Jonna Engström-Öst

Ecosystem Consequences of Cyanobacteria in the Northern Baltic Sea

Abstract Cyanobacteria of the Baltic Sea have multiple effects on organisms that influence the food chain dynamics on several trophic levels. Cyanobacteria contain several bioactive compounds, such as alkaloids, peptides, and lipopolysaccharides. A group of nonribosomally produced oligopeptides, namely microcystins and nodularin, are tumor promoters and cause oxidative stress in the affected cells. Zooplankton graze on cyanobacteria, and when ingested, the hepatotoxins (nodularin) decrease the egg production of, for example, copepods. However, the observed effects are very variable, because many crustaceans are tolerant to nodularin and because cyanobacteria may complement the diet of grazers in small amounts. Cyanobacterial toxins are transferred through the food web from one trophic level to another. The transfer rate is relatively low in the pelagic food web, but reduced feeding and growth rates of fish larvae have been observed. In the benthic food web, especially in blue mussels, nodularin concentrations are high, and benthic feeding juvenile flounders have been observed to disappear from bloom areas. In the littoral ecosystem, gammarids have shown increased mortality and weakening of reproductive success under cyanobacterial exposure. In contrast, mysid shrimps seem to be tolerant to cyanobacterial exposure. In fish larvae, detoxication of nodularin poses a metabolic cost that is reflected as decreased growth and condition, which may increase their susceptibility to predation. Cyanobacterial filaments and aggregates also interfere with both hydromechanical and visual feeding of planktivores. The feeding appendages of mysid shrimps may clog, and the filaments interfere with prey detection of pike larvae. On the other hand, a cyanobacterial bloom may provide a refuge for both zooplankton and small fish. As the decaying bloom also provides an ample source of organic carbon and nutrients for the organisms of the microbial loop, the zooplankton species capable of selective feeding may thrive in bloom conditions. Cyanobacteria also compete for nutrients with other primary producers and change the nitrogen (N) : phosphorus (P) balance of their environment by their N-fixation. Further, the bioactive compounds of cyanobacteria directly influence other primary producers, favoring cyanobacteria, chlorophytes, dinoflagellates, and nanoflagellates and inhibiting cryptophytes. As the selective grazers also shift the grazing pressure on other species than cyanobacteria, changes in the structure and functioning of the Baltic Sea communities and ecosystems are likely to occur during the cyanobacterial bloom season.

Climate Change and Eutrophication Induced Shifts in Northern Summer Plankton Communities

Marine ecosystems are undergoing substantial changes due to human-induced pressures. Analysis of long-term data series is a valuable tool for understanding naturally and anthropogenically induced changes in plankton communities. In the present study, seasonal monitoring data were collected in three sub-basins of the northern Baltic Sea between 1979 and 2011 and statistically analysed for trends and interactions between surface water hydrography, inorganic nutrient concentrations and phyto- and zooplankton community composition. The most conspicuous hydrographic change was a significant increase in late summer surface water temperatures over the study period. In addition, salinity decreased and dissolved inorganic nutrient concentrations increased in some basins. Based on redundancy analysis (RDA), warming was the key environmental factor explaining the observed changes in plankton communities: the general increase in total phytoplankton biomass, Cyanophyceae, Prymnesiophyceae and Chrysophyceae, and decrease in Cryptophyceae throughout the study area, as well as increase in rotifers and decrease in total zooplankton, cladoceran and copepod abundances in some basins. We conclude that the plankton communities in the Baltic Sea have shifted towards a food web structure with smaller sized organisms, leading to decreased energy available for grazing zooplankton and planktivorous fish. The shift is most probably due to complex interactions between warming, eutrophication and increased top-down pressure due to overexploitation of resources, and the resulting trophic cascades.

Turbidity decreases anti-predator behaviour in pike larvae, Esox lucius

SynopsisWe tested how algal turbidity and light conditions influence anti-predator behaviour of first-feeding pike. Results showed that pike larvae were able to detect the predator by both chemical and visual signals in turbid water. However, the anti-predator behaviour was reduced in turbid water compared with clear water. Larvae hid in the vegetation in the presence of predator cues more in clear water than in turbid water. The attack rate on zooplankton in clear water was lower in the presence of predator cues, whereas no such difference was detected in turbid water. Both of these results indicate that turbidity acted as a refuge for larvae. Light proved to be an important regulating factor for feeding pike in the absence of predators, demonstrated as lowered attack rates in 50 light level in both clear and turbid water. This indicates that long-term turbidity may be critical for small larvae, which need to feed continuously to survive.

The Relevance of Marine Chemical Ecology to Plankton and Ecosystem Function: An Emerging Field

Marine chemical ecology comprises the study of the production and interaction of bioactive molecules affecting organism behavior and function. Here we focus on bioactive compounds and interactions associated with phytoplankton, particularly bloom-forming diatoms, prymnesiophytes and dinoflagellates. Planktonic bioactive metabolites are structurally and functionally diverse and some may have multiple simultaneous functions including roles in chemical defense (antipredator, allelopathic and antibacterial compounds), and/or cell-to-cell signaling (e.g., polyunsaturated aldehydes (PUAs) of diatoms). Among inducible chemical defenses in response to grazing, there is high species-specific variability in the effects on grazers, ranging from severe physical incapacitation and/or death to no apparent physiological response, depending on predator susceptibility and detoxification capability. Most bioactive compounds are present in very low concentrations, in both the producing organism and the surrounding aqueous medium. Furthermore, bioactivity may be subject to synergistic interactions with other natural and anthropogenic environmental toxicants. Most, if not all phycotoxins are classic secondary metabolites, but many other bioactive metabolites are simple molecules derived from primary metabolism (e.g., PUAs in diatoms, dimethylsulfoniopropionate (DMSP) in prymnesiophytes). Producing cells do not seem to suffer physiological impact due to their synthesis. Functional genome sequence data and gene expression analysis will provide insights into regulatory and metabolic pathways in producer organisms, as well as identification of mechanisms of action in target organisms. Understanding chemical ecological responses to environmental triggers and chemically-mediated species interactions will help define crucial chemical and molecular processes that help maintain biodiversity and ecosystem functionality.

Maternal Effects May Act as an Adaptation Mechanism for Copepods Facing pH and Temperature Changes

Acidification of the seas, caused by increased dissolution of CO2 into surface water, and global warming challenge the adaptation mechanisms of marine organisms. In boreal coastal environments, temperature and pH vary greatly seasonally, but sometimes also rapidly within hours due to upwelling events. We studied if copepod zooplankton living in a fluctuating environment are tolerant to climate change effects predicted for 2100, i.e., a temperature increase of 3°C and a pH decrease of 0.4. Egg production of the copepod Acartia sp. was followed over five consecutive days at four temperature and pH conditions (17°C/ambient pH; 17°C/low pH; 20°C/ambient pH; 20°C/low pH). Egg production was higher in treatments with warmer temperature but the increase was smaller when copepods were simultaneously exposed to warmer temperature and lowered pH. To reveal if maternal effects are important in terms of adaptation to a changing environment, we conducted an egg transplantation experiment, where the produced eggs were moved to a different environment and egg hatching was monitored for three days. When pH changed between the egg production and hatching conditions, it resulted in lower hatching success, but the effect was diminished over the course of the experiment possibly due to improved maternal provisioning. Warmer egg production temperature induced a positive maternal effect and increased the egg hatching rate. Warmer hatching temperature resulted also in earlier hatching. However, the temperature effects appear to be dependent on the ambient sea temperature. Our preliminary results indicate that maternal effects are an important mechanism in the face of environmental change.

Does cyanobacterial toxin accumulate in mysid shrimps and fish via copepods

It has been suggested that pelagic planktivores may receive cyanobacterial toxins indirectly, i.e., by preying on organisms that have ingested cyanobacteria. We tested this hypothesis in laboratory conditions by providing mysid shrimps, Mysis relicta, and three-spined sticklebacks, Gasterosteus aculeatus, with cyanobacteria-fed copepods. The aim of the study was to observe the potential transfer and accumulation of the toxin nodularin, produced by the cyanobacteria Nodularia spumigena, in planktivore tissue during the 10-day trials. The concentration of nodularin was measured by two toxin detection methods, enzyme-linked immunosorbent assay (ELISA) and protein phosphatase (PPase) inhibition assay. The ELISA results showed that the toxin concentrations in mysid tissue were significantly higher than in fish tissue, whereas no differences between species were detected by PPase inhibition assay. The concentrations measured by ELISA suggested that accumulation had taken place in mysids, since the toxin increased with time in the animals. The concentrations, measured by PPase inhibition assay, were significantly higher than the ones measured by ELISA. We conclude that cyanobacterial toxin may accumulate in higher trophic levels via copepods and that the results are more reliable if analysed with several methods.

Projected marine climate change: effects on copepod oxidative status and reproduction

Zooplankton are an important link between primary producers and fish. Therefore, it is crucial to address their responses when predicting effects of climate change on pelagic ecosystems. For realistic community-level predictions, several biotic and abiotic climate-related variables should be examined in combination. We studied the combined effects of ocean acidification and global warming predicted for year 2100 with toxic cyanobacteria on the calanoid copepod, Acartia bifilosa. Acidification together with higher temperature reduced copepod antioxidant capacity. Higher temperature also decreased egg viability, nauplii development, and oxidative status. Exposure to cyanobacteria and its toxin had a negative effect on egg production but, a positive effect on oxidative status and egg viability, giving no net effects on viable egg production. Additionally, nauplii development was enhanced by the presence of cyanobacteria, which partially alleviated the otherwise negative effects of increased temperature and decreased pH on the copepod recruitment. The interactive effects of temperature, acidification, and cyanobacteria on copepods highlight the importance of testing combined effects of climate-related factors when predicting biological responses.

Feeding and Refuge Use by Small Fish in the Presence of Cyanobacteria Blooms

We studied the effect of cyanobacteria on foraging and refuge use in small fish. We measured pike larval feeding in the presence of cyanobacteria by counting leftover prey. Our results showed that feeding by pike larvae on zooplankton prey decreased significantly in the presence of non-toxic cyanobacteria. The behaviour can be due to lowered vision caused by turbidity or clogging of the gills. Further, we tested whether the three-spined stickleback use toxic cyanobacteria as a refuge against predators in a choice experiment. The choice experiment was performed in a Y-maze fluviarum, where the fish could select between two different environments. Our results support the refuge use hypothesis because the three-spined stickleback clearly preferred toxic cyanobacteria to the chemical predator signal. To conclude, cyanobacteria decrease feeding rates in fish larvae, but may function as important refuge for e.g. sticklebacks, during predation pressure in pelagic algal blooms.

Bloom-Forming Cyanobacteria Support Copepod Reproduction and Development in the Baltic Sea

It is commonly accepted that summer cyanobacterial blooms cannot be efficiently utilized by grazers due to low nutritional quality and production of toxins; however the evidence for such effects in situ is often contradictory. Using field and experimental observations on Baltic copepods and bloom-forming diazotrophic filamentous cyanobacteria, we show that cyanobacteria may in fact support zooplankton production during summer. To highlight this side of zooplankton-cyanobacteria interactions, we conducted: (1) a field survey investigating linkages between cyanobacteria, reproduction and growth indices in the copepod Acartia tonsa; (2) an experiment testing relationships between ingestion of the cyanobacterium Nodularia spumigena (measured by molecular diet analysis) and organismal responses (oxidative balance, reproduction and development) in the copepod A. bifilosa; and (3) an analysis of long term (1999–2009) data testing relationships between cyanobacteria and growth indices in nauplii of the copepods, Acartia spp. and Eurytemora affinis, in a coastal area of the northern Baltic proper. In the field survey, N. spumigena had positive effects on copepod egg production and egg viability, effectively increasing their viable egg production. By contrast, Aphanizomenon sp. showed a negative relationship with egg viability yet no significant effect on the viable egg production. In the experiment, ingestion of N. spumigena mixed with green algae Brachiomonas submarina had significant positive effects on copepod oxidative balance, egg viability and development of early nauplial stages, whereas egg production was negatively affected. Finally, the long term data analysis identified cyanobacteria as a significant positive predictor for the nauplial growth in Acartia spp. and E. affinis. Taken together, these results suggest that bloom forming diazotrophic cyanobacteria contribute to feeding and reproduction of zooplankton during summer and create a favorable growth environment for the copepod nauplii.

Long-term monitoring data reveal pH dynamics, trends and variability in the Western Gulf of Finland

Monitoring data on water pH are presented for the period between 1972 and 2009 from the sampling stations Längden and Storgadden, at the entrance to the Gulf of Finland, Baltic Sea. The overall pH in the area ranged from 9.2 to 7.4, on average 8.1, and showed a significant decreasing trend during the winter period corresponding to a median annual decrease of 0.006. The data corroborate previous findings about a seasonal effect, where pH is higher during summer than winter.