Evidence of phagotrophy in Dinophysis fortii (Dinophysiales, Dinophyceae), a dinoflagellate that causes diarrhetic shellfish poisoning (DSP)

Food vacuoles were found in one species of pho‐totrophic Dinophysis, Dinophysis fortii Pavillard, collected in Okkirai Bay. Under transmission electron microscopy, almost 70% of observed food vacuoles were characterized by membranous profiles and contained large numbers of mitochondria. The mitochondria in the food vacuole had different morphologies from those in the D. fortii cytoplasm. This indicates that these vacuoles are not autolytic accumulation bodies, but ‘true’ food vacuoles. Identification of the origin of the contents failed, but the existence of large amounts of foreign mitochondria implies that the contents in the vacuoles were derived from eukaryotic prey. Other than the observation of the food vacuoles, bacterial cells were observed in the flagellar canal. Because the flagellar canal and connecting pusule sacs had been reported to relate to macromolecule uptake, the prey organisms of D. fortii were assumed to be both eukaryotic and prokaryotic organisms.     

Marine microalgae attack and feed on metazoans

Free-living microalgae from the dinoflagellate genus Karlodinium are known to form massive blooms in eutrophic coastal waters worldwide and are often associated with fish kills. Natural bloom populations, recently shown to consist of the two mixotrophic and toxic species Karlodinium armiger and Karlodinium veneficum have caused fast paralysis and mortality of finfish and copepods in the laboratory, and have been associated with reduced metazooplankton biomass in-situ. Here we show that a strain of K. armiger (K-0688) immobilises the common marine copepod Acartia tonsa in a density-dependent manner and collectively ingests the grazer to promote its own growth rate. In contrast, four strains of K. veneficum did not attack or affect the motility and survival of the copepods. Copepod immobilisation by the K. armiger strain was fast (within 15 min) and caused by attacks of swarming cells, likely through the transfer and action of a highly potent but uncharacterised neurotoxin. The copepods grazed and reproduced on a diet of K. armiger at densities below 1000, cells ml⁻¹, but above 3500 cells ml⁻¹ the mixotrophic dinoflagellates immobilised, fed on and killed the copepods. Switching the trophic role of the microalgae from prey to predator of copepods couples population growth to reduced grazing pressure, promoting the persistence of blooms at high densities. K. armiger also fed on three other metazoan organisms offered, suggesting that active predation by mixotrophic dinoflagellates may be directly involved in causing mortalities at several trophic levels in the marine food web.     

The role of C, N and P in dissolved and particulate organic matter as a nutrient source for phytoplankton growth, including toxic species

Phytoplankton have traditionally been regarded as strictly phototrophic, with a well defined position at the base of pelagic food webs. However, recently we have learned that the nutritional demands of a growing number of phytoplankton species can be met, at least partially, or under specific environmental conditions, through heterotrophy. Mixotrophy is the ability of an organism to be both phototrophic and heterotrophic, in the latter case utilizing either organic particles (phagotrophy) or dissolved organic substances (osmotrophy). This finding has direct implications for our view on algal survival strategies, particularly for harmful species, and energy- and nutrient flow in pelagic food webs. Mixotrophic species may outcompete strict autotrophs, e.g. in waters poor in inorganic nutrients or under low light. In the traditional view of the ‘microbial loop’ DOC is thought to be channeled from algal photosynthesis to bacteria and then up the food chain through heterotrophic flagellates, ciliates and mesozooplankton. Are mixotrophic phytoplankton that feed on bacteria also significantly contributing to this transport of photosynthetic carbon up the food chain? How can we estimate the fluxes of carbon and nutrients between different trophic levels in the plankton food web involving phagotrophic algae? These questions largely remain unanswered. In this review we treat evidence for both osmotrophy and phagotrophy in phytoplankton, especially toxic marine species, and some ecological implications of mixotrophy.     

Effects of prey abundance and light intensity on the mixotrophic chrysophyte Poterioochromonas malhamensis from a mesotrophic lake

1. Previous studies of mixotrophy in the flagellate Poterioochromonas malhamensis (Chrysophyceae) were performed on strains that had been in culture for > 30 years. This study aims to compare mixotrophy in a cultured strain with one recently isolated from a mesotrophic lake (Lacawac) in Pennsylvania, U.S.A. 2. P. malhamensis from the lake exhibited a nutritional flexibility similar to that of the culture strain, growing phototrophically but inefficiently in comparison to other nutritional modes (growth rate (μ) = 0.015 h^?1). Supplementing an inorganic salts medium with 1 mM glucose resulted in a doubling of μ to 0.035 h^?1 and 0.033 h^?1 in the light and the dark, respectively. Addition of an algal prey, Nannochloris, to the inorganic salts medium increased growth to rates similar to those observed with glucose. Maximum growth of the lake strain, 0.095 h^?1, was achieved when bacteria was supplied as food. During growth on bacteria, cellular chlorophyll a (Chl a) decreased from 140 fg cell^?1 to 10 fg cell^?1 over 22 h when cultured either in the light or dark. In illuminated cultures, cell-specific Chl a concentration recovered to 185 fg cell^?1 after bacteria became limiting. 3. In contrast to the cultured strain, however, the lake isolate exhibited an inverse relationship between light intensity and ingestion rate. Calculated grazing rates, based upon the ingestion of fluorescently labeled bacteria, were 3.2, 5.2 and 9.4 bacteria flagellate^?1 h^?1, for P. malhamensis incubated in high light, low light and darkness, respectively. Phagotrophy is thus influenced by a light regime in this predominately heterotrophic mixotroph.     

Biomass and feeding activity of phagotrophic mixotrophs in the northwestern Black Sea during the summer 1995

Biomass and activities of planktonicmicroorganisms (bacteria, nanoplankton andmicroplankton) were measured in the northwestern BlackSea during summer 1995. The method based on theuptake of fluorescently labeled prey was chosen todetermine the ingestion rate of bacteria andnanoplankton by phagotrophic microorganisms. Thismethod revealed the presence of mixotrophic organismssuch as ’plastid-retaining ciliates‘ in the wholecoastal area. Mixotrophic ciliates were dominated bymicro-sized forms and maximum biomasses were recorded inthe water masses characterised by low nutrientconcentrations but high food particle concentrations. Mixotrophic nanoflagellates were absentand mixotrophic dinoflagellates were observed at onestation only. Mixotrophic ciliates were shown to ingestpreferably bacteria while mixotrophic dinoflagellateswere grazing almost exclusively on nanoflagellates.Although the biomass of mixotrophic organisms weresignificantly lower than those of aplastidic protozoa,their feeding activity contributed to 14 and 24% ofthe ingestion of bacteria and nanoplankton, respectively.This is due to the high specificingestion rate of mixotrophic micro-sized ciliates anddinoflagellates, which were two and three times higher,respectively, than the specific ingestion rate ofbacteria and nanoplankton by aplastidic protozoa. Thissuggests a significant contribution of phagotrophicmixotrophs to the microbial network of thenorthwestern Black Sea. This revised version was published online in July 2006 with corrections to the Cover Date.     

Impact of a Flood Event on the Planktonic Food Web of the Schelde Estuary (Belgium) in Spring 1998

To evaluate the effect of short-term changes in discharge on plankton dynamics, a station in the upper reaches of the Schelde estuary was monitored during 1 month in spring 1998 with a sampling frequency of 1–2 days. During this monitoring period, a flood event occurred during which discharge increased about 5-fold. This flood event had a strong effect on the composition of the planktonic community. Rotifers were strongly negatively affected by the flood event while densities of heterotrophic nanoflagellates and scuticociliates increased. Chlorophyll a concentration and abundance of bacteria, oligotrich ciliates and crustacean zooplankton did not respond clearly to the flood event. Although the flood event lasted only a few days it took more than 2 weeks for the planktonic community to return to its original composition.     

PLANKTONIC SARCODINES: MICROHABITAT FOR OCEANIC DINOFLAGELLATES1

Two morphologically distinct species of free-swimming dinoflagellates belonging to the genus Gyrodinium utilize the spine and rhizopodial environments of planktonic foraminifera and colonial radiolaria as microhabitats. Up to 84% of the sarcodines examined in a given population were associated with these dinoflagellates at densities up to 20,000 cells per sarcodine in some radiolarian colonies. Both dinoflagellate species possess chloroplasts, indicating they are capable of autotrophy. ¹⁴C-labelling experiments with the radiolarian-associated dinoflagellate demonstrate that it can take up inorganic carbon under both light and dark conditions. Ultrastructural evidence suggests the foraminiferal dinoflagellate may be capable of phagotrophy. Hence, these algae should be considered mixotrophs. An unusual cytoplasmic extension used for attachment and possibly feeding occurs in the foraminiferal-associated Gyrodinium and is documented with electron microscopy. Ultrastructural examination suggests this organelle may be hydrostatically controlled and may be an extension of the sac pusule.     

Significance of predation by protists in aquatic microbial food webs

Predation in aquatic microbial food webs is dominated by phagotrophic protists, yet these microorganisms are still understudied compared to bacteria and phytoplankton. In pelagic ecosystems, predaceous protists are ubiquitous, range in size from 2 μm flagellates to >100 μm ciliates and dinoflagellates, and exhibit a wide array of feeding strategies. Their trophic states run the gamut from strictly phagotrophic, to mixotrophic: partly autotrophic and partly phagotrophic, to primarily autotrophic but capable of phagotrophy. Protists are a major source of mortality for both heterotrophic and autotrophic bacteria. They compete with herbivorous meso- and macro-zooplankton for all size classes of phytoplankton. Protist grazing may affect the rate of organic sinking flux from the euphotic zone. Protist excretions are an important source of remineralized nutrients, and of colloidal and dissolved trace metals such as iron, in aquatic systems. Work on predation by protists is being facilitated by methodological advances, e.g., molecular genetic analysis of protistan diversity and application of flow cytometry to study population growth and feeding rates. Examples of new research areas are studies of impact of protistan predation on the community structure of prey assemblages and of chemical communication between predator and prey in microbial food webs. This revised version was published online in August 2006 with corrections to the Cover Date.     

Short‐term temperature change may impact freshwater carbon flux: a microbial perspective

Small freshwater bodies are abundant and economically and ecologically important on a global scale. Within these, protozoa play an important role in structuring planktonic food webs and sequestering CO₂. We hypothesized that short‐term (～20 days) fluctuations, of 2–10 °C, will significantly alter carbon flux associated with predator–prey interactions within the microbial planktonic food web. We examined the model ciliate, Urotricha farcta, which is abundant and common; it was fed the autotrophic flagellate Cryptomonas sp., which is also common. Laboratory experiments were conducted over relevant ranges: 8–24 °C; 0–2 × 10⁵ prey mL^?1. Mechanistic‐phenomenological multiple regressions were developed and fit to the data to obtain relationships for (1) growth rate and volume changes of the flagellate vs. temperature and (2) growth rates, grazing, and cell volume change of the ciliate vs. temperature and prey concentration. Responses revealed interaction between temperature and prey levels on all ciliate parameters, indicating it is inappropriate to apply simple temperature corrections (e.g. Q₁₀) to such functions. The potential impact of such temperature changes on carbon flux was illustrated using a simple ciliate–flagellate predator–prey model, with and without the top grazer, Daphnia, added. The model indicated that predator–prey pulses occurred over 20 days, with the ciliate controlling the prey population. For ciliates and prey, carbon production peaked at 20 °C and rapidly decreased above and below this maximum; differences between minimum and maximum were approximately fourfold, for both prey and ciliate, with low levels at 25–30 °C and 10–15 °C. Including literature data to parameterize, the influence of the grazer Daphnia did not alter the prediction that the ciliate may control short‐term flagellate pulses and temperature will influence these in a nonintuitive fashion.     

Planktonic food web in marine mesocosms in the Eastern Mediterranean: bottom-up or top-down regulation?

A mesocosm experiment was conducted in order to studythe structure of the planktonic food web. The dynamicsof pico-, nano- and microplankton populations werefollowed during 40 days in four large (40 m³)enclosures. In three tanks a gradient of addednutrients (nitrogen and phosphorus) was applied, whilea fourth tank was used as a control. On day 14, thetop predator (sea bream Sparus aurata larvae)was introduced into the tanks and part of the watercolumn in each tank was isolated in a plastic bagwithout fish larvae, to act as a control forpredation. Physical parameters, chlorophyll aand nutrient concentrations, as well as planktonconcentrations were monitored. A diatom bloom wasobserved in all four tanks, in the first phase endingwith silicate depletion. Flagellate and dinoflagellateabundance subsequently increased, these organismsbeing limited by zooplankton grazing. The zooplanktonpopulations were controlled by both resources (mostlyflagellates) and predation (by fish larvae) asindicated by the results of the control experiments. This revised version was published online in July 2006 with corrections to the Cover Date.     

微型浮游生物生态学研究概述

最近一二十年来,原绿藻和微食物网的重大发现已使人们充分认识到微型浮游生物在水域生态系统的养分循环和能量流动中的重要意义,也为微型浮游生物的研究提出了新的方向。对微型浮游生物的主要类群,即微型浮游植物、异养细菌和微型浮游动物的生态学研究进展作了概述,在此基础上讨论了类群间的生态关系和微食物网的研究动向。最后对微型游生物生态学的继续研究提出了几点看法。     

海洋中的凝集网与透明胞外聚合颗粒物

透明胞外聚合颗粒物(TEP)是海洋中大量存在的能被爱尔新蓝(alcian blue)染色的由酸性多糖组成的透明胶状颗粒物,主要来源于浮游植物,由于其透明的特性而被长期忽视。TEP同时具有胶体和颗粒物的特性。作为胶体,TEP为细菌提供了栖息场所与降解基质,同时TEP可以吸收痕量元素,以改变这些元素的生物地球化学过程。作为颗粒物,TEP可以聚集并沉降,由于其高的碳含量,会在很大程度上影响海洋的碳通量。由于TEP可以被中型浮游动物所摄食,所以TEP可以连接并缩短微食物环和经典食物链,在海洋生态系统中起很重要的作用。介绍了TEP的定义、测量方法、来源、形成、及其与浮游植物的关系和其生态功能。     

δ15N of zooplankton species in subarctic lakes in northern Sweden: effects of diet and trophic fractionation

1. To assess the use of stable nitrogen isotopes (δ¹⁵N) for reconstructing trophic relationships in planktonic food webs, crustacean zooplankton species and pelagic dissolved and particulate matter were analysed in 14 subarctic lakes in northern Sweden. The lakes are situated along an altitudinal gradient and show a substantial variation in nutrient content and energy mobilization by bacterioplankton and phytoplankton. 2. The δ¹⁵N of dissolved and particulate matter was comparatively low, suggesting efficient N recycling and low losses of depleted N from the pelagic zone of these unproductive lakes. 3. Copepods had a systematically higher δ¹⁵N than cladocerans, with an average difference of 3.1–4.9‰ within lakes, implying different trophic positions of the two groups. Comparisons of nitrogen pools and energy fluxes suggest that the low cladoceran δ¹⁵N was a result of feeding on bacteria. 4. The difference in δ¹⁵N between copepods and cladocerans declined with decreasing bacterioplankton production among lakes, due either to increasing trophic isotope fractionation or decreasing relative importance of bacteria in the diet of cladocerans.     

持久性有机污染物在水生食物网中的传递行为

食物网是持久性有机污染物(POPs)在水生生态系统中传递的重要途径,了解其传递行为与机制是POPs生态暴露风险评价的科学基础。从4个方面展开了讨论和分析:(1)食物网主要特征(营养级和食物链长度)与POPs环境行为的关系;(2)POPs在底栖及底栖-浮游耦合食物网中的环境行为;(3)微食物网对POPs环境行为的作用;(4)食物网的变化对POPs环境行为的影响。主要结论如下:(1)已有研究对水生生物中POPs生物放大作用存在较大争议。一般营养级越高,POPs生物富集性越强,但由于各种生态和生理性质的影响,也存在例外情况。食物链长度与POPs生物富集性呈正相关。(2)POPs通过底栖食物网将沉积物中的POPs向上传递,底栖-浮游食物网的耦合提高了高营养级消费者的暴露风险,目前就POPs在底栖食物网中的生物放大性是否大于浮游食物网存在争议。(3)微生物具有较大的比表面积,是吸附POPs的重要载体。另,沉积物中的微生物通过分解有机质,将POPs释放到水柱中。微生物降解也是环境中POPs脱离环境的重要途径。(4)在内、外压力下,食物网结构和功能发生变化,使物质和能量的传递方向和效率发生改变,并与环境理化性质的变化互相耦合,影响POPs的环境行为。当前研究的重点多集中在POPs在浮游食物网,尤其是高营养级浮游食物网中的环境行为,对POPs在底栖及底栖-浮游耦合食物网和微食物网中环境行为的研究相对缺乏。有关POPs在食物网中环境行为的研究多集中在食物网的某个部分,时间尺度较短,缺乏对POPs环境行为动态变化的研究,未来需深入开展多尺度和多角度的POPs在食物网中环境行为的动态变化研究。新型POPs的生产和使用量不断增加,但有关其在食物网中环境行为的相关分析还较为匮乏,需加强研究。