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Heterotrophic feeding of hermatypic corals in Luhuitou Sanya

  • Corresponding author: HUANG Hui, huanghui@scsio.ac.cn
  • Received Date: 2020-09-11
    Accepted Date: 2020-10-22
    Available Online: 2021-09-15
  • The acquisition of energy and nutrients is the basis of sustaining the life activities of hermatypic corals, which mainly depends on the alimentation mode. Hermatypic corals are mixotrophic organisms, both autotrophic and heterotrophic. Photosynthesis by zooxanthellae is the basic form of autotrophy, but little is known about the heterotrophic feeding. To know more about it, three representative species in the Sanya Luhuitou Bay, Galaxea fascicularis, Pocillopora damicornis and Acropora muricata were selected in this study to test their feeding habits. Their feeding reaction to Artemia salina, copepod used in aquarium, yeast extract liquor and aquatic coral food were observed. What’s more, G. fascicularis’s feeding rate and digestion of A. salina were probed into. G. fascicularis ingests four kinds of food mentioned above, while A. muricata ingests none of them and P. damicornis only ingests A. salina and aquatic coral food. It’s reported for the first time that P. damicornis ingests A. salina by mesenterial filaments and it ingests aquatic coral food through the cooperation between polyps. Moreover, G. fascicularis’s feeding rate of A. salina and the density of A. salina nauplii well fitted into the Michaelis-Menten model. A. salina was completely digested by G. fascicularis in 3 h. The research can deepen our knowledge about the feeding of hermatypic corals, especially in the process of artificial coral breeding.
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  • [1] Crossland C J, Hatcher B G, Smith S V. Role of coral reefs in global ocean production[J]. Coral Reefs, 1991, 10(2): 55-64. doi: 10.1007/BF00571824
    [2] Fisher R P, O’Leary R A, Low-Choy S, et al. Species richness on coral reefs and the pursuit of convergent global estimates[J]. Current Biology, 2015, 25(4): 500-505. doi: 10.1016/j.cub.2014.12.022
    [3] Yonge C M. Studies on the physiology of corals: I. feeding mechanisms and food[J]. Scientific Reports/Great Barrier Reef Expedition, 1930, 1: 13-57.
    [4] Yonge C M, Nicholls A G. Studies on the physiology of corals: IV. the structure, distribution and physiology of the zooxanthellae[J]. Scientific Reports/Great Barrier Reef Expedition, 1931, 1: 135-176.
    [5] Muscatine L, Falkowski P G, Porter J W, et al. Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata[J]. Proceedings of the Royal Society B: Biological Sciences, 1984, 222(1227): 181-202. doi: 10.1098/rspb.1984.0058
    [6] Houlbrèque F, Ferrier-Pagès C. Heterotrophy in tropical scleractinian corals[J]. Biological Reviews, 2009, 84(1): 1-17. doi: 10.1111/j.1469-185X.2008.00058.x
    [7] Titlyanov E A, Titlyanova T V. Reef-building corals—symbiotic autotrophic organisms: 1. general structure, feeding pattern, and light-dependent distribution in the shelf[J]. Russian Journal of Marine Biology, 2002, 28(S1): S1-S15. doi: 10.1023/A:1021836204655
    [8] Anthony K R N, Fabricius K E. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity[J]. Journal of Experimental Marine Biology and Ecology, 2000, 252(2): 221-253. doi: 10.1016/S0022-0981(00)00237-9
    [9] Grover R, Maguer J F, Allemand D, et al. Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata[J]. Journal of Experimental Biology, 2008, 211(6): 860-865. doi: 10.1242/jeb.012807
    [10] Sebens K P, Vandersall K S, Savina L A, et al. Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure[J]. Marine Biology, 1996, 127(2): 303-317. doi: 10.1007/BF00942116
    [11] Conti-Jerpe I E, Thompson P D, Wong C W M, et al. Trophic strategy and bleaching resistance in reef-building corals[J]. Science Advances, 2020, 6(15): eaaz5443. doi: 10.1126/sciadv.aaz5443
    [12] Carpenter K E, Abrar M, Aeby G, et al. One-third of reef-building corals face elevated extinction risk from climate change and local impacts[J]. Science, 2008, 321(5888): 560-563. doi: 10.1126/science.1159196
    [13] Leal M C, Ferrier-Pagès C, Petersen D, et al. Coral aquaculture: applying scientific knowledge to ex situ production[J]. Reviews in Aquaculture, 2016, 8(2): 136-153. doi: 10.1111/raq.12087
    [14] Delbeek J C. Coral farming: past, present and future trends[J]. Aquarium Sciences and Conservation, 2001, 3(1-3): 171-181. doi: 10.1023/A:1011306125934
    [15] Forsman Z H, Kimokeo B K, Bird C E, et al. Coral farming: effects of light, water motion and artificial foods[J]. Journal of the Marine Biological Association of the United Kingdom, 2012, 92(4): 721-729. doi: 10.1017/s0025315411001500
    [16] Wijgerde T, Diantari R, Lewaru M W, et al. Extracoelenteric zooplankton feeding is a key mechanism of nutrient acquisition for the scleractinian coral Galaxea fascicularis[J]. Journal of Experimental Biology, 2011, 214(20): 3351-3357. doi: 10.1242/jeb.058354
    [17] Tagliafico A, Rangel S, Kelaher B, et al. Optimizing heterotrophic feeding rates of three commercially important scleractinian corals[J]. Aquaculture, 2018, 483: 96-101. doi: 10.1016/j.aquaculture.2017.10.013
    [18] 王尔栋, 王钟, 陈国华, 等. 珊瑚对型轮虫和丰年虫无节幼体的捕食机制初探[J]. 水产养殖, 2014, 35(1): 1-4. doi: 10.3969/j.issn.1004-2091.2014.01.001Wang E D, Wang Z, Chen G H, et al. Explore the prey mechanism of coral on biological live bait s-type Rotifer and Artemia nauplii[J]. Journal of Aquaculture, 2014, 35(1): 1-4 (in Chinese). doi: 10.3969/j.issn.1004-2091.2014.01.001
    [19] 杨阳楚翘, 洪文霆, 王淑红. 共生珊瑚异养营养研究进展[J]. 应用生态学报, 2017, 28(12): 4143-4149. doi: 10.13287/j.1001-9332.201712.032Yang Y C Q, Hong W T, Wang S H. Progress of heterotrophic studies on symbiotic corals[J]. Chinese Journal of Applied Ecology, 2017, 28(12): 4143-4149 (in Chinese). doi: 10.13287/j.1001-9332.201712.032
    [20] 张浴阳. 三亚鹿回头鹿角杯形珊瑚恢复力研究[D]. 北京: 中国科学院大学, 2015.Zhang Y Y. The study of recovery capacity of Pocillopora damicornis on Luhuitou Reef, Sanya[D]. Beijing: University of Chinese Academy of Sciences, 2015 (in Chinese).
    [21] Hii Y S, Soo C L, Liew H C. Feeding of scleractinian coral, Galaxea fascicularis, on Artemia salina nauplii in captivity[J]. Aquaculture International, 2009, 17(4): 363-376. doi: 10.1007/s10499-008-9208-4
    [22] Porter J W. Autotrophy, heterotrophy, and resource partitioning in Caribbean reef-building corals[J]. The American Naturalist, 1976, 110(975): 731-742. doi: 10.1086/283100
    [23] Palardy J E, Grottoli A G, Matthews K A. Effects of upwelling, depth, morphology and polyp size on feeding in three species of panamanian corals[J]. Marine Ecology Progress Series, 2005, 300: 79-89. doi: 10.3354/meps300079
    [24] Palardy J E, Grottoli A G, Matthews K A. Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific[J]. Journal of Experimental Marine Biology and Ecology, 2006, 331(1): 99-107. doi: 10.1016/j.jembe.2005.10.001
    [25] Palardy J E, Rodrigues L J, Grottoli A G. The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths[J]. Journal of Experimental Marine Biology and Ecology, 2008, 367(2): 180-188. doi: 10.1016/j.jembe.2008.09.015
    [26] Raz-Bahat M, Douek J, Moiseeva E, et al. The digestive system of the stony coral Stylophora pistillata[J]. Cell and Tissue Research, 2017, 368(2): 311-323. doi: 10.1007/s00441-016-2555-y
    [27] Smith J N, Strahl J, Noonan S H C, et al. Reduced heterotrophy in the stony coral Galaxea fascicularis after life-long exposure to elevated carbon dioxide[J]. Scientific Reports, 2016, 6(1): 27019. doi: 10.1038/srep27019
    [28] Ferrier-Pagès C, Allemand D, Gattuso J P, et al. Microheterotrophy in the zooxanthellate coral Stylophora pistillata: Effects of light and ciliate density[J]. Limnology and Oceanography, 1998, 43(7): 1639-1648. doi: 10.4319/lo.1998.43.7.1639
    [29] Grottoli A G, Rodrigues L J, Palardy J E, et al. Heterotrophic plasticity and resilience in bleached corals[J]. Nature, 2006, 440(7088): 1186-1189. doi: 10.1038/nature04565
    [30] Shu J, Hou L, Ma R, et al. In situ fabrication of Li4Ti5O12@CNT composites and their superior lithium storage properties[J]. RSC Advances, 2012, 2(27): 10306-10309. doi: 10.1039/C2RA21603E
    [31] Sebens K P, Helmuth B, Carrington E, et al. Effects of water flow on growth and energetics of the scleractinian coral Agaricia tenuifolia in Belize[J]. Coral Reefs, 2003, 22(1): 35-47. doi: 10.1007/s00338-003-0277-6
    [32] Lewis J B. Experimental tests of suspension feeding in Atlantic reef corals[J]. Marine Biology, 1976, 36(2): 147-150. doi: 10.1007/BF00388437
    [33] Petersen D, Wietheger A, Laterveer M. Influence of different food sources on the initial development of sexual recruits of reefbuilding corals in aquaculture[J]. Aquaculture, 2008, 277(3-4): 174-178. doi: 10.1016/j.aquaculture.2008.02.034
    [34] Sebens K P, Grace S P, Helmuth B, et al. Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa and Porites porites, in a field enclosure[J]. Marine Biology, 1998, 131(2): 347-360. doi: 10.1007/s002270050328
    [35] Lewis J B. Processes of organic production on coral reefs[J]. Biological Reviews, 1977, 52(3): 305-347. doi: 10.1111/j.1469-185X.1977.tb00836.x
    [36] Goldberg W M. Coral food, feeding, nutrition, and secretion: a review[M]//Kloc M, Kubiak J Z. Marine organisms as model systems in biology and medicine. Cham: Springer, 2018: 377-421.
    [37] Roff G, Dove S G, Dunn S R. Mesenterial filaments make a clean sweep of substrates for coral growth[J]. Coral Reefs, 2009, 28(1): 79. doi: 10.1007/s00338-008-0424-1
    [38] Mullen A D, Treibitz T, Roberts P L D, et al. Underwater microscopy for in situ studies of benthic ecosystems[J]. Nature Communications, 2016, 7(1): 12093. doi: 10.1038/ncomms12093
    [39] Musco L, Fernández T V, Caroselli E, et al. Protocooperation among small polyps allows the coral Astroides calycularis to prey on large jellyfish[J]. Ecology, 2018, 99(10): 2400-2401. doi: 10.1002/ecy.2413
    [40] Ferrier-Pagès C, Rottier C, Beraud E, et al. Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: effect on the rates of photosynthesis[J]. Journal of Experimental Marine Biology and Ecology, 2010, 390(2): 118-124. doi: 10.1016/j.jembe.2010.05.007
    [41] Rossi S, Ribes M, Coma R, et al. Temporal variability in zooplankton prey capture rate of the passive suspension feeder Leptogorgia sarmentosa (Cnidaria: Octocorallia), a case study[J]. Marine Biology, 2004, 144(1): 89-99. doi: 10.1007/s00227-003-1168-7
    [42] Porter J W. Zooplankton feeding by the Caribbean reef-building coral Montastrea cavernosa[C]//Proceedings of the 2nd International Coral Reef Symposium. Brisbane: Great Barrier Reef Committee, 1974: 111-125.
    [43] Coffroth M A. Ingestion and incorporation of coral mucus aggregates by a gorgonian soft coral[J]. Marine Ecology Progress Series, 1984, 17(2): 193-199. doi: 10.3354/meps017193
    [44] Sebens K P, Koehl M A R. Predation on zooplankton by the benthic anthozoans Alcyonium siderium (Alcyonacea) and Metridium senile (Actiniaria) in the New England subtidal[J]. Marine Biology, 1984, 81(3): 255-271. doi: 10.1007/BF00393220
    [45] Lewis J B. Heterotrophy in corals: Zooplankton predation by the hydrocoral Millepora complanata[J]. Marine Ecology Progress Series, 1992, 90: 251-256. doi: 10.3354/meps090251
    [46] 俞晓磊, 江雷, 罗勇, 等. 异养营养对丛生盔形珊瑚代谢及共生藻光合生理的影响[J]. 海洋科学, 2019, 43(12): 81-88. doi: 10.11759/hykx20190625003Yu X L, Jiang L, Luo Y, et al. Effects of heterotrophy on the metabolism and symbiont photosynthetic physiology of Galaxea fascicularis[J]. Marine Sciences, 2019, 43(12): 81-88 (in Chinese). doi: 10.11759/hykx20190625003
    [47] Hall N M, Berry K L E, Rintoul L, et al. Microplastic ingestion by scleractinian corals[J]. Marine Biology, 2015, 162(3): 725-732. doi: 10.1007/s00227-015-2619-7
    [48] Li X B, Huang H, Lian J S, et al. Spatial and temporal variations in sediment accumulation and their impacts on coral communities in the Sanya Coral Reef Reserve, Hainan, China[J]. Deep Sea Research Part II: Topical Studies in Oceanography, 2013, 96: 88-96. doi: 10.1016/j.dsr2.2013.04.015
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Heterotrophic feeding of hermatypic corals in Luhuitou Sanya

    Corresponding author: HUANG Hui, huanghui@scsio.ac.cn
  • 1. Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou    510301, China
  • 2. Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya    572000, China
  • 3. Hainan Key Laboratory of Tropical Marine Biotechnology, Sanya    572000, China
  • 4. University of Chinese Academy of Sciences, Beijing    100049, China

Abstract: The acquisition of energy and nutrients is the basis of sustaining the life activities of hermatypic corals, which mainly depends on the alimentation mode. Hermatypic corals are mixotrophic organisms, both autotrophic and heterotrophic. Photosynthesis by zooxanthellae is the basic form of autotrophy, but little is known about the heterotrophic feeding. To know more about it, three representative species in the Sanya Luhuitou Bay, Galaxea fascicularis, Pocillopora damicornis and Acropora muricata were selected in this study to test their feeding habits. Their feeding reaction to Artemia salina, copepod used in aquarium, yeast extract liquor and aquatic coral food were observed. What’s more, G. fascicularis’s feeding rate and digestion of A. salina were probed into. G. fascicularis ingests four kinds of food mentioned above, while A. muricata ingests none of them and P. damicornis only ingests A. salina and aquatic coral food. It’s reported for the first time that P. damicornis ingests A. salina by mesenterial filaments and it ingests aquatic coral food through the cooperation between polyps. Moreover, G. fascicularis’s feeding rate of A. salina and the density of A. salina nauplii well fitted into the Michaelis-Menten model. A. salina was completely digested by G. fascicularis in 3 h. The research can deepen our knowledge about the feeding of hermatypic corals, especially in the process of artificial coral breeding.

  • 珊瑚礁生态系统具有的极高生产力和生物多样性,素有“海洋中的热带雨林”的美称[1-2]。其中,造礁石珊瑚作为珊瑚礁生态系统的框架生物,其营养方式一直以来备受学者关注。早在20世纪30年代初,就有学者通过实验证实了造礁石珊瑚不仅与陆地植物一样拥有极高的光合作用活性,还能进行异养营养[3-4]。但在过去的一段时间里,国内外学者关注与研究的焦点主要集中在造礁石珊瑚共生虫黄藻(zooxanthella)的光合自养。目前,人们认识到珊瑚共生虫黄藻光合作用所生成的糖类和脂类等含碳物质是造礁石珊瑚能量与营养物质的主要来源[5],同时也对光合自养的机理、过程等有了全面且深入的认知。然而,至今人们对造礁石珊瑚异养营养的研究仍相对较少。

    异养营养作为造礁石珊瑚另一种重要的营养方式,对于其生长与分布至关重要[6]。有研究指出,光合自养生成的糖类、甘油和脂类等含碳物质,因其无法补充造礁石珊瑚所需的氮、磷等其他营养元素而被称为“垃圾食物”(junk food)[7]。而通过对浮游生物、颗粒有机物和溶解有机物等的摄食,造礁石珊瑚能够额外获得氮、磷等各种元素的补充,这对于珊瑚的生长发育具有重要意义[8-10]。总体来说,光合自养是造礁石珊瑚获得能量的主要途径,但异养营养对于许多种珊瑚的正常生长发育同样不可或缺[11],两种营养方式的协调与平衡是造礁石珊瑚赖以生存的基础。

    在全球珊瑚礁生态系统退化的背景下[12],水族贸易、医药产业和珊瑚礁生态修复工程对于人工养殖的造礁石珊瑚的需求日益增长[13]。然而,造礁石珊瑚的人工养殖历史较短[14],在应用人工饵料进行饲喂方面,仅有少数学者开展了研究。例如Forsman等[15]关注人工养殖3种造礁石珊瑚的饵料选择问题,提出不同种珊瑚的最适饲养条件具有种间差异。Wijgerde等[16]关注丛生盔形珊瑚(Galaxea fascicularis)对丰年虫无节幼体的摄食过程,提出丛生盔形珊瑚可以通过释放肠系膜(mesenterial filaments)对食物进行体外消化,这一摄食方式对其摄入外源营养具有重要作用。Tagliafico等[17]关注3种造礁石珊瑚在昼夜条件下对丰年虫无节幼体摄食速率的变化,提出不同种珊瑚的最大摄食速率具有种间差异,且昼夜变化不大。国内仅有王尔栋等[18]通过饲喂实验,提出超小型轮虫与丰年虫无节幼体是适合珊瑚异养摄食的生物活饵料。总体来看,关于造礁石珊瑚异养摄食人工饵料方面的研究仍处于起步阶段[19],对于造礁石珊瑚在人工养殖时的饵料选择,造礁石珊瑚的摄食方式、摄食取向和摄食速率等诸多方面仍需开展深入研究。

    本研究选择我国三亚鹿回头海域的3种代表性造礁石珊瑚—丛生盔形珊瑚、鹿角杯形珊瑚(Pocillopora damicornis)和美丽鹿角珊瑚(Acropora muricata)为对象,以4种不同尺寸的颗粒有机物—丰年虫无节幼体(Artemia salina)、水族用桡足类、水族珊瑚粮和酵母浸出粉溶液为饵料,在实验室内观察3种造礁石珊瑚对4种食物的摄食取向和摄食方式,结合珊瑚自身特点,讨论影响其摄食差异的原因。在此基础上,通过构建摄食动力学曲线探究丛生盔形珊瑚摄食速率,并利用解剖法研究其消化过程,对其摄食生物学过程进行深入研究。研究结果将有助于进一步认识造礁石珊瑚的摄食特征,可为造礁石珊瑚人工养殖过程中的饵料选择提供借鉴,并为在野外进行造礁石珊瑚摄食生态学的研究提供参考。

    • 2019年3月11日于中国科学院海南热带海洋生物实验站外侧鹿回头海域 (18°12′N, 109°28′E) 2~3 m水深处采集丛生盔形珊瑚、鹿角杯形珊瑚和美丽鹿角珊瑚各3株(约100 cm2/株)。使用斜口钳与剪刀将丛生盔形珊瑚分离成单个珊瑚杯(n=100),鹿角杯形珊瑚和美丽鹿角珊瑚则分剪成长度约5 cm的短枝(n=10)。然后使用阿隆发胶将珊瑚单杯或短枝固定于陶瓷基座(图1),移入室内的珊瑚养殖系统暂养,珊瑚养殖系统条件稳定在pH值8.1,温度26.5 °C,盐度约34,光合有效辐射100 μmol /(m2·s),该光照强度接近鹿回头礁区夏季3 m水深处的白天平均光强[20],21 d后开展饵料投喂实验。此外,实验前用cellSens Standard软件在解剖镜下拍摄珊瑚杯口并计量杯口大小、触手长度及触手数量(n=10)。

      Figure 1.  Three species of hermatypic corals

    • 随机选取4个丛生盔形珊瑚单杯、4个鹿角杯形珊瑚短枝和4个美丽鹿角珊瑚短枝,置于150 mL烧杯中,分别加入丰年虫无节幼体(无棣海吉水产有限公司)、水族用桡足类(德国JBL公司)、酵母浸出粉溶液(上海博微生物科技有限公司)及水族珊瑚粮(美国Two Little Fish公司),其中水族珊瑚粮主要成分为鱼糜、虾糜和丰年虫卵等组成的有机碎屑 (表1)。在解剖镜下观察3种珊瑚对4种食物的摄食方式和摄食取向,并用cellSens Standard软件拍照记录,实验重复5次,每次间隔1天开展。

      食物名称
      food
      食物类型
      food type
      粗蛋白含量/%
      crude protein content
      尺寸/μm(n=10)
      size
      水族用桡足类 copepod used in aquarium 小型浮游生物 microplankton 55.6 556~893
      丰年虫无节幼体 Artemia salina 小型浮游生物 microplankton 54.6 328~517
      水族珊瑚粮 aquatic coral food 有机碎屑 organic detritus 51.2 68~322
      酵母浸出粉溶液 yeast extract liquor 有机溶液 organic solution 72.3 溶液 solution

      Table 1.  Size, food type and crude protein content of four kinds of food

    • 随机选取90个在室内珊瑚养殖体系暂养的丛生盔形珊瑚单杯,将其随机分为6组,每组15个单杯,分别置于6个装有1 L砂滤海水的2 L大烧杯中培养适应1 h。在大多数珊瑚的触手完全伸展时,用密度分别为2 000、4 000、6 000、8 000、10 000和12 000个/L的丰年虫无节幼体活体饲喂珊瑚。1 h后将珊瑚取出,采用浮游生物计数法,取10 mL水样进行丰年虫无节幼体的计数,重复5次后取平均值,估算烧杯中剩余的丰年虫无节幼体数量。实验连续进行7 d,每天饲喂1次,实验数据用SigmaPlot 12.5软件进行分析并作图,摄食速率以平均值±标准误表示。用米氏方程$V = \dfrac{{V_{\rm{max}} \cdot \left[ S \right]}}{{K_m + \left[ S \right]}}$拟合曲线得出VmaxKm。式中S为丰年虫无节幼体密度,V为每小时丛生盔形珊瑚摄食量,Vmax为每小时丛生盔形珊瑚最大摄食量,Km为每小时丛生盔形珊瑚摄食量为最大摄食量一半时的丰年虫无节幼体密度。

    • 随机选取18个丛生盔形珊瑚单杯,每6个为一组,分为3组,将每组中的6个单杯分别放在6个500 mL小烧杯中,在每个小烧杯中饲喂丛生盔形珊瑚20个丰年虫无节幼体。一定时间间隔后(时间间隔分别为0.5、1、1.5、2、2.5和3 h),用无水乙醇固定丛生盔形珊瑚,24 h后用针筒提取丛生盔形珊瑚体内残余的食物成分。在解剖镜下观察其摄食丰年虫无节幼体后的消化产物,记录丰年虫经过不同消化时间后在珊瑚体内的形态变化状况,并根据其形态完整性估测其被消化情况[21],实验重复3次。

    2.   结果
    • 摄食食物种类最多的丛生盔形珊瑚杯口最大(杯口直径均值为768 μm)、触手最长(长度均值为1 550 μm)且数量最多(48个);只对2种食物有摄食现象的鹿角杯形珊瑚次之(杯口直径均值为365 μm,触手长度均值为276 μm,触手数目为12个);对4种食物均没有摄食现象的美丽鹿角珊瑚杯口最小(杯口直径均值为223 μm)、触手最短(长度均值为88 μm)且触手数目最少(12个) (表2)。

      物种
      species
      水族用桡足类
      copepod used in aquarium
      丰年虫无节幼体
      A. salina
      水族珊瑚粮
      aquatic coral food
      酵母浸出粉溶液
      yeast extract liquor
      丛生盔形珊瑚 G. fascicularis + + + +
      鹿角杯形珊瑚 P. damicornis + +
      美丽鹿角珊瑚 A. muricata
      注:+.珊瑚对食物表现出摄食行为,−.珊瑚对食物未表现出摄食行为
      Notes: +. ingestion, −. no ingestion

      Table 2.  Feeding performance of three hermatypic corals to four kinds of food

      丛生盔形珊瑚对水族用桡足类、丰年虫无节幼体和水族珊瑚粮的摄食现象表现为其触手将食物聚集到杯口上方,随后杯口打开,食物被吞入后杯口闭合,而对酵母浸出粉溶液的摄食现象表现为其触手异常活跃,杯口不断开合。鹿角杯形珊瑚在摄食丰年虫无节幼体时,表现出相邻水螅体之间相互协助摄食的现象,一个水螅体的触手会将丰年虫无节幼体推入另一水螅体的杯口,帮助其摄食。解剖镜下观察发现,鹿角杯形珊瑚只有少部分水螅体表现出摄食现象,且每个水螅体的摄食量较少,约为每杯1~2个丰年虫无节幼体或水族珊瑚粮。此外,丛生盔形珊瑚和鹿角杯形珊瑚还可以释放肠系膜包围食物,对食物进行体外消化,待食物部分消化后再吞回包有食物的肠系膜(图版Ⅰ-eⅠ-h)。

      Figure 图版Ⅰ.  Feeding patterns of G. fascicularis and P. damicornis

    • 在1 h的摄食时间内,丛生盔形珊瑚对丰年虫无节幼体的摄食量(V)与丰年虫无节幼体密度(S)呈正相关。用米氏方程$V = \dfrac{{V_{\rm{max}} \cdot \left[ S \right]}}{{K_m + \left[ S \right]}}$拟合得$V = \dfrac{{81 \cdot \left[ S \right]}}{{5\; 458 + \left[ S \right]}}$,即每小时每个丛生盔形珊瑚水螅体的最大摄食量(Vmax)为81个/L;每小时每个丛生盔形珊瑚水螅体摄食量为最大摄食量一半时的丰年虫无节幼体密度Km为5 438个/L(R2 =0.997 8)(图2)。

      Figure 2.  Feeding rate of G. fascicularis at different density of A. salina

    • 丰年虫无节幼体主要由头部、翼部和躯干组成,通过分析各部分的完整性可估测其被消化情况。在丛生盔形珊瑚体内消化0.5 h后的丰年虫无节幼体个体完整,翼部、头部、躯干部清晰可见;1 h后翼部残缺,躯干处出现扭曲;1.5 h后躯干处开始出现残缺;2 h后翼部消失,躯干开始解体;2.5 h后躯干逐渐解体;3 h后只剩下头部眼点,丰年虫无节幼体基本被消化殆尽(图版Ⅱ)。

      Figure 图版Ⅱ.  A. salina digested by G. fascicularis

    3.   讨论
    • 造礁石珊瑚摄食能力主要与其自身形状[10, 22-23]、水螅体大小[10, 23-24]及触手和刺细胞类型[6]等特征有关。在本研究中,水螅体杯口越大、触手越长且数量越多的珊瑚摄食食物种类越多。3种珊瑚摄食的食物尺寸均比其杯口小(图版Ⅰ),这可能是由于造礁石珊瑚的碳酸钙骨骼决定了杯口的大小,从而限制了其可摄食食物的尺寸。与本研究类似,Palardy等[25]研究发现,常见造礁石珊瑚对不同类型的浮游动物的摄食选择性不强,但会偏爱粒径小的食物。珊瑚水螅体杯口大小是食物进入珊瑚水螅体的限制性因素,水螅体的大小同时关系到可摄入食物的容量。水螅体内消化循环腔的肠系膜是珊瑚消化食物的主要场所[26],因此,水螅体的大小在一定程度上反映了珊瑚的摄食与消化能力。珊瑚的触手是其捕获水体中颗粒有机物的重要工具,发达的触手将有利于其充分利用周围的食物。在本研究中,丛生盔形珊瑚具有发达的触手,其可伸长数倍于平常长度以抓捕距离较远的食物,并将包裹住的食物推入杯口。不同种类珊瑚的杯口大小和触手数目是决定其摄食食物尺寸的重要因素,因此在珊瑚的人工饲养过程中,需根据不同珊瑚的自身特点选择适合其摄食的相应尺寸食物。对于同种珊瑚理想饵料的选择而言,进一步的研究应当定量计算同种珊瑚在摄食不同尺寸食物达到最大摄食量一半时物质与能量的输入,并探究摄食前后珊瑚自身的生理状态和营养状况变化,以选择该种珊瑚的理想饵料。综合考虑养殖成本,丰年虫无节幼体被广泛应用于水产养殖,具有价格低廉、制作方便的特点,是杯口口径较大珊瑚人工养殖的理想饵料。

      再者,环境因子的变化也会影响造礁石珊瑚的摄食能力,Smith等[27]的研究表明珊瑚的摄食受水体pH值的影响。本研究发现,鹿角杯形珊瑚和美丽鹿角珊瑚对酵母浸出粉溶液均无摄食现象,而且在加入酵母浸出粉溶液后触手紧闭,这可能与酵母浸出粉溶液呈酸性有关(2%溶液pH值为6.9)。而丛生盔形珊瑚对酵母浸出粉溶液仍然表现出摄食现象(图版Ⅰ-d),故推测丛生盔形珊瑚在酸化条件下的摄食能力可能比另两种珊瑚更强。此外,以往的研究表明,光照[28]、温度[29-30]、水流[31]以及食物的种类与密度[32-33]等也是影响造礁石珊瑚异养摄食的重要因素。因此,在造礁石珊瑚的人工饲喂过程中,还需注意环境因素对珊瑚摄食的影响。

      珊瑚摄食方式的多样性是衡量其摄食能力的重要指标。珊瑚的摄食方式多样,包括触手抓取、黏液吸附、刺细胞捕获和渗透营养等[34-35],许多种类的造礁石珊瑚还能够通过肠系膜和黏液在体外捕获并消化食物[36]。本研究发现,当大量食物聚集在丛生盔形珊瑚和鹿角杯形珊瑚的杯口时,两种珊瑚可吐出肠系膜包裹食物,并在体外直接消化,待食物部分消化后再吞回包有食物的肠系膜。丛生盔形珊瑚通过肠系膜摄食食物的现象已有报道,而鹿角杯形珊瑚通过肠系膜摄食食物的现象是首次被发现。Roff等[37]的研究表明,与美丽鹿角珊瑚形态结构相似的佳丽鹿角珊瑚(A. pulchra)能利用释放到体外的肠系膜扫食周围基底上的沉积碎屑颗粒,而本研究中的美丽鹿角珊瑚并没有表现出通过肠系膜摄食食物的现象。此外,在鹿角杯形珊瑚通过触手抓取丰年虫无节幼体时,相邻水螅体之间表现出相互协助摄食的现象。与之相似,Mullen等[38]曾报道柱状珊瑚(Stylophora sp.)在摄食丰年虫时表现出水螅体之间相互协作的现象,水螅体间的相互协作将有助于珊瑚摄食到较大体积和较多数量的食物[39]。因此,肠系膜较发达的珊瑚具有吞食较大尺寸食物的潜力,水螅体间的相互协作将有利于珊瑚抓取杯口附近的食物,且珊瑚多样的摄食方式将有利于其充分利用环境中的食物。

      在本实验中,丛生盔形珊瑚不仅表现出食性广泛,相比另外2种珊瑚,其对于丰年虫无节幼体的摄食量也较大。通过构建摄食动力学曲线探究其摄食速率的特征,结果发现其单位时间对丰年虫无节幼体的摄食量与丰年虫无节幼体密度符合米氏方程。在造礁石珊瑚摄食速率方面的研究上,曾有学者通过饲喂实验探究珊瑚摄食量与食物浓度的关系并与传统的Michaelis-Menten摄食模型进行比较[17, 21],以探索饲喂珊瑚时最合适的投饵量。例如,Hii等[21]在丛生盔形珊瑚摄食丰年虫无节幼体的实验中,曾通过拟合米氏方程,计算出1 h摄食量为最大摄食量一半时的丰年虫无节幼体密度(Km)为5 320个/L,1 h丛生盔形珊瑚最大摄食量(Vmax)为76.9个/L,这与本实验的结果相符合,两海区丛生盔形珊瑚的摄食能力之间没有明显差异。而在Ferrier-Pagès等[40]的实验中,当丰年虫无节幼体密度为每个水螅体30个/L时,丛生盔形珊瑚的摄食量却为9个/L,摄食速率高于本研究结果。这可能与该实验中丛生盔形珊瑚并没有分成单杯,在食物密度较低时水螅体间通过相互协作捕获食物可能会提高其摄食速率有关。另外,FerrierPagès等[28]曾报道单位时间柱状珊瑚对纤毛虫的摄食量与纤毛虫密度呈正相关:当纤毛虫密度从200个/mL上升到800个/mL时,柱状珊瑚对纤毛虫的摄食速率提高了2 000倍。目前,关于珊瑚对于不同种食物的摄食动力学研究还有待补充,进一步研究不同种珊瑚的摄食速率有利于在人工养殖珊瑚时选取合适的投饵量,从而避免饵料的浪费和水质的恶化。

      丛生盔形珊瑚具有较强的消化能力。本研究表明,被摄食的丰年虫无节幼体能在丛生盔形珊瑚体内被逐渐消解,其消化周期约为3 h。珊瑚对于不同食物的消化时间并不相同,消化时间与珊瑚水螅体大小、食物种类和温度等因素有关[41]。Porter[42]认为从捕获猎物到完全消化,珊瑚虫平均需要消耗1.5~2 h。Hii等[21]曾报道丛生盔形珊瑚对丰年虫无节幼体的消化从摄食后10 min开始,3 h后基本完成。这与本实验的结果相符合,也证明了两海区丛生盔形珊瑚对丰年虫无节幼体的消化能力没有明显差异。不同种珊瑚消化食物的能力存在差异,Coffroth[43]和Sebens等[44]发现软珊瑚(Pseudoplexaura porosa)一般在3~6 h能完全消化其所摄食的食物;Lewis[45]则发现多孔螅(Millepora complanata)24 h后只消化了食物的91%。相对而言,丛生盔形珊瑚表现出较强的消化能力。

      丛生盔形珊瑚的广食性、高摄食速率和强消化能力一方面有利于其利用水体中的有机物,通过异养营养补充机体能量与营养物质的需求。尤其是在光照不足等胁迫环境中,异养营养的输入有利于丛生盔形珊瑚的生理健康[46];但是另一方面,这也有可能造成其误食无机颗粒或其他有害物质。Hall等[47]的研究发现,珊瑚会摄食海水中的微塑料,且实验条件下其对微塑料的摄食速率与对浮游生物的摄食速率相似。三亚鹿回头海域珊瑚礁位于三亚湾东岸,濒临三亚河入海口和市区,是我国受人为活动和陆源物质输入影响较严重的岸礁[48],其中表现出强异养摄食能力的丛生盔形珊瑚是否会受环境中微塑料等无机颗粒物的影响,有待进一步探究。

    4.   结论
    • 本研究表明,珊瑚自身形态和食物尺寸是决定不同种珊瑚摄食取向的重要因素,而且丛生盔形珊瑚和鹿角杯形珊瑚能够通过直接吞食和吐出肠系膜两种方式捕获食物。通过对丛生盔形珊瑚摄食速率的研究,发现其对丰年虫无节幼体的摄食速率与饵料密度的关系符合米氏方程,这表明丛生盔形珊瑚的摄食速率受食物分布的影响。此外,本研究还证实丛生盔形珊瑚具有较强的消化能力,对丰年虫无节幼体的消化周期约为3 h。以上结论能为造礁石珊瑚人工养殖的饵料选择提供借鉴,并为进一步在野外条件下进行造礁石珊瑚的摄食生态学研究提供参考。

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