稳定同位素技术在鲨鱼摄食和洄游行为研究中的应用

随着稳定同位素分析技术的不断成熟,其在生态学领域中的应用也增长迅速,并成为动物摄食生态学的重要研究工具.鲨鱼因其在生物系统进化过程中的独特地位和海洋生态系统中的重要作用已成为海洋食物网研究的重点,然而国内针对鲨鱼摄食习性和洄游行为等方面的研究仍处于起步阶段.本文在总结了国内外鲨鱼稳定同位素分析组织样品选取和样品预处理方法的基础上,系统归纳了稳定同位素技术在鲨鱼摄食生态学,尤其在其摄食和洄游行为研究领域中的应用,着重分析稳定同位素技术在鲨鱼稳定同位素判别值和更新速率、食性分析、营养级评估、洄游路径分析和生态位分布等核心问题上的应用现状和发展前景,以期为国内学者开展鲨鱼类基础生物、生态学研究提供有益参考.     

黄东海生态系统食物网连续营养谱的建立: 来自碳氮稳定同位素方法的结果

应用天然存在的碳氮稳定同位素方法研究了黄东海生态系统食物网的营养结构, 初步建立了从浮游植物到顶级捕食者的水体食物网连续营养谱, 并结合底栖生物碳同位素资料勾勒出黄东海食物网营养结构图, 与根据1985~1986年主要资源种群生物量绘制的黄海简化食物网和营养结构图基本一致并略有改进. 结果证明, 稳定同位素方法是未来研究从病毒到顶级捕食者完整海洋食物网连续营养谱以及食物网稳定性的一个潜在的有用手段.     

基于碳、氮稳定同位素技术的东太湖水生食物网结构

稳定同位素技术是研究生态系统食物网中物质循环与能量流动的有效技术之一。碳稳定同位素比值(δ13C)常用来分析消费者食物来源,而氮稳定同位素比值(δ15N)常用来确定生物在食物网中的营养位置。本研究应用碳、氮稳定同位素技术构建了东太湖食物网结构。结果表明:东太湖食物网主要由两条营养传递途径组成,即浮游植物为初级生产者的浮游营养传递途径和苦草等大型水生植物为初级生产者的近岸底层营养传递途径,湖中9种主要鱼虾类能量主要来自近岸底层传递;翘嘴鲌(Erythroculter ilishaeformis)、鳜(Siniperca chuatsi)和鲶(Silurus sp.)作为湖泊中的顶极捕食者,具有相对最高的营养级,并占据食物网的顶层。     

柔鱼科近缘种茎柔鱼与鸢乌贼营养生态位及相互关系

同域近缘种由于进化选择的压力,会形成不同的行为适应策略。研究同域近缘种生态位格局,有助于理解近缘物种的竞争和共存机制,是深入了解种群动态变化的基础性问题。选取东太平洋赤道海域的柔鱼科头足类近缘种茎柔鱼和鸢乌贼为研究对象,利用生物地球化学示踪物(稳定同位素和脂肪酸)分析两种头足类的营养生态位及相互关系。结果显示,茎柔鱼和鸢乌贼肌肉的部分必需脂肪酸(C18∶2n6、C20∶2n6、C20∶3n3、C20∶4n6和C20∶5n3)含量存在差异,说明二者食物来源不同,但其碳、氮稳定同位素比值无显著差异,可能是因为相同个体大小的茎柔鱼和鸢乌贼营养级相近,且摄食空间相似。这些结果在营养生态位的分析结果中也得到了验证,稳定同位素营养生态位的重叠程度高于脂肪酸营养生态位,表明脂肪酸组成更能体现同域近缘种的食性差异。本研究可加深对头足类进化过程中摄食行为适应机制的理解,并为评估同域近缘种的营养生态位关系提供有益参考。     

应用碳氮稳定同位素技术研究江豚(Neophocaena asiaeorientalis ssp. sunameri)食性

稳定同位素技术已广泛地用于分析生态系统中食物网的食物来源和营养级关系,但在海洋哺乳动物食性方面应用较少。通过分析2012年4—6月在辽东湾沿岸海域搁浅而死亡的江豚样本和同时期(6月)取自辽东湾海域主要渔获物的碳氮稳定同位素比值,研究了江豚(Neophocaena asiaeorientalis ssp.sunameri)及其可能摄食饵料的碳氮稳定同位素组成。结果表明:江豚δ13C值为(-18.4±0.3)‰,δ15N值为(13.8±0.4)‰。28种可能生物饵料的δ13C值的范围为-19.5‰—-17.0‰,δ~(15)N值的范围为11.4‰—14.0‰。江豚的营养级为4.5,高于传统胃含物分析法的研究结果。28种测试生物的营养级位于3.8—4.6之间。江豚的食物来源主要以鱼类为主,对食物种类的喜食顺序为中上层鱼类中下层鱼类底层鱼类头足类虾类蟹类,其平均贡献率分别为43.9%、18.2%、13.1%、10.0%、8.8%、6.0%。江豚碳氮稳定同位素比值与体长无明显的线性关系,碳营养源较为稳定,氮营养源复杂多变。     

不同时期北部湾日本带鱼营养生态位差异

基于2008—2009年和2018年对北部湾日本带鱼的采样,通过测定碳氮稳定同位素,计算其营养级、营养生态位等指标,对比分析10年前后日本带鱼营养生态位的差异,探究其生态适应能力的变动。结果表明: 2个时期北部湾日本带鱼碳稳定同位素(δ¹³C)值差异明显,2018年δ¹³C值范围变窄,平均值变小,推测日本带鱼食物来源由偏中上层向偏中下层水域转变;氮稳定同位素(δ¹⁵N)值的范围和平均值基本保持不变,营养级范围和平均值(3.38和3.43)变化不明显,说明近10年来北部湾日本带鱼在生态系统中的营养层次比较稳定。日本带鱼δ¹³C值与肛长相关性不显著,δ¹⁵N则为极显著正相关性。在营养生态位方面,2018年的生态位指标均出现不同程度的下降,下降幅度的范围为1.1%~32.1%;生态位总面积和核心生态位面积分别由20.20和4.68缩小至14.20和3.18,说明北部湾日本带鱼的营养生态位发生了显著变化,对资源利用能力和环境适应能力下降。推测,10年来北部湾日本带鱼的营养级变化不明显,但由于食物来源发生变化,营养来源多样性下降,营养生态位变小。     

应用脂肪酸组成研究热带东太平洋同域中上层鲨鱼营养生态位分化

物种对食物资源利用方式的差异,即营养生态位分化是物种共存的先决条件之一,对种间营养生态位的比较研究有助于了解同域分布物种的共存机制。脂肪酸组成可反映生物较长时间尺度的摄食信息,对探讨物种间营养生态位分化具有重要指示作用。热带东太平洋主要栖息有8种大型中上层鲨鱼,大青鲨(Prionace glauca)、大眼长尾鲨(Alopias superciliosus)、镰状真鲨(Carcharhinus falciformis)、长鳍真鲨(Carcharhinus longimanus)、浅海长尾鲨(Alopias pelagicus)、尖吻鲭鲨(Isurus oxyrinchus)、路氏双髻鲨(Sphyrna lewini)和锤头双髻鲨(Sphyrna zygaena),通过比较其肌肉脂肪酸组成,分析种间食性差异,营养关系及营养生态位分化。结果表明,尖吻鲭鲨营养级相对较高,大青鲨相对较低。3种鼠鲨与5种真鲨存在食性差异或栖息地隔离。浅海长尾鲨与大眼长尾鲨营养生态位重叠程度较高,存在激烈的资源竞争。大青鲨与镰状真鲨生态位宽度较大,表征其对环境的可塑性较强;尖吻鲭鲨和路氏双髻鲨生态位宽度较小,表现为其食性的特化。本研究解释了脂肪酸组成分析在鲨鱼摄食研究中的潜在应用,对分析大洋性鲨鱼的营养生态位分化,资源分配方式及同域共存机制有一定的应用价值。     

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磷虾[相对重要指数百分比(IRI)=87.6%,出现频率(F)=57.6%]、小拟哲水蚤(IRI=3.2%,F=15.3%)和细足法虫戎(IRI=2.1%,F=13.1%);同位素分析显示,桡足类是鳀的主要食物来源,其次是磷虾类,端足类的食源贡献率最小,不足1%。鳀食物组成昼夜差异明显,摄食强度白天比晚上高,下午最高,午夜最低;叉长90 mm是鳀食性转变的拐点,小于90 mm的鳀主要摄食浮游动物,大于90 mm的鳀主要摄食浮游动物,兼食小型鱼类。鳀的δ¹³C值范围为-21.66‰～-18.14‰,平均值为(-19.92±0.86)‰;δ¹⁵N值范围为4.07‰～10.78‰,平均值为(8.14±2.48)‰;鳀的δ¹³C和δ¹⁵N比值与叉长呈极显著正相关。基于胃含物分析的鳀营养级为3.4,基于δ¹⁵N稳定同位素的鳀营养级为2.7。本研究可为中上层小型鱼类在生态系统中的营养地位提供参考依据,为构建食物网营养通道提供基础资料。     

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.     

基于多组织稳定同位素比值的热带大西洋4种鲨鱼营养生态位分化

不同代谢速率组织间的碳、氮稳定同位素比值(δ¹³C和δ¹⁵N)可以反映生物不同时间尺度的摄食信息,对探讨物种间摄食、栖息地利用和营养生态位的变化具有重要的指示作用。本研究以在大西洋热带海域兼捕的大青鲨、长鳍鲭鲨、拟锥齿鲨和尖吻鲭鲨为对象,通过测定其肌肉、肝脏和血液的δ¹³C和δ¹⁵N值,探讨4种鲨鱼营养生态位分化。结果表明: 与长鳍鲭鲨相比,尖吻鲭鲨、拟锥齿鲨和大青鲨的δ¹⁵N值相似且相对较高;大青鲨与其他鲨鱼存在摄食隔离,表现出独特的营养生态位;尖吻鲭鲨营养生态位宽幅最大,摄食食物种类和(或)栖息环境类型更多样化,其与拟锥齿鲨的营养生态位重叠度最高,说明两种鲨鱼具有潜在的资源竞争关系。尖吻鲭鲨、拟锥齿鲨和大青鲨组织间的δ¹³C、δ¹⁵N差值与其叉长均无显著相关关系,说明3种鲨鱼近期内无明显摄食变化;而长鳍鲭鲨的肝脏、血液和肌肉组织的δ¹⁵N差值与叉长显著相关,说明长鳍鲭鲨在短期内存在摄食变化。肝脏和血液的δ¹³C、δ¹⁵N值的相似性反映了两种组织整合摄食时间周期相近,其较高的代谢速率可以反映相对短时间周期的摄食信息。     

The Role of Sharks and Longline Fisheries in a Pelagic Ecosystem of the Central Pacific

The increased exploitation of pelagic sharks by longline fisheries raised questions about changes in the food webs that include sharks as apex predators. We used a version of Ecopath/Ecosim models to evaluate changes in trophic interactions due to shark exploitation in the Central North Pacific. Fisheries targeted on blue sharks tend to produce compensatory responses that favor other shark species and billfishes, but they have only modest effects on the majority of food web components. Modest levels of intraguild predation (adult sharks that eat juvenile sharks) produce strong, nonlinear responses in shark populations. In general, analysis of the Central North Pacific model reveals that sharks are not keystone predators, but that increases in longline fisheries can have profound effects on the food webs that support sharks. Received 19 April 2001; accepted 2 October 2001.     

New insights on the trophic ecology of blue (Prionace glauca) and shortfin mako sharks (Isurus oxyrinchus) from the oceanic eastern South Pacific

The blue shark (Prionace glauca) and the shortfin mako shark (Isurus oxyrinchus) are two large and highly migratory sharks distributed in most oceans. Although they are often caught in the south Pacific Ocean long-line fisheries, their trophic ecology is poorly understood. Stable isotopes with Bayesian mixing and dependence concentration models were performed to determine the diet and trophic differences between the two species in the South-eastern Pacific Ocean. According to the mixing models, fishes are the most important prey of these sharks. Dolphin calves and remains were found in the stomachs of both species, which represents a novel finding in trophic ecology of South Pacific sharks. Intra-specific differences were found in P. glauca, but not in specimens of I. oxyrinchus. The two sharks showed a high degree of diet overlap (73%), primarily over mackerel and dolphin carcasses. Our results indicate that blue and shortfin mako sharks have a generalist feeding strategy in the eastern Pacific Ocean, with a strong preference for teleost fishes and also for dolphin carcasses. Therefore, trophic studies are useful to understand energy flow through the food web, and the trophic position of key species.     

Establishment of trophic continuum in the food web of the Yellow Sea and East China Sea ecosystem: Insight from carbon and nitrogen stable isotopes

The determination of trophic level for the biology in a marine ecosystem is very important as alteration of its structure and function may be reflected in the tro-phic level of component species. A change in trophic level indicates variation in an organism’s feeding bi-ology or in the pathway of energy flow from primary producers to the consumer. The gut content analysis is a traditional method for studying trophodynamics of food web in marine ecosystems. Species composition and amounts in al…     

Trophic complexity of small fish in nearshore food webs

Small nearshore fishes are an important part of lacustrine and functional diversity and link pelagic and benthic habitats by serving as prey for larger nearshore and offshore fishes. However, the trophic complexity of these small nearshore fishes is often unrecognized and detailed studies of their role in food webs are lacking. Here, we examined niche space patterns of small nearshore fish species using Bayesian analyses of carbon and nitrogen stable isotope data in nine freshwater lakes that are among the largest lakes in Minnesota. We found considerable variability in niche areas within species and high variability in niche overlap across species. At the assemblage level, niche overlap (average diet overlap of all species pairs at a lake) decreased as whole-lake species richness increased, possibly indicating a greater degree of resource specialization in more speciose lakes. Overall fish niche space was weakly but significantly related to niche space of their invertebrate prey. Although nearshore benthic resources contributed to fish diets in all lakes, all fish species also had non-negligible and variable contributions from pelagic zooplankton. This inter- and intraspecific variability in trophic niche space likely contributes to the multi-level trophic complexity, functional diversity, and potentially food web resilience to ecosystem changes.

     

Establishment of trophic continuum in the food web of the Yellow Sea and East China Sea ecosystem: Insight from carbon and nitrogen stable isotopes

Stable carbon and nitrogen isotope ratios (δ¹³C and δ¹⁵N) are used to study the trophic structure of food web in the Yellow Sea and East China Sea ecosystem. The trophic continuum of pelagic food web from phytoplankton to top preyer was elementarily established, and a trophic structure diagram in the Yellow Sea and East China Sea was outlined in combination with carbon isotopic data of benthic organisms, which is basically consistent with and makes some improvements on the simplified Yellow Sea food web and the trophic structure diagram drawn based on the biomass of main resource population during 1985–1986. This result indicates that the stable isotope method is a potential useful means for further studying the complete marine food web trophic continuum from viruses to top predators and food web stability.     

Diet,trophic interactions and possible ecological role of commercial sharks and batoids in northern Peruvian waters

The Peruvian sea represents one of the most productive ocean ecosystems and possesses one of the largest elasmobranch fisheries in the Pacific Ocean. Ecosystem-based management of these fisheries will require information on the trophic ecology of elasmobranchs. This study aimed to understand the diet, trophic interactions and the role of nine commercial elasmobranch species in northern Peru through the analysis of stomach contents. A total of 865 non-empty stomachs were analysed. Off northern Peru, elasmobranchs function as upper-trophic-level species consuming 78 prey items, predominantly teleosts and cephalopods. Two distinctive trophic assemblages were identified: (a) sharks (smooth hammerhead shark Sphyrna zygaena, thresher shark Alopias spp. and blue shark Prionace glauca) that feed mainly on cephalopods in the pelagic ecosystem; and (b) sharks and batoids (Chilean eagle ray Myliobatis chilensis, humpback smooth-hound Mustelus whitneyi, spotted houndshark Triakis maculata, Pacific guitarfish Pseudobatos planiceps, copper shark Carcharhinus brachyurus and school shark Galeorhinus galeus) that feed mainly on teleosts and invertebrates in the benthonic and pelagic coastal ecosystem. This study reveals for the first time the diet of T. maculata and the importance of elasmobranchs as predators of abundant and commercial species (i.e., jumbo squid Dosidicus gigas and Peruvian anchovy Engraulis ringens). The results of this study can assist in the design of an ecosystem-based management for the northern Peruvian sea and the conservation of these highly exploited, threatened or poorly understood group of predators in one of the most productive marine ecosystems.     

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.