How does eutrophication affect the role of grazers in harmful algal bloom dynamics?

Population dynamics of harmful algal bloom species are regulated both from the “bottom-up” by factors that affect their growth rate and from the “top-down” by factors that affect their loss rates. While it might seem apparent that eutrophication would have the greatest impact on factors affecting growth rates of phytoplankton (nutrient supply, light availability) the roles of top-down controls, including grazers and pathogens, cannot be ignored in studies of harmful bloom dynamics. Lags between the growth of phytoplankton and zooplankton populations, or disruption of zooplankton populations by adverse environmental conditions may be important factors in the initiation of plankton blooms under eutrophic conditions. Grazers that avoid feeding on harmful species and actively graze on competing species may also play important roles in bloom initiation. Grazers that are not affected by phytoplankton toxins and have growth rates comparable to phytoplankton (e.g. protozoan grazers) may have the potential to control the initiation of blooms. If the inhibition of grazers varies with cell density for blooms of toxic phytoplankton, eutrophication may increase the chances of blooms reaching threshold densities for grazer inhibition. In addition, secondary effects of eutrophication, including hypoxia and change in pH may adversely affect grazer populations, and further release HAB species from top-down control. The Texas brown tide (Aureoumbra lagunensis) blooms provide evidence for the role of grazer disruption in bloom initiation and the importance of high densities of brown tide cells in continued suppression of grazers.     

Recruitment of Planktonic Dinoflagellates: Importance of Benthic Resting Stages and Resuspension Events

Many factors have ken put forward to account for the development of nuisance phytoplankton blooms in coastal zones. Usually hydrological factors as temperature or salinity stratification and adequate nutrient and trace metal availability are held responsible for the phenomenon. The most frequent causative organisms for nuisance blooms are dinoflagellates, many of which have a dormant stage (resting cyst) in their life cycle. The role of the complex life-strategies of these forms in initiating bloom formation is the focus of this study. Special attention is given to 25 different dinoflagellate resting cyst types isolated from recent German North Sea and Baltic Sea sediments, and their germination frequency under different environmental conditions. Also, the role of cyst resuspension in relationship to the timing, persistence and recurrence of dinoflagellate blooms is extensive discussed.     

“Windows of opportunity” for dinoflagellate blooms: Reduced microzooplankton net growth coupled to eutrophication

Links between eutrophication, plankton community structure, microzooplankton grazing and dinoflagellate abundance were investigated in two tributaries of the Chesapeake Bay, the Choptank and Patuxent Rivers (MD, USA). Sampling and experiments were conducted during the spring of consecutive dry (below average freshwater flow) and wet (above average freshwater flow) years. During the wet year (2003), dissolved inorganic nitrogen, phytoplankton, and copepod biomass, but not microzooplankton abundance, were greater than in the dry year. In 2003, but not 2002, small cell size photosynthetic dinoflagellates were abundant and blooms occurred in both rivers. Average potential microzooplankton grazing pressure on small dinoflagellates was spatially and temporally variable, but was not significantly different between years. Our data suggest that the variability in microzooplankton grazing pressure provided “windows of opportunity” for net growth of dinoflagellates in response to nutrient loading. The lack of net population growth of micrograzers in response to increases in dinoflagellate prey allowed dinoflagellate blooms to reach relatively high densities, however grazing also appeared to be important in limitation or demise of some blooms. We hypothesize that uncoupling of micrograzer–prey dynamics was partly due to strong top-down control by copepods of microzooplankton in the proportionately more eutrophic year, and perhaps also due to inhibition of microzooplankton grazing/growth once dinoflagellate densities are high.     

Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals

Many dinoflagellate species form dormant resting cysts as a part of their life cycle, and in some freshwater species, hatching of these cysts can be delayed by the presence of water-borne signals from grazing zooplankton. Some marine dinoflagellates can form temporary cysts, which may function to resist unfavourable short-term environmental conditions. We investigated whether the marine dinoflagellate Alexandrium ostenfeldii is able to induce an increased resistance to the parasitic flagellate Parvilucifera infectans by forming temporary cysts. We performed several laboratory experiments where dinoflagellates were exposed either to direct contact with parasites or to filtered water from cultures of parasite-infected conspecifics (parasite-derived signals). Infection by P. infectans is lethal to motile A. ostenfeldii cells, but temporary cysts were more resistant to parasite infection. Furthermore, A. ostenfeldii induced a shift in life-history stage (from motile cells to temporary cysts) when exposed to parasite-derived water-borne signals. The response was relaxed within a couple of hours, indicating that A. ostenfeldii may use this behaviour as a short-term escape mechanism to avoid parasite infection. The results suggest that intraspecies chemical communication evoked by biotic interactions can be an important mechanism controlling life-history shifts in marine dinoflagellates, which may have implications for the development of toxic algal blooms.     

Macroalgal palatability and the flux of ciguatera toxins through marine food webs

The benthic dinoflagellate Gambierdiscus toxicus produces polyether toxins that cause ciguatera fish poisoning in humans. The toxins initially enter food webs when fish forage on macroalgae, or other substrates, hosting this epiphytic dinoflagellate. Population studies of G. toxicus and risk assessments in ciguatera-prone regions often rely on quantifying dinoflagellates on macroalgae. Underlying these studies is the assumption that the algae sampled represent a readily consumable resource equally available for benthic grazers. However, many algal hosts of G. toxicus possess a variety of defenses against grazing, and host–dinoflagellate associations may act as toxin sources or sinks depending on their palatability. Marine macroalgae may tolerate or avoid herbivory by exhibiting fast growth, by having poor nutritional quality, by utilizing spatial or temporal escapes or by using chemical or structural defenses. Thus, rapidly consumed algae that cope with herbivores by growing fast, such as many filamentous turfs, could be responsible for a high toxin flux even at low dinoflagellate densities. In contrast, ubiquitous unpalatable algae with much higher dinoflagellate densities might contribute little to toxin flux, and effectively act as refuges for G. toxicus. To date, G. toxicus has been reported from 56 algal genera, two cyanobacteria, one diatom, and one seagrass; 63% of these contain species that are defended from fish grazing and other grazers via chemical, morphological or structural defenses, by low nutritional quality, or by a combination of defensive strategies. High dinoflagellate densities on unpalatable macroalgae could indicate passive accumulation of cells on undisturbed hosts, rather than population explosions or active toxin sources for food webs. Understanding the flow of ciguatoxins in nature requires consideration of the ecology of both G. toxicus and its algal hosts. The complexity of marine algal–herbivore interactions also has consequences for other benthic dinoflagellates that produce toxins, which accumulate in consumers.     

Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC

Seaweed responses to eutrophication and their role in coastal eutrophication processes were compared at 8 different sites along the European coasts from the Baltic to the Mediterranean as part of the EU-ENVIRONMENT Project Marine Eutrophication and benthic Macrophytes (EUMAC). Structural and functional changes of marine benthic vegetation typical of eutrophic waters, in particular mass development (blooms) of certain seaweeds, are not merely the result of increased nutrient loading, but must be attributed to complex interactions of primary and secondary effects during the eutrophication process. Due to species-specific physiological properties of the algae (nutrient kinetics, growth potential, light, temperature requirements), the combined effects of abiotic and biotic factors on juvenile or adult developmental stages control the development of algal blooms in different ways. In particular the role of light, temperature, water motion and oxygen depletion, as well as of grazers, on early and adult developmental stages of the algae are considered. The result are discussed in the context of coastal eutrophication control and management. This revised version was published online in June 2006 with corrections to the Cover Date.     

Parasitic Life Styles of Marine Dinoflagellates1

Several genera of marine dinoflagellates contain species that have evolved parasitic life styles. Dinoflagellate infections have been reported for a wide range of host organisms including sarcodines. ciliates, free-living dinoflagellates, various invertebrates, and a few vertebrates. Some dinoflagellates even parasitize other parasitic dinoflagellates. Most species are obligately parasitic and rely on heterotrophy as their sole means of nutrition; however, some are mixotrophic, as they possess chloroplasts during part or all of their life cycle. Many are ectoparasites that use highly specialized structures to attach to their host and feed, while others are intracellular parasites that feed by osmotrophy. Parasitic dinoflagellates often have adverse effects on their host that can lead to reproductive castration or death. The ecological importance of parasitic dinoflagellates is particularly evident during epidemic outbreaks that cause mass mortality of host organisms. Species that infect fish can pose threats to aquaculture. while other species can make commercially important crustacea unpalatable. In the planktonic realm, parasitic dinoflagellates influence the structure and function of the microbial food web. They compete with copepods and other grazers by utilizing ciliates as hosts and can stimulate rapid recycling of nutrients by causing the decline of toxic and non-toxic red tides.     

Parasites and phytoplankton, with special emphasis on dinoflagellate infections

Planktonic members of most algal groups are known to harbor intracellular symbionts, including viruses, bacteria, fungi, and protozoa. Among the dinoflagellates, viral and bacterial associations were recognized a quarter century ago, yet their impact on host populations remains largely unresolved. By contrast, fungal and protozoan infections of dinoflagellates are well documented and generally viewed as playing major roles in host population dynamics. Our understanding of fungal parasites is largely based on studies for freshwater diatoms and dinoflagellates, although fungal infections are known for some marine phytoplankton. In freshwater systems, fungal chytrids have been linked to mass mortalities of host organisms, suppression or retardation of phytoplankton blooms, and selective effects on species composition leading to successional changes in plankton communities. Parasitic dinoflagellates of the genus Amoebophrya and the newly described Perkinsozoa, Parvilucifera infectans, are widely distributed in coastal waters of the world where they commonly infect photosynthetic and heterotrophic dinoflagellates. Recent work indicates that these parasites can have significant impacts on host physiology, behavior, and bloom dynamics. Thus, parasitism needs to be carefully considered in developing concepts about plankton dynamics and the flow of material in marine food webs.     

MIXOTROPHY AND NITROGEN UPTAKE BY PFIESTERIA PISCICIDA (DINOPHYCEAE)

The nutritional versatility of dinoflagellates is a complicating factor in identifying potential links between nutrient enrichment and the proliferation of harmful algal blooms. For example, although dinoflagellates associated with harmful algal blooms (e.g. red tides) are generally considered to be phototrophic and use inorganic nutrients such as nitrate or phosphate, many of these species also have pronounced heterotrophic capabilities either as osmotrophs or phagotrophs. Recently, the widespread occurrence of the heterotrophic toxic dinoflagellate, Pfiesteria piscicida Steidinger et Burkholder, has been documented in turbid estuarine waters. Pfiesteria piscicida has a relatively proficient grazing ability, but also has an ability to function as a phototroph by acquiring chloroplasts from algal prey, a process termed kleptoplastidy. We tested the ability of kleptoplastidic P. piscicida to take up ¹⁵N-labeled NH     , NO     , urea, or glutamate. The photosynthetic activity of these cultures was verified, in part, by use of the fluorochrome, primulin, which indicated a positive relationship between photosynthetic starch production and growth irradiance. All four N substrates were taken up by P. piscicida , and the highest uptake rates were in the range cited for phytoplankton and were similar to N uptake estimates for phagotrophic P. piscicida . The demonstration of direct nutrient acquisition by kleptoplastidic P. piscicida suggests that the response of the dinoflagellate to nutrient enrichment is complex, and that the specific pathway of nutrient stimulation (e.g. indirect stimulation through enhancement of phytoplankton prey abundance vs. direct stimulation by saprotrophic nutrient uptake) may depend on P. piscicida 's nutritional state (phagotrophy vs. phototrophy).     

Copepods induce paralytic shellfish toxin production in marine dinoflagellates

Among the thousands of unicellular phytoplankton species described in the sea, some frequently occurring and bloom-forming marine dinoflagellates are known to produce the potent neurotoxins causing paralytic shellfish poisoning. The natural function of these toxins is not clear, although they have been hypothesized to act as a chemical defence towards grazers. Here, we show that waterborne cues from the copepod Acartia tonsa induce paralytic shellfish toxin (PST) production in the harmful algal bloom-forming dinoflagellate Alexandrium minutum. Induced A. minutum contained up to 2.5 times more toxins than controls and was more resistant to further copepod grazing. Ingestion of non-toxic alternative prey was not affected by the presence of induced A. minutum. The ability of A. minutum to sense and respond to the presence of grazers by increased PST production and increased resistance to grazing may facilitate the formation of harmful algal blooms in the sea.     

Ecological impacts of parasitic chytrids,syndiniales and perkinsids on populations of marine photosynthetic dinoflagellates

Parasitism is a widespread interaction that plays significant roles in ecosystem balance and evolution. Historically the biology of zoosporic parasites is often a neglected field when studying aquatic ecological dynamics, especially in marine ecosystems. In the marine environment, dinoflagellates represent a significantly large component of primary production, and may be infected by a variety of fungal and fungus-like parasites including chytrids, syndiniales, and perkinsids as well as other microorganisms. The relationship between these organisms and their dinoflagellate hosts constitutes a highly significant pathosystem given the increasing importance of aquaculture. Because of their small size and lack of morphological characteristics these organisms are difficult to identify. This review compares the taxonomy, life cycle, host range, infection strategies, and ecological roles of species of Parvilucifera, Amoebophrya and Dinomyces which are parasites of dinoflagellates. Most of these species have only been described recently. Implications for environmental management are discussed.     

POSITIVE FEEDBACK AND THE DEVELOPMENT AND PERSISTENCE OF ECOSYSTEM DISRUPTIVE ALGAL BLOOMS1

Harmful algal blooms (HABs) have occurred with increasing frequency in recent years with eutrophication and other anthropogenic alterations of coastal ecosystems. Many of these blooms severely alter or degrade ecosystem function, and are referred to here as ecosystem disruptive algal blooms (EDABs). These blooms are often caused by toxic or unpalatable species that decrease grazing rates by planktonic and benthic herbivores, and thereby disrupt the transfer of nutrients and energy to higher trophic levels, and decrease nutrient recycling. Many factors, such as nutrient availability and herbivore grazing have been proposed to separately influence EDAB dynamics, but interactions among these factors have rarely been considered. Here we discuss positive feedback interactions among nutrient availability, herbivore grazing, and nutrient regeneration, which have the potential to substantially influence the dynamics of EDAB events. The positive feedbacks result from a reduction of grazing rates on EDAB species caused by toxicity or unpalatability of these algae, which promotes the proliferation of the EDAB species. The decreased rates also lower grazer‐mediated recycling of nutrients and thereby decrease nutrient availability. Since many EDAB species are well‐adapted to nutrient‐stressed environments and many exhibit increased toxin production and toxicity under nutrient limitation, positive feedbacks are established which can greatly increase the rate of bloom development and the adverse effects on the ecosystem. An understanding of how these feedbacks interact with other regulating factors, such as benthic/pelagic nutrient coupling, physical forcing, and life cycles of EDAB species provides a substantial future challenge.     

Interplay between the parasite Amoebophrya sp. (Alveolata) and the cyst formation of the red tide dinoflagellate Scrippsiella trochoidea

Syndiniales (Alveolata) are marine parasites of a wide range of hosts, from unicellular organisms to Metazoa. Many Syndiniales obligatorily kill their hosts to accomplish their life cycle. This is the case for Amoebophrya spp. infecting dinoflagellates. However, several dinoflagellate species known to be infected by these parasites produce diploid resting cysts as part of their life history. These resting cysts may survive several seasons in the sediment before germinating. How these parasites survive during the dormancy of their host remained an open question. We successfully established infections by Amoebophrya sp. in the red tide dinoflagellate Scrippsiella trochoidea. This host strain was homothallic and able to continuously produce typical calcified cysts covered by calcareous spines. Presence of the parasite significantly speeded up the host cyst production, and cysts produced were the only cells to resist infections. However, some of them were clearly infected, probably earlier in their formation. After 10 months, cysts produced in presence of the parasite were able to germinate and new infective cycles of the parasite were rapidly observed. Thus, a very novel relationship for protists is demonstrated, one in which parasite and host simultaneously enter dormancy, emerging months later to propagate both species.     

Dinoflagellate diversity and distribution

Dinoflagellates are common to abundant in both marine and freshwater environments. They are particularly diverse in the marine plankton where some cause “red tides” and other harmful blooms. More than 2,000 extant species have been described, only half of which are photosynthetic. They include autotrophs, mixotrophs and grazers. They are biochemically diverse, varying in photosynthetic pigments and toxin production ability. Some are important sources of bioluminescence in the ocean. They can host intracellular symbionts or be endosymbionts themselves. Most of the photosynthetic “zooxanthellae” of invertebrate hosts are mutualistic dinoflagellate symbionts, including all those essential to reef-building corals. Roughly 5% are parasitic on aquatic organisms. The fossil record, consisting of more than 2,500 species, shows a rapid radiation of cysts, starting in the Triassic, peaking in the Cretaceous, and declining throughout the Cenozoic. Marine species with a benthic, dormant cyst stage are confined to the continental shelf and fossil cysts can be used as markers of ancient coastlines. Northern and southern hemispheres contain virtually identical communities within similar latitudes, separated by a belt of circumtropical species. A few endemics are present in tropical and polar waters. Some benthic dinoflagellates are exclusively tropical, including a distinct phycophilic community, some of which are responsible for ciguatera fish poisoning. In lakes chemical and grazing effects can be important. Predatory dinoflagellates co-occur with their prey, often diatoms. Special Issue: Protist diversity and geographic distribution. Guest editor: W. Foissner.     

有害甲藻孢囊的分类鉴定研究进展

有害甲藻孢囊主要是指能产生毒素和(或)能引起有害藻华发生并对水生态系统产生各种危害效应的甲藻孢囊。我国沿海共记录了10属18种,占全球有害甲藻孢囊的3/4。这些有害甲藻孢囊广泛分布于我国沿海,会对水产养殖业造成严重的经济损失,甚至会威胁人类的身体健康。因此,有害甲藻孢囊的多样性及分布越来越受到人们的关注。对有害甲藻孢囊的准确判断不仅对研究其多样性及分布至关重要,而且有助于水产品的安全检验和有害藻华的早期预警。对有害甲藻孢囊的分类主要存在鉴定困难、鉴定不准确等问题。本文综述了有害甲藻孢囊的危害、中国沿海有害甲藻孢囊的种类和分布,以及有害甲藻孢囊的鉴定等3个方面的研究进展,并提出利用孢囊及营养细胞的形态学特征、分子生物学、毒理学等多学科研究手段准确鉴定有害甲藻孢囊的建议。     

Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic ecosystems

Fungal parasitism is recurrent in plankton communities, especially in the form of parasitic chytrids. However, few attempts have been made to study the community structure and activity of parasites at the natural community level. To analyse the dynamics of zoosporic fungal parasites (i.e. chytrids) of phytoplankton, samples were collected from February to December 2007 in two freshwater lakes. Infective chytrids were omnipresent in lakes, with higher diversity of parasites and infected phytoplankton than in previous studies. The abundance and biomass of parasites were significantly higher in the productive Lake Aydat than in the oligomesotrophic Lake Pavin, while the infection prevalence in both lakes were similar and averaged about 20%. The host species composition and their size appeared as critical for chytrid infectivity, the larger hosts being more vulnerable, including pennate diatoms and desmids in both lakes. The highest prevalence (98%) was noted for the autumn bloom of the cyanobacterium Anabaena flosaquae facing the parasite Rhizosiphon crassum in Lake Aydat. Because parasites killed their hosts, this implies that cyanobacterial blooms, and other large size inedible phytoplankton blooms as well, may not totally represent trophic bottlenecks because their zoosporic parasites can release dissolved substrates for microbial processes through host destruction, and provide energetic particles as zoospores for grazers. Overall, we conclude that the parasitism by zoosporic fungi represents an important ecological driving force in the food web dynamics of aquatic ecosystems, and infer general empirical models on chytrid seasonality and trophodynamics in lakes.     

Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition?

Photosynthetic dinoflagellates contain a diverse collection of plastid types, a situation believed to have arisen from multiple endosymbiotic events. In addition, a number of heterotrophic (phagotrophic) dinoflagellates possess the ability to acquire chloroplasts temporarily by engulfing algae and retaining their chloroplasts in a functional state. These latter relationships typically last from a few days to weeks, at which point the chloroplasts lose function, are digested and replaced with newly acquired plastids. A novel and abundant dinoflagellate related to the icthyotoxic genera Karenia and Karlodinium was recently discovered by us in the Ross Sea, Antarctica. Sequencing of its plastid small subunit ribosomal gene indicated that it did not share evolutionary history with the plastids of Karenia or Karlodinium, but was closely related to the free-living haptophyte Phaeocystis antarctica, a species that often dominates phytoplankton blooms in the Ross Sea. Chloroplast uptake was observed to occur rapidly (within 2 days), with retention in cultures being long-lived (several months) but not permanent. The dinoflagellate was also incapable of growing indefinitely in continuous darkness with algae as prey. Our findings may indicate an emerging endosymbiotic event yielding a dinoflagellate that is presently neither purely phototrophic nor purely heterotrophic, but occupies a niche juxtaposed between these contrasting nutritional modes.