稳定同位素分析在鸟类食性及营养级结构中的应用

稳定同位素分析(stable isotope analysis,SIA)自20世纪70年代末引入鸟类生态学领域以来,在研究鸟类食性和营养级结构方面展现了强大的发展潜力和广泛的应用前景。总结了该技术在鸟类食源组成和营养级结构方面研究的前期准备、实验流程、数据分析和研究进展等,重点阐述了其在鸟类保护与管理方面的应用。鉴于稳定同位素在生物体内存在分馏现象,从鸟类不同组织和部位对营养级富集因子、转化周期、同位素印记的差异,提出了完善该方法的建议和应用前景。     

Dietary ontogeny and niche shift to piscivory in lacustrine brown trout Salmo trutta revealed by stomach content and stable isotope analyses

The feeding ecology and ontogeny of a large size range of brown trout Salmo trutta in Lake Fyresvatnet, southern Norway, were examined by stomach content and stable isotope analyses. According to the stomach contents, the S. trutta changed their diet at c. 30 cm total length (L_T). The smaller size classes fed on benthic invertebrates and surface insects, whereas larger S. trutta (>30 cm) fed mainly on whitefish Coregonus lavaretus. A similar, but more gradual shift to piscivory in the size range 25–30 cm was found when using the stable isotope mixing model SIAR to reveal dietary ontogeny. The δ¹³C isotopic signature confirmed that S. trutta independent of size predominantly relied upon benthic energy sources, suggesting that the littoral zone was the primary foraging habitat for both invertebrate and piscivorous feeders. The δ¹⁵N values and trophic position increased with predator length, ranging from an average of 3·60 for small‐sized S. trutta (<15 cm) to 4·15 for large‐sized fish (>35 cm). The S. trutta exhibited a relatively slow growth rate during the predominant invertebrate feeding stages up to 7 years of age and 28 cm L_T, whereas fish above this size and age displayed a rapid growth rate of 9–11 cm year^?1, demonstrating the profitability of piscivorous feeding.     

Integrating stomach content and stable isotope analyses to elucidate the feeding habits of non-native sharptooth catfish <Emphasis Type="Italic">Clarias gariepinus</Emphasis>

Sharptooth catfish Clarias gariepinus was introduced into the Eastern Cape Province, South Africa, in 1976 and there are concerns about its possible negative impacts on native biota. This study investigated its trophic impact by examining its feeding habits. Stomach content and stable isotope analyses were compared from three localities—the Great Fish River, Sundays River and Glen Melville Dam. Stomach content analysis indicated a catholic diet dominated by fish particularly in all localities. Spatially, however, the diets revealed differences based on the dominance of macrophytes that were only present in the rivers, and aquatic invertebrates that appeared more diverse within the Great Fish River compared to other localities. By contrast, stable isotopes revealed a more generalised feeding pattern with no clear dominance of particular prey. Stable isotopes further showed that the catfish was a complex predator, with large catfish being top predators whereas smaller size groups appeared to feed lower in the food chain. An ontogenetic shift in diet was evident, with small fish predominantly consuming aquatic invertebrates and shifting towards fish with increasing size. High dietary overlap suggests the potential risk associated catfish feeding, especially the potential of piscivory by small catfish that are more likely to persist in shallow and marginal where endangered indigenous minnows occur. The alteration of environmental conditions, especially flow by inter-basin water transfer (IBWT) schemes, was inferred to have had a probable influence its invasion success. Occurrence of other invaders, which was facilitated by the IBWT together with the catfish, posits the risk of invasion meltdown within the study systems.     

Differential leucocyte cell counts from the pygoscelid penguins of Antarctica

Differential leucocyte counts were obtained for three cogeneric species of wild antarctic penguins, Pygoscelis adelie (adelie), Pygoscelis papua (gentoo), and Pygoscelis antarctica (chinstrap). Significant differences between the differential leucocyte counts of the three species were not observed.     

Blood fatty acids indicate inter- and intra-annual variation in the diet of Adélie penguins: Comparison with stomach content and stable isotope analysis

Adélie penguin (Pygoscelis adeliae) diet is an important indicator of prevailing environmental conditions and resource availability. In this study, dietary variation within and between years was studied with fatty acid signature analysis (FASA), stomach content analysis (SCA) and stable isotope analysis (SIA). We profiled the fatty acid (FA) composition of whole blood collected from adult penguins throughout the breeding season, and from chicks during the crèche period, in 2001 and 2002. Differences were detected in FA profiles between years, breeding stage and age (adults vs. chicks). These patterns broadly corresponded to those observed from SCA and SIA, with a mix of krill and fish consumed in the early part of the breeding season in both years, krill dominating the diet during the chick-rearing periods in 2001, and fish in 2002. Different metabolic and physiological demands between stages, and ages, may also influence FA profiles but warrants further investigation. In-situ calibrations of adult FA blood profiles were made using corresponding stomach samples to quantify diet composition. Using linear discriminate function analysis, we classified adult FA profiles into 3 meal-types: krill, fish or mixed. A higher proportion of adults had fish-like profiles during the arrival and guard periods. Krill-like profiles dominated during the incubation and crèche periods, although there were a relatively high proportion of fish-like and mixed profiles as well. These patterns corresponded to results from SCA and SIA. This study demonstrates that FASA has the potential to be integrated with other dietary tools to enhance diet monitoring studies, which are currently integral to ecosystem management and conservation measures. The in-situ calibration method used offers a simple and effective alternative to more rigorous calibration techniques developed elsewhere.     

Applications of stable isotope analyses to avian ecology

In the past 20 years the use of stable isotope analysis has become increasingly common in ecological studies. In fact, in some instances these techniques have yielded remarkable insights into the foraging preferences and migrations of birds. Despite these advances and the potential of the approach, it is possibly still not as widely used as might be expected. In this paper we aim to illustrate the potential of the approach in the hope of encouraging more avian ecologists to think again about how these techniques might provide insights in the systems on which they work. We discuss some of the principles behind the approach, and review some of the more recent ornithological studies that have used stable isotope techniques to trace trophic pathways or infer migratory origins. We follow this by discussing some of the latest ideas on how stable isotopes may be used to generate community metrics and close by detailing the important assumptions and caveats that should be considered before undertaking any studies using this technique.     

Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants

Aims Mycorrhizas (fungal roots) play vital roles in plant nutrient acquisition, performance and productivity in terrestrial ecosystems. Arbuscular mycorrhizas (AM) and ectomycorrhizas (EM) are mostly important since soil nutrients, including NH₄⁺, NO₃^? and phosphorus, are translocated from mycorrhizal fungi to plants. Individual species, genera and even families of plants could be interconnected by mycorrhizal mycelia to form common mycorrhizal networks (CMNs). The function of CMNs is to provide pathways for movement or transfer of nutrients from one plant to another. In the past four decades, both ¹⁵N external labeling or enrichment (usually expressed as atom%) and ¹⁵N naturally occurring abundance (δ¹⁵N, ‰) techniques have been employed to trace the direction and magnitude of N transfer between plants, with their own advantages and limitations.     

Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout

Stable isotopes can illuminate resource usage by organisms, but effective interpretation is predicated on laboratory validation. Here we develop stable isotope clocks to track resource shifts in anadromous rainbow trout (Oncorhynchus mykiss). We used a diet-switch experiment and model fitting to quantify N stable isotope (δ¹⁵N) turnover rates and discrimination factors for seven tissues: plasma, liver, fin, mucus, red blood cells, muscle, and scales. Among tissues, diet-tissue δ¹⁵N discrimination factors ranged from 1.3 to 3.4 ‰. Model-supported tissue turnover half-lives ranged from 9.0 (fin) to 27.7 (scale) days. We evaluated six tissue turnover models using Akaike’s information criterion corrected for small sample sizes. The use of equilibrium tissue values was supported in all tissues and two-compartment models were supported in plasma, liver, and mucus. Using parameter estimates and their uncertainty we developed stable isotope clocks to estimate the time since resource shifts. Longer turnover tissues provided accurate estimates of time since resource switch for durations approximately twice their half-life. Faster turnover tissues provided even higher precision estimates, but only within their half-life post-switch. Averaging estimates of time since resource shift from multiple tissues provided the highest precision estimates of time since resource shift for the longest duration (up to 64 days). This study therefore provides insight into physiological processes that underpin stable isotope patterns, explicitly tests alternative models, and quantifies key parameters that are the foundation of field-based stable isotope analysis.     

The use of stable isotope ratios in whitebait otolith carbonate to identify the source of prey for Western Australian penguins

A methodology has been developed and used to investigate a direct link between juvenile whitebait (Hyperlophus vittatus), the key prey species sampled from the stomachs of Little Penguins (Eudyptula minor), and the specific nursery area of that prey. A unique application of existing methodology initially involved the measurement of the stable isotopes of oxygen (δ¹⁸O:δ¹⁶O) and carbon (δ¹³C:δ¹²C) in sagittal otolith carbonate, using standard mass spectrometric techniques. The results indicated that the inshore distribution of juvenile (0+ year old) whitebait between Cockburn Sound and Koombana Bay, Western Australia consisted of a number of separate assemblages. Measured differences in stable oxygen isotope ratios were attributed to variations in freshwater input to the embayments that provided the whitebait habitats. In contrast, the measured stable carbon isotope ratios probably resulted from the different isotopic compositions of the food webs in the various habitats. Secondly, a comparison of the average value of carbon and oxygen isotope signatures of pooled otoliths from samples of whitebait from a number of different nearshore coastal sites (assemblages), with that of whitebait obtained from the stomachs of penguins at their main breeding site (Penguin Island) indicated that the values from the penguins resemble most closely those of the average otolith values obtained from whitebait from only one site (Becher Point). Assuming that the whitebait sampled were representative of the whitebait in the nearshore habitats and the diets of the penguins, then these results imply that at the time of sampling the penguins were feeding on whitebait from only one site.     

Evaluating the utility of stable isotope analyses of archived freshwater sample materials

We evaluated the potential utility of stable isotope analysis of tissues commonly archived by aquatic biologists. Previous studies with chemically preserved samples have shown contradictory results, which present an obstacle for the use of archived sample materials. We tested the effects of ethanol and formalin preservation on zooplankton and of ethanol on benthic macroinvertebrate δ¹³C and δ¹⁵N values. We found that neither formalin nor ethanol had a significant effect on δ¹³C and δ¹⁵N values of preserved zooplankton. Nor did ethanol significantly affect δ¹³C or δ¹⁵N values of macroinvertebrates. However, ethanol preservation slightly, but significantly decreased C:N ratios of both zooplankton and macroinvertebrates, probably reflecting some extraction of lipids. Overall, the effects of preservatives on δ¹³C and δ¹⁵N values that we observed were minor. We also compared δ¹³C and δ¹⁵N values analysed from roach scales and perch operculum bones with those analysed from muscle tissue. Decalcification of scales and operculum bones only slightly improved our comparison to muscle tissue δ¹³C and δ¹⁵N values. Decalcified scales had slightly higher δ¹³C and lower δ¹⁵N values. Similarly, decalcified operculum bones showed slightly increased δ¹³C and decreased δ¹⁵N values to those for fish muscle. Our results confirm that scales and operculum bones can provide a suitable proxy for fish muscle in isotope studies with minor correction. We conclude that various archived sample materials can indeed be used with confidence for historical reconstructions of freshwater food webs by stable isotope analysis. Handling editor: K. Martens     

基于胃含物分析和稳定同位素技术研究鳀的摄食生态

鳀是重要的渔业资源捕捞对象,同时也是生态系统营养动力学研究的关键种.基于2020年和2008-2009年东海区采集的鳀样品,结合胃含物分析和肌肉碳、氮稳定同位素技术,分析了鳀的食物组成、食性昼夜差异、不同发育阶段的食性转变及其营养级,研究鳀的摄食生态.胃含物分析显示,鳀主要摄食浮游甲壳类和小型鱼类,优势饵料依次为太平洋...     

Evaluating gull diets: a comparison of conventional methods and stable isotope analysis

ABSTRACT Samples such as regurgitated pellets and food remains have traditionally been used in studies of bird diets, but these can produce biased estimates depending on the digestibility of different foods. Stable isotope analysis has been developed as a method for assessing bird diets that is not biased by digestibility. These two methods may provide complementary or conflicting information on diets of birds, but are rarely compared directly. We analyzed carbon and nitrogen stable isotope ratios of feathers of Glaucous Gull (Larus hyperboreus) chicks from eight breeding colonies in northern Alaska, and used a Bayesian mixing model to generate a probability distribution for the contribution of each food group to diets. We compared these model results with probability distributions from conventional diet samples (pellets and food remains) from the same colonies and time periods. Relative to the stable isotope estimates, conventional analysis often overestimated the contributions of birds and small mammals to gull diets and often underestimated the contributions of fish and zooplankton. Both methods gave similar estimates for the contributions of scavenged caribou, miscellaneous marine foods, and garbage to diets. Pellets and food remains therefore may be useful for assessing the importance of garbage relative to certain other foods in diets of gulls and similar birds, but are clearly inappropriate for estimating the potential impact of gulls on birds, small mammals, or fish. However, conventional samples provide more species‐level information than stable isotope analysis, so a combined approach would be most useful for diet analysis and assessing a predator's impact on particular prey groups.     

Ferox Trout (Salmo trutta) as `Russian dolls': complementary gut content and stable isotope analyses of the Loch Ness foodweb

1. Conventional collection methods for pelagic fish species (netting, trawling) are impractical or prohibited in Loch Ness, U.K. To investigate trophic relationships at the top of the Loch Ness food web, an alternative strategy, angling, provided samples of the top predator, the purely piscivorous ferox trout ( Salmo trutta ).
2. The gut contents of these fish provided further samples of prey-fish, and subsequent examination of prey-fish guts revealed their dietary intake, analogous to the famous nested `Russian dolls'. Each trophic level separated by gut content analysis provided further complementary samples for stable isotope analysis and thus information on the longer term, assimilated diet.
3. Ferox trout exhibited considerable cannibalism to supplement a diet of Arctic charr ( Salvelinus alpinus ). However, conspecifics stemmed from a lower isotopic baseline in relation to charr, so ferox trout exhibited a lower trophic level than predicted (4.3) by using the δ¹⁵N values. Charr displayed dietary specialisation with increasing length, and isotopic values supported by the gut data placed the charr at a trophic level of 3.5. The isotope data also indicated that charr carbon was primarily autochthonous in origin.     

Assessing the trophic ecology of three sympatric squid in the marine ecosystem off the Patagonian Shelf by combining stomach content and stable isotopic analyses

Squid species are important components of the Southern Atlantic Ocean ecosystems, as they prey on a wide range of crustaceans, fish and cephalopods. As a result of this trophic interaction and their high abundance, they are considered reliable indicators of energy transfer and biomass in the food web. We identified Illex argentinus, Doryteuthis gahi and Onykia ingens as the most important squid species interacting on the Patagonian shelf, and used isotope analysis and stomach content identification to assess the feeding ecology and interaction of these squids in the ecosystem. Our results describe trophic interactions by direct predation of O. ingens and I. argentinus on D. gahi, and a trophic overlap of the three squid, and indicate a higher trophic level and differences in the foraging areas for mature and maturing D. gahi inferred through δ¹⁵N and δ¹³C concentrations. These differences were related to the segregation and different habitat of large mature D. gahi and suggest a food enrichment of C and N based on feeding sources other than those used by small maturing D. gahi and I. argentinus and O. ingens.     

Annual and seasonal changes in diets of martens: evidence from stable isotope analysis

Theory predicts that generalist predators will switch to alternative prey when preferred foods are not readily available. Studies on the feeding ecology of the American marten (Martes americana) throughout North America suggest that this mustelid is a generalist predator feeding largely on voles (Microtus sp.; Clethrionomys sp.). We investigated seasonal and annual changes in diets of martens in response to the changing abundance of small rodents (Peromyscus keeni, and Microtus longicaudus) on Chichagof Island, Southeast Alaska, using stable isotope analysis. We hypothesized that martens would feed primarily on small rodents during years with high abundance of these prey species, whereas during years of low abundance of prey, martens would switch to feed primarily on the seasonally available carcasses of salmon. We also hypothesized that home-range location on the landscape (i.e., access to salmon streams) would determine the type of food consumed by martens, and martens feeding on preferred prey would exhibit better body condition than those feeding on other foods. We live-captured 75 martens repeatedly, from mid-February to mid-December 1992–1994. We also obtained marten carcasses from trappers during late autumn 1991 and 1992, from which we randomly sub-sampled 165 individuals. Using stable isotope ratios and a multiple-source mixing model, we inferred that salmon carcasses composed a large portion of the diet of martens in autumn during years of low abundance of rodents (1991 and 1992). When small rodents were available in high numbers (1993 and 1994), they composed the bulk of the diet of martens in autumn, despite salmon carcasses being equally available in all years. Selection for small rodents occurred only in seasons in which abundance of small rodents was low. Logistic regression revealed that individuals with access to salmon streams were more likely to incorporate salmon carcasses in their diet during years of low abundance of small rodents. Using stable isotope analysis on repeated samples from the same individuals, we explored some of the factors underlying feeding habits of individuals under variable ecological conditions. We were unable to demonstrate that body weights of live-captured male and female martens differed significantly between individuals feeding on marine-derived or terrestrial diets. Therefore, martens, as true generalist predators, switched to alternative prey when their principal food was not readily available on a seasonal or annual basis. Although salmon carcasses were not a preferred food for martens, they provided a suitable alternative to maintain body condition during years when small rodents were not readily available. Received: 1 May 1996 / Accepted: 24 February 1997     

Conservation of biotrophy in Hygrophoraceae inferred from combined stable isotope and phylogenetic analyses

The nutritional modes of genera in Hygrophoraceae (Basidiomycota: Agaricales), apart from the ectomycorrhizal Hygrophorus and lichen-forming taxa, are uncertain. New δ(15)N and δ(13)C values were obtained from 15 taxa under Hygrophoraceae collected in central Massachusetts and combined with isotopic datasets from five prior studies including a further 12 species using a data standardization method to allow cross-site comparison. Based on these data, we inferred the probable nutritional modes for species of Hygrophorus, Hygrocybe, Humidicutis, Cuphophyllus and Gliophorus. A phylogeny of Hygrophoraceae was constructed by maximum likelihood analysis of nuclear ribosomal 28S and 5.8S sequences and standardized δ(15)N and δ(13)C values were used for parsimony optimization on this phylogeny. Our results supported a mode of biotrophy in Hygrocybe, Humidicutis, Cuphophyllus and Gliophorus quantitatively unlike that in more than 450 other fungal taxa sampled in the present and prior studies. Parsimony optimization of stable isotope data suggests moderate conservation of nutritional strategies in Hygrophoraceae and a single switch to a predominantly ectomycorrhizal life strategy in the lineage leading to Hygrophorus. We conclude that Hygrophoraceae of previously unknown nutritional status are unlikely to be saprotrophs and are probably in symbiosis with bryophytes or other understory plants.     

Comparing pellet and stable isotope analyses of nestling Bonelli's Eagle Aquila fasciata diet

Diet analyses are central to the study of avian trophic ecology, and stable isotope analyses have made an increasing contribution in the last two decades. Few isotopic studies have assessed the diet of raptor species, which are more frequently analysed by conventional diet methods such as pellet analysis. In this study, we compare prey consumption estimates of nestling Bonelli's Eagles Aquila fasciata from conventional pellet analysis (in terms of items and biomass) and stable isotopic mixing models (SIAR) using δ¹³C, δ¹⁵N and δ³⁴S of feathers. The pellet analysis showed that European Rabbits Oryctolagus cuniculus, pigeons (mainly Common Wood Pigeons Columba palumbus and Domestic Pigeons Columba livia dom.), Red‐legged Partridges Alectoris rufa, passerines, Yellow‐legged Gulls Larus michahellis and Eurasian Red Squirrels Sciurus vulgaris were the main prey, so they were selected for diet reconstructions in SIAR. At the population level, mean prey consumption estimates were similar for pellets (both items and biomass) and SIAR. At the territory level, the weighted kappa statistic showed good ordinal scale agreement in main prey consumption between items or biomass and SIAR. Although the intraclass correlation coefficient showed poor method agreement when considering all prey in the same analysis, the intraclass correlation coefficients for each prey category showed significant agreement between pellets and SIAR when estimating the consumption of Rabbits, pigeons and Gulls, with lower agreement for passerines and Squirrels. Lastly, there was poor method agreement for estimates of Partridges. Our results suggest an overall agreement between the pellet analysis and SIAR when estimating nestling Bonelli's Eagle diet at both the population and, to a lesser extent, the territory level, supporting the usefulness of isotopic mixing models when identifying the terrestrial and marine components of raptor diets.