Advances in Marine Sciences
Vol.03 No.03(2016), Article ID:18435,11 pages
10.12677/AMS.2016.33011

Ecology of Mixotrophic Planktonic Flagellate and Ciliate in the Sea

Chaofeng Wang1,2,3, Wuchang Zhang1,2*, Li Zhao1,2, Yuan Zhao1,2, Tian Xiao1,2

1Key Laboratory of Marine Ecology and Environmental Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao Shandong

2Laboratory of Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao Shandong

3University of Chinese Academy of Sciences, Beijing

Received: Aug. 3rd, 2016; accepted: Aug. 26th, 2016; published: Aug. 30th, 2016

Copyright © 2016 by authors and Hans Publishers Inc.

This work is licensed under the Creative Commons Attribution International License (CC BY).

http://creativecommons.org/licenses/by/4.0/

ABSTRACT

Mixotrophic microplankton are those that can carry out photosynthesis and ingestive behavior simultaneously. Mixotrophy makes mixotrophic microzooplankton be producer and consumer. Thus it’s a challenge for traditional phytoplankton-zooplankton dichotomy and the study of ecological model. The distribution of mixotrophic microzooplankton in the sea is the foundation to understand their ecological function. In this study, we summarized the counting method and the result of mixotrophic flagellate and ciliate in the sea in previous studies. For mixotrophic flagellate, its percentage of abundance in flagellate with plastid in different sea regions was mostly less than 50%. Taxonomically, more than ten mixotrophic ciliates species were identified up to now. As the most easily identified mixotrophic ciliates, Laboea strobila mainly appeared in temperate zone and polar sea region. Percentage of mixotrophic ciliates abundance and biomass in different sea regions was mostly less than 70%. Overall, the research about taxonomy and ecology of mixotrophic flagellate and ciliate in natural sea region was scarcely carried out. In China the knowledge gap of mixotrophic microzooplankton has been indentified and is being focused on in some related research.

Keywords:Mixotrophy, Ciliate, Flagellate, Microzooplankton

自然海区混合营养浮游鞭毛虫和纤毛虫生态学

王超锋1,2,3,张武昌1,2 *,赵丽1,2,赵苑1,2,肖天1,2

1中国科学院海洋研究所海洋生态与环境重点实验室,山东 青岛

2青岛海洋科学与技术国家实验室海洋生态与环境科学功能实验室,山东 青岛

3中国科学院大学,北京

收稿日期:2016年8月3日;录用日期:2016年8月26日;发布日期:2016年8月30日

摘 要

海洋浮游生物的混合营养是指一种生物既能进行光合自养,又能进行摄食营养。混合营养使得这种生物既是生产者,又是消费者,因此对传统的食物链和生态模型研究是个挑战。混合营养的海洋浮游生物在自然海区的分布是理解它们在自然海区生态功能的基础,本文综述了自然海区混合营养浮游生物的重要类群--鞭毛虫和纤毛虫的计数方法和结果。混合营养鞭毛虫在不同海区占含色素鞭毛虫的比例多小于50%。混合营养寡毛类纤毛虫的种类大约十余种,其中球果螺体虫(Laboea strobila)是混合营养纤毛虫的重要类群,多分布在温带和极地海区;不同海区混合营养纤毛虫丰度和生物量所占比例多低于70%。总体来看,混合营养型海洋浮游生物生态特征在自然海区的研究较少,我国在这方面的研究才刚起步。

关键词 :混合营养,鞭毛虫,纤毛虫,微型浮游动物

1. 引言

海洋浮游生物被分为浮游植物和浮游动物,在经典的生物营养模式分类中,浮游植物是自养生物,利用阳光合成有机物、固定能量;浮游动物是异养生物,利用浮游植物合成的有机物。但是人们很早就意识到海洋中的原生生物(protist)在同一个体中同时存在自养和异养两种营养方式,这种模式被称为混合营养(mixotrophy)。异养的方式有两种,一种是渗透营养(osmotrophy),一种是吞噬营养(phagotrophy)。广义的混合营养中所指的异养方式可以是其中的任何一种,根据这个定义,几乎所有的浮游植物都是混合营养者,因为它们都可以通过渗透营养吸收溶解有机物分子 [1] [2] 。吞噬营养方式意味着饵料生物的死亡,是生物之间营养关系的具体体现。Flynn等(2013)建议用自养和吞噬营养共同存在于一种生物的营养方式来定义混合营养,本文即采取这个定义 [3] 。

在自然海区浮游生物里的混合营养生物主要是鞭毛虫和纤毛虫。鞭毛虫最初被认为是自养的,但是后来发现可以进行异养营养;纤毛虫最初被认为是异养的,后来发现某些种类可以行光合自养营养。Stoecker (1998)将混合营养分成三种类型,I,“理想的混合营养”,即自养和异养的贡献一样多,在自然界中这一类型非常罕见,II,以自养为主的藻类,III,以异养为主的原生动物 [4] 。Caron (2000)则仅分为后两类,并且认为藻类中的混合营养者是具叶绿体的原生生物,其在后来获得吞噬营养的能力,是像动物的植物,这些类群主要有混合营养的鞭毛虫和甲藻;而原生动物中的混合营养者是异养的原生动物摄食藻类细胞后,保留了其叶绿体,并使得叶绿体在一段时间内参与光合作用,因此是像植物的动物,这些类群主要有浮游纤毛虫 [5] 。甲藻是浮游植物的重要类群,其混合营养在浮游植物研究中有广泛的开展。混合营养鞭毛虫和纤毛虫的研究则落后很多,在自然海区的丰度和分布情况还没有充分的研究。本文只介绍鞭毛虫和纤毛虫的混合营养,重点介绍自然海区混合营养鞭毛虫、纤毛虫分别在总鞭毛虫和总纤毛虫丰度和生物量中的比例,以期为我国的同类研究提供参考。

2. 混合营养鞭毛虫

2.1. 发现混合营养鞭毛虫的历史

在1950年代,人们就意识到了藻类的异养营养方式。一些海洋浮游植物在无菌培养(没有其他生物)时,仅靠无机营养盐不能培养成功 [5] 。这些浮游植物能合成大部分有机物质,但是需要其他生物(通常是细菌)的存在才能生长。细菌为藻类提供了生长因子(维生素、特殊脂肪),而藻类可能为细菌制造有机质从而作为生长的基质。在后来的藻类无菌培养液中加入有机质后,很多藻类的无菌培养获得成功 [5] 。但是这一时期,人们认为藻类摄入有机营养的方式为胞饮作用。现在已经知道,许多藻类也能进行吞噬摄食 [5] 。

在海洋微食物环概念提出以前,就有含色素的鞭毛虫体内有外来颗粒的报道 [6] ,这些结果都是在研究其他内容时的偶然发现(incidental)。最早是Kofoid和Swezy (1921)发现一些藻类中含有食物泡 [7] ,其他的学者在自养鞭毛虫体内发现有机颗粒,但并不说明吞噬异养,也有可能是共生或寄生。因此这些结果只是疑似吞噬异养,并不是其直接的证据 [8] 。微食物环概念首次提出细菌可被异养鞭毛虫摄食,最初关注的是异养鞭毛虫的摄食 [9] - [11] 。自从微食物环概念提出之后,人们开始认真审视含色素鞭毛虫对细菌的摄食。Porter (1988)将这一时期对含色素鞭毛虫混合营养的研究称为再发现(rediscover) [8] 。

首先就是要确认含色素鞭毛虫能摄食细菌,进行异养营养。尽管没有切实的证据,Porter等(1985)将含色素鞭毛虫列入到细菌的摄食者中:“含色素鞭毛虫和无色素鞭毛虫分类学上的亲缘关系很近,因此结构也很相似,故含色素鞭毛虫可能和它的异养亲缘类群一样通过利用颗粒状的饵料进行异养” [12] 。Fenchel (1982)报道一个体内有小的不活动的叶绿体的鞭毛虫摄食细菌 [9] 。Bird和Kalff (1986)在实验室内用荧光微球投喂含色素的chrysophytes,用荧光显微镜观察生物体内有没有荧光微球,发现有摄食行为 [13] 。Estep等(1986)用从马尾藻海分离的14种含色素的chrysomonad进行克隆培养,在实验室中将其放入米粒培养的细菌溶液中,发现它们和在藻类培养液中生长一样好,电镜观察表明它们确实摄食了细菌 [14] 。从此含色素鞭毛虫能够摄食细菌被证实。

2.2. 混合营养鞭毛虫所占丰度和生物量的比例

第二个关注的内容是混合营养鞭毛虫占自养鞭毛虫的比例。最初计数鞭毛虫都是用光学显微镜和电镜,含色素鞭毛虫和异养鞭毛虫区分不明显,研究者大多将所有的鞭毛虫都归为自养 [15] - [19] 。上世纪80年代,人们开始探寻更好的鉴别和计数含色素鞭毛虫的方法。Davis和Sieburth (1982)首先使用荧光显微镜方法,先在紫外光激发光下找到鞭毛虫,再切换到蓝光激发光下确认鞭毛虫有无红色自发荧光以区分自然海区含色素鞭毛虫(有红色自发荧光)和异养的鞭毛虫 [20] ,对自然海区含色素鞭毛虫的鉴别和计数工作从此开展起来。Davis和Sieburth (1984)通过将研究样品先用表面荧光显微镜检查鉴别自养异养,再用电镜检查可自养种的形态,从而区分其中的纯自养鞭毛虫和含色素鞭毛虫 [11] 。

含色素的鞭毛虫并不一定摄食饵料行异养营养,因此含色素的鞭毛虫并不都是混合营养鞭毛虫,只有那些摄食饵料的含色素鞭毛虫才是混合营养鞭毛虫。Arenovski等(1995)是第一个估计混合营养鞭毛虫丰度的学者 [21] ,先通过表面荧光显微镜检查含色素鞭毛虫和异养鞭毛虫的丰度,再通过添加人工饵料培养实验,确定摄食饵料的含色素鞭毛虫在含色素鞭毛虫丰度中的比例,从而估计混合营养鞭毛虫在含色素鞭毛虫中的比例。目前用这种方法进行的研究较少(表1),混合营养鞭毛虫丰度占自养鞭毛虫丰度的比

Table 1. Percentage of mixtrophic flagellates in flagellates with pigment

表1. 混和营养鞭毛虫占含色素鞭毛虫的比例

例最大为50%。这个比例随水深增加而减少,例如在马尾藻海,表层混合营养鞭毛虫丰度占自养鞭毛虫的比例为50%,在叶绿素最大层只有不到0.5% [27] 。

3. 混合营养纤毛虫

有关混合营养的无壳纤毛虫的研究历史较短,海洋浮游无壳纤毛虫最初是被认为异养的,但是后来发现某些种类细胞内含有叶绿体和眼点。Norris (1967)在印度洋78 m水深处采得的一个纤毛虫体内排列有金黄色的物体,他怀疑这是某种金藻(Chrysophyceae)的叶绿体,而不是整个藻体 [30] 。Blackbourn等 (1973)用电镜观察纤毛虫的细胞切片,发现了完整的藻类叶绿体,从而确认浮游纤毛虫体内确实有来自藻类的叶绿体 [31] 。Laval-Peuto和Febvre (1986)用透射电镜在附属曳尾虫(Tontonia appendiculariformis)中发现了数百种质体,并由此推断这种纤毛虫是营混合营养的 [32] 。McManus和Fuhrman (1986)分析了球果螺体虫(Laboea strobila)的色素组成包括叶绿素和藻红蛋白(phycoerythrin) [33] 。Jonsson (1987)和Stoecker等(1987)则测定了寡毛类纤毛虫对无机碳的吸收 [34] [35] 。Stoecker等(1987)和Laval-Peuto和Rassoulzadegan (1988)用表面荧光显微镜方法确定纤毛虫是否含有外来色素体 [35] [36] 。纤毛虫体内的色素体有的是单独的色素体,有的是处于食物泡中,Laval-Peuto和Rassoulzadegan (1988)推测这些纤毛虫可能通过摄食行为获得这些色素体(混合营养),但是并不确定,为谨慎起见,他们建议将这些纤毛虫统称为含有质体的纤毛虫(plastidic ciliates) [36] ,在以后的研究中,有的沿用这一称呼 [37] - [42] ,有的则称为混合营养纤毛虫(mixotrophic ciliates)。Stoecker等(1994, 1996)则把含叶绿体的纤毛虫等同于混合营养纤毛虫 [40] [41] 。

此处的关键问题是一些异养的纤毛虫体内也含有还没有充分消化的色素体,区分这种情况和混合营养的纤毛虫成为难题。Stoecker等(1987)和Laval-Peuto和Rassoulzadegan (1988)认为严格自养的纤毛虫摄食浮游植物后,在浮游植物被破坏之前,体内也会有未降解的植物色素,会对结果有影响 [35] [36] 。纤毛虫获取的叶绿体通常排列在细胞周边的表膜下 [43] ,Modigh (2001)把叶绿体遍布纤毛虫细胞的个体视作混合营养 [42] 。

3.1. 混合营养纤毛虫类群

中缢虫是研究最多的混合营养纤毛虫,其形态很容易辨认,本文仅对形态复杂的寡毛类混合营养纤毛虫进行论述。目前已确认的混合营养寡毛类纤毛虫种类有13种(表2),其中螺体虫属(Laboea)仅有球果螺体虫一种,曳尾虫属(Tontonia)有2种,急游虫属(Strombidium)有6种,而欧米虫属(Omegastrombidium)、拟曳尾虫(Paratontonia)、伪曳尾虫属(Pseudotontonia)及拟盗虫属(Strombidinopsis)均仅有1种。在个体形态方面,由于球果螺体虫(呈锥形,有4~5圈螺纹) (图1(a))、曳尾虫属个体较大(图1(b)),且具有突出的尾部,形态容易辨认,通过光学显微镜下镜检进行计数研究 [46] - [48] 。

Table 2. Species of mixtrophic ciliates

表2. 混合营养纤毛虫种类

(a)(b)

Figure 1. Photomicrographs of Laboea strobila (a) and Paratontonia sp. (b) fixed with Lugol iodine solution (optical microscopy). Scale bar means 20 μm

图1. Lugol试剂固定后的(a)球果螺体虫(Laboea strobila)和(b)曳尾虫属(Paratontonia sp.)图片(光学显微镜拍摄),比例尺20 μm

3.2. 混合营养纤毛虫的计数方法

对自然海区中自养、混养和异养纤毛虫的丰度的调查起始于Stoecker等(1989) [38] 。不同研究学者采用的计数方法不同。

方法一:荧光显微镜观察计数。用倒置荧光显微镜观察,叶绿体在蓝光下有红色荧光,从而区分有叶绿体的纤毛虫和不具叶绿体(严格异养)的纤毛虫。制备显微镜观察样品的方法有:1) 用100 g l−1的hexamethylenetetramine缓冲成20%甲醛(formaldehyde)试剂25 ml,加入225 ml海水样品,最终成为终浓度2%的甲醛固定海水。放入黑暗中4℃保存,5周内分析完毕。如果纤毛虫在水体中丰度较低,就需要浓缩,可以2) 把自然海水中的纤毛虫用10 μm筛绢逆向过滤(reverse filtration technique)的方法浓缩500倍,用borax-buffered甲醛试剂(终浓度为3%)固定。这些样品的100 ml分样放入沉降杯,用倒置荧光显微镜检查计数 [49] [50] 。也可以3)将采集的样品过滤到黑膜上,DAPI染色后在荧光显微镜下镜检 [37] 。镜检时,每个样品检查约30个个体 [51] 。

值得一提的是,严格异养的纤毛虫摄食浮游植物后,在浮游植物被破坏之前,体内也会有未降解的植物色素,会对结果有影响 [38] [44] 。Modigh (2001)把叶绿体遍布纤毛虫细胞的个体视作混合营养 [42] 。

方法二:光学显微镜计数,通过形态判断混合营养纤毛虫。由于螺体虫和曳尾虫个体较大,形态容易辨认,所以Dolan等(1991, 1995, 1999)将它们作为混合营养纤毛虫的代表,通过Lugol试剂固定样品后在光学显微镜下镜检,而其他混合营养纤毛虫(如急游虫属种类)通常个体较小,不作为混合营养纤毛虫来计数 [46] - [48] 。

3.3. 混合营养纤毛虫所占丰度和生物量的比例

混合营养纤毛虫在不同研究海区所占丰度和生物量的比例不同(表3),不同学者对混合营养纤毛虫的鉴定及计数方式有些差异,如Stoecker等(1987)对所有有机质体进行计数 [35] ,而Martin和Montagnes (1993)则认为螺体虫属、曳尾虫属、具甲急游虫等是主要的混合营养纤毛虫 [52] 。混合营养纤毛虫在不同海区的丰度和生物量所占比例多低于70%,近岸海区所占比例比大洋海区稍高,在地中海其所占比例可高达93% [48] 。

3.4. 混合营养纤毛虫对叶绿素的贡献

将混合营养纤毛虫分离出来,测定其叶绿素,估计出单个个体平均的叶绿素含量,可结合丰度估计混合营养纤毛虫对叶绿素的贡献 [53] 。在7~8月,在冰岛、格陵兰附件海域和巴伦支海等北方海域(Nordic Seas),单个细胞Strombidium sp. A、Strombidium sp. B、Laboea strobila、Tontonia sp.的叶绿素含量分别为52 pg cell−1、30 pg cell−1、82 pg cell−1、21 pg cell−1,混合营养纤毛虫的叶绿素占总叶绿素的比例小于15%,但在叶绿素浓度低(<0.2 g/L)的站位,混合营养纤毛虫Strombidium sp.自己占的比例就高达24% [53] 。在温带近岸区域,球果螺体虫的叶绿素含量可占到叶绿素浓度的2%~3% [33] 。

3.5. 混合营养纤毛虫代表——球果螺体虫(Laboea strobila)

球果螺体虫是含色素纤毛虫中个体最大的种,体积约为1.1 × 105 μm3 [35] ,固定后体积约为8.1 × 104 μm3 [38] ,它的螺纹使得它很容易分辨。球果螺体虫分布海区为温带和极区。极地海区如加拿大东部北冰洋 [59] 、冰岛和格陵兰岛附近海域 [55] ,温带海区有伍兹霍尔海域 [35] 、美国乔治滩 [38] [43] 、切萨皮克湾 [46] 、新西兰周围海域 [60] 、挪威峡湾 [37] 、地中海沿岸 [42] [48] 等海域。

Stoecker (1989)在地中海研究发现Laboea strobila的最大丰度达到1.7 × 103 ind/L,平均丰度占到含色素纤毛虫的4.7% [38] ;在地中海的Catalan sea最大丰度135 ind/L,最大丰度出现在5 m水层 [45] ;在切

Table 3. Percentage of mixtrophic ciliates in the abundance and biomass of total ciliates in different sea regions

表3. 不同海区混合营养纤毛虫占纤毛虫(无壳和砂壳纤毛虫)丰度和生物量的比例

*占无壳纤毛虫的比例,NBSW:受黑海水团影响的爱琴海北部海区,Nother:不受黑海水团影响的爱琴海北部海区。

萨皮克湾的球果螺体虫最大丰度1800 ind/L,出现在2 m水层 [44] 。球果螺体虫的生物量可占到含色素纤毛虫的46% [35] 。

在垂直分布研究中,Dale (1987)发现球果螺体虫在水深5~10 m之间昼夜迁移 [61] 。Stoecker等(1989)发现球果螺体虫在早上日出前会升到表层,但是在中午表层和10 m (次表层)丰度相当 [38] 。球果螺体虫所处的水层可能与虫体寻找最佳光强进行光合作用有关。在季节分布相关研究中,在一年中球果螺体虫在春季丰度最大,其他季节丰度很低 [42] 。

在对球果螺体虫体内叶绿素含量研究中,McManus和Fuhrman (1986)利用一系列假设,估计球果螺体虫的叶绿素含量为49 pg cell−1 [33] 。叶绿素在每个球果螺体虫体内平均浓度为82 pg cell−1 [53] ,叶绿体在细胞体内有功能,但是不能再生,在球果螺体虫体内大约停留2周 [43] ,所以需要不断获取新叶绿体。Stoecker等(1987)测定的球果螺体虫的叶绿素含量为187 pg cell−1 [35] 。实验室培养的球果螺体虫的叶绿素含量在100~500 pg cell−1 [38] 。

4. 结语

微食物网中各种生物的摄食营养关系纵横交织,微型浮游生物的混合营养现象使得营养关系更加错综复杂。然而,目前对混合营养的研究还比较缓慢,主要由于1) 长久以来,人们习惯了植物(生产者)动物(摄食者)二分法的观念,需要时间慢慢接受混合营养的生活方式,2) 在生态模型中为混合营养生物找到位置是个挑战,3) 研究方法过于复杂。Flynn等(2013)呼吁科学家要加强对浮游生物混合营养的研究 [62] 。我国的科学家也已开始关注该研究方向 [63] ,戴聪杰等(2005)曾对混合营养型浮游生物生态学进行了综述报道 [64] ,但主要关注于室内研究,本文则强调现场调查。近年来,相关研究在国内相继开展,含色素的鞭毛虫的丰度在部分研究中得以统计,但混合营养鞭毛虫的丰度仍未真正估算;混合营养纤毛虫中也仅有螺体虫的丰度有所报道 [65] 。相信在更多学者的关注下,我国在自然海区微型浮游生物的混合营养研究将迅速开展并取得重要成果。

基金项目

本文得到下列课题资助:国家自然科学基金41576164,中国科学院战略性先导科技专项XDA110302022,973项目2014CB441504。

文章引用

王超锋,张武昌,赵 丽,赵 苑,肖 天. 自然海区混合营养浮游鞭毛虫和纤毛虫生态学
Ecology of Mixotrophic Planktonic Flagellate and Ciliate in the Sea[J]. 海洋科学前沿, 2016, 03(03): 73-83. http://dx.doi.org/10.12677/AMS.2016.33011

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