How bad are invaders in coastal waters? The case of the American slipper limpet Crepidula fornicata in western Europe

Introduced species are assumed to exert a variety of negative ecological effects in their new environments. However, rigid studies on such effects are still rare. Using a case study we exemplify pitfalls and obstacles for research on ecological effects of invaders and highlight the need for a concise framework. The suspension feeding gastropod Crepidula fornicata was accidentally introduced with American oysters to Europe and was soon after defamed as an ‘oyster pest’ although no evidence was provided in justification. Recently, small-scale experiments with C. fornicata and the Pacific oyster Crassostrea gigas failed to prove competition. As an epizootic, however, C. fornicata is impeding native mussels Mytilus edulis but at the same time provides protection against starfish predation. It also may serve as a sink for infectious trematode parasites and hence be beneficial for bivalve basibionts. Another positive effect of C. fornicata, especially at the coast of France where it is superabundant, may be that it causes a shift of phytoplankton blooms from toxic flagellates to diatoms. The multiple interactions with recipient coastal ecosystems result in a complex interplay of negative as well as positive effects of the invader on native biota. Positive effects of invaders might occur with the same frequency as negative ones, and the general prejudice that introduced species exert per se a negative effect may dictate the outcome of research. We argue that considering both, negative as well as positive effects of an introduced species is needed to eventually enable us to evaluate the overall effect of an invasion on recipient ecosystems. Besides pointing to the importance of positive effects, this case study also shows that research on effects of introduced species should (1) be species specific, (2) consider different spatial scales, (3) clarify which stage of an invasive process is under observation and (4) clearly distinguish between ecological effects, human-relevant impacts and the ethical judgment of both. A concise framework for research on ecological effects of introduced species – which still has to be developed – should incorporate these aspects.     

Food web structure in the high Arctic Canada Basin: evidence from δ13C and δ15N analysis

The food-web structure of the Arctic deep Canada Basin was investigated in summer 2002 using carbon and nitrogen stable isotope tracers. Overall food-web length of the range of organisms sampled occupied four trophic levels, based on 3.8 trophic level enrichment (¹⁵N range: 5.3–17.7). It was, thus, 0.5–1 trophic levels longer than food webs in both Arctic shelf and temperate deep-sea systems. The food sources, pelagic particulate organic matter (POM) (¹³C=–25.8, ¹⁵N=5.3) and ice POM (¹³C=–26.9, ¹⁵N=4.1), were not significantly different. Organisms of all habitats, ice-associated, pelagic and benthic, covered a large range of ¹⁵N values. In general, ice-associated crustaceans (¹⁵N range 4.6–12.4, mean 6.9) and pelagic species (¹⁵N range 5.9–16.5, mean 11.5) were depleted relative to benthic invertebrates (¹⁵N range 4.6–17.7, mean 13.2). The predominantly herbivorous and predatory sympagic and pelagic species constitute a shorter food chain that is based on fresh material produced in the water column. Many benthic invertebrates were deposit feeders, relying on largely refractory material. However, sufficient fresh phytodetritus appeared to arrive at the seafloor to support some benthic suspension and surface deposit feeders on a low trophic level (e.g., crinoids, cumaceans). The enriched signatures of benthic deposit feeders and predators may be a consequence of low primary production in the high Arctic and the subsequent high degree of reworking of organic material.     

Variability in δ13C and δ15N trophic discrimination factors for teleost fishes: a meta-analysis of temperature and dietary effects

Reviews in Fish Biology and Fisheries - Stable isotope analysis (SIA) is widely used to assess animal diet and movements, requiring accurate estimates of trophic discrimination factors (TDFs)....     

Functional diversity in an Amazonian rainforest of French Guyana: a dual isotope approach (δ15N and δ13C)

Functional aspects of biodiversity were investigated in a lowland tropical rainforest in French Guyana (5°2′N, annual precipitation 2200 mm). We assessed leaf δ¹⁵N as a presumptive indicator of symbiotic N₂ fixation, and leaf and wood cellulose δ¹³C as an indicator of leaf intrinsic water-use efficiency (CO₂ assimilation rate/leaf conductance for water vapour) in dominant trees of 21 species selected for their representativeness in the forest cover, their ecological strategy (pioneers or late successional stage species, shade tolerance) or their potential ability for N₂ fixation. Similar measurements were made in trees of native species growing in a nearby plantation after severe perturbation (clear cutting, mechanical soil disturbance). Bulk soil δ¹⁵N was spatially quite uniform in the forest (range 3–5‰), whereas average leaf δ¹⁵N ranged from −0.3‰ to 3.5‰ in the different species. Three species only, Diplotropis purpurea, Recordoxylon speciosum (Fabaceae), and Sclerolobium melinonii (Caesalpiniaceae), had root bacterial nodules, which was also associated with leaf N concentrations higher than 20 mg g⁻¹. Although nodulated trees displayed significantly lower leaf δ¹⁵N values than non-nodulated trees, leaf δ¹⁵N did not prove a straightforward indicator of symbiotic fixation, since there was a clear overlap of δ¹⁵N values for nodulated and non-nodulated species at the lower end of the δ¹⁵N range. Perturbation did not markedly affect the difference δ¹⁵N_soil−δ¹⁵N_leaf, and thus the isotopic data provide no evidence of an alteration in the different N acquisition patterns. Extremely large interspecific differences in sunlit leaf δ¹³C were observed in the forest (average values from −31.4 to −26.7‰), corresponding to intrinsic water-use efficiencies (ratio CO₂ assimilation rate/leaf conductance for water vapour) varying over a threefold range. Wood cellulose δ¹³C was positively related to total leaf δ¹³C, the former values being 2–3‰ higher than the latter ones. Leaf δ¹³C was not related to leaf δ¹⁵N at either intraspecific or interspecific levels. δ¹³C of sunlit leaves was highest in shade hemitolerant emergent species and was lower in heliophilic, but also in shade-tolerant species. For a given species, leaf δ¹³C did not differ between the pristine forest and the disturbed plantation conditions. Our results are not in accord with the concept of existence of functional types of species characterized by common suites of traits underlying niche differentiation; rather, they support the hypothesis that each trait leads to a separate grouping of species. Received: 18 August 1997 / Accepted: 14 April 1998     

Reliability of δ13C and δ15N in faeces for reconstructing savanna herbivore diet

We tested the reliability of herbivore faecal δ¹³C and δ¹⁵N values for reconstructing diet through review of an extensive database derived from a 3-year study of ungulates in South Africa's Kruger National Park. Faeces are a useful material for stable isotope studies of diet because they record dietary turnover at very short time scales, and because sampling is non-invasive. However, the validity of faecal isotope proxies may be questioned because they represent only undigested food remains. Results from Kruger Park confirm that free-ranging browsers have faecal δ¹³C consistent with C₃ feeding, grazer faeces are C₄, and mixed-feeder faeces intermediate. Although the respective ranges do not overlap, there is significant variation in faecal δ¹³C of browsers and grazers (～2.0–4.0‰) across space and through time. We demonstrate that most (～70%) of this variation can be ascribed to corresponding patterns of variation in the δ¹³C of C₃ and C₄ plants, respectively, re-enforcing the fidelity of faecal isotope proxies for diet but highlighting a need for mixing models that control for variations in plant δ¹³C in order to achieve accurate diet reconstructions. Predictions for the effects of climate (rainfall) and ecophysiology on ¹⁵N-abundance variations in mammals do not persist in faeces. Rather, faecal δ¹⁵N tracks changes in plant δ¹⁵N, with further fractionation occurring primarily due to variations in dietary protein (reflected by %N). Controlling for these effects, we show that a dual-isotope multiple source mixing model (Isosource) can extend diet reconstructions for African savanna herbivores beyond simplified C₃/C₄ distinctions, although further understanding of variations in mammal δ¹⁵N are needed for greater confidence in this approach.     

Temporal records of δ13C and δ15N in North Pacific pinnipeds: inferences regarding environmental change and diet

Sea lion and seal populations in Alaskan waters underwent various degrees of decline during the latter half of the twentieth century and the cause(s) for the declines remain uncertain. The stable carbon (¹³C/¹²C) and nitrogen (¹⁵N/¹⁴N) isotope ratios in bone collagen from wild Steller sea lions (Eumetopias jubatus), northern fur seals (Callorhinus ursinus) and harbor seals (Phoca vitulina) from the Bering Sea and Gulf of Alaska were measured for the period 1951-1997 to test the hypothesis that a change in trophic level may have occurred during this interval and contributed to the population declines. A significant change in '¹⁵N in pinniped tissues over time would imply a marked change in trophic level. No significant change in bone collagen '¹⁵N was found for any of the three species during the past 47 years in either the Bering Sea or the Gulf of Alaska. However, the ¹⁵N in the Steller sea lion collagen was significantly higher than both northern fur seals and harbor seals. A significant decline in '¹³C (almost 2 ‰ over the 47 years) was evident in Steller sea lions, while a declining trend, though not significant, was evident in harbor seals and northern fur seals. Changes in foraging location, in combination with a trophic shift, may offer one possible explanation. Nevertheless, a decrease in '¹³C over time with no accompanying change in '¹⁵N suggests an environmental change affecting the base of the foodweb rather than a trophic level change due to prey switching. A decline in the seasonal primary production in the region, possibly resulting from decreased phytoplankton growth rates, would exhibit itself as a decline in '¹³C. Declining production could be an indication of a reduced carrying capacity in the North Pacific Ocean. Sufficient quantities of optimal prey species may have fallen below threshold sustaining densities for these pinnipeds, particularly for yearlings and subadults who have not yet developed adequate foraging skills.     

δ13C and δ15N indicators of fish and shrimp community diet and trophic structure in a mangrove ecosystem in Thailand

Stable carbon and nitrogen isotope ratios were used to elucidate primary carbon sources and trophic relationships of the fish and shrimp community in the Klong Ngao mangrove ecosystem, southern Thailand. There were no significant differences in isotopic compositions of biota between mangrove and offshore sites (Welch–Aspin test). The δ¹⁵N values of eight fish species and two shrimp species at both sites were also not significantly different by the test, meaning that at both sites they feed on the same diets due to the discharge of large quantities of mangrove sediments. The δ¹⁵N isotopic enrichment of consumers suggested that there are four trophic levels in the Klong Ngao food web, with at least two fish species capable of switching feeding strategies and thus altering their apparent trophic positions. Phytoplankton culture experiments indicated that mangrove-derived sediments could play an important role in stimulating phytoplankton growth for low turbidity offshore areas, thus providing an alternate food source. The isotopic associations among sources and consumers indicated that mangroves were the major carbon source supporting aquatic food webs in the Klong Ngao ecosystem.     

Ecosystem structure and soil-surface conditions drive the variability in the foliar δ13C and δ15N of Stipa tenacissima in semiarid Mediterranean steppes

We evaluated the effects of ecosystem composition and structure (species richness and diversity, cover and spatial attributes of vegetation), abiotic factors (climate and topographical features) and the condition of the bare-ground areas (evaluated using soil-surface indicators) on the performance of Stipa tenacissima [evaluated using foliar ¹³C, ¹⁵N, nitrogen concentration and the carbon-to-nitrogen (C:N) ratio] in 15 steppes of SE Spain. Foliar ¹³C values of S. tenacissima showed a low degree of variation in the studied steppes, with average values ranging from –24.1 to –22.9. Higher variation was found in the ¹⁵N values, which ranged from –5.5 to –2.4. The nitrogen concentration and the C:N ratio varied between 5.0 and 8.0 mg g^–1, and between 55.4 and 85.3, respectively. The ¹³C values became less negative with increasing spatial aggregation of perennial vegetation, while the C:N values increased with increasing perennial vegetation cover. The ¹⁵N values became more negative with increasing infiltration in the bare-ground areas, but the nitrogen concentration was not related to any of the environmental variables measured. Our results suggest that the relative importance of ecosystem structure and soil-surface conditions in the bare ground areas was higher than that of abiotic factors as determinants of the performance of S. tenacissima. The results also show that even subtle changes in these ecosystem features may lead to modifications in plant performance in semiarid S. tenacissima steppes, and thus to modifications in the associated ecosystem functions in the mid- to long-term.     

Research article: small-scale spatial variation of δ13C and δ15N isotopes in Antarctic carbon sources and consumers

Regional food web studies that fail to account for small-scale isotopic variability can lead to a mismatch between an organism’s inferred and true trophic position. Misinterpretation of trophic status may result, substantially limiting spatial and temporal comparability of food web studies. We sampled several carbon sources and consumers in a nested design to assess the variability of food web members across small spatial scales (100 s of m to several km) in regions around the Windmill Islands and Vestfold Hills in East Antarctica. For carbon sources, δ¹³C in sea ice POM was particularly variable between locations (km apart) and between sites (100 s of m apart) with replicate samples varying by up to 16‰. Macroalgae δ¹³C was less variable (replicate samples ranging up to 6.9‰ for the red alga Iridaea cordata), yet still differed between locations. Sediment POM and pelagic POM were the least variable, displaying minimal differences between locations or sites for δ¹³C and δ¹⁵N. Three out of eight consumers were significantly different between locations for δ¹³C, and five out of eight for δ¹⁵N, with the fish Trematomus bernacchii the most variable for both δ¹³C and δ¹⁵N. At smaller scales, the amphipod Paramorea walkeri showed significant variation between sites in δ¹³C but not in δ¹⁵N. We attribute small-scale variability to the dynamic physical environment for carbon sources in coastal systems and a close coupling of diet to habitat for consumers. We highlight the need to account for small-scale spatial variation in sampling designs for regional food web studies.     

Differences in δ15N and δ13C between embryonic and maternal tissues of the ovoviviparous bluntnose sixgill shark Hexanchus griseus

Stable nitrogen (δ¹⁵N) and carbon (δ¹³C) isotope ratios from muscle, liver and yolk were analysed from the mother and embryos of an ovoviviparous shark, Hexanchus griseus. Embryonic liver and muscle had similar δ¹⁵N and δ¹³C ratios or were depleted in heavy isotopes, compared to the same maternal somatic and reproductive yolk tissues, but no relationship existed between δ¹⁵N or δ¹³C and embryo length, as expected, because a switch to placental nourishment is lacking in this species. This study expands the understanding of maternal nourishment and embryonic stable isotope differences in ovoviviparous sharks.     

Long-term changes of the δ15N natural abundance of plants and soil in a temperate grassland

Tracing back the N use efficiency of long-term fertilizer trials is important for future management recommendations. Here we tested the changes in natural N-isotope composition as an indicator for N- management within a long-term fertilization lysimeter experiment in a low mountain range pasture ecosystem at Rengen (Eifel Mountains), Germany. Cattle slurry (δ¹⁵N?=?8.9?±?0.5‰) and mineral fertilizers (calcium ammonium nitrate; δ¹⁵N?=??1.0?±?0.2‰) were applied at a rate between 0 and 480 kg N ha^?1?yr^?1 throughout 20 years from 1985 onwards. In 2006, samples were taken from different grass species, coarse and fine particulate soil organic matter, bulk soil and leachates. Total soil N content hardly changed during fertilization experiment. As also N leaching has been small within the stagnant water regime, most N was lost through the gaseous phase beside plant uptake and cutting. Unlike N uptake by plants, the process of N volatilization resulted in strong discrimination against the ¹⁵N isotope. As a consequence, the δ¹⁵N values of top soil samples increased from 1.8?±?0.4‰ to 6.0?±?0.4‰ and that of the plants from ?1.2?±?1.3‰ to 4.8?±?1.2‰ with increasing N fertilizer rate. Samples receiving organic fertilizer were most enriched in δ¹⁵N. The results suggest that parts of the fertilizer N signal was preserved in soils and even discovered in soil organic matter pools with slow N turnover. However, a ¹⁵N/¹⁴N isotope fractionation of up to 1.5‰ added to the δ¹⁵N values recovered in soils and plants, rendering the increase in δ¹⁵N value a powerful indicator to long-term inefficient N usage and past N management in the terrestrial environment.     

Linking Isotopes and Panmixia: High Within-Colony Variation in Feather δ2H, δ13C,and δ15N across the Range of the American White Pelican

Complete panmixia across the entire range of a species is a relatively rare phenomenon; however, this pattern may be found in species that have limited philopatry and frequent dispersal. American white pelicans (Pelecanus erythrorhyncos) provide a unique opportunity to examine the role of long-distance dispersal in facilitating gene flow in a species recently reported as panmictic across its broad breeding range. This species is also undergoing a range expansion, with new colonies arising hundreds of kilometers outside previous range boundaries. In this study, we use a multiple stable isotope (δ²H, δ¹³C, δ¹⁵N) approach to examine feather isotopic structuring at 19 pelican colonies across North America, with the goal of establishing an isotopic basemap that could be used for assigning individuals at newly established breeding sites to source colonies. Within-colony isotopic variation was extremely high, exceeding 100‰ in δ²H within some colonies (with relatively high variation also observed for δ¹³C and δ¹⁵N). The high degree of within-site variation greatly limited the utility of assignment-based approaches (42% cross-validation success rate; range: 0–90% success). Furthermore, clustering algorithms identified four likely isotopic clusters; however, those clusters were generally unrelated to geographic location. Taken together, the high degree of within-site isotopic variation and lack of geographically-defined isotopic clusters preclude the establishment of an isotopic basemap for American white pelicans, but may indicate that a high incidence of long-distance dispersal is facilitating gene flow, leading to genetic panmixia.     

Effects of anticoagulants on stable-isotope values (δ13C and δ15N) of shark blood components

The effects of anticoagulant EDTA and sodium heparin (SH) on stable carbon δ¹³C and nitrogen δ¹⁵N isotopic values of red blood cells (RBC) and blood plasma in juvenile blacktip reef sharks Carcharhinus melanopterus were analysed. Plasma preserved with anticoagulants was not isotopically distinct from plasma stored in no-additive control tubes but RBC δ¹⁵N values exhibited small enrichments when preserved with EDTA and SH. Results suggest EDTA and SH are viable anticoagulants for stable isotopic analyses of blood fractions but further studies are advised to validate results.     

Spatial Variation in δ15N and δ13C Isotopes in the San Juan River, New Mexico and Utah: Implications for the Conservation of Native Fishes

Synopsis Spatial patterns of resource use by small-bodied fishes in the San Juan River were examined using stable isotopes. Using δ¹⁵N of fishes as an index of trophic position, our data suggest both native and non-native fishes primarily consumed macro-invertebrates. The δ¹³C of these fishes further suggested a detritus-based food web, from which most species fed on chironomids in low-velocity habitats. A two-way ANOVA revealed a significant interaction between trophic level of fish species and longitudinal position in the river. This interaction was primarily attributed to a decline in trophic level of non-native red shiner Cyprinella lutrensis, relative to other species, in upstream reaches of the river. In addition, ANCOVA results suggest trophic position of fishes was dependent on channel type (primary vs. secondary), as there was less variability in resource use in secondary channels. These data provided a spatial framework of trophic interactions that can be used to predict the outcome of management actions. Overall, we confirmed high overlap in resource used between native and non-native fishes. However, spatial variation in trophic interactions both longitudinally and laterally in the river present a challenge to resource managers attempting to managing entire river systems.     

Patterns of δ^13C and δ^15N in wolverine Gulo gulo tissues from the Brooks Range,Alaska

Knowledge of carnivore diets is essential to understand how carnivore populations respond demographically to variations in prey abundance. Analysis of stable isotopes is a useful complement to traditional methods of analyzing carnivore diets. We used data on δ^13C and δ^15N in wolverine tissues to investigate patterns of seasonal and annual diet variation in a wolverine Gulo gulo population in the western Brooks Range, Alaska, USA. The stable isotope ratios in wolverine tissues generally reflected that of terrestrial carnivores, corroborating previous diet studies on wolverines. We also found variation in δ^13C and δ^15N both between muscle samples collected over several years and between tissues with different assimilation rates, even after correcting for isotopic fractionation. This suggests both annual and seasonal diet variation. Our results indicate that data on δ^13C and δ^15N holds promise for qualitative assessments of wolverine diet changes over time. Such temporal variation may be important indicators of ecological responses to environmental perturbations, and we suggest that more refined studies of stable isotopes may be an important tool when studying temporal change in diets of wolverines and similar carnivores [ Current Zoology 55 （3）： 188- 192, 2009].     

Determining the appropriate pretreatment procedures and the utility of liver tissue for bulk stable isotope (δ13C and δ15N) studies in sharks

Stable-isotope analysis (SIA) provides a valuable tool to address complex questions pertaining to elasmobranch ecology. Liver, a metabolically active, high turnover tissue (~166 days for 95% turnover), has the potential to reveal novel insights into recent feeding/movement behaviours of this diverse group. To date, limited work has used this tissue, but ecological application of SIA in liver requires consideration of tissue preparation techniques given the potential for high concentrations of urea and lipid that could bias δ¹³C and δ¹⁵N values (i.e., result in artificially lower δ¹³C and δ¹⁵N values). Here we investigated the effectiveness of (a) deionized water washing (WW) for urea removal from liver tissue and (b) chloroform-methanol for extraction of lipids from this lipid rich tissue. We then (a) established C:N thresholds for deriving ecologically relevant liver isotopic values given complications of removing all lipid and (b) undertook a preliminary comparison of δ¹³C values between tissue pairs (muscle and liver) to test if observed isotopic differences correlated with known movement behaviour. Tests were conducted on four large shark species: the dusky (DUS, Carcharhinus obscurus), sand tiger (RAG, Carcharias taurus), scalloped hammerhead (SCA, Sphyrna lewini) and white shark (GRE, Carcharodon carcharias). There was no significant difference in δ¹⁵N values between lipid-extracted (LE) liver and lipid-extracted/water washed (WW) treatments, however, WW resulted in significant increases in %N, δ¹³C and %C. Following lipid extraction (repeated three times), some samples were still biased by lipids. Our species-specific “C:N thresholds” provide a method to derive ecologically viable isotope data given the complexities of this lipid rich tissue (C:N thresholds of 4.0, 3.6, 4.7 and 3.9 for DUS, RAG, SCA and GRE liver_LEWW tissue, respectively). The preliminary comparison of C:N threshold corrected liver and muscle δ¹³C values corresponded with movement/habitat behaviours for each shark; minor differences in δ¹³C values were observed for known regional movements of DUS and RAG (δ¹³C_Diffs = 0.24 ± 0.99‰ and 0.57 ± 0.38‰, respectively), while SCA and GRE showed greater differences (1.24 ± 0.63‰ and 1.08 ± 0.71‰, respectively) correlated to large-scale movements between temperate/tropical and pelagic/coastal environments. These data provide an approach for the successful application of liver δ¹³C and δ¹⁵N values to examine elasmobranch ecology.     

Experimentally Derived δ13C and δ15N Discrimination Factors for Gray Wolves and the Impact of Prior Information in Bayesian Mixing Models

Stable isotope analysis of diet has become a common tool in conservation research. However, the multiple sources of uncertainty inherent in this analysis framework involve consequences that have not been thoroughly addressed. Uncertainty arises from the choice of trophic discrimination factors, and for Bayesian stable isotope mixing models (SIMMs), the specification of prior information; the combined effect of these aspects has not been explicitly tested. We used a captive feeding study of gray wolves (Canis lupus) to determine the first experimentally-derived trophic discrimination factors of C and N for this large carnivore of broad conservation interest. Using the estimated diet in our controlled system and data from a published study on wild wolves and their prey in Montana, USA, we then investigated the simultaneous effect of discrimination factors and prior information on diet reconstruction with Bayesian SIMMs. Discrimination factors for gray wolves and their prey were 1.97‰ for δ¹³C and 3.04‰ for δ¹⁵N. Specifying wolf discrimination factors, as opposed to the commonly used red fox (Vulpes vulpes) factors, made little practical difference to estimates of wolf diet, but prior information had a strong effect on bias, precision, and accuracy of posterior estimates. Without specifying prior information in our Bayesian SIMM, it was not possible to produce SIMM posteriors statistically similar to the estimated diet in our controlled study or the diet of wild wolves. Our study demonstrates the critical effect of prior information on estimates of animal diets using Bayesian SIMMs, and suggests species-specific trophic discrimination factors are of secondary importance. When using stable isotope analysis to inform conservation decisions researchers should understand the limits of their data. It may be difficult to obtain useful information from SIMMs if informative priors are omitted and species-specific discrimination factors are unavailable.     

Origin of carbon in agricultural soil profiles deduced from depth gradients of C:N ratios,carbon fractions, δ13C and δ15N values

Plant and Soil - Agricultural soils in Germany store 2.54 Pg of organic carbon (C). However, information about how and when this C entered the soils is limited. This study illustrates how depth...