Factors inducing morphological transition in harmful algal bloom-forming species Phaeocystis globosa with emphasis on predator chemical cue

The microalga Phaeocystis globosa is recognized as a harmful alga and also one of the few keystone phytoplankton genera that shape the structure and function of marine ecosystems.P.globosa possess a complex polymorphic life cycle,exhibiting phase alternation between free-living cells of approximately 3-6μm in diameter and gelatinous colonies(palmelloid stage)reaching several millimeters.The knowledge on the factors that induced the morphological transition of P.globosa in the last two decades was reviewed.Emphasis is given to infochemicals,an additional biological factor induced by predator,with the attempt to reveal a relevant mechanism of induced morphological defense.

Changes of Water Temperature and Harmful Algal Bloom in the Daya Bay in the Northern South China Sea

Economic development around the Daya Bay, China has profoundly affected the marine environment in the bay area in recent years, particularly since the operation of Daya Bay Nuclear Power Station （DNPS） in 1994. This study analyzed the changes of water temperature and harmful algal blooms （HABs） for two periods： 1983-1993 and 1994-2004, using in situ and satellite data. Results showed that yearly mean surface water temperature （SWT） and Chl-a concentration （Chl-a） increased by 1.1 ℃ and 1.9 mg/m^3, respectively, after 1994. The monthly occurrence of HAB was found to have increased also. HABs appeared only in spring and autumn before 1994, but occurred all the year round after 1994. SWT, Chl-a and HABs all increased significantly in May. Those changes were associated with environmental changes in this area, such as thermal discharge from the DNPS and enhancement of eutrophication from human activities around the Daya Bay.

Effects of temperature, salinity, and irradiance on the growth of harmful algal bloom species Phaeocystis globosa Scherffel(Prymnesiophyceae) isolated from the South China Sea

Blooms of Phaeocystis globosa have been frequently reported in Chinese coastal waters, causing serious damage to marine ecosystems. To better understand the ecological characteristics of P. globosa in Chinese coastal waters that facilitate its rapid expansion, the effects of temperature, salinity and irradiance on the growth of P. globosa from the South China Sea were examined in the laboratory. The saturating irradiance for the growth ofP. globosa （Is） was 60 μmol/（m^2·s）, which was lower than those of other harmful algal species （70-114μmol/（m^2·s））. A moderate growth rate of 0.22/d was observed at 2 μmol/（m^2·s） （the minimum irradiance in the experiment）, and photo-inhibition did not occur at 230 μmol/（m^2·s） （the maximum irradiance in the experiment）. Exposed to 42 different combinations of temperatures （10- 31 ℃） and salinities （10-40） under saturating irradiance, P. globosa exhibited its maximum specific growth rate of 0.80/d at the combinations of 24℃ and 35, and 27℃ and 40. The optimum growth rates （〉0.80/d） were observed at temperatures ranging from 24 to 27℃ and salinities from 35 to 40. While P. globosa was able to grow well at temperatures from 20℃ to 31℃ and salinities from 20 to 40, it could not grow at temperatures lower than 15℃ or salinities lower than 15. Factorial analysis revealed that temperature and salinity has similar influences on the growth of this species. This strain ofP. globosa not only prefers higher temperatures and higher salinity, but also possesses a flexible nutrient competing strategy, adapted to lower irradiance. Therefore, the P. globosa population from South China Sea should belong to a new ecotype. There is also a potentially high risk of blooms developing in this area throughout the year.

Temporal and spatial characteristics of harmful algal blooms in Qingdao Waters,China

Qingdao waters,including both the semi-enclosed Jiaozhou Bay(JB) and the adjacent water out of JB(OJB),have been the areas that are most frequently affected by harmful algal blooms(HABs) in the western Yellow Sea(west of 124°E).In this research,HAB occurrences in Qingdao waters from 1990 to 2009 were investigated using spatial tools in geographic information system(GIS) and are discussed in terms of their connection to temporal variation.Additionally,the effects of each HAB occurrence were further evaluated using a simple model.The calculated results were then visualized using a GIS software to indicate the effects of HABs in Qingdao waters during the entire period.As a result,the OJB was proven to be responsible for the frequent HAB occurrences in Qingdao waters after 2000,although JB was traditionally believed to be the principle source of HAB occurrences in Qingdao waters.In addition,increasing nitrogen and N/P structure imbalance were essential for increasing HAB occurrences in Qingdao waters throughout the entire period,especially for the recent HAB occurrences in the OJB.The results of this research would improve the current understanding on HAB occurrences in Qingdao waters,which would benefit HAB monitoring and the implementation of a control strategy in China as well.

I mpact of several harmful algal bloom(HAB) causing species, on life history characteristics of rotifer Brachionus plicatilis Müller

In recent years, harmful algal blooms(HABs) have occurred frequently along the coast of China, and have been exhibiting succession from diatom- to dinofl agellate-dominated blooms. To examine the eff ects of dif ferent diatom and dinofl agellate HABs, the life history parameters of rotifers(B rachionus plicatilis Müller) were measured after exposure to dif ferent concentrations of HAB species. The HAB species examined included a diatom(S keletonema costatum) and four dinofl agellates( Prorocentrum donghaiense, Alexandrium catenella, Prorocentrum lima and Karlodinium venefi cum). Compared with the control treatment(CT), the diatom S. costatum showed no adverse impacts on rotifers. Exposure to dinofl agellates at densities equivalent to those measured in the fi eld resulted in a reduction in all the life history parameters measured. This included a reduction in: lifetime egg production(CT: 20.34 eggs/ind.) reduced to 10.11, 3.22, 4.17, 7.16 eggs/ind., life span(CT: 394.53 h) reduced to 261.11, 162.90, 203.67, 196 h, net reproductive rate(CT: 19.51/ind.) reduced to 3.01, 1.26, 3.53, 5.96/ind., fi nite rate of increase(CT: 1.47/d) reduced to 1.16, 1.03, 1.33, 1.38/d, and intrinsic rate of population increase(CT: 0.39/d) reduced to 0.15, 0.03, 0.28, 0.32/d, for the dinofl agellates P. donghaiense, A. catenella, P. lima and K. venefi cum, respectively. The results showed that the diatom S. costatum had no detrimental consequences on the reproduction and growth of B. plicatilis, however, the four dinofl agellates tested did show adverse ef fects. This suggests that dinofl agellate HABs may suppress microzooplankton, resulting in an increase in algal numbers.

A numerical model study on multi-species harmful algal blooms coupled with background ecological fields

Based on systematized physical, chemical, and biological modules, a multi-species harmful algal bloom （HAB） model coupled with background ecological fields was established. This model schematically embod-ied that HAB causative algal species and the background ecological system, quantified as total biomass, were significantly different in terms of the chemical and biological processes during a HAB while the inter-action between the two was present. The model also included a competition and interaction mechanism between the HAB algal species or populations. The Droop equation was optimized by considering tempera-ture, salinity, and suspended material impact factors in the parameterization of algal growth rate with the nutrient threshold. Two HAB processes in the springs of 2004 and 2005 were simulated using this model. Both simulation results showed consistent trends with corresponding HAB processes observed in the East China Sea, which indicated the rationality of the model. This study made certain progress in modeling HABs, which has great application potential for HAB diagnosis, prediction, and prevention.

Sustainable Utilization of Agricultural Straw for Harmful Algal Blooms Control:A Review

The use of agricultural straw for algal bloom control has been studied for more than 30 years.In this article,we have reviewed the promising potentials of using agricultural straw as source of anti-algal agents,including the effectiveness of each major straw type so far used in this regard,and the investigated algal species.Various pre-treatment methods have also been widely reviewed.Significant progress has been made in natural product chemistry and molecular biology with regards to agricultural straw,especially in relation to the extraction of antialgal allelochemicals,degradation processes of agricultural straws and the mechanisms through which these inhibitions occur.The development of biotechnologies using agricultural straw to successfully inhibit growth of bloom forming algae has been generally accepted as environmentally friendly.The current research status and that of the future should include isolation and discovery of antialgal allelochemicals,development of models that would illustrate the sequence of physiologic events that match the species-specific inhibitor phenomenon,and products fit in the field applications.

Harmful algal bloom-forming dinofl agellate Prorocentrum donghaiense inhibits the growth and photosynthesis of seaweed Sargassum fusiformis embryos

Harmful algal bloom(HAB)is an ecological disaster to local mariculture.At present,its impact on macrophytes has not been well studied.In this study,we cultivated sexually propagated embryos of S argassum fusiformis-an edible seaweed-in Prorocentrum donghaiense suspensions at different cell densities(0,0.50×10^(5),0.75×10^(5),1.00×10^(5),and 1.50×10^(5) cells/mL)for 10 days,during which growth and photosynthetic activities of the embryos were determined,and a monocultivation was set up for comparison.Results show that the relative growth rate and photosynthetic activities of the embryos co-cultivated with P.donghaiense were inhibited mostly and significantly in the cell densities of 0.75×10^(5),1.00×10^(5),and 1.50×10^(5) cells/mL,and the inhibitory effects increased in overall with increased cell densities.The maximum relative electron transport rates(rETR max)and apparent photosynthetic efficiency(a)of co-cultivated embryos were all significantly lower than monocultivation ones on the 10 th day.Furthermore,the photosynthetic activity detected by chlorophyll-a fluorescence transient(i.e.,OJIP),the electron transport among electron transfer accepters of PSII(photosystem II)and that from PSII to PSI(photosystem I)was restricted,which is probably responsible for the decreases of rETR max andain the co-cultivated embryos.In addition,parts of the photosynthetic reaction centers of PSII in the co-cultivated embryos were inactivated.Therefore,P.donghaiense bloom could restrain the development and photosynthetic activities of S.fusiformis embryos,reduce the seedlings stock,and eventually hinder the development of S.fusiformis production industry.

Does reduced sediment load contribute to increased outbreaks of harmful algal blooms off the Changjiang Estuary?

Harmful algal blooms（HABs） have been increasingly frequent in coastal waters around the world over the last several decades. Accelerated coastal eutrophication, resulting from the increased anthropogenic loadings of nutrients, is commonly assumed to be the primary cause of this increase. However, although important,accelerated coastal eutrophication may not be the only explanation for the increasing blooms or toxic outbreaks in estuarine waters. Changes in riverine material fluxes other than nutrients, such as sediment load, may significantly affect biological activities and HAB incidence in estuarine and coastal waters. A case study off the Changjiang（Yangtze River） Estuary indicated that with the increasing riverine loadings of nutrients, the sediment load from the Changjiang River has been reduced by 70% over the past four decades. A comparison of long-term data revealed that the phytoplankton biomass maximum has expanded to a region of much lower salinity due to the drastic reduction in riverine sediment load and the subsequent improvement in light penetration in the Changjiang River plume. Furthermore, there was an apparent mirror-image relationship between the sediment load from the Changjiang River and the HAB incidence off the Changjiang Estuary over the past four decades, and the number of HAB incidents was significantly negatively correlated with the sediment load. Therefore, it is argued that the drastic decline in sediment load from the Changjiang River reduced turbidity in the Changjiang Estuary and thus contributed to the increased frequency of HABs in the buoyant discharge plumes.

Effects of modified clay on cysts of Scrippsiella trochoidea for harmful algal bloom control

We present results on the effect of modified clay on cyst formation of Scrippsiella trochoidea in harmful algal bloom （HAB）. Modified clay （in concentration of 0, 0.1, 0.5, and 1.0 g/L） were added to cultures, and observations were made on cysts of S. trochoidea under controlled laboratory conditions. Results indicate that the removal rate of algal cells reached 97.7% at the clay concentration of 1.0 g/L. The cyst formation rate increased from 4.6% to 24.6% when the concentration of clay was increased from 0 to 1.0 g/L. Two cyst metamorphs were observed： spinal calcareous cysts and smooth noncalcareous ones. The proportion of the spinal cysts decreased from 76.9% to 24.1% when clay concentration increased from 0 to 1.0 g/L. In addition, modified clay affected cyst germination. The germination rate decreased with the increases in the clay concentrations. Non-calcareous cysts had a lower germination rate with a longer germination time. We conclude that modified clay could depress algal cell multiplication and promote formation of temporal cysts of S. trochoidea, which may help in controlling HAB outbreaks.

Increased diversity and environmental threat of harmful algal blooms in the Southern Yellow Sea,China

Harmful algal blooms(HABs)in the Southern Yellow Sea(SYS)have shown a trend of increasing diversity and detrimental ef fects.While the Bohai Sea,East China Sea,and South China Sea have experienced a high incidence of HABs since the 1980s,the Yellow Sea provides a relatively healthy ecological environment in which fewer HABs have been documented before the 21s t century.Yet largescale blooms of the green macroalga Ulva prolifera(so-called“green tides”)have occurred annually since 2007 in the Yellow Sea.Six people were poisoned and one person died in Lianyungang in 2008 due to ingestion of algal toxins.Moreover,the Yellow Sea experienced co-occurrence of harmful red tides,green tides,and golden tides in 2017.This combination of events,rare worldwide,indicates the potential for further deterioration of the marine environment in the Yellow Sea,which may be related to climate change,aquaculture,and other human activities.Using the SYS as an example,we collected data of the frequency and scale of HABs over the years,as well as that of marine algal toxins,and analyzed the trend in the diversity of HABs in the SYS,to explore the causes and impacts of HABs,as well as the interrelationships among dif ferent types of HABs,including harmful red tides,green tides,and golden tides.We also attempted to improve our understanding of HAB evolution under the influence of global climate change and intensified human activities.

Overview of harmful algal blooms(red tides)in Hong Kong during 1975–2021

Hong Kong has a long historical record of harmful algal blooms(HABs).In the 1980s-1990s,HABs were mainly pollution-related and most of the events happened in estuaries and enclosed embayment such as Tolo Harbour and Port Shelter.The major cause of HABs in 1980s-1990s was closely related to nutrients enrichment;included but not limited to changes in the concentration and ratio of soluble N and P in seawater.The major causative organisms of HABs in Hong Kong by then were meso-plankton such as selected species of diatoms and dinofl agellates.Sometimes,zooplankton was also a cause of red tides(the common name of HABs).There has been gradual change after the 2000s.It is attributed to higher and higher influences from the region,namely the Zhujiang(Pearl)River delta.There are increasing influences from Chinese mainland due to extraordinary social and economic growths during the past 20 years.In the past10 years,HABs in Hong Kong was mainly subject to regional impacts in the Zhujiang River delta.Both the duration period and covered areas have been enlarged which overwhelmed the localized influences of stream pollution and self-contamination of aquaculture zones.More flagellates of uncommon happening become dominant species in HAB now.Nevertheless,the seasonal impact of Noctiluca scintillans in late winter to mid spring remained.

HPLC Pigment Profiles of 31 Harmful Algal Bloom Species Isolated from the Coastal Sea Areas of China

Chemotaxonomy based on diagnostic pigments is now a routine tool for macroscopic determination of the composition and abundance of phytoplankton in various aquatic environments. Since the taxonomic capability of this method depends on the relationships between diagnostic pigments and chlorophyll a of classified groups, it is critical to calibrate it by using pigment relationships obtained from representative and/or dominant species local to targeted investigation area. In this study, pigment profiles of 31 harmful algal bloom(HAB) species isolated from the coastal sea areas of China were analyzed with high performance liquid chromatography(HPLC). Pigment compositions, cellular pigment densities and ratios of pigments to chlorophyll a were determined and calculated. Among all these species, 25 kinds of pigments were detected, of which fucoxanthin, peridinin, 19'-butanoyloxyfucoxanthin, 19'-hexanoyloxyfucoxanthin, violaxanthin, and antheraxanthin were diagnostic pigments. Cellular pigment density was basically independent of species and environmental conditions, and therefore was recommended as a bridge to compare the results of HPLC-CHEMTAX technique with the traditional microscopy method. Pigment ratios of algal species isolated from the coast of China, especially the diagnostic pigment ratios, were higher than those from other locations. According to these results, pigment ratio ranges of four classes of phytoplankton common off the coast of China were summarized for using in the current chemotaxonomic method. Moreover, the differences of pigments ratios among different species under the same culturing conditions were consistent with their biological differences. Such differences have the potential to be used to classify the phytoplankton below class, which is meaningful for monitoring HABs by HPLC-CHEMTAX.

Harmful Algal Bloom Research in China

Proliferations of harmful algae in coastal waters, i.e., harmful algal blooms (HABs), popularly known as 'red tides,' have attracted the concern of governments and scientists worldwide. In recent years, HABs have occurred in China with increasing frequency and scope. These outbreaks have seriously affected the economy along the coast through fish kills, heavy losses in aquaculture, threats to human health, and other effects detrimental to the marine ecosystem. Therefore, it is important to pay special attention to the ecology and oceanography studies related to the outbreak of HABs. Only through the combination of the advancement of such knowledge with the strengthening of the monitoring network can we develop a HAB warning system for the sustainable development of the coastal economy.

First harmful algal bloom record of tycoplanktonic dinoflagellate Prorocentrum lima(Ehrenberg)F.Stein,1878 in the Dardanelles(Turkish Straits System,Turkey)

This study focused on daily variations and harmful algal bloom features of toxic dinoflagellate Prorocentrum lima(Ehrenberg)F.Stein(P.lima),1878 in middle summer period(9th July-6th August 2013)in the Dardanelles.Harmful algal bloom of P.lima was recorded for the first time in the Turkish Straits System.Density of P.lima reached to 2.40×10^(6)cells/L and exhibited four excessive blooms over 1.0×10^(6)cells/L during the study.The contribution of P.lima to both Prorocentrum spp.and dinoflagellates reached to 100%,particularly at the moment of the harmful algal bloom attested by regresion(R≥0.70)and correlation findings(R≥0.80).Nutrient concentrations were lower than previous levels due to excessive blooms.Concentrations of NO^(-)_(2)+NO^(-)_(3),PO^(-3)_(4)and SiO_(4)varied between 0.20 and 0.78μmol/L[(0.44±0.17)μmol/L],0.08 and 0.18μmol/L[(0.12±0.03)μmol/L]and 0.25 and 0.65μmol/L[(0.41±0.09)μmol/L]respectively.During the bloom,nutrient ratios were more different than redfield ratios due to eutrophication(NO^(-)_(2)+NO^(-)_(3)/PO^(-3)_(4)=4.04±1.74;SiO_(4)/PO^(-3)_(4)=3.79±1.24;SiO_(4)/NO^(-)_(2)+NO^(-)_(3)=1.04±0.36).Chlorophyll a concentration reached to 8.52μg/L(average:4.82±2.29 mg/L)in the bloom period.Temperature[(24.70±0.44)°C],salinity[(22.9±0.49)ppt],pH(8.23±0.15)and dissolved oxygen levels(7.35±0.60 mg/L)were approximately constant.The compact bloom of P.lima,similar to excessive blooms of other dinoflagellates and diatoms,was associated not only with eutrophication,but also with ocean warming interactions.Results revealed that it will be possible to reach to millions of cell number of P.lima(2.40×10^(6)cells/L)in eutrophied waters characterized by high chlorophyll a biomass(8.52μg/L).

Harmful algal blooms in fresh and marine water systems： The role of toxin producing phytoplankton

In this paper, we have investigated a model with three interacting species： non-toxic phy- toplankton, toxic phytoplankton and zooplankton with Holling type II and III functional responses over the space and time. The role of toxin producing phytoplankton （TPP） has been studied. We have presented the theoretical analysis of pattern formation in spatially distributed population with local diffusion. The paper highlights the hetero- geneity of HABs over space and time. The choice of parameter values and the functional response is important to study the effect of TPP, also it would depend more on the non- linearity of the system. With the help of numerical simulations, we have observed the spatial and spatiotemporal patterns for plankton system. This study demonstrates that TPP plays an important role in controlling the dynamics. We have observed that prey＇s anti-predator efforts promote predator switching. It has been found that high predation of TPP helps for the coexistence of toxic, non-toxic phytoplankton and zooplankton population.

Physical Hydrography and Algal Bloom Transport in Hong Kong Waters

In sub-tropical coastal waters around Hong Kong, algal blooms and red tides are usually first sighted in the Mirs Bay, in the eastern waters of Hong Kong. A calibrated three-dimensional hydrodynamic model for the Pearl River Estuary （Delft3D） has been applied to the study of the physical hydrography of Hong Kong waters and its relationship with algal bloom transport patterns in the dry and wet seasons. The general 3D hydrodynamic circulation and salinity structure in the partially-mixed estuary are presented. Extensive numerical surface drogue tracking experiments are performed for algal blooms that are initiated in the Mirs Bay under different seasonal, wind and tidal conditions. The probability of bloom impact on the Victoria Harbour and nearby urban coastal waters is estimated. The computations show that： i） In the wet season （May - August）, algal blooms initiated in the Mirs Bay will move in a clockwise direction out of the bay, and be transported away from Hong Kong due to SW monsoon winds which drive the SW to NE coastal current; ii） In the dry season （November- April）, algal blooms initiated in the northeast Mirs Bay will move in an anti-clockwise direction and be carried away into southern waters due to the NE to SW coastal current driven by the NE monsoon winds; the bloom typically flows past the east edge of the Victoria Harbeur and nearby waters. Finally, the role of hydrodynamic transport in an important episodic event -- the spring 1998 massive red tide -- is quantitatively examined. It is shown that the strong NE to E wind during late March to early April, coupled with the diurnal tide at the beginning of April, significantly increased the probability of bloom transport into the Port Shelter and East Lamma Channel, resulting in the massive fish kill. The results provide a basis for risk assessment of harmful algal bloom （HAB） impact on urban coastal waters around the Victoria Habour.

STABILITY AND BIFURCATION BEHAVIORS ANALYSIS IN A NONLINEAR HARMFUL ALGAL DYNAMICAL MODEL

A food chain made up of two typical algae and a zooplankton was considered. Based on ecological eutrophication, interaction of the algal and the prey of the zooplankton, a nutrient nonlinear dynamic system was constructed. Using the methods of the modern nonlinear dynamics, the bifurcation behaviors and stability of the model equations by changing the control parameter r were discussed. The value of r for bifurcation point was calculated, and the stability of the limit cycle was also discussed. The result shows that through quasi-periodicity bifurcation the system is lost in chaos.

Laboratory simulation of dissolved oxygen reduction and ammonia nitrogen generation in the decay stage of harmful algae bloom

To evaluate how the decay of bloom-forming algae affect the coastal dissolved oxygen,a laboratory simulation was conducted in terms of three typical harmful algae,Alexandrium catenella,Prorocentrum donghaiense,and Skeletonema costatum.Algae of same biomass(55μg/mL)were conducted in lightproof columns,and the cell density,dissolved oxygen(DO),and ammonia nitrogen of different layers were monitored at certain time series.Results show that the decomposition of algae significantly decreased the DO,and increased the ammonia nitrogen in all layers;and significant deference between different species was observed.The A.catenella treatment showed the lowest DO(average concentration of 3.4 mg/L)and the highest ammonia nitrogen(average concentration of 0.98 mg/L)at the end of test,followed by P.donghaiense;and the S.costatum showed relatively high DO and low ammonia nitrogen due to slow decay rate.Results indicate that decomposition of harmful bloom algae,especially dinoflagellate,would cause significantly DO depletion and toxic ammonia nitrogen increase,which will detrimentally affect both pelagic and benthic ecosystem.

Assessment of the consecutive harmful dinoflagellate blooms during 2015 in the Izmit Bay(the Marmara Sea)

A series of red tides were observed during 2015 in the Izmit Bay（the Marmara Sea） which is located in the most industrialized and populated region of Turkey. Six samplings were carried out in this area following the red tides.Nitrite-N, nitrate-N, ammonia, silica and orthophosphate concentrations were analyzed spectrophotometrically.Physicochemical conditions were measured by CTD probe. Plankton quantification was performed using counting chambers under microscopes. Prorocentrum micans was the most abundant species, except on May 14,2015, when Noctiluca scintillans was dominant. The abundance of P. micans reached average 18×10~6 ind./L on May 3, 2015 in the Karamürsel station, simultaneously with elevated levels of NH_3 and o-PO_4^（3–）. The sample was also abundant in dead amphipods（（72±12） ind./L） that had been covered by mucilage aggregates produced by P.micans. The highest biomass（calculated by carbon） was recorded as（268±26.0） mg/L on May 14 in the Hereke station. Beside the anthropogenic wastewater discharges, unknown sources and resuspensions caused increases in nutrient levels. After long term northeaster gusts（35 km/h for 5 d） an upwelling occurred on November 6, 2015 after wind-induced sediment resuspension. Although nutrient discharges remarkably decreased over 30 years through established wastewater treatment plants, harmful phytoplankton blooms still occur. Comparing the present results with other studies in nearby Mediterranean seas reveals that the most intense harmful dinoflagellate bloom in recent years occurred in the Izmit Bay. Therefore, additional protection measures necessary for a cleaner Izmit Bay. These incidents also demonstrate that contaminants, accumulated in sediment,may have long-lasting effects on enclosed marine ecosystems.