生态学报  2015, Vol. 35 Issue (24): 7931-7940

文章信息

刘松林, 江志坚, 吴云超, 张景平, 黄小平
LIU Songlin, JIANG Zhijian, WU Yunchao, ZHANG Jingping, HUANG Xiaoping
海草床育幼功能及其机理
Nursery function of seagrass beds and its mechanisms
生态学报, 2015, 35(24): 7931-7940
Acta Ecologica Sinica, 2015, 35(24): 7931-7940
http://dx.doi.org/10.5846/stxb201406181269

文章历史

收稿日期: 2014-06-18
网络出版日期: 2015-05-21
海草床育幼功能及其机理
刘松林1, 2, 3, 江志坚1, 2, 吴云超1, 2, 3, 张景平1, 2, 黄小平1, 2     
1. 中国科学院南海海洋研究所, 中国科学院热带海洋生物资源与生态重点实验室, 广州 510301;
2. 中国科学院南海海洋研究所, 广东省应用海洋生物学重点实验室, 广州 510301;
3. 中国科学院大学, 北京 100049
摘要: 海草床是近岸海域中生产力极高的生态系统,是许多海洋水生动物的重要育幼场所。从生物幼体的密度、生长率、存活率和生境迁移4个方面阐述海草床育幼功能,并从食源和捕食压力两个方面探讨海草床育幼功能机理。许多生物幼体在海草床都呈现出较高的密度、生长率和存活率,并且在个体发育到一定阶段从海草床向成体栖息环境迁移。丰富的食物来源或较低的捕食压力可能是海草床具有育幼功能的主要原因,但不同的生物幼体对海草床的利用有差异,海草床育幼功能的机理在不同环境条件下也存在差异。提出未来海草床育幼功能的重点研究方向:(1)量化海草床对成体栖息环境贡献量;(2)全球气候变化和人类活动对海草床育幼功能的影响;(3)海草床育幼功能对海草床斑块效应和边缘效应的响应,以期为促进我国海草床育幼研究和海草床生态系统保护提供依据。
关键词: 海草床    生物幼体    育幼功能    机理    
Nursery function of seagrass beds and its mechanisms
LIU Songlin1, 2, 3, JIANG Zhijian1, 2, WU Yunchao1, 2, 3, ZHANG Jingping1, 2, HUANG Xiaoping1, 2     
1. Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China;
2. Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China;
3. University of Chinese Academy of Sciences, Beijing 100049, China
Abstract: Seagrass beds cover about 0.15% of the global ocean and contribute 1% of the net primary production of the ocean. They are important nursery habitats for economic fishes and invertebrates such as red drum (Sciaenops ocellatus), Atlantic cod (Gadus morhua), queen conch (Strombus gigas), and blue crab (Callinectes sapidus). The nursery function of seagrass beds has been widely recognized because the biomass and density of juvenile fishes and invertebrates in seagrass beds are higher than in other habitats along the coast. We systematically reviewed the literature on the nursery function of seagrass beds. We evaluated the seagrass nursery function based on the juveniles' density, growth rate, survival rate, and migration to adult habitats. The factors of food availability and predation risk were also summarized to explain the mechanism of nursery function. High density of juvenile organisms was the identifying factor of the nursery function of seagrass beds, and many juveniles in the seagrass beds showed high growth and survival rates, and migrated to adult habitats during juvenile ontogeny. Primarily, abundant food or lower predation pressure seemed to enable the seagrass nursery function. Seagrass leaves, epiphytes, and phytoplankton assemblages, which served as important food sources for many herbivorous juveniles, were abundant in seagrass ecosystems. In addition, some smaller macrofauna such as copepods, amphipods, and polychaetes showed high densities in the seagrass beds. Predator abundance, structural heterogeneity, and turbidity in seagrass beds contributed either directly or indirectly to predation risk. These mechanisms were not mutually exclusive in that high structural complexity in seagrass beds could provide more living space, higher food sources, and a reduction in predation risk for juveniles. However, different juvenile species inhabited the seagrass ecosystems for different purposes, and the mechanisms of seagrass nursery function also varied with different environmental conditions. Finally, future research directions of seagrass nursery function are indicated: (1) to quantify the contribution of migration of individuals from seagrass bed to adult habitats; (2) to clarify the impact of global climate change and human activities on the nursery function of seagrass beds; and (3) to investigate the response of nursery function to the "patch effect" and "edge effect" of seagrass beds. We believe that this study provides scientific perspectives for protecting the seagrass ecosystem in China.
Key words: seagrass bed    juveniles    nursery function    mechanism    

海草床生态系统是近岸海域中生产力极高的生态系统[1],虽然仅占全球海洋面积的0.15%,但却贡献了全球海洋1%的净初级生产力[2]。近年来,海草床的生态功能与经济价值逐渐被人们所认识[3]。研究表明,海草床是许多经济鱼类和无脊椎动物的重要育幼场所,如大西洋鲭鱼(Scomber scombrus)、红鼓鱼(Sciaenops ocellatus)、蚝隆头鱼(Tautoga onitis)、大西洋鳕(Gadus morhua)、女王凤凰螺(Strombus gigas)、青蟹(Carcinus maenas)、蓝蟹(Callinectes sapidus)等[4, 5],而且海草床比沿岸其它生境具有更高水生动物幼体的生物量和密度。因此,海草床的育幼功能得到了广泛的认可[4, 6, 7]

关于育幼功能,Deegan[8]认为是指某些鱼类来到河口产卵孵化生长后离开该区域;而Beck等[6]认为,若单位面积的某一生境区域能够比其它生境吸引更多的某些生物幼体,并能正常生长,就称该区域具有育幼功能;而且相比于其它栖息环境,育幼栖息环境对成体栖息环境要有更大的贡献。生物幼体在育幼栖息环境下的生长,以及育幼环境向成体栖息环境的贡献量是育幼功能的重要特征[9],主要从4个方面进行比较:(1)生物幼体的密度;(2)生物幼体的生长率;(3)生物幼体的存活率;(4)生物向成体生境的迁移运动[6]

国外学者对海草床的育幼功能开展了较多研究,主要涉及海草床与其它生境的育幼功能比较[10, 11, 12],海草床育幼功能的机理分析[13, 14]等方面。前人研究表明,海草床能够为生物幼体提供良好的栖息环境,在海草床分布具有较高的生物幼体密度,并且在促进生物幼体生长率、存活率、提供食物来源和庇护场所等具有重要作用[4, 7]

目前,对海草床生态系统育幼功能的研究主要集中于北美洲和大洋洲地区[4],而在我国未见相关的研究报道。因此,亟待开展对我国海草床育幼功能的研究。本文将对国外关于海草床育幼功能的特征和机理的研究进行回顾和总结,为我国的海草床育幼研究提供借鉴,并为我国的海草床生物资源保护和可持续开发利用提供科学依据。

1 海草床育幼功能的特征

近岸海域的生境类型多样,包括海草床、红树林、珊瑚礁、盐沼等[15]。目前,大多数研究主要通过比较海草床与其它生境生物幼体的密度、生长速率、存活率以及幼体生长后向成体生境的迁移运动,来研究海草床育幼功能的特征[4, 7]

1.1 海草床生物幼体的密度

生物幼体的密度是反映某生境是否具有育幼功能的决定性指标[6]。对于鱼类幼体密度的研究,主要是通过直接拖网调查[16, 17]和可视化调查(浮潜或水肺潜水)[12, 18]。上述两种方法都具有各自的优缺点:拖网捕获方法的优点是能够获得鱼类的样本,而缺点是会低估鱼类的密度和数量[19],并且由于网口大小的原因,可能导致有些个体较小的鱼不能被捕获[16];可视化调查方法的优点是迅速、栖息地不被破坏以及可重复性调查等[19],但其缺点是有些鱼类可能会被调查者所吸引或是惊散,且不同的调查者在估算鱼类数量和密度时会有差异[20, 21]。因此,这两种调查方式会获得差异较大的结果,如Harmelin和Francour[22]在波喜荡草(Posidonia oceanica)海草床利用拖网捕捞和可视化调查方法进行对比研究时,发现拖网能够捕获更多的底栖鱼类,而可视化调查则能够观察到鲷科(Sparids)和隆头鱼科(Labrids)等更多的中层食浮游生物鱼类。

海草床中的不同生物幼体密度与其它邻近的栖息环境相比有着显著的差异。Nagelkerken等[18]在加勒比海博奈尔岛(Bonaire Island)对16种幼鱼进行可视化调查研究,发现黄仿石鲈(Haemulon flavolineatum)、蓝仿石鲈(Haemulon sciurus)、黄尾笛鲷(Ocyurus chrysurus)、小带刺尾鱼(Acanthurus chirurgus)和绿鹦鲷(Sparisoma viride)这5种幼鱼在海草床的密度显著高于邻近红树林及珊瑚礁的密度,其中黄仿石鲈在海草床的密度最大,为115.3 条/1000 m2,表明海草床是这5种幼鱼的重要育幼场所。同样,Aguilar-Perera和Appeldoorn[12]在波多黎各西南部红树林-海草-珊瑚礁相连的栖息环境对20种幼鱼进行可视化调查,发现黄仿石鲈蓝仿石鲈和普氏仿石鲈(Haemulon plumieri)在海草床的密度也显著较高,表明海草床是这3种幼鱼重要的育幼场所。另外,幼鱼在同一海草床不同区域的密度也具有差异。Dorenbosch等[23]在加勒比海阿鲁巴岛(Aruba Island)利用可视化调查方法,研究龟裂泰来藻(Thalassia testudinum)海草床下的幼鱼密度,发现距离珊瑚礁最远的海草床区域有着最高的育幼种幼鱼密度,接近210 条/100 m2,而距离珊瑚礁最近的海草床区域,其育幼种幼鱼密度最小,接近50 条/100 m2

同时,无脊椎动物幼体在海草床的分布也具有一定的变化特征。例如,Heck和Thoman[24]在美国低纬度的约克河(York River)河口和高纬度的派森岛(Parson′s Island)对海草床的蓝蟹进行了为期2a的拖网调查,发现约克河河口海草床蓝蟹幼体的数量比其邻近的无植物裸露区域显著高,并且也比派森岛海草床区域显著高,表明低纬度海草床区域是蓝蟹的重要育幼场所;Murphey和Fonseca[25]在斑块状海草床和连续性海草床对桃红对虾(Penaeus duorarum)进行了为期1a的调查,发现连续性海草床区域桃红对虾的密度显著高于斑块状海草床区域,特别是在夏季7、8月份,连续性海草床区域的桃红对虾密度是斑块状海草床区域的3倍。

1.2 海草床生物幼体的生长率

生物幼体生长率是评判生境育幼功能质量的重要指标[26, 27],主要通过野外围隔实验(Field Enclosure Experiments)[10, 11, 27, 28]或实验室模拟实验[29, 30]来获取。对于鱼类幼体生长率的测定,主要包括体长、体重[10, 27]或耳石日生长量[11]等指标;而对于无脊椎动物幼体,则主要通过测定其生物学指标(壳长和壳宽等)来计算其生长率[28, 29, 30]

许多研究表明,海草床生境下生物幼体的生长率比其它无植被生境下的显著高[10, 11, 14, 29, 30]。例如,Stuns等[11]对红鼓鱼幼体进行了7 d的野外围隔实验研究,发现在莱氏二药藻(Halodule wrightii) 区域红鼓鱼幼体的生长率最高,为0.42 mm/d,在互花米草(Spartina alterniflora)生长的盐沼区域次之,为0.4 mm/d,而在蚝壳礁和无植物覆盖的裸露区域,红鼓鱼幼体生长率分别为0.12 mm/d和0.21 mm/d;Stoner等[30]通过实验室模拟不同栖息环境对女王凤凰螺幼体生长率影响的研究,发现在龟裂泰来藻环境下的生长率最高,为62 μm/d,在蠕形绒枝藻(Dasycladus vermicularis)环境下的生长率次之,为55 μm/d,而在大型藻类、礁石以及海草碎屑环境中的生长率为32—45 μm/d,在拟刚毛藻属(Cladophoropsis spp.)、沙质裸露以及过滤海水环境下的生长率最小,仅7—19 μm/d。然而,Sogard[10]通过野外围隔实验研究,发现美洲拟鲽(Pseudopleuronectes americanus)幼体在大叶藻(Zostera marina)海草床的生长率,与邻近的无植被区域无显著差异。

另外,也有研究发现,生物幼体的生长率还受到海草床生境中温度、溶解氧和沉积物类型等理化因子的影响[10, 27]。例如,美洲拟鲽的生长率与沉积物中砂石的含量呈显著正相关[10]; Phelan等[27]对美洲拟鲽和蚝隆头鱼幼体进行野外围隔实验,发现相对于生境类型,温度和溶解氧这两个环境因子对这两种幼鱼的生长率影响更大。

1.3 海草床生物幼体的存活率

生物幼体的存活率是反映生境是否具有育幼功能的重要指标[18]。对生物幼体存活率的研究主要通过野外束缚实验(Field Tethering Experiments)[31, 32, 33]或实验室模拟[34, 35, 36]进行,并通过计算实验种幼体在单位时间被捕食者的捕食几率来说明其存活率。

大多数研究表明,生物幼体在海草床的存活率显著高于邻近无植物裸露区域[4, 35]。例如,Rooker等[35]以瞬时死亡率[37]为比较参数,在菱体兔牙鲷(Lagodon rhomboides)的捕食作用下,红鼓鱼幼体在无植物的裸露区域的死亡率为0.166—0.189 h-1predater-1(单位时间、单位捕食者的死亡率),而在莱氏二药藻和龟裂泰来藻海草床区域分别为0.047—0.069 h-1predater-1和0.021—0.046 h-1predater-1。同样,生物幼体在海草床和邻近栖息环境的存活率也存在差异[32, 36, 38, 39]。例如,Chittaro等[32]通过90 min的野外束缚实验,研究银仿石鲈(Haemulon chrysargyreum)幼体在不同栖息环境下的存活率,发现在海草床的存活率接近40%,而在珊瑚礁区域仅为15%;Dance等[38]研究发现糙海参(Holothuria scabra)幼体在海草床边缘区域3 d后的存活率为70%,而在珊瑚礁区域,糙海参幼体48 h后全部被捕食。Orth和van Montfrans[36]通过室内模拟蓝蟹在不同栖息环境受底鳉(Fundulus heteroclitus)捕食作用下的存活率,发现在大叶藻栖息环境下,蓝蟹的后期幼体和一龄幼体的存活率分别为44%—57%和87%,而在互花米草栖息环境下的存活率仅分别为18%—19%和43%—48%。然而,Lipcius等[39]在约克河河口研究中发现,蓝蟹幼体在海草床的存活率为20%,在邻近的盐沼区域的存活率却高达80%。

另外,海草床的面积和茎枝密度等也会影响生物幼体的存活率[33, 40]。例如,哈克斯岛(Harkers Island)的蓝蟹存活率和海草床茎枝密度之间就有明显的函数关系,在大斑块海草床(>100 m2)为双曲线关系:Y=X0.14/2.5+ X0.14(r2=0.63,P<0.05),而在小斑块的海草床(1—3 m2)却为线性关系:Y=0.0002X+0.5(r2=0.83,P<0.01)[33]

1.4 海草床生物的迁移运动

生物从幼体栖息环境到成体栖息环境的迁移运动,是评价幼体栖息环境育幼功能的重要指标,也是评价这一生境为该生物幼体育幼场所最直接的检验方式[6, 41]。有些在海草床生存的生物幼体生长后会向成体栖息环境迁移,例如,热带和亚热带海草床中许多珊瑚礁鱼类幼体在海草床生长,而后向珊瑚礁栖息环境迁移[42, 43, 44]。然而,温带海草床生物向成体栖息环境的迁移研究较少[45, 46]

研究鱼类迁移运动的方法主要为调查对比鱼类在各栖息环境下的密度和体长的空间分布规律[18, 44, 47]、食源分析[48, 49]、耳石微化学分析[45, 50]和人工标记[51, 52]等方法。Cocheret de la Morinière等[47]在加勒比海的库拉索岛(Curaao Island)对9种鱼进行体长的空间分布调查,发现小带刺尾鱼、蓝仿石鲈、灰笛鲷(Lutjanus griseus)和八带笛鲷(Lutjanus apodus) 这4种鱼在海草床的平均体长分别为11、11.5、12.6 cm和11.3 cm,而在珊瑚礁区域的平均体长分别为17、21.5、16.6 cm和18.5 cm,两个生境下4种鱼体长分布差异显著,表明这4种鱼的幼体阶段是在海草床生活,随后向珊瑚礁区域迁移运动。Cocheret de la Morinière等[48]和Verweij等[49]通过比较海草床灰笛鲷、八带笛鲷和黄尾笛鲷幼体和珊瑚礁成体这3种鱼肌肉组织的δ13C,发现在珊瑚礁的鱼成体δ13C显著小于海草床的幼体,表明上述鱼类在海草床和珊瑚礁的食物来源存在差异,这3种鱼类幼体阶段在海草床生活,随后向珊瑚礁区域迁移。Gillanders和Kingsford[45]比较温带海草床和岩礁区绿唇蓝鱼(Achoerodus viridis)幼体生长期耳石中微量元素的含量,发现两种栖息环境中绿唇蓝鱼耳石中锰、钡和锶的含量存在显著差异,表明岩礁栖息环境中41%绿唇蓝鱼的幼体阶段在海草床区域。Verweij等[51]通过对海草床中叉长为13.2—21 cm八带笛鲷亚成体进行外部标记,研究其迁移,结果发现叉长为17.8—20 cm的鱼体从海草床迁移到邻近的珊瑚礁区域。

生物个体从海草床育幼环境向成体栖息环境迁移的原因,主要是摄食或躲避捕食的需要[42, 48, 53]。例如,Nakamura等[42]对海草床太平洋黄尾龙占(Lethrinus atkinsoni)幼体的胃含物分析,发现随着体长的增加,其对大型底栖动物,如腹足类、双壳类等的需求显著提高,表明摄食需求是太平洋黄尾龙占从海草床向珊瑚礁区域迁移的主要原因。而Grol等[53]在西班牙湾口区海草床和邻近珊瑚礁生境研究黄仿石鲈的存活率和生长率,发现幼体的存活率分别为24%和0%,差异显著;而随着鱼体的生长存活率分别为56%和77%,珊瑚礁生境下鱼的生长率显著高于海草床的,表明控制其向珊瑚礁生境迁移的主要原因是躲避捕食的需要。

然而,并不是所有生活于海草床的生物幼体都以海草床作为育幼场所,而且不同的生物幼体在海草床的育幼特征也不一样。因此,根据育幼功能指标来确定以海草床作为育幼场所的典型生物幼体见表 1

表1 海草床典型生物幼体 Table 1 Typical juvenile species in seagrass beds
育幼功能 Nursery function代表幼体种类 Typical juvenile species参考文献 References
密度黄仿石鲈Haemulon flavolineatum[12, 18, 54]
Density蓝仿石鲈Haemulon sciurus[12, 18]
普氏仿石鲈Haemulon plumieri[12]
菱体兔牙鲷Lagodon rhomboides[14]
黄尾笛鲷Ocyurus chrysurus[18]
小带刺尾鱼Acanthus chirurgus[18, 55]
绿鹦鲷Sparisoma viridae[18]
蓝蟹Callinectes sapidus[24]
桃红对虾Penaeus duorarum[25]
月尾刺尾鱼Acanthurus bahianus[55]
虹彩鹦嘴鱼Scarus guacamaia[55]
普氏细棘鰕虎鱼Acentrogobius pflaumii[56]
大西洋鳕鱼Gadus morhua[57]
生长率菱体兔牙鲷L. rhomboides[14]
Growth rate蚝隆头鱼Tautoga onitis[10]
红鼓鱼Sciaenops ocellatus[11, 27]
美洲拟鲽Pseudopleuronectes americanus[27]
蓝蟹C. sapidus[29]
女王凤凰螺Strombus gigas[30]
存活率银仿石鲈Haemulon chrysargyreum[32]
Survival rate蓝蟹C. sapidus[29, 33, 36]
红鼓鱼S. ocellatus[35]
糙海参Holothuria scabra[38]
黄仿石鲈H. flavolineatum[58]
迁移运动太平洋黄尾龙占 Lethrinus atkinsoni[44]
Movement桔带裸颊鲷Lethrinus obsoletus[44]
隆背笛鲷Lutjanus gibbus[44]
条斑副绯鲤Parupeneus barberinus[44]
绿蓝唇鱼Achoerodus viridis[45]
无备平鲉Sebastes inermis[46]
小带刺尾鱼A. chirurgus [47]
蓝仿石鲈H. sciurus[47]
八带笛鲷Lutjanus apodus[47, 48, 51]
灰笛鲷Lutjanus griseus[47, 48, 52]
黄尾笛鲷O. chrysurus[49]
黄仿石鲈H. flavolineatum[54]
2 海草床育 幼功能的机理

海草床育幼功能的机理主要有两个方面:(1)食物来源,海草床可以为生物幼体提供丰富的食物;(2)被捕食风险,海草床低密度的捕食者、复杂的环境多相性以及高浑浊度的水环境形成了较小的捕食风险[7, 18, 55]。但这两个方面并不对立,如海草床茎枝密度越大,栖息地结构越复杂,能够为小型生物和附生生物提供更多的栖息环境,降低被捕食几率,也提供了丰富的食物来源[7]。同时,不同的生物幼体对海草床的需求不同,如植食性和营白天觅食的底栖鱼类主要以海草床作为摄食场所,而营夜间觅食的鱼类却主要以海草床作为躲避捕食的栖息场所[55]

2.1 食物来源

海草床不仅为海洋水生动物提供良好的栖息地[59],还为其提供丰富的有机碳食源[60]。例如,海草床中的海草、海草碎屑、海草上的附生藻类或浮游藻类等初级生产者,为许多鱼类和无脊椎动物的幼体提供了丰富的食物[61, 62]。并且在底质环境下,海草床比邻近的珊瑚礁和无植被裸露区域分布有更高密度的桡足类 (Copepoda)、端足目(Amphipoda)、多毛类(Polychaetes),它们是生物幼体重要的食物来源[42, 63]

海草床下的丰富食物来源,可促进生物幼体的生长[10, 11, 14],如红鼓鱼[11]、蓝蟹[29]、女王凤凰螺[30]等生物幼体在海草床都有较高的生长率。相关研究表明,海草床下丰富食物能够吸引生物幼体[13, 55, 56]。例如,Horinouchi 和Sano[56]通过人为改变大叶藻植株密度,发现普氏细棘鰕虎鱼(Acentrogobius pflaumii)幼体的密度甚至在海草被完全移除的区域都比无植物的沙质裸露区域显著高;Verwey等[55]通过人工材料模拟海草结构研究鱼类的行为,发现小带刺尾鱼、月尾刺尾鱼 (Acanthurus bahianus)和虹彩鹦嘴鱼(Scarus guacamaia) 幼体,在有食源供应的海草床数量是无食源供应的海草床的2.4倍。另外,许多营夜间捕食的鱼类昼间以其它栖息环境作为躲避捕食的栖息场所,而夜间则会运动到海草床进行捕食[54, 64, 65],如石鲈科(Haemulidae)和笛鲷科(Lutjanidae)鱼类幼体在夜间从其它栖息环境到海草床摄食异足目(Tanaidacea)和十足目(Decapoda)等底栖生物[64];Verweij等[54]通过研究黄仿石鲈的捕食行为,发现体长为 10—15 cm的亚成体鱼主要栖息于红树林区域,而夜间它们主要在海草床摄食。

2.2 被捕食风险

海草床捕食者的丰度、栖息地环境多相性及水环境的浑浊度是影响被捕食风险大小的重要因素[7]。研究表明,捕食者在海草床的丰度比其它邻近的生境少,生物幼体的存活率相对较高[58, 66]。例如,Dorenbosch等[58]在加勒比海库拉索岛比较海草床、珊瑚礁、红树林等栖息环境下捕食者的密度以及黄仿石鲈幼体的存活率,发现海草床下捕食者的密度和种类丰富度最低,而海草床下黄仿石鲈幼体的存活率最高。迄今为止,大部分研究是关于海草床栖息环境多相性对被捕食风险的影响[67, 68]。栖息环境的多相性能够为生物幼体提供良好的庇护场所[69],许多生物幼体选择海草床作为自己良好的庇护场所,如银仿石鲈[32]、红鼓鱼[35]、糙海参[38]、蓝蟹[36]等幼体在海草床都呈现较高的存活率;同时Gotceitas等[57]通过室内模拟实验比较捕食者的存在与否对大西洋鳕鱼幼体的影响,发现没有捕食者时幼体主要栖息于裸露的砂质环境,而在捕食者出现后幼体主要以海草床为庇护场所,表明海草床能够为幼体提供良好的保护。海草茎枝密度越高,海草床多相性结构越高,生物幼体被捕食的几率越低[70]。如蓝蟹幼体存活率随着海草茎枝密度的增加而上升[33, 40]。同样,在美国德州南部,莱氏二药藻茎枝密度是龟裂泰来藻的8—10倍[71],在莱氏二药藻海草床的红鼓鱼丰度比在龟裂泰来藻的显著高,有接近75%的红鼓鱼分布在莱氏二药藻海草床,这可能是因为红鼓鱼在莱氏二药藻栖息能够降低被捕食的几率[72]

栖息环境浑浊度增加可能会降低幼体被捕食的风险存在一定争议[73, 74]。例如,浑浊度通过影响三刺鱼(Gasterosteus aculeatus)幼体的分布和活动水平,来降低其被捕食风险[73];不过维氏双边鱼(Ambassis vachelli)和短棘鲾(Leiognathus equulus)的丰度却与河口的浑浊度并没有相关关系[74]。然而,水体浑浊度上升会降低透光性,限制海草生长,使海草床退化[75],进而会影响海草床育幼功能[76]。目前,关于海草床水体高浑浊度对生物幼体育幼的影响机理尚不清楚,仍需深入研究。

3 研究展望

尽管海草床的育幼功能已被广泛认可,但大多数研究仅从育幼功能单个指标来探讨海草床育幼功能[4]。而Beck等[6]提出的育幼功能4个方面,迄今为止在海草床还没有被同时证实[7],且大多数研究没能明确阐明生物从海草床向成体生物栖息环境的迁移运动[4, 7]。国外对海草床育幼的研究开展较多,我国尚未有相关研究报道,明显滞后。因此,针对我国在海草床育幼方面研究的不足,结合目前国外学者研究的热点,提出几个可能成为海草床育幼功能和机理的研究趋势。

(1)量化海草床对成体栖息环境贡献量。未来对于海草床育幼功能的研究将尽可能地从育幼功能的四个方面阐述[6],尤其是生物的迁移运动,需结合稳定性同位素[49]、耳石微化学[50]或人工标记技术[77]等方法来探讨海草床生物幼体向成体栖息环境的迁移运动,以量化海草床栖息环境对成体栖息环境的贡献量[7]

(2)全球气候变化和人类活动对海草床的育幼功能的影响。海草床栖息环境理化性质(盐度、温度、pH值、营养盐和溶解氧等)发生改变,影响海草床的育幼功能特征[78]。如溶解氧影响菱体兔牙鲷和绒须石首鱼(Micropogonias undulatus)幼体对海草床栖息环境的利用[79];温度上升影响海草床生物群落结构[80]。但目前关于环境变化对海草床育幼功能影响的研究还较少。因此,建立长期的海草床育幼功能的研究系统,对于评价和预测环境改变对海洋渔业的影响具有重要意义[78]

(3)海草床育幼功能对其斑块效应和边缘效应的响应。全球全球海草床呈退化趋势[81],退化海草床会增加海草床斑块效应和边缘效应,从而影响海草床的育幼功能[76]。例如,海草床边缘及斑块的大小、形状影响生物幼体的存活率、生长率以及其分布的丰度[76, 82]。因此,加强生物幼体对海草床斑块效应和边缘效应响应的研究,可以更好地揭示海草床育幼功能的机理和变化机制。

致谢: 感谢中国科学院南海海洋研究所张霞副研究员和沈萍萍副研究员对写作的帮助。

参考文献
[1] Duarte C M, Chiscano C L. Seagrass biomass and production: a reassessment. Aquatic Botany, 1999, 65(1/4): 159-174.
[2] Hemminga M A, Duarte C M. Seagrass Ecology. Cambridge: Cambridge University Press, 2000.
[3] Costanza R, d'Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O'Neill R V, Paruelo J, Raskin R G, Sutton P, van den Belt M. The value of the world's ecosystem services and natural capital. Nature, 1997, 387(6630): 253-260.
[4] Heck K L Jr, Hays G, Orth R J. Critical evaluation of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series, 2003, 253: 123-136.
[5] Schmidt A L, Coll M, Romanuk T N, Lotze H K. Ecosystem structure and services in eelgrass Zostera marina and rockweed Ascophyllum nodosum habitats. Marine Ecology Progress Series, 2011, 437: 51-68.
[6] Beck M W, Heck K L Jr, Able K W, Childers D L, Eggleston D B, Gillanders B M, Halpern B, Hays C G, Hoshino K, Minello T J, Orth R J, Sheridan P F, Weinstein M R. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience, 2001, 51(8): 633-641.
[7] Nagelkerken I. Evaluation of nursery function of mangroves and seagrass beds for tropical decapods and reef fishes: patterns and underlying mechanisms // Nagelkerken I. Ecological Connectivity among Tropical Coastal Ecosystems. Netherlands: Springer, 2009: 357-399.
[8] Deegan L A. Nutrient and energy transport between estuaries and coastal marine ecosystems by fish migration. Canadian Journal of Fisheries and Aquatic Sciences, 1993, 50(1): 74-79.
[9] Adams A J, Dahlgren C P, Kellison G. T, Kendall M S, Layman C A, Ley J A, Nagelkerken I, Serafy J E. Nursery function of tropical back-reef systems. Marine Ecology Progress Series, 2006, 318:287-301.
[10] Sogard S M. Variability in growth rates of juvenile fishes in different estuarine habitats. Marine Ecology Progress Series, 1992, 85: 35-53.
[11] Stunz G W, Minello T J, Levin P S. Growth of newly settled red drum Sciaenops ocellatus in different estuarine habitat types. Marine Ecology Progress Series, 2002, 238: 227-236.
[12] Aguilar-Perera A, Appeldoorn R S. Variation in juvenile fish density along the mangrove-seagrass-coral reef continuum in SW Puerto Rico. Marine Ecology Progress Series, 2007, 348: 139-148.
[13] Horinouchi M. Distribution patterns of benthic juvenile gobies in and around seagrass habitats: effectiveness of seagrass shelter against predators. Estuarine, Coastal and Shelf Science, 2007, 72(4): 657-664.
[14] Levin P, Petrik R, Malone J. Interactive effects of habitat selection, food supply and predation on recruitment of an estuarine fish. Oecologia, 1997, 112(1): 55-63.
[15] Barbier E B, Hacker S D, Kennedy C, Koch E W,Stier A C, Silliman B R. The value of estuarine and coastal ecosystem services. Ecological Monographs, 2011, 81(2): 169-193.
[16] Nagelkerken I, Kleijnen S, Klop T, van den Brand R A C J, de la Moriniere E C, van der Velde G. Dependence of Caribbean reef fishes on mangroves and seagrass beds as nursery habitats: a comparison of fish faunas between bays with and without mangroves/seagrass beds. Marine Ecology Progress Series, 2001, 214: 225-235.
[17] Polte P, Asmus H. Influence of seagrass beds (Zostera noltii) on the species composition of juvenile fishes temporarily visiting the intertidal zone of the Wadden Sea. Journal of Sea Research, 2006, 55(3): 244-252.
[18] Nagelkerken I, van der Velde G, Gorissen M W, Meijer G J, van't Hof T, den Hartog C. Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuarine, Coastal and Shelf Science, 2000, 51(1): 31-44.
[19] English S, Wilkinson C, Baker V. Survey Manual for Tropical Marine Resources. Townsville: Australian Institute of Marine Science, 1994.
[20] Cheal A J, Thompson A A. Comparing visual counts of coral reef fish: implications of transect width and species selection. Marine Ecology Progress Series, 1997, 158: 241-248.
[21] Thompson A A, Mapstone B D. Observer effects and training in underwater visual surveys of reef fishes. Marine Ecology Progress Series, 1997, 154: 53-63.
[22] Harmelin-Vivien M L, Francour P. Trawling or visual censuses? Methodological bias in the assessment of fish populations in seagrass beds. Marine Ecology, 1992, 13(1): 41-51.
[23] Dorenbosch M, Verberk W C E P, Nagelkerken I, van der Velde G. Influence of habitat configuration on connectivity between fish assemblages of Caribbean seagrass beds, mangroves and coral reefs. Marine Ecology Progress Series, 2007, 334: 103-116.
[24] Heck K L Jr, Thoman T A. The nursery role of seagrass meadows in the upper and lower reaches of the Chesapeake bay. Estuaries, 1984, 7(1): 70-92.
[25] Murphey P L, Fonseca M S. Role of high and low energy seagrass beds as nursery areas for Penaeus duorarum in North Carolina. Marine Ecology Progress Series, 1995, 121: 91-98.
[26] Gibson R N. Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Netherlands Journal of Sea Research, 1994, 32(2): 191-206.
[27] Phelan B A, Goldberg R, Bejda A J, Pereira J, Hagan S, Clark P, Studholme A L, Calabrese A, Able K W. Estuarine and habitat-related differences in growth rates of young-of-the-year winter flounder (Pseudopleuronectes americanus) and tautog (Tautoga onitis) in three northeastern US estuaries. Journal of Experimental Marine Biology and Ecology, 2000, 247(1): 1-28.
[28] Seitz R D, Lipcius R N, Seebo M S. Food availability and growth of the blue crab in seagrass and unvegetated nurseries of Chesapeake Bay. Journal of Experimental Marine Biology and Ecology, 2005, 319(1): 57-68.
[29] Perkins-Visser E, Wolcott T G, Wolcott D L. Nursery role of seagrass beds: enhanced growth of juvenile blue crabs (Callinectes sapidus Rathbun). Journal of Experimental Marine Biology and Ecology, 1996, 198(2): 155-173.
[30] Stoner A W, Ray M, Glazer R A, McCarthy K J. Metamorphic responses to natural substrata in a gastropod larva: decisions related to postlarval growth and habitat preference. Journal of Experimental Marine Biology and Ecology, 1996, 205(1/2): 229-243.
[31] Bullard S G, Hay M E. Plankton tethering to assess spatial patterns of predation risk over a coral reef and seagrass bed. Marine Ecology Progress Series, 2002, 225: 17-28.
[32] Chittaro P M, Usseglio P, Sale P F. Variation in fish density, assemblage composition and relative rates of predation among mangrove, seagrass and coral reef habitats. Environmental Biology of Fishes, 2005, 72(2): 175-187.
[33] Hovel K A, Fonseca M S. Influence of seagrass landscape structure on the juvenile blue crab habitat-survival function. Marine Ecology Progress Series, 2005, 300: 179-191.
[34] Pile A J, Lipcius R N, van Montfrans J, Orth R J. Density-dependent settler-recruit-juvenile relationships in blue crabs. Ecological Monographs, 1996, 66(3): 277-300.
[35] Rooker J R, Holt G J, Holt S A. Vulnerability of newly settled red drum (Sciaenops ocellatus) to predatory fish: is early-life survival enhanced by seagrass meadows? Marine Biology, 1998, 131(1): 145-151.
[36] Orth R J, van Montfrans J. Habitat quality and prey size as determinants of survival in post-larval and early juvenile instars of the blue crab Callinectes sapidus. Marine Ecology Progress Series, 2002, 231: 205-213.
[37] Fuiman L A. The interplay of ontogeny and scaling in the interactions of fish larvae and their predators. Journal of Fish Biology, 1994, 45(Supplement A): 55-79.
[38] Dance S K, Lane I, Bell J D. Variation in short-term survival of cultured sandfish (Holothuria scabra) released in mangrove-seagrass and coral reef flat habitats in Solomon Islands. Aquaculture, 2003, 220(1/4): 495-505.
[39] Lipcius R N, Seitz R D, Seebo M S, Colón-Carrión D. Density, abundance and survival of the blue crab in seagrass and unstructured salt marsh nurseries of Chesapeake Bay. Journal of Experimental Marine Biology and Ecology, 2005, 319(1/2): 69-80.
[40] Hovel K A, Lipcius R N. Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology, 2001, 82(7): 1814-1829.
[41] Gillanders B M, Able K W, Brown J A, Eggleston D B, Sheridan P F. Evidence of connectivity between juvenile and adult habitats for mobile marine fauna: an important component of nurseries. Marine Ecology Progress Series, 2003, 247: 281-295.
[42] Nakamura Y, Hirota K, Shibuno T, Watanabe Y. Variability in nursery function of tropical seagrass beds during fish ontogeny: timing of ontogenetic habitat shift. Marine Biology, 2012, 159(6): 1305-1315.
[43] Nagelkerken I, Roberts C M, van der Velde G, Dorenbosch M, van Riel M C, Cocheret de la Morinière E, Nienhuis P H. How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale. Marine Ecology Progress Series, 2002, 244: 299-305.
[44] Shibuno T, Nakamura Y, Horinouchi M, Sano M. Habitat use patterns of fishes across the mangrove-seagrass-coral reef seascape at Ishigaki Island, southern Japan. Ichthyological Research, 2008, 55(3): 218-237.
[45] Gillanders B M, Kingsford M J. Elements in otoliths may elucidate the contribution of estuarine recruitment to sustaining coastal reef populations of a temperate reef fish. Marine Ecology Progress Series, 1996, 141(1/3): 13-20.
[46] Guido P, Omori M, Katayama S, Kimura K. Classification of juvenile rockfish, Sebastes inermis, to Zostera and Sargassum beds, using the macrostructure and chemistry of otoliths. Marine Biology, 2004, 145(6): 1243-1255.
[47] Cocheret de la Moriniere E, Pollux B J A, Nagelkerken I, van der Velde G. Post-settlement life cycle migration patterns and habitat preference of coral reef fish that use seagrass and mangrove habitats as nurseries. Estuarine, Coastal and Shelf Science, 2002, 55(2): 309-321.
[48] Cocheret de la Morinière E, Pollux B J A, Nagelkerken I, Hemminga M A, Huiskes A H L, van der Velde G. Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Marine Ecology Progress Series, 2003, 246: 279-289.
[49] Verweij M C, Nagelkerken I, Hans I, Ruseler S M, Mason P R D. Seagrass nurseries contribute to coral reef fish populations. Limnology and Oceanography, 2008, 53(4): 1540-1547.
[50] Gillanders B M. Using elemental chemistry of fish otoliths to determine connectivity between estuarine and coastal habitats. Estuarine, Coastal and Shelf Science, 2005, 64(1): 47-57.
[51] Verweij Marieke C, Nagelkerken I. Short and long-term movement and site fidelity of juvenile Haemulidae in back-reef habitats of a Caribbean embayment. Hydrobiologia, 2007, 592(1): 257-270.
[52] Luo J G, Serafy J E, Sponaugle S, Teare P B,Kieckbusch D. Movement of gray snapper Lutjanus griseus among subtropical seagrass, mangrove, and coral reef habitats. Marine Ecology Progress Series, 2009, 380: 255-269.
[53] Grol M G G, Nagelkerken I, Rypel A L, Layman C A. Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of a coral reef fish. Oecologia, 2011, 165(1): 79-88.
[54] Verweij M C, Nagelkerken I, Wartenbergh S L J, Pen I R, van der Velde G. Caribbean mangroves and seagrass beds as daytime feeding habitats for juvenile French grunts, Haemulon flavolineatum. Marine Biology, 2006, 149(6): 1291-1299.
[55] Verwey M C, Nagelkerken I, de Graaff D, Peeters M, Bakker E J, van der Velde G. Structure, food and shade attract juvenile coral reef fish to mangrove and seagrass habitats: a field experiment. Marine Ecology Progress Series, 2006, 306: 257-268.
[56] Horinouchi M, Sano M. Effects of changes in seagrass shoot density and leaf height on the abundance of juveniles of Acentrogobius pflaumii in a Zostera marina bed. Ichthyological Research, 2001, 48(2): 179-185.
[57] Gotceitas V, Fraser S, Brown J A. Use of eelgrass beds (Zostera marina) by juvenile Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences, 1997, 54(6): 1306-1319.
[58] Dorenbosch M, Grol M G G, de Groene A, van der Velde G, Nagelkerken I. Piscivore assemblages and predation pressure affect relative safety of some back-reef habitats for juvenile fish in a Caribbean bay. Marine Ecology Progress Series, 2009, 379: 181-196.
[59] Bertelli C M, Unsworth R K F. Protecting the hand that feeds us: Seagrass (Zostera marina) serves as commercial juvenile fish habitat. Marine Pollution Bulletin, 2014, 83(2): 425-429.
[60] Park H J, Choy E J, Lee K S, Kang C K. Trophic transfer between coastal habitats in a seagrass-dominated macrotidal embayment system as determined by stable isotope and fatty acid signatures. Marine and Freshwater Research, 2013, 64(12): 1169-1183.
[61] Gullström M, Berkström M, Öhman M C, Bodin M, Dahlberg M. Scale-dependent patterns of variability of a grazing parrotfish (Leptoscarus vaigiensis) in a tropical seagrass-dominated seascape. Marine Biology, 2011, 158(7): 1483-1495.
[62] Lugendo B R, Nagelkerken I, van der Velde G, Mgaya Y D. The importance of mangroves, mud and sand flats, and seagrass beds as feeding areas for juvenile fishes in Chwaka Bay, Zanzibar: gut content and stable isotope analyses. Journal of Fish Biology, 2006, 69(6): 1639-1661.
[63] Nakamura Y, Sano M. Comparison of invertebrate abundance in a seagrass bed and adjacent coral and sand areas at Amitori Bay, Iriomote Island, Japan. Fisheries Science, 2005, 71(3): 543-550.
[64] Robblee M B, Zieman J C. Diel variation in the fish fauna of a tropical seagrass feeding ground. Bulletin of Marine Science, 1984, 34(3): 335-345.
[65] Nagelkerken I, Dorenbosch M, Verberk W, Cocheret de la Morinière E, van der Velde G. Day-night shifts of fishes between shallow-water biotopes of a Caribbean bay, with emphasis on the nocturnal feeding of Haemulidae and Lutjanidae. Marine Ecology Progress Series, 2000, 194: 55-64.
[66] Wilson S K, Street S, Sato T. Discarded queen conch (Strombus gigas) shells as shelter sites for fish. Marine Biology, 2005, 147(1): 179-188.
[67] Orth R J, Heck K L Jr, van Montfrans J. Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries, 1984, 7(4): 339-350.
[68] Horinouchi M. Review of the effects of within-patch scale structural complexity on seagrass fishes. Journal of Experimental Marine Biology and Ecology, 2007, 350(1): 111-129.
[69] Crowder L B, Cooper W E. Habitat structural complexity and the interaction between bluegills and their prey. Ecology, 1982, 63(6): 1802-1813.
[70] Savino J F, Stein R A. Behavioural interactions between fish predators and their prey: effects of plant density. Animal Behaviour, 1989, 37(Part 2): 311-321.
[71] Czerny A B, Dunton K H. The effects of in situ light reduction on the growth of two subtropical seagrasses, Thalassia testudinum and Halodule wrightii. Estuaries, 1995, 18(2): 418-427.
[72] Rooker J R, Holt S A. Utilization of subtropical seagrass meadows by newly settled red drum Sciaenops ocellatus: patterns of distribution and growth. Marine Ecology Progress Series, 1997, 158: 139-149.
[73] Ajemian M J, Sohel S, Mattila J. Effects of turbidity and habitat complexity on antipredator behavior of three-spined sticklebacks (Gasterosteus aculeatus). Environmental Biology of Fishes, 2014, doi: 10.1007/s10641-014-0235-x.
[74] Johnston R, Sheaves M, Molony B. Are distributions of fishes in tropical estuaries influenced by turbidity over small spatial scales? Journal of Fish Biology, 2007, 71(3): 657-671.
[75] Erftemeijer P L A, Lewis R R R III. Environmental impacts of dredging on seagrasses: A review. Marine Pollution Bulletin, 2006, 52(12): 1553-1572.
[76] Carroll J M, Peterson B J. Ecological trade-offs in seascape ecology: bay scallop survival and growth across a seagrass seascape. Landscape Ecology, 2013, 28(7): 1401-1413.
[77] Gillanders B M. Tools for studying biological marine ecosystem interactions-natural and artificial tags // Nagelkerken I. Ecological Connectivity among Tropical Coastal Ecosystems. Netherlands: Springer, 2009: 457-492.
[78] Jones C M. Can we predict the future: juvenile finfish and their seagrass nurseries in the Chesapeake Bay. ICES Journal of Marine Science, 2014, 71(3): 681-688.
[79] Froeschke J T, Stunz G W. Hierarchical and interactive habitat selection in response to abiotic and biotic factors: the effect of hypoxia on habitat selection of juvenile estuarine fishes. Environmental Biology of Fishes, 2012, 93(1): 31-41.
[80] Sobocinski K L, Orth R J, Fabrizio M C, Latour R J. Historical comparison of fish community structure in lower Chesapeake Bay seagrass habitats. Estuaries and Coasts, 2013, 36(4): 775-794.
[81] Waycott M, Duarte C M, Carruthers T J B, Orth R J, Dennison W C, Olyarnik S, Calladine A, Fourqurean J W, Heck K L Jr, Hughes A R, Kendrick G A, Kenworthy W J, Short F T, Williams S L. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(30): 12377-12381.
[82] Smith T M, Hindell J S, Jenkins G P, Connolly R M, Keough M J. Edge effects in patchy seagrass landscapes: The role of predation in determining fish distribution. Journal of Experimental Marine Biology and Ecology, 2011, 399(1): 8-16.