Stable Isotope Analysis in Primatology: A Critical Review

Stable isotope analysis has become an important tool in ecology over the last 25 years. A wealth of ecological information is stored in animal tissues in the relative abundances of the stable isotopes of several elements, particularly carbon and nitrogen, because these isotopes navigate through ecological processes in predictable ways. Stable carbon and nitrogen isotopes have been measured in most primate taxonomic groups and have yielded information about dietary content, dietary variability, and habitat use. Stable isotopes have recently proven useful for addressing more fine‐grained questions about niche dynamics and anthropogenic effects on feeding ecology. Here, we discuss stable carbon and nitrogen isotope systematics and critically review the published stable carbon and nitrogen isotope data for modern primates with a focus on the problems and prospects for future stable isotope applications in primatology. Am. J. Primatol. 74:969‐989, 2012. © 2012 Wiley Periodicals, Inc.     

Stable isotopes as one of nature's ecological recorders

Analyses of the natural variation in stable isotopes of components of ecological systems have provided new insights into how these systems function across paleoecological to modern timescales and across a wide range of spatial scales. Isotope abundances of the molecules in biological materials and geochemical profiles are viewed as recorders that can be used to reconstruct ecological processes or to trace ecological activities. Here, we review key short-, medium- and long-term recording capacities of stable isotopes that are currently being applied to ecological questions. The melding of advances in genetics, biochemical profiling and spatial analysis with those in isotope analyses and modeling sophistication opens the door to an exciting future in ecological research.     

硫稳定同位素技术在生态学研究中的应用

随着人为SO₂释放的增加, 硫稳定同位素的动态已成为生物地球化学循环过程中研究的热点。该文对天然硫稳定同位素在大气自然过程中的硫来源分析及其在森林生态系统、农田生态系统和水域生态系统中的硫动态研究, 人为添加的硫稳定同位素在生态环境中的应用及硫稳定同位素技术在我国酸雨研究中的潜在贡献等进行了综述, 并从硫稳定同位素技术应用研究的范围、分析手段及源解析模型方面介绍了可能的发展方向。     

Testing the long-term stability of marine isoscapes in shelf seas using jellyfish tissues

Maps of the spatial distribution of stable isotope ratios across wide geographic areas (isoscapes) are increasingly used to study mechanisms of nutrient flux, movements of animals, and to improve trophic information derived from stable isotope analyses. Isoscapes are usually constructed from reference samples collected from known geographic positions, a time consuming and costly process. In this study, we test the temporal stability of isoscapes of carbon and nitrogen isotopes across the North Sea over a ten-year period. Using jellyfish tissues as reference organisms, we show that hydrodynamic and biogeochemical processes controlling the distribution of carbon and nitrogen isotope values, and thus that the underlying isoscapes, are temporally stable. Remarkably, broad geographic variations in stable carbon and nitrogen isotope distributions across the North Sea are consistent with previously published variations seen in archaeological cod bones from the ninth to seventeenth centuries, despite dramatic changes in land use in the past 1,000 years. Stable isotope-based studies of trophic interactions or movements in animals with lifespans of a year or more in shelf ecosystems can consequently be referenced to previously published isoscape models, and do not require construction of temporally explicit isotope baseline corrections. Scyphomedusan jellyfish are excellent reference organisms for ecological stable isotope analyses in pelagic ecosystems, due to their widespread distributions, well-defined life histories, and fast tissue growth.     

Stable isotope ecology in insects: a review

1. The use of stable isotope analysis (SIA) in ecological research has dramatically increased in recent years largely because it allows researchers to investigate ecological questions that have been previously difficult to address. 2. Ecological applications of SIA include estimating fundamental niche space and overlap, evaluating trophic or species level interactions, and investigating food web structure. Increasingly, researchers have been incorporating SIA in studies of animal migration, disease transmission, diet composition, nutrient assimilation, and body condition among others. 3. Studies using SIA to evaluate the ecology of terrestrial insects have lagged behind other taxonomic groups. This poor representation of stable isotope studies in publications likely stems from a lack of familiarity of entomologists with this technique. 4. An improved understanding of SIA, as well as the advantages and disadvantages specifically related to insect research, will benefit the field of entomology. In addition, insect-model systems provide unique opportunities for entomologists to incorporate SIA in their research to advance our knowledge of insect biology and the stable isotope ecology of insects. 5. We provide background information on stable isotopes, explain sources of isotopic variation, describe the processes of how isotopes are differentially routed and incorporated into an individual's tissues, explain the principles that influence isotopic fractionation and discrimination, highlight different methods and advancements in SIA, review innovative stable isotope studies, and provide an overview of common mistakes, considerations, and future directions entomologists can explore.     

Stable isotopes of carbon and nitrogen in soil ecological studies

The development of stable isotope techniques is one of the main methodological advances in ecology of the last decades of the 20th century. Many biogeochemical processes are accompanied by changes in the ratio between stable isotopes of carbon and nitrogen (¹²C/¹³C and ¹⁴N/¹⁵N), which allows different ecosystem components and different ecosystems to be distinguished by their isotopic composition. Analysis of isotopic composition makes it possible to trace matter and energy flows through biological systems and to evaluate the rate of many ecological processes. The main concepts and methods of stable isotope ecology and patterns of stable isotope fractionation during organic matter decomposition are considered with special emphasis on the fractionation of isotopes in food chains and the use of stable isotope studies of trophic relationships between soil animals in the field.     

15N自然丰度法在生态系统氮素循环研究中的应用

稳定性同位素技术是现代生态学研究中的一门新兴技术,在生态学研究的诸多领域都展示了广阔的应用前景,其中,稳定性同位素＾１５Ｎ自然丰度法近年来在生态系统氮素循环研究中发挥了正在发挥着极为重要的作用,首先简述了自然生态系统氮素循环诸过程中的＾１５Ｎ同位素分馏机制,然后,在此基础上,综述了＾１５Ｎ自然丰度法的基本原理与方法,列举了近年 来此法在生物固氮及氮素转化过程研究中的一些应用实例,并预测了该方法在国     

Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds

When using stable isotopes as dietary tracers it is essential to consider effects of nutritional state on isotopic fractionation. While starvation is known to induce enrichment of ¹⁵N in body tissues, effects of moderate food restriction on isotope signatures have rarely been tested. We conducted two experiments to investigate effects of a 50–55% reduction in food intake on δ¹⁵N and δ¹³C values in blood cells and whole blood of tufted puffin chicks, a species that exhibits a variety of adaptive responses to nutritional deficits. We found that blood from puffin chicks fed ad libitum became enriched in ¹⁵N and ¹³C compared to food-restricted chicks. Our results show that ¹⁵N enrichment is not always associated with food deprivation and argue effects of growth on diet–tissue fractionation of nitrogen stable isotopes (Δ¹⁵N) need to be considered in stable isotope studies. The decrease in δ¹³C of whole blood and blood cells in restricted birds is likely due to incorporation of carbon from ¹³C-depleted lipids into proteins. Effects of nutritional restriction on δ¹⁵N and δ¹³C values were relatively small in both experiments (δ¹⁵N: 0.77 and 0.41‰, δ¹³C: 0.20 and 0.25‰) compared to effects of ecological processes, indicating physiological effects do not preclude the use of carbon and nitrogen stable isotopes in studies of seabird ecology. Nevertheless, our results demonstrate that physiological processes affect nitrogen and carbon stable isotopes in growing birds and we caution isotope ecologists to consider these effects to avoid drawing spurious conclusions.     

稳定同位素技术在土壤跳虫研究上的应用

稳定同位素技术的发展和应用是20世纪90年代生态学研究方法最重要的进步之一.许多生态学过程都伴随着同位素比率的变化,根据这些变化可以追踪生态系统的物质循环和能量流动.近年来,许多学者把稳定同位素技术引入到土壤生态学,主要用于研究土壤碳循环和土壤生物之间的营养关系,在很大程度上提升了对地下生态系统的理解.跳虫作为土壤动物群落的重要组分,它的食性和营养位置一直存在着许多不确定性.稳定同位素技术的应用,为确定跳虫的食物来源、营养位置和营养关系提供了一个强大的工具.本文综述了稳定同位素技术在跳虫食性和营养级研究上的应用,并指出了不足之处以及今后的发展方向.     

The determination of amino acid pool sizes and turnover rates by gas chromatographic mass spectrometric analysis of stable isotope enrichment

Gas chromatography mass spectrometry has been used to determine the 15N enrichment of plasma glycine of rabbits at various times following the intravenous administration of 15N-glycine. These data were used to prepare isotope enrichment time decay curves for eleven individual animals. The slopes and intercepts of least squares lines that describe the decay curves were considerably more accurately than those reported in similar studies employing radioactive tracers. Individual glycine pool sizes (13.8-37.4 micronmoles per 100 g body wt), turnovers rates (2.66-3.36 pools h-1) and flux (50.4-99.7 micronmoles h-1 per 100 g body wt) were estimated from these parameters in a group of animals and compared with the literature values. These results demonstrate that low risk non-radioactive stable isotopes can be substituted for radioactive tracers in studies of human amino acid metabolism, with considerable saving in time and without loss in accuracy, when gas chromatography mass spectrometry is used to determine plasma amino acid and stable isotope enrichment.     

15N自然丰度法在生态系统氮素循环研究中的应用

稳定性同位素技术是现代生态学研究中的一门新兴技术,在生态学研究的诸多领域都展示了广阔的应用前景。其中,稳定性同位素     

基于稳定同位素的干旱半干旱区SPAC水分运移过程研究进展

土壤-植物-大气连续体(SPAC)是生态水文学的重点研究对象,其水分运移过程对于干旱半干旱区生态植被建设和水资源综合管理具有重要意义。氢氧稳定同位素较高的灵敏性和准确度有助于揭示这一过程。介绍了氢氧稳定同位素在土壤-大气界面、土壤-地下水界面、土壤-植物界面和植物-大气界面水分补给传输过程中的应用,包括土壤水分来源和蒸发;水分补给入渗机制和滞留时间;植物水分来源和水力再分配;蒸散发分割和叶片吸水的相关研究,同时明确了氢氧稳定同位素技术在应用过程中存在的一些不确定性以及未来亟需加强的方面,以期为利用稳定同位素技术对生态水文过程的研究提供参考依据。     

Quantifying the multiple facets of isotopic diversity: New metrics for stable isotope ecology

Stable isotope analyses have emerged as an insightful tool for ecologists, with quantitative methods being developed to analyse data at the population, community and food web levels. In parallel, functional ecologists have developed metrics to quantify the multiple facets of functional diversity in a n-dimensional space based on functional traits. Here, we transferred and adapted metrics developed by functional ecologists into a set of four isotopic diversity metrics (isotopic divergence, dispersion, evenness and uniqueness) complementary to the existing metrics. Specifically, these new metrics are mathematically independent of the number of organisms analysed and account for the abundance of organisms. They can also be calculated with more than two stable isotopes. In addition, we also provide a procedure for calculating the levels of isotopic overlap (similarity and turnover) between two groups of organisms. These metrics have been implemented into new functions in R made freely available to users and we illustrated their application using stable isotope values from a freshwater fish community. Transferring the framework developed initially for measuring functional diversity to stable isotope ecology will allow more efficient assessments of changes in the multiple facets of isotopic diversity following anthropogenic disturbances.     

The stable isotope ecology of terrestrial plant succession

We review the relevance and use of stable isotopes for the study of plant community succession. Stable isotope measurements provide information on the origin of resources acquired by plants, the processes governing resource uptake and transformation, and the physiological and environmental conditions of plant growth. When combined with measurements of the stable isotope ratio values of soil microbial biomass, soil organic matter and plant litter, isotope measurements of plants can indicate effects of successional changes on ecosystem processes. However, their application to questions of plant succession and ecosystem change is limited by the degree to which the underlying assumptions are met in each study, and complementary measures may be required, depending upon the question of interest. First, we discuss the changes that occur in the stable isotope composition of plants and ecosystems with ontogeny and species replacements, as well as their potential evolutionary significance. Second, we discuss the imprints of plant competition and facilitation on leaf and wood tissue, as well as how stable isotopes can provide novel insights on the mechanisms underlying plant interactions. Finally, we discuss the capacity for stable isotope measurements to serve as a proxy record for past disturbances such as fire, logging and cyclones.     

Insights into the habitat of Middle Permian pareiasaurs (Parareptilia) from preliminary isotopic analyses

Pareiasaurs were an abundant group of large herbivores during Middle and Late Permian times. The habitat of pareiasaurs has proven enigmatic, and ecological interpretations from anatomical and taphonomic data have included aquatic, semi‐aquatic to fully terrestrial lifestyles. Insight into the ecology of extinct taxa can also be gained from stable isotope analyses, and interpretations benefit from studies of multiple, coeval groups. Here, we report the first stable carbon and oxygen isotope analyses from the enamel, dentine and bone of pareiasaurs and contemporaneous therapsids (dinocephalians and therocephalians), in specimens recovered from the Permian Tapinocephalus to lower Pristerognathus Assemblage Zones of South Africa. Previous ecological inferences for dinocephalians (riparian to terrestrial) and therocephalians (terrestrial) are less ambiguous than reconstructions for pareiasaurs and provide an independent reference for interpreting stable isotope measurements. Oxygen isotopes of enamel carbonate were indistinguishable between pareiasaurs and therocephalians, which had higher values than dinocephalians. The data suggest that dinocephalians and pareiasaurs (megaherbivores) inhabited different ecological niches and that pareiasaurs may have shared a terrestrial habitat with therocephalians (carnivores). Our results agree with earlier suggestions of a terrestrial lifestyle among pareiasaurs and provide evidence of niche partitioning among large coeval Capitanian herbivores of South Africa.     

Stable isotope methods in biological and ecological studies of arthropods

This is an eclectic review and analysis of contemporary and promising stable isotope methodologies to study the biology and ecology of arthropods. It is augmented with literature from other disciplines, indicative of the potential for knowledge transfer. It is demonstrated that stable isotopes can be used to understand fundamental processes in the biology and ecology of arthropods, which range from nutrition and resource allocation to dispersal, food‐web structure, predation, etc. It is concluded that falling costs and reduced complexity of isotope analysis, besides the emergence of new analytical methods, are likely to improve access to isotope technology for arthropod studies still further. Stable isotopes pose no environmental threat and do not change the chemistry or biology of the target organism or system. These therefore represent ideal tracers for field and ecophysiological studies, thereby avoiding reductionist experimentation and encouraging more holistic approaches. Considering (i) the ease with which insects and other arthropods can be marked, (ii) minimal impact of the label on their behaviour, physiology, and ecology, and (iii) environmental safety, we advocate more widespread application of stable isotope technology in arthropod studies and present a variety of potential uses.     

Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology

The idea that interspecific variation in trophic morphology among closely related species effectively permits resource partitioning has driven research on ecological radiation since Darwin first described variation in beak morphology among Geospiza. Marine turtles comprise an ecological radiation in which interspecific differences in trophic morphology have similarly been implicated as a pathway to ecopartition the marine realm, in both extant and extinct species. Because marine turtles are charismatic flagship species of conservation concern, their trophic ecology has been studied intensively using stable isotope analyses to gain insights into habitat use and diet, principally to inform conservation management. This legion of studies provides an unparalleled opportunity to examine ecological partitioning across numerous hierarchical levels that heretofore has not been applied to any other ecological radiation. Our contribution aims to provide a quantitative analysis of interspecific variation and a comprehensive review of intraspecific variation in trophic ecology across different hierarchical levels marshalling insights about realised trophic ecology derived from stable isotopes. We reviewed 113 stable isotope studies, mostly involving single species, and conducted a meta‐analysis of data from adults to elucidate differences in trophic ecology among species. Our study reveals a more intricate hierarchy of ecopartitioning by marine turtles than previously recognised based on trophic morphology and dietary analyses. We found strong statistical support for interspecific partitioning, as well as a continuum of intraspecific trophic sub‐specialisation in most species across several hierarchical levels. This ubiquity of trophic specialisation across many hierarchical levels exposes a far more complex view of trophic ecology and resource‐axis exploitation than suggested by species diversity alone. Not only do species segregate along many widely understood axes such as body size, macrohabitat, and trophic morphology but the general pattern revealed by isotopic studies is one of microhabitat segregation and variation in foraging behaviour within species, within populations, and among individuals. These findings are highly relevant to conservation management because they imply ecological non‐exchangeability, which introduces a new dimension beyond that of genetic stocks which drives current conservation planning. Perhaps the most remarkable finding from our data synthesis is that four of six marine turtle species forage across several trophic levels. This pattern is unlike that seen in other large marine predators, which forage at a single trophic level according to stable isotopes. This finding affirms suggestions that marine turtles are robust sentinels of ocean health and likely stabilise marine food webs. This insight has broader significance for studies of marine food webs and trophic ecology of large marine predators. Beyond insights concerning marine turtle ecology and conservation, our findings also have broader implications for the study of ecological radiations. Particularly, the unrecognised complexity of ecopartitioning beyond that predicted by trophic morphology suggests that this dominant approach in adaptive radiation research likely underestimates the degree of resource overlap and that interspecific disparities in trophic morphology may often over‐predict the degree of realised ecopartitioning. Hence, our findings suggest that stable isotopes can profitably be applied to study other ecological radiations and may reveal trophic variation beyond that reflected by trophic morphology.     

稳定性同位素技术与Keeling曲线法在陆地生态系统碳/水交换研究中的应用

稳定性同位素技术和Keeling曲线法是现代生态学研究的重要手段和方法之一。稳定性同位素能够整合生态系统复杂的生物学、生态学和生物地球化学过程在时间和空间尺度上对环境变化的响应。Keeling曲线法是以生物过程前后物质平衡理论为基础,将CO₂或H₂O的同位素组成(δD、δ¹³C或δ¹⁸O)与其对应浓度测量结合起来,将生态系统净碳通量区分为光合固定和呼吸释放通量,或将整个生态系统水分蒸散区分为植物蒸腾和土壤蒸发。在全球尺度上,稳定性同位素技术、Keeling曲线法与全球尺度陆地生态系统模型相结合,还可区分陆地生态系统和海洋生态系统对全球碳通量的贡献以及不同植被类型(C₃或C₄)在全球CO₂同化量中所占的比例。然而,生态系统的异质性使得稳定性同位素技术和Keeling曲线法从冠层尺度外推到生态系统、区域或全球尺度时存在有一定程度的不确定性。此外,取样时间、地点的选取也会影响最终的研究结果。尽管如此,随着分析手段的不断精确和研究方法的日趋完善,稳定性同位素技术和Keeling曲线法与其它测量方法(如微气象法)的有机结合将成为未来陆地生态系统碳/水交换研究的重要手段和方法之一。     

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.     

Carbon isotopes in functional soil ecology

Soil is an integral part of terrestrial ecosystems. Many soil ecologists interested in soil ecosystem functioning rely, to some degree, on stable isotope methodologies. The study of the natural abundance of carbon isotopes, especially (13)C but also (14)C, in the environment and the use of stable carbon isotope tracers have proved very useful in investigating the soil carbon cycle and soil trophic relationships. Recent methodological and technical advances have greatly extended the possibilities for the application of stable carbon isotopes to terrestrial ecology and have vastly improved our knowledge of belowground ecosystem functioning and will continue to do so. A better understanding of soil processes is invaluable in predicting the future impacts of global environmental change on terrestrial ecosystems.