Abstract
Outbreaks of scyphozoan Aurelia coerulea and Nemopilema nomurai in the coastal sea of China are managed in recent years because they have severely jeopardized local socioeconomic development and ecological health. In this study, we propose specific strategies to control these blooms based on the different physio-ecological characteristics of their polyps, which can produce medusae by strobilation. High densities of A. coerulea polyps can survive chronically on the surfaces of some artificial constructions submerged in harbors or bays, China. Through buddings, they can resist the invasion of biofouling organisms and proliferate on the surfaces of some fouling organisms (e.g., ascidians, and bryozoans). However, N. nomurai polyps have not been recorded in natural environment. The in situ experiments found that polyps on settling plates fail to survive via podocysts due to severe biofouling invasion and post-strobilated degeneration in late spring and summer. As a result, the population size following is strongly dependent on the sexual recruitment of medusae during late summer and autumn. Therefore, we suggest that the reasonable governance strategy is to manage polyp populations together with biofouling organisms for A. coerulea blooms, however, with a focus on the medusa stage (particularly young medusae) to decrease the sexual reproduction in N. nomurai blooms. Accordingly, massive occurrences of A. coerulea in Qingdao Middle Port, China were alleviated by eliminating polyps and biofouling organisms on the undersurfaces of floating docks and then brushing the surfaces with modified alloprene paints. Some applicable control measures, including resource utilization of N. nomurai medusae and more severe and earlier summer fishing moratoriums, were used to possibly help restrain outbreaks of N. nomurai in Chinese coastal waters.
Introduction
In recent decades, frequent jellyfish blooms around the globe have had detrimental ecological and socioeconomic nuisance such as stinging bathers, clogging the cooling water intakes of coastal power plants, disturbing normal fishery production, as well as threatening fishery resources (; ). Jellyfish blooms have been frequently claimed to result from anthropogenic disturbances to the coastal environment including climate change, eutrophication, overfishing, development of aquaculture, and habitat modification (; ; ; ), although robust evidence supporting these assertions is lacking (). The Chinese coastal waters are also one of the jellyfish blooming hotspots, where the outbreaks of Aurelia coerulea von Lendenfeld, 1884 () and Nemopilema nomurai Kishinouye, 1922 () have frequently appeared in the last two decades (; ).
A. coerulea occurs mainly in neritic regions, such as harbors and bays, along the Chinese coast (; Zheng et al., 2014; ). Frequent outbreaks of A. coerulea had damaged the normal operation of coastal infrastructures and the development of shallow sea aquaculture. In July 2014, a massive aggregation of A. coerulea clogged the cooling water intake of the Hong Yanhe nuclear power plant, Liaoning (Figure 1), causing the outage of two reactors (). The biomass of medusae salvaged around the cooling water intake was >10 tons in just 1 week (). The clogging cases of the cooling water intakes resulting from medusa aggregations also frequently occurred in several coal-fired power plants located in Qingdao and Qin Huangdao, China (). For example, a serious clog appearing in the Qingdao power plant threatened the normal power supply of partial areas in July 2009 (Ren, 2009). Recently, outbreaks of A. coerulea have also occurred in many artificial sea cucumber culture ponds along the Bohai and Yellow seas (e.g., in Laoting, Dongying, and Rongcheng, Figure 1), which have been regarded as the cause of sea cucumber vomiting because ephyrae could sting them (; ). In addition, A. coerulea blooms might also affect the community structure of zooplankton. In the northern Jiaozhou Bay, A. coerulea medusae frequently appeared in great numbers in June and July () when the abundance of total zooplankton (except Noctiluca scintillans), in particular, copepods significantly decreased in 2009, a year with a large bloom of A. coerulea, in comparison with 2008 and 2010, which were non-blooming years ().
Figure 1
N. nomurai is considered as a long-distance transport species (), distributed in East Asian marginal seas (; Yoon et al., 2014; ; ; ). Its blooms (medusa abundance ≥1 ind·100m−2) occurred in 5 out of 10 years from 2000 to 2009 in the southern Yellow Sea (sYS) and northern East China Sea (nECS), but have been relatively modest from 2010 to 2019 (; Zhao et al., 2016; ). The bloom only appeared in 2012, and no blooms (medusa abundance <1 ind·100m−2) occurred in the other years. However, the published total hospital-based records of N. nomurai stings have increased more than threefold since 2012 in Qingdao, Weihai, and Qin Huangdao (>7331 cases) in comparison with that before 2007 (about 1950 cases) (; ; ; ). In Liaodong Bay, Bohai Sea, N. nomurai also seriously threatened the Hong Yanhe nuclear power plant, with the maximal catches of medusae near its cooling water intakes reaching 986-1160 kg·h-1 per net in August 2015 (Zhang et al., 2019). Similar to reports from Japanese and Korean waters (; Yoon et al., 2008; ), the outbreaks of N. nomurai have also negatively affected fishery production in the coastal sea of China by clogging and destroying nets, decreasing fish catches, increasing the amount of labor required to select fish, and stinging fishermen (; Zheng et al., 2014). In addition, frequent N. nomurai blooms might influence phytoplankton and micro-zooplankton communities as well as fishery stocks. For example, in June 2012 (a blooming year with medusa abundance ≥1 ind·100m−2), in the southern sYS, the size compositions of ciliates, the dominant group of micro-zooplankton, tended to be smaller at the mature stage (i.e., the period that N. nomurai biomass increased to more than 10 t·km−2) than at the developing stage (i.e., the period that N. nomurai biomass was less than 10 t·km−2) of N. nomurai blooms, while the phytoplankton compositions shifted to be fewer diatoms and cryptophytes but more dinoflagellates (). In N. nomurai-dense regions of the nECS, the number of fish species and catch per unit effort (CPUE) declined in summer 2003 (a blooming year with medusa abundance ≥1 ind·100m−2) compared to 1999-2001 (non-blooming years with medusa abundance <1 ind·100m−2) ().
In order to reduce economic losses and harm to humans, jellyfish blooms have been actively addressed in many areas in recent years. The early warning measures had been widely reported to indirectly relieve the adverse effects of jellyfish blooms. For example, in the Mediterranean coast, the Medjellyrisk Project created a western and central Mediterranean Basin forecasting platform to foresee the probability of a jellyfish bloom arising based on stranded and near-to-coast jellyfish presence data from Spain, Italy, Tunisia, and Malta in combination with Species Distribution Model (). It was accessible through a free downloadable mobile app (Medjelly) and the project’s webpage, which could help warn beach users of the risk of stings. On the Great Barrier Reef, Australia, blooms of Irukandji jellyfish were forecast based on wind conditions, which largely coincide with relaxation of the prevailing southeasterly trade winds (). To alleviate the damages of N. nomurai blooms to Japanese fishery production, developed a method of forecasting the annual blooming intensity of N. nomurai in Japan based on on-deck sighting surveys from ferries en route from the sYS and nECS to the Sea of Japan in July. This blooming forecast effectively helps fishermen prepare for possible jellyfish encounters well in advance ().
Comparatively speaking, jellyfish blooms have also been directly controlled by some affected enterprises. For instance, to address the threat of large jellyfish aggregations (e.g., Chrysaora hysoscella) on salmon aquaculture, the bubble curtains were made by releasing compressed air from a perforated tube at depth, forming a plume of bubbles that entrain the water to create a vertical current as the jellyfish barriers in Ireland (). To prevent clogging caused by jellyfish aggregations in cooling water intakes, some local power plants in Japan have built structures such as arresting barriers, channel networks, jellyfish conveyers, and crushers to intercept and channel the influx of massive medusae and facilitate the removal of the entrapped medusae (). For the sake of reducing economic losses from A. coerulea blooms in Korean coastal areas, waterjets and scrapers have been used to remove A. coerulea polyps since 2012. This approach decreased the appearance of medusae in Lake Shihwa for 3 consecutive years (). To reduce the bycatches of N. nomurai in the Japanese fishery production, various jellyfish excluders such as a bottom trawl fishing gear with an intercepting net and a vent in its main net have been applied (; ). In particular, during the months of the densest N. nomurai aggregations (October-December) in 2009, some modified set nets, consisting of leading nets with an enlarged mesh size, bypass nets, and a partition net, were also introduced to effectively remove entrapped N. nomurai medusae (usually less than a hundred medusae were trapped per net per day) in fish catches (). On the whole, various control methods have been used to reduce the impacts of jellyfish blooms. But most of them adopted a strategy of disposing of easily-visible medusae, and few were involved in the other stages of jellyfish life cycle with interspecific specificity. In the coastal sea of China, the management of A. coerulea and N. nomurai blooms has also been carried out accompanied by recent studies on the blooming mechanisms to improve the ecological environment inshore and alleviate the economic losses resulting from such blooms. In this review, we suggest specific control strategies based on the different physio-ecological characteristics of their polyps in the life cycles and discuss some current control measures in China.
Specific control strategies
The controls of jellyfish blooms first need to take into account the jellyfish-centered mechanisms of the outbreaks. The life cycle of scyphozoans is characterized by generational alternation, involving a sexually reproducing medusa and an asexually reproducing benthic polyp (). The polyp is the key stage that could produce medusae through strobilation to realize the transformation from benthic to pelagic living (). A. coerulea polyps are found most often on the surfaces of some artificial substrates (e.g., floating docks, concrete platforms) submerged in the harbors and bays along the Chinese coasts (; ), as is the case in other regions (; ; ; ). However, N. nomurai polyps have not yet been recorded, although the areas around estuaries, such as the Changjiang estuary and innermost estuaries of northern Liaodong Bay, are considered to be the major habitats of N. nomurai polyps according to the recorded appearances of early pelagic N. nomurai larvae (i.e., ephyrae, metephyrae and juvenile medusae; ; Yoon et al., 2014; ; ).
On the other hand, A. coerulea and N. nomurai polyps show different asexual reproduction modes and ecophysiological responses to environmental changes including temperature, food supply, and biofouling invasion in the natural environment (; ; ; ), despite both generally having to grow and settle on the surfaces of hard substrates (; ). A. coerulea polyps have multiple asexual modes for propagation (). They are able to produce podocysts under starvation conditions (; ), and multiply rapidly via various buddings at warm temperatures (≥18°C) and abundant food supply (). However, polyps of N. nomurai only proliferate asexually through podocysts (; ; ). Under identical temperature and food conditions, polyps with multiple asexual modes could proliferate to higher densities compared with mono-mode polyps (). Moreover, through buddings, A. coerulea polyps on the substrates can expand to spaces not occupied by neighboring biofouling organisms (Figure 2A) and even proliferate on the surfaces of some fouling organisms against their invasion (; ). For example, on the undersurface of a floating dock “Haiou” in Jiaozhou Bay, China, A. coerulea polyps were found to grow on the surfaces of many ascidians, bryozoans, and mussels (e.g., Styela clava, Watersipora subtorquata, and Mytilus galloprovincialis) besides on the areas without macro-fouling organisms (Figures 2B-E) like some other Aurelia spp. (; ; ). However, in situ N. nomurai polyps on the plastic plates cultivated in Jiaozhou Bay were gradually covered by some neighboring fouling organisms (Figure 2F, ; ). Ultimately, they could not survive in the combination of severe biofouling invasion and post-strobilated degeneration in late spring and summer (; ; ). Thus, the polyp population following strongly depended on the sexual recruitment of medusae in late summer and autumn (; ). These different ecophysiological characteristics indicate that the focus of A. coerulea bloom control should be on polyps and biofouling organisms, whereas the focus of N. nomurai bloom control should be on medusae (particularly young medusae) to decrease the sexual reproduction rate.
Figure 2
Control case of A. coerulea blooms in Qingdao middle port harbor
The coastal industries, such as nuclear power plants, in China, have generally addressed local population explosions of A. coerulea by establishing a series of barrier nets and capturing medusae. Recently, the control of A. coerulea blooms by managing A. coerulea polyps and biofouling organisms was successfully conducted in Qingdao Middle Port harbor, China (Figures 3A, B; ), where A. coerulea frequently appeared in large numbers from June to July in recent decade (). In 2014, dense A. coerulea polyp colonies were found inhabiting the undersides of some docks at a depth of about 1.8m in Qingdao Middle Port (), indicating that these docks are one of the sources of medusa blooms there.
Figure 3
On the undersurfaces of these floating docks, A. coerulea polyps settled on some areas without macro-fouling organisms as well as on the body surfaces of some fouling organisms (e.g., ascidians, bryozoans, and mussels) (). Two docks (I, II) were the main polyp hotspots, where the average density of polyps reached 2634.63 ± 490.20 ind·m–2 in June 2014 (; Figure 3B). Thus, both docks were selected for the control of A. coerulea blooms in the harbor. Docks I and II were transferred to a nearby shipyard in early April 2015 and 2016, respectively, to avoid the release of massive A. coerulea ephyrae. A. coerulea polyps and biofouling organisms on the undersurfaces of both docks were scraped away completely. Then the modified paint manufactured by the Yantai federal chemical company, China, consisting of alloprene, plasticizer, cuprous oxide, and pigment, was brushed on the undersurface of the dock I in three layers at a thickness of 50-75 μm (). Dock II was left untreated as a control group. After being sun-dried, both docks were then returned to their original positions in July 2015 and 2016, respectively ().
From June 2015 to June 2018, the abundance of A. coerulea medusae observed near the seawater surface in the Qingdao Middle Port declined dramatically by 66–81% compared with 2014, reaching its lowest value in 2017 (; Figure 3C). In June 2019, the medusa abundance was only 42% less than that in 2014. Only a few biofilms developed on the undersurface of Dock I 1 month later (Figure 4A); after 2 years, a few macro-fouling organisms were found. They mainly included barnacles, mussels, and ascidians with densities of 238.10 ± 64.70 ind·m-2, 92.00 ± 75.94 ind·m-2, and 33.55 ± 27.61 ind·m-2, respectively (; Figure 4B). A. coerulea polyps occurred at a very low density of 1.08 ± 3.02 ind·m-2 in the third year post-treatment, when ascidians and mussels were the dominating biofouling organisms (densities of 155.84 ± 87.35 ind·m-2 and 309.52 ± 120.85 ind·m-2, respectively; Figure 4C). In contrast, many biofouling organisms were found on the undersurface of Dock II 1 year later, with ascidians, oysters, and mussels being the main taxa (densities of 179.30 ± 127.07 ind·m-2, 106.06 ± 83.33 ind·m-2, and 55.56 ± 50.44 ind·m-2, respectively; Figure 4D). After 2 years, numerous A. coerulea polyps were discovered in September, the density of which had exceeded the initial level (3512.31 ± 2229.78 ind·m-2) (). The dominating biofouling organisms were ascidians, barnacles, and mussels, with densities of 284.10 ± 170.09 ind·m-2, 252.53 ± 257.32 ind·m-2, and 150.25 ± 201.47 ind·m-2, respectively. Thus, applying modified alloprene paint to the undersurface of Dock I effectively inhibited the resettlement of A. coerulea polyps on there in comparison with Dock II during 3 years. It follows that the long-term control of A. coerulea blooms in the harbor, where polyps massively inhabit the surfaces of movable floating docks, may be accomplished by regular maintenance of these structures using modified alloprene paint.
Figure 4
In addition, A. coerulea polyps are also capable of settling in large numbers on the permanent infrastructures submerged in the sea, such as bridge piers and fixed platforms (; ). For these immovable constructions, physical methods of eliminating polyps, such as waterjets or mechanical scraping, could be adopted (; ), although their inhibition on the resettlement of A. coerulea polyps on substrate surfaces may be less effective than antifouling paint (). Compared to capturing medusae and establishing a series of arresting nets to solve A. coerulea blooms, methods of eliminating polyps have a lower cost (), and have the potential to prevent the formation of A. coerulea blooms at their source and decrease the risks of outbreaks in affected areas ahead of time.
Applicable measures to suppress N. nomurai blooms
Resource utilization of N. nomurai medusae
In China, the edible species Rhopilema esculentum is popular seafood with a long history and good market value, which has been an important Chinese jellyfish fishery (). In recent decades, as the production of R. esculentum sharply declined (; ) and N. nomurai frequently bloomed in the coastal sea of China (; ), the Chinese fishermen have started to massively capture N. nomurai medusae in the nearshore waters of many coastal cities, where jellyfish manufacturing districts have been established to process them into new edible jellyfish products alternative to R. esculentum for improving the local fishery economy. For example, in Huangshan village, Qingdao, massive N. nomurai medusae were captured nearby by a kind of specialized jellyfish net with a mesh size of about 18cm from July to October. Then they were made into various jellyfish products (e.g., salted jellyfish, instant jellyfish, and other dishes). Thus, the market share of N. nomurai has exceeded 95% of all jellyfish production in some cities, such as Qingdao and Tangshan (Zheng et al., 2014). According to statistics, the annual catch of N. nomurai has increased continuously in the Bohai and Yellow seas from 2009 to 2013 (Figure 5A; ). In particular, in Tangshan, Hebei Province, China (Figure 1), since 2009, N. nomurai catches have been more than twice annually compared with those in 2008 (Figure 5B, Zheng et al., 2014). This resource utilization of N. nomurai medusae can conduce to decreasing the number of medusae and their sexual reproduction in the adjacent seas, which may be one of the potential reasons for the decline in N. nomurai blooms in the 2010s as compared with that in the 2000s. Thus, the long-term persistence of this measure might reduce the possibility of N. nomurai blooms in the coastal seas of China.
Figure 5
More severe and earlier summer fishing moratorium
In the marine ecosystem, jellyfish and fish were generally adversaries (). N. nomurai could compete with fish for copepods (). They also ingest fish eggs and larvae from species such as Paralichthys olivaceus and Sebastes schlegeli (). In addition, some fish (e.g., Thamnaconus septentrionalis and Pampus argenteus) also prey on N. nomurai (; ; ). Thus, changes in the governance of fishery resources also affect the abundance of N. nomurai in the Bohai Sea, Yellow Sea, and nECS. To maintain fish stocks and enhance fishery production, a summer fishing moratorium came into effect in 1995. Its duration was gradually prolonged in different regions over the last two decades. For example, in the 27-35°N areas of Chinese coastal seas, which include the major birthplaces and high-density areas (31.5-35°N) of N. nomurai in the sYS and nECS (Zhang et al., 2012; ; Zuo et al., 2016), the summer fish moratorium extended from July 1 to August 31 in 1995, then from June 16 to September 15 in 1998, and from June 1 to September 16 in 2009 (). In Bohai Sea, the summer fish moratorium also changed from June 16 to September 1 in 2004 into from June 1 to September 1 in 2009 (). Since 2017, the longest summer fishing moratorium was imposed with tougher enforcement from May 1 to September 16 in the 26.5-35°N areas and from May 1 to September 1 in the north of 35°N, respectively (; ). The advancement of the moratorium onset time to May 1 might play an important role in regulating both the biomass of N. nomurai and the fishery resource. When the fishing ban is implemented later than early June, the overfishing of adult and juvenile fish (e.g., P. argenteus, Larimichthys polyactis, and Trichiurus lepturus; ; ) might create more suitable conditions in spring (e.g., abundant zooplankton bait and reduced fish predation rate) for the development of early pelagic N. nomurai larvae, which are weakly competitive compared with medusae. Therefore, these larvae can grow well into medusae within 1 month (; ). When the fishing ban began to be implemented more rigorously and forcefully in early May 2017, these conditions favorable to early pelagic N. nomurai larvae may reduce as the annual fish catches decreased (Figure 6) and fishery resources were forecast to improve during the summer fishing moratorium (; ; ). Thus this might contribute to the weakening of outbreaks of N. nomurai in these years.
Figure 6
Other experimental control measures
Some additional physical and chemical measures have been examined experimentally in the laboratory to solve the problems of jellyfish blooms along the Chinese coasts. designed a monolithic trawl net 5m long with a mouth of 2m×2m, at the bottom of which a circular steel ring 50cm in diameter with 16 crossed steel wires inside was installed. The medusae are captured and crushed while the net is towed at sea. However, this equipment awaits further testing in terms of its feasibility and efficiency in destroying medusae. Some drugs, such as “tea saponin”, comprising saponins extracted from plants, have been reported to be capable of killing the polyps, ephyrae, or medusae of jellyfish at low concentrations (; ). However, because of their lethal effects on many microorganisms, algae, and zooplankton (), the method that treats jellyfish blooms by using a large amount of the drugs, might produce serious secondary damage to the marine ecosystem. Therefore, these drugs have limitations concerning field application.
Prospects
It is a general perception that coastal anthropogenic stressors (e.g., climate change, eutrophication, increase of man-made structures, and overfishing) are responsible for jellyfish blooms (; ; ). However, the particular causes of medusa outbreaks differ among species (). For example, the frequent outbreaks of A. coerulea are closely associated with the increase of artificial substrates in the coastal sea of China (; ; ). Therefore, to decrease A. coerulea blooms, government administration policies relevant to inshore artificial constructions need to be formulated. For example, agencies that manage marine development should require the regular application of antifouling paint to the undersurfaces of floating constructions and the elimination of A. coerulea polyps on the surfaces of fixed platforms in the harbors. In contrast, the control of N. nomurai blooms may require an expansion of medusa utilization as a food source or as other beneficial products and strict enforcement of the current summer fishing moratorium. Thus, for the health of the marine ecosystem in China, reasonable management of these two jellyfish blooms will require a long-term commitment and perseverance.
Funding
This research was supported by the National Natural Science Foundation of China (grant no. 42176136, 42130411, and 42076166), the Natural Science Foundation of Shandong Province (grant no. ZR2020KE047), Mount Tai Scholar Climbing Plan to SS, and Huiquan Scholar to SF.
Acknowledgments
We are very grateful to Pro. Jiansheng Li for providing the data on N. nomurai catches in the Bohai and Yellow seas for this study. We also thank Associate Pro. Huilian Liu for helping us identify the species of fouling organisms.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Statements
Author contributions
SF carried out the field investigation, and data analysis, and drafted the manuscript. SS, CL, and FZ contributed to the project administration, conceptualization, and paper editing. All authors contributed to the article and approved the submitted version.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Summary
Keywords
jellyfish blooms, control, biofouling organisms, polyps, medusae
Citation
Feng S, Sun S, Li C and Zhang F (2022) Controls of Aurelia coerulea and Nemopilema nomurai (Cnidaria: Scyphozoa) blooms in the coastal sea of China: Strategies and measures. Front. Mar. Sci. 9:946830. doi: 10.3389/fmars.2022.946830
Received
18 May 2022
Accepted
09 September 2022
Published
27 September 2022
Volume
9 - 2022
Edited by
Yuanyuan Feng, Shanghai Jiao Tong University, China
Reviewed by
Jinho Chae, Marine Environmental Research and Information Laboratory, South Korea; Doojin Hwang, Chonnam National University, South Korea
Updates
Copyright
© 2022 Feng, Sun, Li and Zhang.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Song Sun, sunsong@qdio.ac.cn; Fang Zhang, zhangfang@qdio.ac.cn
This article was submitted to Marine Ecosystem Ecology, a section of the journal Frontiers in Marine Science
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