of P. akamusi and A. woodiana. δ¹³C and δ¹⁵N values thus failed to distinguish the foods of these consumers. The δ³⁴S values of sediment and S. quadrata histrica were lower than those of water column sulfate, suggesting that this consumer incorporated reduced sulfur derived from sulfate reduction in the sediment by ingesting detritus. In contrast, the δ³⁴S values of P. akamusi and A. woodiana were higher than that of S. quadrata histrica, suggesting that they incorporated sulfur derived from water column sulfate by ingesting POM. Consequently, δ¹³C, δ¹⁵N and δ³⁴S signatures provide complementary estimates of foods for consumers in this freshwater lake.     

Global dataset for carbon and nitrogen stable isotope ratios of lotic periphyton

Carbon and nitrogen stable isotope ratios (δ¹³C and δ¹⁵N) have been widely employed in food web analysis. In lotic environments, periphyton is a major primary producer that makes a large contribution to food web production as well as carbon and nitrogen cycling. While the δ¹³C and δ¹⁵N values have many advantages as a natural tracer, the controls over their high spatial and temporal variability in stream periphyton are not well known. Here, we present the global dataset of δ¹³C and δ¹⁵N values of lotic periphyton from 54 published and two unpublished sources, including 978 observations from 148 streams/rivers in 38 regions around the world, from arctic to tropical sites. The 54 published sources were articles recorded during the period of 1994–2016 in 25 academic journals. The two unpublished sources were from the authors’ own data. The dataset showed that δ¹³C and δ¹⁵N values of periphyton ranged from ?47.3 to ?9.3‰ and from ?5.6 to + 22.6‰, respectively. The dataset also includes physicochemical factors (altitude, coordinates, catchment area, width, depth, geology, vegetation, canopy coverage, biome, season, presence of anadromous salmon, temperature, pH, current velocity, and discharge), nutrient data (nitrate and ammonium concentrations), and algal attributes (chlorophyll a concentration, algal species compositions, and carbonates removal) in streams/rivers studied, all of which may help interpret the δ¹³C and δ¹⁵N values of periphyton. The metadata file outlines structure of all the data and with references for data sources, providing a resource for future food web studies in stream and river ecosystems.     

Evidence for dynamic resource partitioning between two sympatric reef shark species within the British Indian Ocean Territory

Stable-isotope analyses (δ¹³C, δ¹⁵N and δ³⁴S) of multiple tissues (fin, muscle, red blood cells and plasma), revealed ontogenetic shifts in resource use by grey reef sharks Carcharhinus amblyrhynchos and resource partitioning with silvertip sharks Carcharhinus albimarginatus within the British Indian Ocean Territory marine protected area (MPA). Resource partitioning varied temporally, with C. albimarginatus feeding on more pelagic prey during October to January, potentially attributable to an influx of pelagic prey from outside the MPA at that time. Reef sharks may therefore be affected by processes outside an MPA, even if the sharks do not leave the MPA.     

Resource partitioning between two young-of-year cownose rays Rhinoptera bonasus and R. brasiliensis within a communal nursery inferred by trophic biomarkers

Although interspecific trophic interactions plays a principal role within elasmobranch communal nurseries, little is known over variation in foraging strategies adopted by young-of-year of sympatric species. To test the hypothesis of dietary resource partitioning between batoids within a communal nursery, we investigated two cownose ray species, Rhinoptera bonasus and R. brasiliensis, which occur in heterospecific groups, a strategy predicted to increase survival and foraging success. Using two biochemical tracers, fatty acids (FA) and stable isotopes (δ¹⁵N and δ¹³C), the combined effects of maternal investment and the formation of heterospecific groups implying competition for, or partitioning of available food resources were investigated. Through univariate and multivariate analyses of biochemical tracers in several tissues (fin clip, muscle, liver, red blood cells; RBC) and plasma, our results revealed significant interspecific differences in tracers between the two species. Total FAs (∑saturated FA, ∑monounsaturated FA and ∑polyunsaturated FA) and trophic biomarkers (i.e., docosahexaenoic acid, arachidonic acid, oleic acid and δ¹⁵N) were the principle tracers responsible for the differences detected. These data revealed that R. brasiliensis was less enriched in physiologically important essential FAs than R. bonasus. Our findings suggest that these congeneric species differ in maternal investment strategy and moderately partition food resources over relatively fine spatial scales within a single nursery habitat to limit competition. These results provide further knowledge on the foraging strategies adopted by batoids in communal nursery areas, information that is required for improving spatial conservation and management planning.     

Thermal habitat segregation among morphotypes of whitefish (Coregonus lavaretus: Salmonidae) and invasive vendace (C. albula): a mechanism for co‐existence?

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Feeding strategies and elemental composition in Ponto‐Caspian peracaridans from contrasting environments: can stoichiometric plasticity promote invasion success?

1. Ponto‐Caspian peracaridans, and mysids and amphipods in particular, are among the most successful aquatic invaders. However, species differ in the trophic‐status range of ecosystems they can invade while establishment rates and impacts can vary substantially between habitats. There is limited knowledge of the environmental factors and species characteristics that drive such variation in invasion success. 2. Here we test how trophic level and body stoichiometry vary among peracaridan species and in relation to body size. The amphipod Pontogammarus robustoides and the mysids Limnomysis benedeni and Paramysis lacustris were investigated in ecosystems differing considerably in productivity and nutrient supply, namely an N‐limited eutrophic lagoon and P‐limited mesotrophic lakes. 3. As revealed by stable isotope (¹⁵N/¹⁴N) analysis, herbivory was inferred to be the main feeding mode of L. benedeni. In contrast, the mysid P. lacustris and the amphipod P. robustoides displayed a higher propensity for predatory feeding at larger body sizes, a pattern that was more pronounced in the eutrophic lagoon than in the mesotrophic lakes. 4. Their mean stoichiometric composition (P. robustoides C:N:P 108:20:1, L. benedeni 92:21:1 and P. lacustris 93:22:1) demonstrates that these peracaridans are rich in nutrients, especially nitrogen. They all exhibited the same ontogenetic pattern of reduced stoichiometric regulation during juvenile stages and stricter homoeostasis at older stages. 5. The higher P content in juveniles of all peracaridan species from the lagoon indicates higher potential somatic and population growth rates than those in the mesotrophic lakes. Such a difference may explain the substantially faster rates of invader establishment observed in the lagoon in comparison with lakes of low trophy. 6. Due to differences in ontogenetic and habitat‐induced variation, the study species differed significantly in stoichiometric variability, which was lowest in L. benedeni and highest in P. robustoides. The ranges of species‐specific variation in stoichiometric ratios corresponded to the trophic (by chlorophyll a) and nutrient stoichiometry (N:P) ranges of lentic waters successfully invaded by these species in Lithuania. 7. Stoichiometric plasticity, which should be associated with flexibility of feeding strategy, may enhance the potential of peracaridan species to successfully invade habitats with differing trophy and nutrient supply. The optimal feeding strategy should be omnivory with a propensity for predatory feeding, which can be adjusted with respect to ontogenetic nutrient demands and resource availability. Invading species may have a stronger effect on the local biota in ecosystems with high P levels, which promote growth, and N limitation that should favour predation.     

Morphological and trophic specialization in a subterranean amphipod assemblage

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Comparison of the exploitation of methane-derived carbon by tubicolous and non-tubicolous chironomid larvae in a temperate eutrophic lake

Carbon and nitrogen stable isotope ratios (δ¹³C and δ¹⁵N) in three sympatric species of larval chironomids were analyzed in a temperate eutrophic shallow lake in Japan. Markedly lower δ¹³C values were reported in Chironomus plumosus (?51.2 ‰) and Tanypus sp. (?43.5 ‰) than those in photoautotrophic carbon sources [particulate organic matter (POM) and sediment]. There were positive correlations between δ¹³C and δ¹⁵N in the two chironomid species. These results indicated that they assimilated carbon derived from biogenic methane by exploiting methane-oxidizing bacteria (MOB). In contrast, Propsilocerus akamusi exhibited similar δ¹³C values to those of POM or sediment. A δ¹³C-based isotope mixing model was used to estimate the dietary contributions of MOB to each chironomid species. The mean contributions ranged from 11 to 15 % in C. plumosus, 13 to 19 % in Tanypus sp., but only up to 5 % in P. akamusi. In an aquarium, we observed that individuals of C. plumosus and Tanypus sp., which exhibited low δ¹³C values, built U-shaped larval tubes in the sediment, and an oxidized layer developed around these tubes. Propsilocerus akamusi did not exhibit this behavior. These results suggest that tube building may provide larval chironomids with greater access to methane-derived carbon through increased opportunities to feed on MOB.     

Effects of leaf litter and its fungal colonization on the diet of Limnomysis benedeni (Crustacea: Mysida)

The strong invasive freshwater mysid Limnomysis benedeni, a detritivorous–herbivorous feeder, has a preference for small food particles, but also feeds on leaf litter. Here, we tested whether leaf litter consumption by L. benedeni depends on the tree species and leaf conditioning (two types of physical and biological leaf conditioning). At the physical leaf conditioning, L. benedeni was fed with shortly leached or extensively leached leaves of five tree species in laboratory food assays. The mysid consumed shortly leached leaves of Copper Beech, Lombardy Poplar, Common Oak, and especially White Willow, and did not feed on shortly leached Black Alder leaves. The consumption of extensively leached leaves by L. benedeni did not depend on the tree species. Overall, 74% of the variation of the leaf consumption by L. benedeni was explained by the significant interaction of the factors carbon content and polyphenol content of the leaves, caused the feeding strategy of L. benedeni. For the biological leaf conditioning, the mysids consumed to a high degree naturally conditioned leaves, followed by leaves colonized by one of three fungi, but oomycete-colonized leaf litter and autoclaved leaves were consumed at similar low levels. Our results indicate that L. benedeni feeds on different types of conditioned leaves to different extents, and therefore may affect leaf litter degradation in many invaded freshwaters.     

One meadow for two sparrows: resource partitioning in a high elevation habitat

Resource partitioning is the basis of the coexistence of sympatric species and has therefore received much attention in ecological studies. However, how variation in environmental conditions (and particularly natural variation in resource availability) can influence resource partitioning in free-ranging animals is not well understood. In the present study, we addressed the hypothesis that natural changes in the availability of food resources affect food partitioning between sympatric species. To do so, we examined temporal changes in the plasma isotopic signature (δ(15)N and δ(13)C) of syntopic Lincoln's sparrows Melospiza lincolnii and white-crowned sparrows Zonotrichia leucophrys, in parallel with seasonal changes in habitat maturity and food availability from spring to early summer. We found no apparent trophic segregation between Lincoln's and white-crowned sparrows when resources were scarce in spring. But, interestingly, as resource availability and the number of breeding birds increased, Lincoln's sparrows showed lower δ(15)N values than white-crowned sparrows, as they consumed more prey from lower trophic levels and less prey from higher trophic levels. This feeding divergence between sympatric species may be explained (1) by a change in foraging preferences and opportunities for Lincoln's sparrows and (2) by the abundance of competitors that increased faster than resources, thus promoting interspecific competition and trophic segregation. These results provide clear evidence that trophic segregation is dynamically tied to variation in environmental conditions, which are therefore fundamental to consider when examining resource partitioning between co-existing species.     

Factors influencing stable nitrogen isotope ratios in wing membranes of insectivorous bat species: A field study

Nitrogen stable isotope analysis studies have become a useful tool in dietary studies to quantify differences in diet composition among species or individuals. However, laboratory studies have revealed several factors that influence the nitrogen isotope ratios (δ¹⁵N) in animal tissues (e.g. habitat, amount of ingested food, and metabolic rate). The influence of these factors has not been validated for free-ranging bat species, which is important for interpreting nitrogen isotope data in field studies. In this study, we measured δ¹⁵N from wing membranes (δ¹⁵N_w) and habitat samples (δ¹⁵N_h; soil and leaf, or sediment) to test for effects of diet, age, and individual energy demand in three free-living bat species (Myotis daubentonii, Nyctalus noctula and Nyctalus leisleri). We hypothesised that based on differences in diet composition δ¹⁵N_w values should increase in the sequence M. daubentonii, N. leisleri, and highest N. noctula. Furthermore, juveniles should have significantly lower δ¹⁵N_w compared to their mothers. Thirdly, the δ¹⁵N_w values of reproductively active individuals should be significantly higher than those of non-reproductive individuals. Values of δ¹⁵N_w were significantly influenced by differences in feeding ecology among species and individual reproductive status, but not by animal age. Our results show that species feeding on primary consumers have lower δ¹⁵N_w values than species feeding on secondary and tertiary consumers. Further, independent young did not differ in their δ¹⁵N_w values from adults suggesting that their tissues already reflect the insect diet. The effect of reproductive status varied among species which might reflect intra-specific differences in foraging behaviour of generalist vs. specialist species. In this study, we demonstrated that δ¹⁵N can provide information on the dietary range of bats, but researchers should account for variation owing to reproductive status, habitat, and species.     

Unique seasonal forage bases within a local population of bottlenose dolphin (Tursiops truncatus)

Using photo‐identification data, bottlenose dolphin (Tursiops truncatus) populations can be differentiated based on their use of particular estuaries or coastal habitats. Questions remain, however, about the validity of such fine‐scale population partitioning and whether the resulting assemblages utilize unique forage bases. To address the issue of forage base use, stable isotopes of carbon (δ¹³C), nitrogen (δ¹⁵N) and sulfur (δ³⁴S) were analyzed from skin tissues (n= 74) of bottlenose dolphins sampled seasonally along the coast and in three estuaries near Charleston, South Carolina. Autumn values of δ³⁴S, δ¹⁵N, and δ¹³C and summer values of δ³⁴S indicated that dolphins sampled from these four assemblages utilized unique forage bases, despite limited sample sizes. Likewise, autumn and spring differences in δ¹⁵N and δ¹³C values were evident in the North Edisto River, and in δ³⁴S from dolphins sampled from all three estuarine assemblages; no seasonal differences were identified in the coastal assemblage. Results demonstrate the importance of considering spatial and temporal variation in forage base when developing local management plans for bottlenose dolphin and highlight the discriminatory power of δ³⁴S for estuarine and coastal marine mammals. These results also suggest that stable isotopes could be developed as a complementary tool for photo‐identification based partitioning of bottlenose dolphin populations.     

Questioning assumptions of trophic behavior in a broadly ranging marine predator guild

We evaluated whether existing assumptions regarding the trophic ecology of a poorly‐studied predator guild, northwest (NW) Atlantic skates (family: Rajidae), were supported across broad geographic scales. Four hypotheses were tested using carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotope values as a proxy for foraging behavior: 1) species exhibit ontogenetic shifts in habitat and thus display a shift in ¹³C with differential use of the continental shelf; 2) species exhibit ontogenetic prey shifts (i.e. from smaller to larger prey items) and become enriched in ¹⁵N; 3) individuals acquire energy from spatially confined local resource pools and exhibit limited displacement; and 4) species exhibit similarly sized and highly overlapping trophic niches. We found some evidence for ontogenetic shifts in habitat‐use (δ¹³C) for thorny and little skate and diet (δ¹⁵N) of thorny and winter skate and hypothesize that individuals exhibit gradual trophic niche transition, especially in δ¹⁵N space, rather than a clear and distinct shift in diet throughout ontogeny. Spatial isoscapes generated for little, thorny, and winter skate highlighted distinct spatial patterns in isotopic composition across the coastal shelf. For little and thorny skate, patterns mimicked expected spatial variability in the isotopic composition of phytoplankton/POM, suggesting limited displacement and utilization of spatially confined resource pools. Winter skate, however, exhibited a much narrower range of δ¹³C and δ¹⁵N values, suggesting individuals may use resources from a more confined latitudinal range. Although high total trophic niche overlap was observed between some species (e.g. little and thorny skate), sympatric species (e.g. little and winter skate) exhibited a degree of trophic niche separation. These findings offer new insight into the trophic dynamics of a poorly‐studied, vulnerable group of predators, and highlight a need to re‐examine assumptions pertaining to aspects of their ecology.     

Identifying critical habitat for freshwater turtles: integrating long-term monitoring tools to enhance conservation and management

The effective conservation and management of threatened species requires comprehensive knowledge about resource utilisation. Here we integrated tissue stable isotope analysis and biotelemetry to identify the predominant dietary resources of two sympatric species of freshwater turtle, and locate where those items were acquired. We deployed an array of underwater acoustic telemetry receivers to autonomously, simultaneously, and continuously, monitor the movements of the threatened Elseya albagula and Elusor macrurus, over a 12-month period. Stable isotope (SI) values (δ¹³C and δ¹⁵N) were measured within the carapace of each species, and compared with SI values within potential food items. The integration of movement information and carapace SI data revealed that whilst these species had overlapping home ranges, there was less than 5% probability of inter-species dietary niche overlap. E. macrurus acquired food items consisting of bivalves, gastropods and aquatic insects within rocky riffles whilst E. albagula fed on filamentous algae and crustaceans foraged from the muddy and vegetated shallow margins of deep water pools. Our findings differ from stomach content analysis and mark-recapture studies, which reported these species to have similar habitat and resource requirements. We argue that the observed disparity is because our methods provided a weighted measure of an individual’s dietary preference and habitat utilisation over a broad time-scale, whilst stomach content analysis and mark-recapture studies offer only a single observation of an individual’s dietary preference. The research demonstrates the utility of integrating passive acoustic telemetry and carapace stable isotope analysis for identifying critical habitat for freshwater turtles.     

A local gammarid uses kairomones to avoid predation by the invasive crustaceans Dikerogammarus villosus and Orconectes limosus

Since the 1980s the Ponto-Caspian gammarid Dikerogammarus villosus has spread throughout Europe while displacing native species and is predicted to invade further continents. After it was introduced into Europe in the 1890s the North American crayfish Orconectes limosus spread throughout Europe and served as a vector to displace native crayfish as well. In Lake Constance (Germany) the previously dominant gammarid Gammarus roeselii is subjected to both of these invasive crustaceans. In our experiments both species placed predation pressure on G. roeselii. Kairomone perception tests in a Y-maze revealed the capability of the gammarids G. roeselii and D. villosus to perceive and avoid the scent of the predator crayfish O. limosus. Both species also avoided the kairomone of the other gammarid, but did not avoid the scent of their own species. This taxa specific behavior suggests that taxa specific signals are used. This behavior can help the gammarids avoid shelters previously occupied by predators.