Home Journals Articles Updates About
CN
image
收藏切换
Application of DNA metabarcoding to characterize the diet of the moon jellyfish Aurelia coerulea polyps and ephyrae
收藏切换
PDF
Tingting Sun1, 2, Lei Wang1, 2, Jianmin Zhao1, 3, Zhijun Dong1, 3, *
Acta Oceanologica Sinica | 2021, 40(8) : 160 - 167
Less
收藏切换
Acta Oceanologica Sinica | 2021, 40(8): 160-167
• Marine Biology •
Application of DNA metabarcoding to characterize the diet of the moon jellyfish Aurelia coerulea polyps and ephyrae
Full
Tingting Sun1, 2, Lei Wang1, 2, Jianmin Zhao1, 3, Zhijun Dong1, 3, *
Affiliations
  • 1 Muping Coastal Environment Research Station, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai 264003, China
  • 2 University of Chinese Academy of Sciences, Beijing 100049, China
  • 3 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China
Published: 2021-08-25 doi: 10.1007/s13131-021-1800-8
Outline
收藏切换

Dietary studies of polyps and ephyrae are important to understand the formation and magnitude of jellyfish blooms and provide important insights into the marine food web. However, the diet of polyps and ephyrae in situ is largely unknown. Here, prey species of the polyps and ephyrae of the moon jellyfish Aurelia coerulea in situ were identified using high-throughput DNA sequencing techniques. The results show that A. coerulea polyps and ephyrae consume a variety of prey items. The polyps consume both planktonic and benthic prey, including hydromedusae, copepods, ciliates, polychaetes, stauromedusae, and phytoplankton. A. coerulea ephyrae mainly feed on copepods and hydromedusae. Gelatinous zooplankton, including Rathkea octopunctata and Sarsia tubulosa, were frequently found as part of the diet of A. coerulea polyps and ephyrae. The utilization of high-throughput sequencing technique is a useful tool for studying the diet of polyps and ephyrae in the field, complementing the traditional techniques towards a better understanding of the complex role of gelatinous animals in marine ecosystems.

Aurelia coerulea  /  in situ  /  dietary analysis  /  feeding  /  high-throughput sequencing
Tingting Sun, Lei Wang, Jianmin Zhao, Zhijun Dong. Application of DNA metabarcoding to characterize the diet of the moon jellyfish Aurelia coerulea polyps and ephyrae[J]. Acta Oceanologica Sinica, 2021 , 40 (8) : 160 -167 . DOI: 10.1007/s13131-021-1800-8
Full Text
Less
1 Introduction
Less
The moon jellyfish Aurelia spp. is widely distributed in harbors, bays and coastal waters throughout the East Asian margin sea, the Mediterranean coast of France, the Atlantic, Australia, and the east coast of North America (Dawson et al., 2005; Dong et al., 2015; Scorrano et al., 2017). As many as 12 Aurelia species or subspecies been described previously (Dong, 2019), Aurelia sp.1 is now recognized as the previously recorded species A. coerulea (Scorrano et al., 2017), which is widely distributed in Chinese coastal waters (Dong et al., 2015). The high abundances reached during their frequent blooms can have negative influences on various coastal industries, including the coastal power plant industry, local fisheries and aquaculture (Purcell et al., 2013; Dong et al., 2014). Seawater temperature increases, eutrophication, and habitat modifications have been suggested as possible factors contributing to the blooms of A. coerulea in coastal waters (Dong et al., 2010; Purcell, 2012).
A. coerulea have the typical metagenetic life cycle characteristic of most scyphozoans, comprising alternate generations of asexual benthic polyps and sexual pelagic medusae (Arai, 1997). While the medusae are the “problematic” and conspicuous stage, the tiny, inconspicuous polyps play a key role in determining the times and intensity of blooms by producing and releasing ephyrae into the water column through a process known as strobilation. Therefore, factors controlling growth and mortality of polyps and ephyrae influence the magnitude of medusa blooms (e.g., Purcell et al., 2009; Han and Uye, 2010; Lucas et al., 2012).
Empirical evidence suggests that growth and mortality of polyps and ephyrae are influenced by a combination of factors, among which food plays a major role (Han and Uye, 2010; Kogovšek et al., 2010; Schiariti et al., 2014; Wang and Li, 2015). Production of new polyps significantly increases with increasing food availability in the blooming jellyfish Aurelia spp. (Han and Uye, 2010; Schiariti et al., 2014). Results from Wang and Li (2015) showed that abundant food conditions increase ephyrae survival rate and enhance individual development, and thus producing large populations of medusae. Therefore, knowledge of the diet of polyps and ephyrae is key to understanding the factors that affect medusae recruitment, the formation and magnitude of jellyfish blooms.
Adult Aurelia spp. have been well studied as a top-down controller within the classical food web, preying on crustacean zooplankton (e.g., Purcell and Sturdevant 2001; Titelman and Hansson, 2006; Uye, 2011; Riisgård and Madsen, 2011), and possibly also microplankton (Båmstedt, 1990; Graham and Kroutil, 2001; Purcell and Sturdevant, 2001; Uye and Shimauchi, 2005; Malej et al., 2007; Lo and Chen, 2008). However, studies dealing with the diet of polyps and ephyrae are much scarcer and most describe laboratory observations. It has been shown that polyps of A. coerulea can prey on copepods, molluscs, fish larvae, planulae, and phytoplankton (Gröndahl, 1988, 1989; Tsikhon-Lukanina et al., 1996; Östman, 1997; Kamiyama, 2013; Wang et al., 2015). Planktonic ciliates could also be part of the diet of polyps (Kamiyama, 2013). On the other hand, ephyrae of A. coerulea prey on mesozooplankton, microzooplankton and phytoplankton (Sullivan et al., 1997; Båmstedt et al., 2001). In addition, it has been demonstrated that A. labiata ephyrae possess the ability to assimilate and metabolize dissolved organic matter (Skikne et al., 2009). However, the dietary composition of the polyps and ephyrae in the field are largely unknown.
Traditionally, in situ dietary analysis of scyphozoans has been mainly conducted by microscopic examination of gastric contents (Graham and Kroutil, 2001; Purcell and Sturdevant, 2001; Uye and Shimauchi, 2005). However, microscopic examination of gastric contents has limitations, especially in the early life stages (e.g., polyps, ephyrae) due to their small size. Additionally, it is difficult to identify species from semi-digested fragments of marine organisms and ingested prey often lacks diagnostic taxonomic features (Pompanon et al., 2012).
To overcome these difficulties, high-throughput DNA sequencing has been employed extensively in the dietary analyses of bats, penguins, seals and fish (Deagle et al., 2010; Bohmann et al., 2011; Albaina et al., 2016; Su et al., 2018; Brassea-Pérez et al., 2019). In addition, this technique has been used to study the diets of larvae and has greatly enhanced the speed and resolution of the dietary analyses in the early life stages of marine organisms (O’Rorke et al., 2012, 2014; Hirai et al., 2017; Kodama et al., 2017). Therefore, the aim of this study was to reveal the dietary composition of A. coerulea polyps and ephyrae using for the first time the high-throughput DNA sequencing techniques.
2 Materials and methods
Less
2.1 Sample collection
Polyps and ephyrae of A. coerulea were collected from Fenghuang Lake, a coastal marine lake located in Shidao Bay on the southern Yellow Sea, China. It covers an area of 1.39 km2 and has an average depth of about 5 m. The dam of Fenghuang Lake is made of concrete. One intake valve and two emptying valves are used to exchange seawater with Shidao Bay (Fig. 1).
Polyps attached to the biogenic reefs formed by tubeworms Hydroides dianthus were collected by scuba divers in March 2016. Immediately after collection, the polyps were gently removed from the substrates using tweezers. Ephyrae were collected in April 2016 by gently trawling a standard plankton net (31.6 cm mouth diameter, 160 μm mesh size). To prevent change in the gut contents of A. coerulea polyps and ephyrae in the sampling progress, the polyp and ephyra samples were preserved on site immediately in sterile neutral Lugol’s solution at 2% final concentration (Hu et al., 2015). At the laboratory, 360 polyps and 360 ephyrae of A. coerulea were sorted using a wide-bore plastic pipette under an Olympus SZX10 stereomicroscope (Olympus Corporation, Tokyo, Japan). The sorted samples were carefully and thoroughly rinsed three times with autoclaved 0.22 μm filtered natural seawater and examined under a stereomicroscope to ensure that no other visible organisms were attached to the body. Thirty polyps and 30 ephyrae were preserved in one autoclaved tube each. Thirty individuals were required for each sample for DNA extraction due to the very small size and high water content of the polyps and ephyrae. In total, in order to maximise the number of prey species identified, 12 samples of polyps and 12 samples of ephyrae were analyzed. They were stored at −80°C after seawater was removed.
2.2 DNA extraction, amplification and sequencing
The polyp and ephyra samples were homogenized and incubated in lysis buffer for three days at 55°C to allow for thorough cell lysis. DNA was extracted following a modified CTAB protocol, and finally eluted in 50 mL of 10 mmol/L Tris-HCl (pH 8.0), as previously reported. Universal eukaryotic primers were used to target the V4 region of the 18S rDNA (528F: 5′-gcctccctcgcgccatcag-GCGGTAATTCCAGCTCCAA-3′; 706R: 5′-gccttgccagcccgctcag-AATCCRAGAATTTCACCTCT-3′). PCR amplification was carried out in a total volume of 30 µL, which contained 15 µL of Phusion High-Fidelity PCR Master Mix (New England Biolabs, Ipswich, MA, USA), 0.22 µmol/L of forward and reverse primers, and 10 ng of template DNA. Following the initial denaturation at 98°C for 1 min, the PCR conditions consisted of 30 cycles of denaturation at 98°C for 10 s, annealing at 50°C for 30 s, and elongation at 72°C for 5 min. The PCR products were purified with GeneJET Gel Extraction Kit (Thermo Fisher Scientific, Waltham, MA, USA) and pooled together at the same concentration prior to sequencing. Sequencing libraries were generated using Illumina Truseq DNA PCR-Free Library Preparation Kit (Illumina, San Diego, CA, USA). Libraries were sequenced on an Illumina HiSeq PE250 platform and 300 bp paired-end reads were generated.
2.3 Bioinformatic analyses
Paired-end reads from the original DNA fragments were merged using FLASH version 1.2.9 (Magoč and Salzberg, 2011) and assigned to each sample according to the unique barcodes. Sequence reads were filtered by QILME quality filters (Caporaso et al., 2010). Sequences with ≥97% similarity were assigned to the same operational taxonomic unit (OTU). Taxonomic assignments of the dominant sequence of each OTU were determined using RDP classifier. Only sequences that were found more than three times in one OTU were kept for further analysis. Sequence homology searches of GenBank were performed with ≥90% similarity level threshold. A phylogenetic tree was established for prey taxa with the neighbor-joining method in MEGA 5.0 (Ballard and Melvin, 2010), using the Tajima-Nei model with 1 000 bootstrap replications.
3 Results
Less
The total number of reads returned from the Illumina HiSeq PE250 platform was 2 087 983. Of these, 1 951 254 reads remained after initial sequence quality control. The average number of sequencing reads for each sample was 81 302±7 940 (mean±SD). A total of 88 718 sequencing reads were retained for further analysis after the removal of the predator sequences. Analysing the sequences against the GenBank database identified 19 prey species with V4 regions of the 18S rRNA which were 100% identical to sequences obtained from the A. coerulea polyps and ephyrae (Table 1).
Based on the next-generation-sequencing analysis (NGS), 44 prey taxa grouped in 10 phyla were recognized as part of the diet of A. coerulea polyps and ephyrae (Fig. 2, Table 1). Of these, 19 prey taxa were found in the A. coerulea ephyrae and 38 prey taxa were found in the A. coerulea polyps, with 13 prey taxa found both in polyps and ephyrae. Cnidaria, Arthropoda and Annelida were the most frequently observed phyla and Hydrozoa, Maxillopoda and Polychaeta were the most frequently observed classes in both the polyps and ephyrae of A. coerulea (Fig. 3a, Table 1). Filifera, Capitata and Harpacticoida were the most frequently observed orders in the polyps, while Calanoida, Capitata, Spionida and Filifera were the most frequently observed orders in the ephyrae (Fig. 3b, Table 1).
A. coerulea ephyrae mainly preyed on pelagic zooplankton, including copepods, hydromedusae and polychaetes (Table 1). The dominant prey taxa of A. coerulea ephyrae were copepods (Eurytemora pacifica), hydromedusae (Sarsia tubulosa and Rathkea octopunctata), and polychaetes (Pseudopolydora paucibranchiata) which accounted for 48%, 18%, 11% and 11% of the dietary contents, respectively. On the other hand, A. coerulea polyps fed on both planktonic and benthic prey, including hydromedusae, copepods, ciliates, polychaetes, stauromedusae, and phytoplankton (Table 1). The dominant prey taxa of A. coerulea polyps were two hydromedusae, R. octopunctata and S. tubulosa, which accounted for 60% and 18% of the dietary contents, respectively. The benthic preys including Thalestridae sp., Amphiascoides atopus, Amonardia sp., Haliclystus sp. were only found in the diets of A. coerulea polyps.
4 Discussion
Less
Traditional microscopic examination of gastric contents has limitations in determining the diet of scyphozoans, especially in the polyps and ephyrae stage due to their small size. Moreover, it is difficult to identify species from semi-digested fragments of marine organisms and ingested prey often lacks diagnostic taxonomic features. In the present study, the results show that high-throughput sequencing techniques can overcome these difficulties and identify individual prey species of A. coerulea polyps and ephyrae in situ in fine resolution. A. coerulea polyps and ephyrae consume a variety of prey items, including both mesozooplankton and micro-plankton.
Previous studies by direct observation of feeding in laboratory have shown that copepods, mollusc and fish larvae, planulae, planktonic ciliates and phytoplankton were preyed upon by the polyps of A. coerulea (Tsikhon-Lukanina et al., 1996; Östman, 1997; Kamiyama, 2013; Wang et al., 2015; Zheng et al., 2015). Few studies have examined the natural feeding ecology of polyps (Gröndahl, 1988; Tsikhon-Lukanina et al., 1996; Östman, 1997). In the few studies that report the natural diets of polyps, there appears to be low selectivity, as a great variety of zooplankton prey are consumed (Gröndahl, 1988; Tsikhon-Lukanina et al., 1996; Östman, 1997). Copepods, hydromedusae, polychaetes, phytoplankton and ciliophorans were detected, in the polyps of A. coerulea in situ, which is in accordance with the previous studies (e.g., Kamiyama, 2013; Wang et al., 2015). Although information about prey availability in the natural environment was not available, the diversity of prey taxa found in this paper confirms the low selectivity of Aurelia polyps. The observations agree with those of Tsikhon-Lukanina et al. (1996), who suggested that the polyps capture both planktonic prey species from the water column and benthic ones from the bottom.
A. coerulea polyps preyed on a more diverse range of species than ephyrae. A. coerulea ephyrae mainly prey on pelagic zooplankton, while A. coerulea polyps feed on both planktonic and benthic prey. Aurelia polyps are generally attached to shells, rocks or artificial structures (Duarte et al., 2013). Therefore, the polyps of A. coerulea could prey on benthic organisms (e.g., benthic copepods, Stauromedusae, Ascidiacea). In addition, zooplankton would be preyed upon when they move close to the polyps due to the characters of diurnal vertical migration or vertical mixing of the water column. Some algae and unidentified particulate organic matter have previously been found to be part of the diet of Aurelia polyps (Tsikhon-Lukanina et al., 1996; Östman, 1997). In accordance with these studies, some microalgae and fungi were detected in the diet of A. coerulea polyps. The possibility that these microalgae and fungi were ingested by the polyps’ prey, such as copepods, cannot be excluded. Once again, further studies are needed in order to comprehend the feeding strategies of Aurelia and its variations through the ontogeny. More recently, it has been shown that planktonic ciliates serve as a food source for growth at the ephyra stage of Aurelia spp. (Zoccarato et al., 2016; Kamiyama, 2018). Ciliates, Pseudovorticella sp.1 were detected in the ephyrae of A. coerulea in situ, which is in accordance with the direct observation of feeding in laboratory studies. Little is known about the mechanisms driving prey selectivity in scyphozoan polyps. Prey of scyphozoan polyps is captured and transported to the mouth by the tentacles. In addition, currents also pass up the column carrying mucus and particles to the tips of the tentacles. Meanwhile, the scyphozoan polyps are sessile and non-visual predators, it is an advantage to be able to feed more diverse types of prey they encountered and contacted.
Interestingly, hydromedusae were the most frequently occurring prey items found in A. coerulea polyps and ephyrae. Consumption of gelatinous prey by adult scyphozoans is a common phenomenon and is widely described in various taxa including Aurelia (Purcell, 1997; Bayha and Dawson, 2010). However, the diet of polyps and ephyrae is probably distinct from that of adults since ontogenetic diet shifts have been described in some species (Graham and Kroutil, 2001), or at least the way that food is captured surely changes according to the morphological changes that occur during the ontogeny (Costello et al., 2008; Carrizo et al., 2016). Adult medusae utilize bell pulsations to generate vortices that transport fluids and prey toward oral arms. However, small ephyrae live within a fluid regime where transporting prey by feeding currents is inefficient (Higgins III et al., 2008). Therefore, the capacity of an ephyra to feed on very sensitive and fast-moving prey, such as copepods, is limited (Sullivan et al., 1997). Studies of gut contents of field collected Aurelia spp. ephyrae have demonstrated that copepods and copepod nauplii are unimportant food sources, even when they are dominant in the plankton. On the other hand, slow-moving prey items (e.g., small ctenophores and hydromedusae) may be easy to catch as they do not attempt to resist capture as energetically as crustacean plankton (Östman, 1997; Sullivan et al., 1997). In addition, high abundance of hydromedusae in the field at the time of collection might explain this high percentage.
Increasing evidence suggests that gelatinous organisms are preyed upon by other marine animals and might also play an important role in the marine pelagic food web (Cardona et al., 2012; Huang, 2013; Jarman et al., 2013; Cardona et al., 2015; Carrizo et al., 2016; McInnes et al., 2017; Thiebot et al., 2017). For example, hydromedusae (R. octopunctata and Clytia hemisphaerica) were the dominant prey species in the two copepods Calanus sinicus and Acartia pacifica from the Yellow Sea and Bohai Sea (Huang, 2013). Cotylorhiza tuberculata and Pelagia noctiluca were the most important species in the diets of swordfish, tuna and turtles from the Western Mediterranean Sea (Cardona et al., 2012). DNA analyses estimated that a substantial portion of the diet of Adélie penguins in the Southern Ocean was made up of groups such as hydromedusae, scyphomedusae, and cubomedusae (Jarman et al., 2013). Sardines from the Western Mediterranean Sea fed predominantly on P. noctiluca (Cardona et al., 2015). McInnes et al. (2017) showed that scyphozoan jellyfish were a common prey of black-browed and Campbell albatross. Recently, Thiebot et al. (2017) used animal-borne video data loggers to record direct observations of predation and revealed that all four species of penguins across the southern oceans prey on jellyfish.
In the present study, the V4 region of the 18S rRNA was amplified from whole specimens of A. coerulea polyps and ephyrae, due to the difficulties in isolating gut contents from the small and fragile polyps and ephyrae. Therefore, the amplified predator sequences accounted for the majority of these fragment data sets. In this study, over 45% of prey sequences were accurately identified to the species level and the majority of prey sequences were identified to the genus level. Therefore, the V4 region of the 18S rRNA was able to identify individual prey species of A. coerulea polyps and ephyrae in situ to an acceptable level of resolution. The use of this region has limitations and is not as specific as those found in mitochondria. For instance, high-throughput DNA sequencing using short mtCOI fragments was recently able to accurately identify over 95% of prey sequences to the species level (Su et al., 2018). However, potential priming sites of these barcodes would not be conserved enough to cover a broad range of taxa, probably leading to a failure or a low rate of amplification (Ficetola et al., 2010). Therefore, further studies are needed to combine a DNA barcode with a broad taxonomic coverage with other DNA barcodes that resolve some of the higher taxonomic units to species level.
5 Conclusion
Less
This study reveals the dietary composition of A. coerulea polyps and ephyrae in the field using the high-throughput DNA sequencing technique. The results show that A. coerulea polyps and ephyrae consume a variety of prey items. A. coerulea polyps consume both planktonic and benthic prey, including hydromedusae, copepods, ciliates, polychaetes, stauromedusae, and phytoplankton. A. coerulea ephyrae mainly feed on plankton, including copepods and hydromedusae. Hydromedusae were the most frequently occurring prey item found in both polyps and ephyrae. The high-throughput sequencing technique is a useful tool for studying the diet of polyps and ephyrae in the field, complementing the traditional techniques to produce a better understanding of the complex role of gelatinous animals in marine ecosystems. Further studies are needed to examine the temporal and geographical variations in the dietary composition of A. coerulea and their environmental plankton communities using the high-throughput sequencing technique.
Acknowledgements
Less
We would like to acknowledge the valuable comments and suggestions of Agustin Schiariti in Instituto Nacional de Investigación y Desarrollo Pesquero. We also appreciate all the foundation items that supported this research.
Funding
Less
  • The National Key Research and Development Program of China under contract No. 2018YFC1406501; the Strategic Priority Research Program of the Chinese Academy of Sciences under contract No. XDA23050301; the National Natural Science Foundation of China under contract No. 41876138; the Instrument Developing Project of the Chinese Academy of Sciences under contract No. YJKYYQ20180047; the Key Research and Development Program of Yantai under contract No. 2018ZHGY073.
References
Less
Albaina A, Aguirre M, Abad D, et al. 2016. 18S rRNA V9 metabarcoding for diet characterization: a critical evaluation with two sympatric zooplanktivorous fish species. Ecology and Evolution, 6(6): 1809–1824, doi: 10.1002/ece3.1986
Arai M N. 1997. A Functional Biology of Scyphozoa. London, UK: Chapman & Hall, 58–91
Ballard J W O, Melvin R G. 2010. Linking the mitochondrial genotype to the organismal phenotype. Molecular Ecology, 19(8): 1523–1539, doi: 10.1111/j.1365-294X.2010.04594.x
Båmstedt U. 1990. Trophodynamics of the scyphomedusae Aurelia aurita. Predation rate in relation to abundance, size and type of prey organism. Journal of Plankton Research, 12(1): 215–229, doi: 10.1093/plankt/12.1.215
Båmstedt U, Wild B, Martinussen M. 2001. Significance of food type for growth of ephyrae Aurelia aurita (Scyphozoa). Marine Biology, 139(4): 641–650, doi: 10.1007/s002270100623
Bayha K M, Dawson M N. 2010. New family of allomorphic jellyfishes, Drymonematidae (Scyphozoa, Discomedusae), emphasizes evolution in the functional morphology and trophic ecology of gelatinous zooplankton. The Biological Bulletin, 219(3): 249–267, doi: 10.1086/BBLv219n3p249
Bohmann K, Monadjem A, Noer C L, et al. 2011. Molecular diet analysis of two African free-tailed bats (Molossidae) using high throughput sequencing. PLoS ONE, 6(6): e21441, doi: 10.1371/journal.pone.0021441
Brassea-Pérez E, Schramm Y, Heckel G, et al. 2019. Metabarcoding analysis of the Pacific harbor seal diet in Mexico. Marine Biology, 166(8): 106, doi: 10.1007/s00227-019-3555-8
Caporaso J G, Kuczynski J, Stombaugh J, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336, doi: 10.1038/nmeth.f.303
Cardona L, de Quevedo I Á, Borrell A, et al. 2012. Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS ONE, 7(3): e31329, doi: 10.1371/journal.pone.0031329
Cardona L, Martínez-Iñigo L, Mateo R, et al. 2015. The role of sardine as prey for pelagic predators in the western Mediterranean Sea assessed using stable isotopes and fatty acids. Marine Ecology Progress Series, 531: 1–14, doi: 10.3354/meps11353
Carrizo S S, Schiariti A, Nagata R M, et al. 2016. Preliminary observations on ephyrae predation by Lychnorhiza lucerna medusa (Scyphozoa; Rhizostomeae). Der Zoologische Garten, 85(1–2): 74–83, doi: 10.1016/j.zoolgart.2015.09.011
Cavalier-Smith T. 1998. A revised six-kingdom system of life. Biological Reviews of the Cambridge Philosophical Society, 73: 203–266, doi: 10.1017/s0006323198005167
Costello J H, Colin S P, Dabiri J O. 2008. Medusan morphospace: phylogenetic constraints, biomechanical solutions, and ecological consequences. Invertebrate Biology, 127(3): 265–290, doi: 10.1111/j.1744-7410.2008.00126.x
Dawson M N, Gupta A S, England M H. 2005. Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. Proceedings of the National Academy of Sciences of the United States of America, 102(34): 11968–11973, doi: 10.1073/pnas.0503811102
Deagle B E, Chiaradia A, McInnes J, et al. 2010. Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out?. Conservation Genetics, 11(5): 2039–2048, doi: 10.1007/s10592-010-0096-6
Dong Zhijun. 2019. Blooms of the moon jellyfish Aurelia: causes, consequences and controls. In: Sheppard C, ed. World Seas: An Environmental Evaluation. 2nd ed. Amsterdam, the Netherlands: Elsevier, 163–171, doi: 10.1016/B978-0-12-805052-1.00008-5
Dong Zhijun, Liu Dongyan, Keesing J K. 2010. Jellyfish blooms in China: dominant species, causes and consequences. Marine Pollution Bulletin, 60(7): 954–963, doi: 10.1016/j.marpolbul.2010.04.022
Dong Zhijun, Liu Dongyan, Keesing J K. 2014. Contrasting trends in populations of Rhopilema esculentum and Aurelia aurita in Chinese waters. In: Pitt K A, Lucas C H, eds. Jellyfish Blooms. Dordrecht, the Netherlands: Springer, 207–218, doi: 10.1007/978-94-007-7015-7_9
Dong Zhijun, Liu Zhongyuan, Liu Dongyan. 2015. Genetic characterization of the scyphozoan jellyfish Aurelia spp. in Chinese coastal waters using mitochondrial markers. Biochemical Systematics and Ecology, 60: 15–23, doi: 10.1016/j.bse.2015.02.018
Duarte C M, Pitt K A, Lucas C H, et al. 2013. Is global ocean sprawl a cause of jellyfish blooms?. Frontiers in Ecology and the Environment, 11(2): 91–97, doi: 10.1890/110246
Ficetola G F, Coissac E, Zundel S, et al. 2010. An In silico approach for the evaluation of DNA barcodes. BMC Genomics, 11: 434, doi: 10.1186/1471-2164-11-434
Graham W M, Kroutil R M. 2001. Size-based prey selectivity and dietary shifts in the jellyfish, Aurelia aurita. Journal of Plankton Research, 23(1): 67–74, doi: 10.1093/plankt/23.1.67
Gröndahl F. 1988. Interactions between polyps of Aurelia aurita and planktonic larvae of scyphozoans: an experimental study. Marine Ecology-Progress Series, 45: 87–93, doi: 10.3354/meps045087
Gröndahl F. 1989. Evidence of gregarious settlement of planula larvae of the scyphozoan Aurelia aurita: an experimental study. Marine Ecology-Progress Series, 56: 119–125, doi: 10.3354/meps056119
Han C H, Uye S I. 2010. Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita s.l. Plankton and Benthos Research, 5(3): 98–105, doi: 10.3800/pbr.5.98
Higgins III J E, Ford M D, Costello J H. 2008. Transitions in morphology, nematocyst distribution, fluid motions, and prey capture during development of the scyphomedusa Cyanea capillata. The Biological Bulletin, 214(1): 29–41, doi: 10.2307/25066657
Hirai J, Hidaka K, Nagai S, et al. 2017. Molecular-based diet analysis of the early post-larvae of Japanese sardine Sardinops melanostictus and Pacific round herring Etrumeus teres. Marine Ecology Progress Series, 564: 99–113, doi: 10.3354/meps12008
Hu Simin, Guo Zhiling, Li Tao, et al. 2015. Molecular analysis of in situ diets of coral reef copepods: evidence of terrestrial plant detritus as a food source in Sanya Bay, China. Journal of Plankton Research, 37(2): 363–371, doi: 10.1093/plankt/fbv014
Huang Yousong. 2013. PCR-based in situ dietary analysis of two common copepods in Bohai Sea and Yellow Sea coastal waters (in Chinese)[dissertation]. Qingdao: Ocean University of China
Jarman S N, McInnes J C, Faux C, et al. 2013. Adélie penguin population diet monitoring by analysis of food DNA in scats. PLoS ONE, 8(12): e82227, doi: 10.1371/journal.pone.0082227
Kamiyama T. 2013. Planktonic ciliates as food for the scyphozoan Aurelia aurita (s.l.): effects on asexual reproduction of the polyp stage. Journal of Experimental Marine Biology and Ecology, 445: 21–28, doi: 10.1016/j.jembe.2013.03.018
Kamiyama T. 2018. Planktonic ciliates as food for the scyphozoan Aurelia coerulea: feeding and growth responses of ephyra and metephyra stages. Journal of Oceanography, 74: 53–63, doi: 10.1007/s10872-017-0438-9
Kodama T, Hirai J, Tamura S, et al. 2017. Diet composition and feeding habits of larval Pacific bluefin tuna Thunnus orientalis in the Sea of Japan: integrated morphological and metagenetic analysis. Marine Ecology Progress Series, 583: 211–226, doi: 10.3354/meps12341
Kogovšek T, Bogunović B, Malej A. 2010. Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series. Hydrobiologia, 645: 81–96, doi: 10.1007/s10750-010-0217-8
Lo W T, Chen I L. 2008. Population succession and feeding of scyphomedusae, Aurelia aurita, in a eutrophic tropical lagoon in Taiwan. Estuarine, Coastal and Shelf Science, 76(2): 227–238, doi: 10.1016/j.ecss.2007.07.015
Lucas C H, Graham W M, Widmer C. 2012. Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Advances in Marine Biology, 63: 133–196, doi: 10.1016/b978-0-12-394282-1.00003-x
Magoč T, Salzberg S L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21): 2957–2963, doi: 10.1093/bioinformatics/btr507
Malej A, Turk V, Lučić D, et al. 2007. Direct and indirect trophic interactions of Aurelia sp. (Scyphozoa) in a stratified marine environment (Mljet Lakes, Adriatic Sea). Marine Biology, 151(3): 827–841, doi: 10.1007/s00227-006-0503-1
McInnes J C, Alderman R, Lea M A, et al. 2017. High occurrence of jellyfish predation by black-browed and Campbell albatross identified by DNA metabarcoding. Molecular Ecology, 26(18): 4831–4845, doi: 10.1111/mec.14245
O’Rorke R, Lavery S, Chow S, et al. 2012. Determining the diet of larvae of western rock lobster (Panulirus cygnus) using high-throughput DNA sequencing techniques. PLoS ONE, 7(8): e42757, doi: 10.1371/journal.pone.0042757
O’Rorke R, Lavery S D, Wang M, et al. 2014. Determining the diet of larvae of the red rock lobster (Jasus edwardsii) using high-throughput DNA sequencing techniques. Marine Biology, 161(3): 551–563, doi: 10.1007/s00227-013-2357-7
Östman C. 1997. Abundance, feeding behaviour and nematocysts of scyphopolyps (Cnidaria) and nematocysts in their predator, the nudibranch Coryphella verrucosa (Mollusca). Hydrobiologia, 355(1): 21–28, doi: 10.1023/A:1003065726381
Pompanon F, Deagle B E, Symondson W O C, et al. 2012. Who is eating what: diet assessment using next generation sequencing. Molecular Ecology, 21(8): 1931–1950, doi: 10.1111/j.1365-294x.2011.05403.x
Purcell J E. 1997. Pelagic cnidarians and ctenophores as predators: selective predation, feeding rates and effects on prey populations. Annales de l'Institute Oceanographique, 73(2): 125–137
Purcell J E. 2012. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annual Review of Marine Science, 4: 209–235, doi: 10.1146/annurev-marine-120709-142751
Purcell J E, Baxter E J, Fuentes V. 2013. Jellyfish as products and problems of aquaculture. In: Allan G, Burnell G, eds. Advances in Aquaculture Hatchery Technology. Cambridge, UK: Woodhead Publishing, 404–430, doi: 10.1533/9780857097460.2.404
Purcell J E, Hoover R A, Schwarck N T. 2009. Interannual variation of strobilation by the scyphozoan Aurelia labiata in relation to polyp density, temperature, salinity, and light conditions in situ. Marine Ecology Progress Series, 375: 139–149, doi: 10.3354/meps07785
Purcell J E, Sturdevant M V. 2001. Prey selection and dietary overlap among zooplanktivorous jellyfish and juvenile fishes in Prince William Sound, Alaska. Marine Ecology Progress Series, 210: 67–83, doi: 10.3354/meps210067
Riisgård H U, Madsen C V. 2011. Clearance rates of ephyrae and small medusae of the common jellyfish Aurelia aurita offered different types of prey. Journal of Sea Research, 65(1): 51–57, doi: 10.1016/j.seares.2010.07.002
Schiariti A, Morandini A C, Jarms G, et al. 2014. Asexual reproduction strategies and blooming potential in Scyphozoa. Marine Ecology Progress Series, 510: 241–253, doi: 10.3354/meps10798
Scorrano S, Aglieri G, Boero F, et al. 2017. Unmasking Aurelia species in the Mediterranean Sea: an integrative morphometric and molecular approach. Zoological Journal of the Linnean Society, 180(2): 243–267, doi: 10.1111/zoj.12494
Skikne S A, Sherlock R E, Robison B H. 2009. Uptake of dissolved organic matter by ephyrae of two species of scyphomedusae. Journal of Plankton Research, 31(12): 1563–1570, doi: 10.1093/plankt/fbp088
Su Maoliang, Liu Huifen, Liang Xuemei, et al. 2018. Dietary analysis of marine fish species: enhancing the detection of prey-specific DNA sequences via high-throughput sequencing using blocking primers. Estuaries and Coasts, 41(2): 560–571, doi: 10.1007/s12237-017-0279-1
Sullivan B K, Suchman C L, Costello J H. 1997. Mechanics of prey selection by ephyrae of the scyphomedusa Aurelia aurita. Marine Biology, 130(2): 213–222, doi: 10.1007/s002270050241
Thiebot J B, Arnould J P Y, Gómez-Laich A, et al. 2017. Jellyfish and other gelata as food for four penguin species-insights from predator-borne videos. Frontiers in Ecology and the Environment, 15(8): 437–441, doi: 10.1002/fee.1529
Titelman J, Hansson L J. 2006. Feeding rates of the jellyfish Aurelia aurita on fish larvae. Marine Biology, 149(2): 297–306, doi: 10.1007/s00227-005-0200-5
Tsikhon-Lukanina E A, Reznichenko O G, Lukasheva T A. 1996. Food consumption by scyphistomae of the jellyfish Aurelia aurita in the Black Sea. Oceanology, 35(6): 815–818
Uye S I. 2011. Human forcing of the copepod-fish-jellyfish triangular trophic relationship. Hydrobiologia, 666(1): 71–83, doi: 10.1007/s10750-010-0208-9
Uye S, Shimauchi H. 2005. Population biomass, feeding, respiration and growth rates, and carbon budget of the scyphomedusa Aurelia aurita in the Inland Sea of Japan. Journal of Plankton Research, 27(3): 237–248, doi: 10.1093/plankt/fbh172
Wang Nan, Li Chaolun. 2015. The effect of temperature and food supply on the growth and ontogeny of Aurelia sp. 1 ephyrae. Hydrobiologia, 754(1): 157–167, doi: 10.1007/s10750-014-1981-7
Wang Yantao, Zheng Shan, Sun Song, et al. 2015. Effect of temperature and food type on asexual reproduction in Aurelia sp. 1 polyps. Hydrobiologia, 754(1): 169–178, doi: 10.1007/s10750-014-2020-4
Zheng Shan, Sun Xiaoxia, Wang Yantao, et al. 2015. Significance of different microalgal species for growth of moon jellyfish ephyrae, Aurelia sp.1. Journal of Ocean University of China, 14(5): 823–828, doi: 10.1007/s11802-015-2775-x
Zoccarato L, Celussi M, Pallavicini A, et al. 2016. Aurelia aurita ephyrae reshape a coastal microbial community. Frontiers in Microbiology, 7: 749, doi: 10.3389/fmicb.2016.00749
Appendix
Less
Year 2021 volume 40 Issue 8
PDF
108
58
Cite this Article
BibTeX
Article Info
doi: 10.1007/s13131-021-1800-8
  • Receive Date：2020-03-16
  • Online Date：2026-03-05
  • Published：2021-08-25
Article Data
Affiliations
History
  • Received：2020-03-16
  • Accepted：2020-11-25
Funding
The National Key Research and Development Program of China under contract No. 2018YFC1406501; the Strategic Priority Research Program of the Chinese Academy of Sciences under contract No. XDA23050301; the National Natural Science Foundation of China under contract No. 41876138; the Instrument Developing Project of the Chinese Academy of Sciences under contract No. YJKYYQ20180047; the Key Research and Development Program of Yantai under contract No. 2018ZHGY073.
Affiliations
    1 Muping Coastal Environment Research Station, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai 264003, China
    2 University of Chinese Academy of Sciences, Beijing 100049, China
    3 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China

Corresponding:

References
Share
https://castjournals.cast.org.cn/joweb/aos/EN/10.1007/s13131-021-1800-8
Share to
QR

Scan QR to access full text

Cite this article
BibTeX
Citations
表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
关闭全屏
  • BibTeX
  • EndNote
  • RefWorks
  • TxT
Links
Articles
Latest Articles
Most Read
Collections
Updates
Events
News
Multimedia
About
About Us
Contact
No. 86 Xueyuan South Road, Haidian District, Beijing
100081
010-62199257
qkjq@cast.org.cn

Copyright © 2025 China Association for Science and Technology. All rights reserved. For all open access content, the relevant licensing terms apply.
Sponsored by the Office of the Leading Group for Cybersecurity and Informatization of CAST, and supported by Science and Technology Review Publishing House