稳定同位素技术在头足类摄食生态学研究中的应用

头足类在海洋食物网营养关系中占有重要地位,然而对其复杂的生活史过程,尤其是摄食生态学信息仍知之甚少.稳定同位素技术作为传统食物网科学研究方法的有力补充,可更深层次地分析头足类的摄食习性和栖息地等方面的重要信息.本文在比较分析国内外头足类摄食生态学研究方法的基础上,系统归纳总结了稳定同位素技术在头足类摄食生态学研究中的发展现状并介绍最新进展情况,着重分析稳定同位素技术在头足类生活史信息,尤其是在摄食生态学研究中的应用现状及发展前景,包括测定样品标准化、头足类生长发育过程中的食性转换和洄游分布等核心问题,以促进其在头足类生物学研究中的应用.     

东太平洋中部中上层鲨鱼群落营养生态位分化

鲨鱼在大洋生态系统中占据着重要的生态地位,其作为顶级捕食者,通过下行效应直接影响生态系统的稳定.稳定同位素技术是目前研究摄食生态学强有力的手段之一,可利用碳氮稳定同位素在食物网中的特性分别指示鲨鱼的食物来源和营养级.本研究选取8种130尾采集自东太平洋中部的中上层鲨鱼,应用稳定同位素绘制其种群生态位图谱,比较不同种群间的生态地位及资源分配方式上的差异.结果表明:不同鲨鱼种群碳、氮稳定同位素比值存在显著差异;8种鲨鱼在东太平洋生态系统中的营养级为4.3~5.4,大青鲨、尖吻鲭鲨与其他6种鲨鱼存在摄食隔离,表现出独特的营养生态地位.这些结果充分证明大洋性中上层鲨鱼并非生态系统的冗余种,其营养生态位的独特性不会被其他捕食者简单地替代和弥补.     

水域生态学中生物稳定同位素样品采集、处理与保存

稳定同位素分析技术由于能够刻画复杂的食物网结构并追踪食物网中的能量流而成为水域生态学研究中的重要手段。但是当水生生物样品采集、处理和保存过程中存在不确定性时, 营养关系分析中的同位素结果可能会产生误导性解释。文章采用数据模拟分析和文献总结的方法, 研究了水域生态系统中样品采集、处理和保存对于稳定同位素的影响, 概括性地建议了水域生态系统中适合应用稳定同位素分析技术开展生态学研究的样品采集、处理和保存的注意事项。但今后仍需进一步评估样品采集、处理和保存对稳定同位素比值的影响效果, 确定化学动力学在水生生物样品采集、处理和保存中的作用, 以进一步完善水生生物样品的采集、处理和保存稳定同位素生态学研究规范。     

海洋生态系统稳定同位素基线的选取

稳定同位素技术在海洋食物网研究中得到了广泛的应用,但在分析海洋生物食性和营养级时,需要选择某种生物或物质的稳定同位素值作为基线.本文综述了河口和海湾、浅海、大洋及深海4类典型海洋生态系统稳定同位素基线的选取,分析了影响稳定同位素基线选择的因素,以及特定化合物稳定同位素在消除基线时空异质性中的潜在价值,并对目前存在的问题以及今后的研究方向进行了展望,以期为国内学者进一步深入开展海洋生态系统的稳定同位素生态学研究提供有益参考.     

脂类抽提对北太平洋柔鱼肌肉碳、氮稳定同位素测定结果的影响

稳定同位素技术可深层次地分析头足类的摄食习性和栖息地等方面的重要信息.稳定同位素分析多选取动物肌肉为研究组织,然而,肌肉中的脂类含量会影响对其稳定同位素信息的准确解析.北太平洋柔鱼是重要的大洋经济性头足类,在海洋生态系统中具有重要的生态地位.本研究选取了53尾北太平洋柔鱼,通过分析脂类抽提对胴体肌肉稳定同位素比值的影响,探讨脂类物质对稳定同位素比值的干扰机制,对比不同碳稳定同位素比值校正模型的适用性,并提出适用于北太平洋柔鱼胴体肌肉δ¹³-C校正模型.结果表明： 北太平洋柔鱼肌肉的脂类抽提会引起稳定同位素测定结果的显著变化,δ¹³-C和δ¹⁵-N分别平均升高0.71‰和0.47‰,在分析组织碳稳定同位素比值时,脂类抽提在样品预处理过程中十分必要,其能消除脂类对样品稳定同位素分析的干扰,从而更加准确地分析研究对象食性与栖息地的变化.在单独进行氮稳定同位素比值分析时,则不需要进行脂类抽提.     

稳定性同位素技术在生物科学中的应用

稳定同位素技术是一项相对新兴的技术,其最早主要应用于地质学和地球化学.近些年来,稳定性同位素技术在农业、医学、环境学、海洋学、石油、化工、冶金等方面的应用也日益广泛.利用稳定性同位素技术还可以解决生物科学中一些传统方法难以解决的问题.对稳定性同位素的相关概念进行了介绍,并对其在植物、动物和微生物生理、生态学领域研究中的应用进行了综述,同时对其在环境保护、兴奋剂检测、毒品和炸药的产地辨别等领域的应用作了概述.     

秘鲁外海茎柔鱼摄食洄游的稳定同位素研究

茎柔鱼是具有高度洄游性的中上层头足类,是生态系统中的关键物种,也是我国远洋渔业重要捕捞对象之一.了解掌握茎柔鱼摄食及洄游信息有助于对其资源进行更合理利用.头足类内壳是一良好的信息载体,其生长发育具有不可逆性且生长贯穿整个生活史过程,包含了头足类生活史过程中的全部信息.本研究通过对秘鲁外海茎柔鱼耳石日龄进行鉴定,建立其内壳叶轴生长方程,根据该生长方程对内壳叶轴进行连续切割,测定其碳、氮稳定同位素比值,并初步分析了其在生长发育过程中的食性转换和洄游习性.结果表明: 茎柔鱼个体在出生180 d后开始洄游活动,且营养层次存在下降趋势.证明了内壳连续取样分析茎柔鱼个体摄食习性和栖息地变化的可行性.     

金枪鱼类耳石微化学研究进展

近年来,基于鱼类钙化物质中微量元素和同位素等微化学成分分析已成为分析鱼类种群结构、生活史及洄游环境史等的一种新兴手段.随着鱼类耳石微化学研究及应用的日渐成熟与完善,该手段也日益成为金枪鱼类生态学研究的良好工具.目前金枪鱼类耳石微化学的研究内容主要包括微量元素和同位素等,其中微量元素是应用研究的重点和热点,其在金枪鱼类,尤其是蓝鳍金枪鱼种群划分、出生源、洄游环境史和生活史分析等方面发挥了重要的作用.但多数研究集中在耳石锶钙比率(Sr/Ca)的变化上,且关于耳石碳氧同位素分馏与温度之间的关系尚无定论.为了开发耳石微化学的巨大价值,有必要加强对其沉积机理的研究,并采用综合研究方法从时空角度分析耳石中多种微量元素的含量及其变化.     

基于稳定同位素的SPAC水碳拆分及耦合研究进展

土壤-植被-大气连续体(SPAC)是陆地水文学、生态学和全球变化领域的重要研究对象,其水碳循环过程及耦合机制是前沿性问题.稳定同位素技术示踪、整合和指示的特征有助于评估分析生态系统固碳和耗水情况.本文在简述稳定同位素应用原理和技术的基础上,重点阐释了基于稳定同位素光学技术的SPAC系统水碳交换研究进展,包括:在净碳通量中拆分光合与呼吸量,在蒸散通量中拆分蒸腾与蒸发量,以及在系统尺度上的水碳耦合研究.新兴的技术和方法实现了生态系统尺度上长期高频的同位素观测,但在测量精准度、生态系统呼吸拆分、非稳态模型适应性、尺度转换和水碳耦合机制等方面存在挑战.本文探讨了现有主要研究成果、局限性以及未来研究展望,以期对稳定同位素生态学领域的新研究和技术发展有所帮助.     

稳定同位素技术在水域生态系统研究中的应用

稳定同位素作为一种天然的示踪物,应用十分广泛,其在水域生态学中的应用也日益受到重视。生物同位素组成总是与其食物同位素组成相一致,能随食物的改变而相应地发生改变,是生物生存状况的理想指示物,为水域生态系统食物网结构与功能、物质流与能量流的研究提供了有力的技术支撑。在综评稳定同位素技术原理与方法的基础上,较为详细地对其应用于水域生态研究的理论基础与进展进行了总结。该方法的应用以水域中生产者同位素组成差异为前提,主要涉及确定食物来源、食物的贡献比例、营养级的确定、食物网结构的构建及鱼类等水生生物的洄游及迁移路线等方面,这些研究对了解生态系统的动态变化与外界环境对其影响具有重要意义。并对我国此类研究的前景和存在问题进行了探讨。     

Characterization of food web structure of the upper continental slope of the Celtic Sea highlighting the trophic ecology of five deep‐sea fishes

In marine ecosystems, the study of trophic relationships has extensively benefited from the development of stable isotope analyses (SIA) as dietary tracers. SIA are particularly useful in elucidating the structure of deep sea food webs given the constraints involved in obtaining gut‐content data from deep trawling. We used carbon and nitrogen stable isotope analyses and Stable Isotope Bayesian Ellipses in R (SIBER) and Stable Isotope Analysis in R (SIAR) routines, to determine the trophic ecology of five deep‐sea fishes from the upper continental slope of the Celtic Sea. SIA made it possible to deduce some general tendencies in food‐web structure and species trophic interactions and confirmed diet determined by gut‐content analysis for the same species, in other ecoregions. More specifically, mixing models revealed that the deep sea species considered are omnivorous and are able to feed on all the sampled taxa. Based on isotopic ratio, no clear differences in fish diet could be detected from one species to another except for rabbit fish, which has benthic affinities. Three species, blackbelly rosefish, greater forkbeard and softhead grenadier showed overlapping isotopic niches. This study is the first attempt to describe the trophic ecology of deep sea species on the Celtic Sea upper continental slope. In the context of the development of ecosystem integrated modeling approaches for managing fisheries in the Celtic sea, and considering the vulnerability of deep‐water species, improving the knowledge on the trophic ecology of these local species is of importance in order to allow their sustainable exploitation.     

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.     

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.     

Using stable isotope analysis to understand the migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias)

The white shark (Carcharodon carcharias) is a wide-ranging apex predator in the northeastern Pacific (NEP). Electronic tagging has demonstrated that white sharks exhibit a regular migratory pattern, occurring at coastal sites during the late summer, autumn and early winter and moving offshore to oceanic habitats during the remainder of the year, although the purpose of these migrations remains unclear. The purpose of this study was to use stable isotope analysis (SIA) to provide insight into the trophic ecology and migratory behaviors of white sharks in the NEP. Between 2006 and 2009, 53 white sharks were biopsied in central California to obtain dermal and muscle tissues, which were analyzed for stable isotope values of carbon (δ(13)C) and nitrogen (δ(15)N). We developed a mixing model that directly incorporates movement data and tissue incorporation (turnover) rates to better estimate the relative importance of different focal areas to white shark diet and elucidate their migratory behavior. Mixing model results for muscle showed a relatively equal dietary contribution from coastal and offshore regions, indicating that white sharks forage in both areas. However, model results indicated that sharks foraged at a higher relative rate in coastal habitats. There was a negative relationship between shark length and muscle δ(13)C and δ(15)N values, which may indicate ontogenetic changes in habitat use related to onset of maturity. The isotopic composition of dermal tissue was consistent with a more rapid incorporation rate than muscle and may represent more recent foraging. Low offshore consumption rates suggest that it is unlikely that foraging is the primary purpose of the offshore migrations. These results demonstrate how SIA can provide insight into the trophic ecology and migratory behavior of marine predators, especially when coupled with electronic tagging data.     

Using stable isotope biogeochemistry to study marine mammal ecology

Stable isotope analysis (SIA) has emerged as a common tool in ecology and has proven especially useful in the study of animal diet, habitat use, movement, and physiology. SIA has been vigorously applied to the study of marine mammals, because most species live in habitats or undergo large migrations/movements that make them difficult to observe. Our review supplies a complete list of published SIA contributions to marine mammal science and highlights informative case examples in four general research areas: (1) physiology and fractionation, (2) foraging ecology and habitat use, (3) ecotoxicology, and (4) historic ecology and paleoecology. We also provide a condensed background of isotopic nomenclature, highlight several physiological considerations important for accurate interpretation of isotopic data, and identify research areas ripe for future growth. Because it is impossible to conduct controlled laboratory experiments on most marine mammal species, future studies in marine mammal ecology must draw on isotopic data collected from other organisms and be cognizant of key assumptions often made in the application of SIA to the study of animal ecology. The review is designed to be accessible to all audiences, from students unfamiliar with SIA to those who have utilized it in published studies.     

Combining stable isotope analysis and conventional techniques to improve knowledge of the diet of the European Roller Coracias garrulus

Diet studies are crucial for understanding the ecology and evolution of species, as well as for establishing appropriate conservation and management strategies. However, they remain methodologically challenging due to variation between seasons, sites, sexes or age groups and even variation between individuals. Due to method‐specific characteristics and biases, a combination of existing techniques can overcome the inherent limitations of each technique and provide a more accurate and broad picture of species’ food preferences. Here, we examine diet information obtained using three different assessment methods to better understand the trophic ecology of the European Roller Coracias garrulus, a species targeted by conservation measures in Europe. First, we analysed regurgitated pellets and video‐recordings to report the diet composition of adult and nestling Rollers, respectively. Secondly, we used stable isotope analysis (SIA) to investigate adult sexual diet segregation as well as to confirm the main findings regarding adult and nestling diets obtained through conventional methods. Based on the analysis of pellets, the diet of adult Rollers was dominated by Coleoptera, whereas camera images revealed that the diet of nestlings was dominated by Orthoptera, mainly grasshoppers and bush crickets. Blood isotopic signatures of adult and nestling Rollers confirmed the results obtained through pellet and video‐recording techniques. Of the three methods, pellet analysis provided the most comprehensive trophic information regarding the detectable prey spectrum and prey species contribution, as well as basic diet information for the SIA. Our results also highlight the potential of SIA for assessing intraspecific variation in diet by sampling individuals of known age and sex, which is often unfeasible through conventional approaches. SIA analysis showed no differences in δ¹³C and δ¹⁵N ratios of blood between males and females and a high degree of overlap amongst isotopic niches, suggesting no sex‐specific partitioning in resource use. Overall, we showed that the combination of different methods could be used to gain new and clearer insights into avian trophic ecology that are essential for informing habitat management aiming to improve availability of foraging resources.     

Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins

Stomach content analysis (SCA) and more recently stable isotope analysis (SIA) integrated with isotopic mixing models have become common methods for dietary studies and provide insight into the foraging ecology of seabirds. However, both methods have drawbacks and biases that may result in difficulties in quantifying inter-annual and species-specific differences in diets. We used these two methods to simultaneously quantify the chick-rearing diet of Chinstrap (Pygoscelis antarctica) and Gentoo (P. papua) penguins and highlight methods of integrating SCA data to increase accuracy of diet composition estimates using SIA. SCA biomass estimates were highly variable and underestimated the importance of soft-bodied prey such as fish. Two-source, isotopic mixing model predictions were less variable and identified inter-annual and species-specific differences in the relative amounts of fish and krill in penguin diets not readily apparent using SCA. In contrast, multi-source isotopic mixing models had difficulty estimating the dietary contribution of fish species occupying similar trophic levels without refinement using SCA-derived otolith data. Overall, our ability to track inter-annual and species-specific differences in penguin diets using SIA was enhanced by integrating SCA data to isotopic mixing modes in three ways: 1) selecting appropriate prey sources, 2) weighting combinations of isotopically similar prey in two-source mixing models and 3) refining predicted contributions of isotopically similar prey in multi-source models.     

Stable-isotope analysis of a deep-sea benthic-fish assemblage: evidence of an enriched benthic food web

In this study, fishes and invertebrates collected from the continental slope (1000 m) of the eastern North Pacific Ocean were analysed using stable-isotope analysis (SIA). Resulting trophic positions (T(P) ) were compared to known diets and habitats from the literature. Dual isotope plots indicated that most species groups (invertebrates and fishes) sorted as expected along the carbon and nitrogen axes, with less intraspecific variability than interspecific variability. Results also indicated an isotopically distinct benthic and pelagic food web, as the benthic food web was more enriched in both nitrogen and carbon isotopes. Trophic positions from SIA supported this finding, resulting in the assignment of fishes to different trophic positions from those expected based on published dietary information. These differences can be explained largely by the habitat of the prey and the percentage of the diet that was scavenged. A mixing model estimated dietary contributions of prey similar to those of the known diet of Bathyraja trachura from stomach-content analysis (SCA). Linear regressions indicated that trophic positions calculated from SIA and SCA, when plotted against B. trachura total length for 32 individuals, exhibited similar variation and patterns. Only the T(P) from SCA yielded significant results (stomach content: P < 0·05, stable isotope: P > 0·05).