渔业科学进展  2024, Vol. 45 Issue (3): 46-54  DOI: 10.19663/j.issn2095-9869.20230309002
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引用本文 

孙威, 吴文广, 刘毅, 仲毅, 王新萌, 张继红. 温度、光照强度和光照周期对铜藻有机碳释放速率的影响[J]. 渔业科学进展, 2024, 45(3): 46-54. DOI: 10.19663/j.issn2095-9869.20230309002.
SUN Wei, WU Wenguang, LIU Yi, ZHONG Yi, WANG Xinmeng, ZHANG Jihong. The Effects of Temperature, Light Intensity, and Photoperiod on the Organic Carbon Release Rate of Sargassum horneri Seaweed[J]. Progress in Fishery Sciences, 2024, 45(3): 46-54. DOI: 10.19663/j.issn2095-9869.20230309002.

基金项目

科学技术部重点研发计划(2020YFA0607603)、国家自然科学基金委员会–山东省人民政府联合基金(U1906216)、山东省自然科学基金(ZR2022QD035)和中国水产科学研究院黄海水产研究所基本科研业务费专项(20603022022012; 20603022022024)共同资助

作者简介

孙威,E-mail: sunw4101998@163.com

通讯作者

张继红,研究员,E-mail: zhangjh@ysfri.ac.cn

文章历史

收稿日期:2023-03-09
收修改稿日期:2023-03-27
温度、光照强度和光照周期对铜藻有机碳释放速率的影响
孙威 1,2, 吴文广 2, 刘毅 2, 仲毅 2, 王新萌 2, 张继红 2     
1. 上海海洋大学水产与生命学院 上海 201306;
2. 中国水产科学研究院黄海水产研究所 农业农村部海洋渔业与可持续发展重点实验室 山东 青岛 266071
摘要:为探究铜藻(Sargassum horneri)的有机碳释放速率、与净初级生产力(NPP)之间的关系及主要的调控因素等问题,本研究采用三变量三水平的正交实验,测定铜藻在不同温度(5、15和25℃)、光照[86、172和258 μmol/(m2·s)]和光照周期(L∶D=6 h∶18 h、L∶D=12 h∶12 h、L∶D=24 h∶0 h,L表示光照时长,D表示黑暗时长)条件下溶解有机碳(DOC)、颗粒有机碳(POC)的释放速率和初级生产力。结果显示,DOC和POC释放速率的范围分别为0.653~4.785 mg/(g·h)和0.066~0.322 mg/(g·h);温度和光照强度分别是铜藻释放DOC和POC的主要调控因素;铜藻在高温、中光、L∶D=6 h∶18 h条件下的DOC释放速率最高[4.785 mg/(g·h)],在高温、高光、L∶D=24 h∶0 h条件下的POC释放速率最高[0.322 mg/(g·h)];铜藻释放的DOC和POC占NPP的比值分别为4%~130%和0.4%~5.9%;DOC释放速率与NPP之间存在负相关关系,POC释放速率与NPP之间无明显相关性。研究结果为深入了解铜藻的生理生态学特性及其对沿海生态系统碳循环的影响提供了科技支撑。
关键词铜藻    净初级生产力    溶解有机碳    颗粒有机碳    
The Effects of Temperature, Light Intensity, and Photoperiod on the Organic Carbon Release Rate of Sargassum horneri Seaweed
SUN Wei 1,2, WU Wenguang 2, LIU Yi 2, ZHONG Yi 2, WANG Xinmeng 2, ZHANG Jihong 2     
1. School of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai 201306, China;
2. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Marine Fisheries and Sustainable Development, Ministry of Agriculture and Rural Affairs, Qingdao 266071, China
Abstract: The ocean is the largest carbon pool on earth and plays an important role in the global carbon cycle. Marine organisms contribute over half of the global carbon fixed by photosynthesis every year. Therefore, much attention has been paid to the role of the ocean in the carbon cycle and carbon sequestration. Macroalgae are an important component of coastal ecosystems, with strong and highly efficient carbon fixation capacity. The net primary productivity (NPP) of macroalgae was higher than that of phytoplankton and other primary producers in coastal waters. Parts of the photosynthates are released into the sea in the form of dissolved organic carbon (DOC) and particulate organic carbon (POC) during algae growth. Dissolved organic carbon and POC have attracted widespread attention because they can play important roles in carbon cycling and carbon sequestration in coastal ecosystems. However, the organic carbon release rate of macroalgae, its relationship with primary productivity, and the regulatory factors require further study. The growth of algae and the organic carbon release are influenced by temperature, light intensity, photoperiod, and other factors. However, organic carbon release rates among algae species might be quite different. Therefore, studying the regulatory effects of different factors on organic carbon release by algae and organic carbon release rate distribution has important implications for quantitatively evaluating the organic carbon release ability of algae and its contribution to the coastal ecosystem carbon cycle.In recent years, Sargassum horneri is the most common wild macroalgae in the Yellow Sea. Its ecological role in the coastal ecosystem has attracted widespread attention. Few studies have focused on organic carbon release by S. horneri. This study conducted an orthogonal experiment to measure DOC and POC release rates of S. horneri at different temperatures (5, 15, and 25 ℃), light intensity [86, 172, and 258 μmol/(m2·s)] and photoperiod (L: D=6 h: 18 h, L: D=12 h: 12 h, L: D=24 h: 0 h, L means light time, D means dark time) to study the organic carbon release rate of S. horneri, its relationship with NPP, and the main regulatory factors. The release rates of DOC were 0.653–4.785 mg/(g·h) and the release rates of POC were 0.066–0.322 mg/(g·h). There is an order of magnitude difference between DOC and POC. This indicated that DOC was the main form of organic carbon released by S. horneri. The highest DOC release rate [4.785 mg/(g·h)] occurred at 25 ℃, 172 μmol/(m2·s) light intensity, and L: D = 6 h: 18 h. The highest POC release rate [0.322 mg/(g·h)] occurred at 25 ℃, 258 μmol/(m2·s) light intensity, and L: D = 24 h: 0 h. The organic carbon release ability of S. horneri is consistent with previous studies of other macroalgae.This study found that changes in temperature and light conditions significantly affect the ability of S. horneri to release organic carbon. Temperature was the main factor affecting the release rate of DOC; the DOC release rate increases with increasing temperature. The DOC release rate initially increases, then decreases with increasing light intensity; it increases with a decrease in the photoperiod. Light intensity was the main factor influencing the POC release rate; increasing light intensity and photoperiod accelerated the POC release rate. However, the POC release rate slightly decreased when the light intensity increased from 172 to 258 μmol/(m2·s). There was a greater POC release rate under extreme temperature stress (5 and 25 ℃).This study showed that a proportion of DOC and POC in NPP were unstable in macroalgae. The range of DOC/NPP was 4%–130%. POC/NPP was relatively concentrated to approximately 0.4%–5.9%. The NPP was significantly lower in the experimental group with a high ratio of organic carbon compared with other experimental groups. The DOC release rate negatively correlated with NPP, but the negative correlation was poor in the low temperature groups. There was no significant correlation between the POC release rate and NPP. POC/NPP was relatively stable [approximately (1±0.6)% when NPP>9 mg C/(g·h)]. The growth pressure of S. horneri was high when NPP<4 mg C/(g·h), and the regulatory effect of organic carbon was manifested as the release under environmental stress, with POC/NPP increasing to 4%–6%. This section was modified for clarity. Please check that your meaning was retained. This study provides scientific and technological support for an in-depth understanding of the contribution by macroalgae to the coastal ecosystem carbon cycle.
Key words: Sargassum horneri    Net primary productivity    Dissolved organic carbon    Particulate organic carbon    

大型藻类能够以有机碳的形式释放光合作用产物,其中,能通过0.7 μm孔径滤膜过滤的部分被定义为溶解有机碳(dissolved organic carbon, DOC),滤膜截留部分则称之为颗粒有机碳(particulate organic carbon, POC) (Baines et al, 1991; Pagano et al, 2014)。大型海藻是沿海生态系统的重要组成部分,其固碳能力强、效率高,作为沿海地区的主要初级生产者,其净初级生产力(net primary productivity, NPP)大于浮游植物等其他生产者(Charpy-Roubaud et al, 1990; Krause-Jensen et al, 2016)。海藻生长过程中释放的DOC和POC能在沿海生态系统的碳循环和碳封存中发挥重要作用(Jiao et al, 2010; 张永雨等, 2017; Weigel et al, 2021)。温度、光照强度和光照周期是影响藻类生长、调控有机碳释放的重要环境因素(Wada et al, 2007; Reed et al, 2015; 李科等, 2017)。关于大型海藻释放有机碳的结果差异较大。已有报道显示,苷苔(Ecklonia cava) DOC释放速率范围为0.05~0.24 mg/(g·h) (Wada et al, 2007);坛紫菜(Pyropia haitanensis) DOC释放速率范围为0~1.67 mg/(g·h),POC的释放速率低于0.005 mg/(g·h) (Xu et al, 2022);角叉菜(Chondrus ocellatus)和亨氏马尾藻(Sargassum henslowianum)等11种大型海藻的DOC释放速率为0~7 mg C/(g·h),POC释放速率为0~17 mg C/(g·h) (Chen et al, 2020)。同一种海藻,因产地来源不同,其有机碳的释放速率也有差异,最高可相差约10倍(Chen et al, 2020)。不同种类海藻释放的DOC与NPP之间的比例也不相同,如坛紫菜释放的DOC仅占NPP的6.3%~25.7% (Xu et al, 2022),苷苔则为18%~62% (Wada et al, 2007),鼠尾藻(Sargassum thunbergii)经干燥胁迫,再复水后,DOC的释放速率要高于NPP (Zhao et al, 2022)。

近年在黄海海域暴发的以铜藻(Sargassum horneri)为主要致灾种的马尾藻金潮引起了广泛关注(郑龙啸等, 2022)。金潮暴发越来越频繁,影响范围越来越广,已经成为继浒苔(Enteromorpha)绿潮之后的又一近海大型海藻灾害(Caselle et al, 2018; 王丹等, 2021)。铜藻在生长时能释放大量的DOC和POC,这些DOC和POC可能对沿海生态系统的碳循环产生较大的影响(张永雨等, 2017)。目前,大型海藻有机碳的释放速率、与初级生产力之间的关系及主要调控因素等问题尚不完全清楚,尤其是缺少关于铜藻释放有机碳的研究。因此,本研究以野生铜藻为对象,通过室内正交实验,探究温度、光照和光照周期对铜藻释放有机碳的影响,以期了解不同因素对铜藻释放有机碳的调控效应、有机碳的释放速率、有机碳释放速率与初级生产力之间的关系等问题,为深入了解铜藻的生理生态学特性及其对沿海生态系统碳循环的影响提供科技支撑。

1 材料与方法 1.1 实验材料与预处理

实验铜藻于2021年底取自山东省荣成市桑沟湾养殖区。铜藻在取样后冷藏运输至实验室,在循环水养殖系统中暂养3 d后,用于实验,暂养水温设置为20 ℃。用0.8 μm孔径的混合纤维滤膜过滤海水,用于后续实验。实验开始前,采用过滤海水清洗铜藻,去除铜藻表层的附着物。

1.2 实验设计

铜藻生长的适宜温度为7.1~20.5 ℃(孙建璋等, 2009)。光照强度小于200 μmol/(m2·s)时,铜藻NPP与光照强度之间线性关系显著,光照强度大于200 μmol/(m2·s)时,线性关系不显著(刘婷, 2019)。基于此,设置温度和光照水平,具体实验设计见表 1。本实验共设温度、光照强度和光照周期3个变量,每个变量设3个水平,分别为低温(5 ℃)、中温(15 ℃)、高温(25 ℃);低光[86 μmol/(m2·s)]、中光[172μmol/(m2·s)]、高光[258 μmol/(m2·s)];光照周期L∶D=6 h∶18 h、L∶D= 12 h∶12 h、L∶D=24 h∶0 h。实验容器为2 L锥形瓶,加入铜藻(3~5 g/L),实验持续24 h,实验中,光照与黑暗的交替顺序为先黑暗后光照。所有实验组均设3个平行,对照组设2个平行。

表 1 L9(34)正交实验设计表 Tab.1 Orthogonal experimental design of L9(34)

在实验开始(0 h)和结束(24 h)时,分别取200 mL水样用于DOC和POC浓度分析,取样前,采用Winkler碘量法测量水体的溶解氧(DO)浓度。水样经0.7 μm孔径WhatmanTM滤膜(450 ℃预处理4 h)过滤后,滤液分装在30 mL棕色玻璃瓶内,用于DOC浓度分析;滤膜用锡纸包裹,用于POC浓度分析。所有样品在分析前均于–20 ℃避光冷冻保存。所有实验用玻璃器皿使用前均酸洗、水洗、纯水润洗、烘干。

1.3 样品分析

DOC测定:使用日本岛津TOC-LCSH总有机碳分析仪测定样品的DOC含量。POC测定:使用德国ELEMENTAR元素分析仪测定样品的POC含量。

1.4 计算方法与数据处理

通过实验前后水体DO浓度的变化来计算铜藻的NPP,计算公式为:

$ {\text{NPP}} = \frac{{\Delta {\text{O}}2}}{{W \times t}} \times \frac{{12}}{{32}} $

式中,NPP为铜藻干质量的净初级生产力[mg C/(g·h)],ΔO2为实验前后水体DO的质量变化,12/32为C与O2的相对分子质量比,W为实验铜藻的干重(g);t为实验时长(h)。

有机碳(DOC、POC)释放速率(rate, R)指单位质量铜藻(干重)在单位时间内引起的水体有机碳(DOC、POC)含量的变化。

$ R = \frac{{\Delta C \times V}}{{W \times t}} \times \frac{{12}}{{32}} $

式中,R为单位质量铜藻(干重)的DOC (POC)释放速率[mg/(g·h)],ΔC为实验前后DOC (POC)浓度变化量(mg/L);V为实验组海水体积(L);W为实验铜藻的干重(g);t为实验时长(h)。

直观分析法是通过对每个因素均值的极差来进行结果分析(滕海英等, 2008)。通过极差可判断影响实验结果的主要因素和次要因素,可通过直观分析表找到各因素水平的最优组合。直观分析表中的$ {\bar K_1} $$ {\bar K_2} $$ {\bar K_3} $分别表示在各因素、各水平下实验结果(NPP、DOC和POC)的平均值,可据此确定实验结果最大时对应的因素水平。R表示同一因素在不同水平下实验结果平均值的极差,R值可表征该因素水平的变动对实验结果影响的大小。

2 实验结果 2.1 铜藻的净初级生产力(NPP)

铜藻的NPP的实验结果见表 2。不同条件下,铜藻NPP在2.785~21.190 mg C/(g·h)之间。直观分析结果显示,本研究中,温度是NPP的主要影响因素,光照强度对NPP的影响最小。各因素在不同水平下对NPP影响的顺序为15 ℃>25 ℃>5 ℃,24 h∶0 h>12 h∶12 h>6 h∶18 h,高光>中光>低光。由此得出,铜藻NPP最高的条件组合为15 ℃、L∶D=24 h∶0 h、高光。

表 2 净初级生产力结果直观分析及最优条件 Tab.2 Visual analysis of NPP results and optimal conditions
2.2 铜藻释放DOC的实验结果分析 2.2.1 温度、光照强度和光照周期对DOC释放速率的影响

铜藻释放DOC的实验结果见表 3。不同条件下,铜藻DOC的释放速率在0.653~4.785 mg/(g·h)之间。直观分析结果显示,铜藻DOC释放速率最高的条件组合为25 ℃、L∶D=6 h∶18 h、中光。温度、光照强度和光照周期对铜藻DOC释放速率的影响由强到弱依次为温度、光照强度、光照周期。在实验温度范围内,DOC的释放速率随温度的升高而增大;DOC的释放速率随着光照强度的增加表现为先升高再降低的趋势;光照时间越少释放速率就越高。

表 3 DOC结果直观分析及最优条件 Tab.3 Visual analysis of DOC results and optimal conditions
2.2.2 铜藻释放的DOC与NPP之间的关系

DOC/NPP的值见图 1a。实验结果显示,不同条件下,铜藻释放的DOC占NPP的比例为4%~130%。其中,共计5组占比低于10%,3组占比为20%~42%,1组占比超过100% (129.5%)。图 1b显示,DOC释放速率与NPP之间存在负相关关系(实验组1和3不符合此规律)。

图 1 DOC/NPP的值(a)与DOC释放速率随NPP的变化趋势(b) Fig.1 The ratio of DOC/NPP (a) and the trend of DOC release rate with NPP (b)
2.3 铜藻释放POC的实验结果分析 2.3.1 温度、光照强度和光照周期对POC释放速率的影响

铜藻释放POC的实验结果见表 4。不同条件下,铜藻POC的释放速率为0.066~0.322 mg/(g·h)。直观分析结果显示,铜藻POC释放速率最高的条件组合为25℃、L∶D=24 h∶0 h、中光。低温(5 ℃)、高温(25 ℃)、延长光照时长都会促进POC的释放。增加光照强度可以加快POC释放速率,但当光照强度从中光增至高光时,POC释放速率反而有小幅度下降。

表 4 POC结果直观分析及最优条件 Tab.4 Visual analysis of POC results and optimal conditions
2.3.2 铜藻释放的POC与NPP之间的关系

POC/NPP的值见图 2。实验结果显示,不同条件下,铜藻释放的POC占NPP的比例为0.4%~5.9%。其中,共计6组占比低于2%,3组占比为4%~5.9%。

图 2 POC占NPP的比例 Fig.2 The ratio of POC to NPP
3 讨论 3.1 DOC和POC的释放速率

本研究发现,室内实验中的DOC和POC释放速率分别在0.653~4.785 mg/(g·h)和0.066~0.322 mg/(g·h)之间。铜藻的DOC释放速率与之前报道的其他马尾藻的DOC释放速率相近(Chen et al, 2020),并高于绿藻、红藻和其他褐藻等大型藻类的DOC释放速率(Paine et al, 2021)。铜藻DOC/NPP在4%~42%之间(实验组9除外),其DOC的释放能力基本符合以往研究中人们对大型藻类的认识(Wada et al, 2007; Watanabe et al, 2020; Xu et al, 2022)。该结果能为精确评估铜藻在不同环境、不同生长时期的有机碳释放通量提供科技支撑。

3.2 温度、光照强度和光照周期对DOC和POC释放速率的影响

本研究表明,温度会显著影响铜藻释放DOC和POC的能力,温度与铜藻DOC释放速率之间正相关,与POC释放速率之间表现为胁迫释放。以往对苷苔的研究支持这一结果,即当温度适合苷苔生长时,其DOC的释放量增加、POC释放量减少(Wada et al, 2007)。Barrón等(2014)在对海草甸的研究中也有温度与DOC释放速率正相关相似发现。

以往的研究显示,海带(Saccharina japonica)和坛紫菜等大型海藻的DOC释放速率与光照强度正相关(尼志杰等, 2022; Xu et al, 2022)。然而,本研究中,铜藻释放DOC的速率与光照之间的关系与之前的研究有所差异。对于铜藻来说,光照与DOC释放速率呈正相关可能只存在于某些特定的光照强度区间内,当光照强度超出该区间时,则没有相关性或表现出负相关。因此,可以合理地推断,不同种海藻DOC释放速率对光照强度变化的响应程度不同。由于本研究中光照强度水平设置较少,无法准确判断该推论是否成立,故还需通过开展多光照强度梯度的单因素实验去进一步论证。另外,在针对光照周期的研究中发现,一个光照周期中,黑暗时间越长,DOC释放速率越高。之前的研究表明,环境压力(低pH、低营养盐、缺水、高温和强光等)是海藻释放DOC的驱动因素,海藻在生长过程中面临环境压力时,会出现细胞膜损伤、渗透压升高甚至组织腐烂等情况,细胞膜损伤会引起细胞内容物的大量泄漏(Thornton et al, 2014; Zhao et al, 2022; Xu et al, 2022)。当藻类处于低营养盐胁迫时,光合固碳速率大于其他大分子物质的合成速率,过量的光合产物会被主动释放到细胞外(Fogg, 1983)。在本研究中,光照时间作为铜藻的生长要素之一,光照时间越短,为铜藻带来的生长压力越大。因此,光照时间与DOC的释放速率负相关。在黑暗条件下,铜藻的呼吸作用能够同时降低海水的pH和DO。已有研究证实,pH降低能够促进大型藻类释放DOC (Iñiguez et al, 2016; Diaz-Pulido et al, 2020)。然而,并非所有的大型藻类释放DOC都受pH的影响,如Paine等(2021)对边花昆布(Ecklonia radiata)、边缘勒诺曼藻(Lenormandia marginata)和拉绒石菜(Plocamium cirrhosum) 3种大型藻类的研究发现,pH的降低并不会影响其释放DOC的速率。因此,不能排除DO降低影响DOC释放的可能,故还需单独开展实验分别探究降低pH和降低DO对海藻释放DOC的影响。以上结果表明,铜藻释放有机碳的机制复杂,受温度、光照强度和光照周期等多种因素影响。本研究为后续铜藻释放有机碳的研究奠定了基础,也可为其他海藻释放有机碳的研究提供参考。

3.3 DOC和POC释放速率与NPP之间的关系

在DOC释放量与NPP之间的关系的研究中,有人提出“光合产物扩散假说”(Fogg, 1983; Marañón et al, 2005; Weigel et al, 2021),认为DOC释放量与光合作用的固碳量成正比,即DOC释放量占NPP的比值应相对恒定。李科等(2017)研究显示,在1个光照周期内,光照时间越长,铜藻的NPP越高,在L∶D=24 h∶0 h时,NPP最高。为探究铜藻在长光照周期条件下的DOC释放情况,本研究设置了连续光照(L∶D=24 h∶0 h)实验。研究发现,在连续光照条件下,铜藻具有最高的NPP和最低的DOC释放速率,即铜藻释放DOC不符合“光合产物扩散假说”。此外,本研究结果表明,铜藻的DOC释放速率与NPP之间呈负相关关系,但5 ℃实验组中的DOC释放速率与NPP之间的负相关性不显著。这可能是由于铜藻酶活性低、代谢缓慢,细胞膜的通透性并未发生改变或改变幅度较小,从而导致低温条件下,铜藻的DOC释放速率和NPP均处于较低水平,再加上受到其他因素多重胁迫,铜藻的生理状态受到影响,致使细胞膜的通透性发生改变,细胞内容物更容易被释放出来。所以,在低温抑制NPP的条件下,铜藻的DOC释放速率并未得到显著提高。本研究发现,实验组9中DOC/NPP>100%,这一结果可能是由于铜藻面临高温和长时间黑暗双重环境压力时,其生理状态受到严重胁迫,DOC大量释放的同时光合速率远低于适宜条件下的光合速率等因素共同造成的。

本研究发现,铜藻的POC释放速率与NPP之间无显著的相关性,POC/NPP (0.4%~5.9%)与鼠尾藻和坛紫菜相近,低于其他种马尾藻(Chen et al, 2020; Xu et al, 2021)。当NPP相对较高[>9 mg C/(g·h)]时,POC/NPP相对稳定,约为(1±0.6)%;当NPP相对较低[<4 mg C/(g·h)]、处于生长逆境时,POC/NPP则会升高至4%~6%。已有研究发现,POC的释放速率有随生长率增加而增加的趋势,但二者间的相关性较弱(Chen et al, 2020; Xu et al, 2022)。本研究发现,增加光照强度或光照时长都能提高NPP和促进POC的释放,即POC释放速率随光照变化的趋势与NPP随光照变化的趋势基本相同。本研究还发现,铜藻在5 ℃时,NPP最低,25 ℃时,NPP最高,但是铜藻在5 ℃和25 ℃时,POC均有较高的释放速率。低温抑制NPP、促进POC释放的结论已在浮游植物中得到验证(Watanabe, 1980; Verity, 1981)。据此可以合理推测,光照变化是观察到POC释放速率与生长率之间有相关性的主要原因,温度变化则是导致二者间相关性较弱的内在原因。明确DOC/NPP和POC/NPP的范围区间,有助于初步估算金潮发生时,铜藻对沿海生态系统碳循环的贡献。

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