Changes in marine dinoflagellate and diatom abundance under climate change

Marine diatoms and dinoflagellates play a variety of key ecosystem roles as important primary producers (diatoms and some dinoflagellates) and grazers (some dinoflagellates). Additionally some are harmful algal bloom (HAB) species and there is widespread concern that HAB species may be increasing accompanied by major negative socio-economic impacts, including threats to human health and marine harvesting1, 2. Using 92,263 samples from the Continuous Plankton Recorder survey, we generated a 50-year (1960–2009) time series of diatom and dinoflagellate occurrence in the northeast Atlantic and North Sea. Dinoflagellates, including both HAB taxa (for example, Prorocentrum spp.) and non-HAB taxa (for example, Ceratium furca), have declined in abundance, particularly since 2006. In contrast, diatom abundance has not shown this decline with some common diatoms, including both HAB (for example, Pseudo-nitzschia spp.) and non-HAB (for example, Thalassiosira spp.) taxa, increasing in abundance. Overall these changes have led to a marked increase in the relative abundance of diatoms versus dinoflagellates. Our analyses, including Granger tests to identify criteria of causality, indicate that this switch is driven by an interaction effect of both increasing sea surface temperatures combined with increasingly windy conditions in summer.

Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp.

Receiving coastal waters and estuaries are among the most nutrient-enriched environments on earth, and one of the symptoms of the resulting eutrophication is the proliferation of opportunistic, fast-growing marine seaweeds. Here, we used a widespread macroalga often involved in blooms, Ulva spp., to investigate how supply of nitrogen (N) and phosphorus (P), the two main potential growth-limiting nutrients, influence macroalgal growth in temperate and tropical coastal waters ranging from low- to high-nutrient supplies. We carried out N and P enrichment field experiments on Ulva spp. in seven coastal systems, with one of these systems represented by three different subestuaries, for a total of nine sites. We showed that rate of growth of Ulva spp. was directly correlated to annual dissolved inorganic nitrogen (DIN) concentrations, where growth increased with increasing DIN concentration. Internal N pools of macroalgal fronds were also linked to increased DIN supply, and algal growth rates were tightly coupled to these internal N pools. The increases in DIN appeared to be related to greater inputs of wastewater to these coastal waters as indicated by high delta 15N signatures of the algae as DIN increased. N and P enrichment experiments showed that rate of macroalgal growth was controlled by supply of DIN where ambient DIN concentrations were low, and by P where DIN concentrations were higher, regardless of latitude or geographic setting. These results suggest that understanding the basis for macroalgal blooms, and management of these harmful phenomena, will require information as to nutrient sources, and actions to reduce supply of N and P in coastal waters concerned.

Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 at tropical reservoir and its relation to environmental variables

Dinoflagellates of the genus Ceratium are chiefly marine but there are rare occurrences in freshwater. In this study we analyze the invasion and progressive establishment of Ceratium furcoides, an exotic species, in the Furnas Reservoir. Samples were taken at 36 points in the reservoir, during the months of March, June, September and December, 2007. Measurements of some physical and chemical variables were simultaneously performed at each site. The occurrence of C. furcoides was registered at 20 sites, with densities varying between 0.57 and 28,564,913.0 ind.m(-3). Blooms of this species were recorded in points which were classified as mesotrophic, coinciding with the places receiving high amounts of untreated domestic sewage. C. furcoides density was correlated with temperature, nutrients (nitrate and nitrite) and water electric conductivity. The highest density was recorded in June when temperature was low. The presence of Ceratium furcoides in the reservoir apparently has not yet affected the reservoir water quality or other plankton communities. However, if it becomes fully established it could perhaps become a problem in the reservoir or even to spread out to other reservoirs in Rio Grande basin.

Invasion of the dinoflagellate Ceratium furcoides (Levander) Langhans 1925 at tropical reservoir and its relation to environmental variables

Dinoflagellates of the genus Ceratium are chiefly marine but there are rare occurrences in freshwater. In this study we analyze the invasion and progressive establishment of Ceratium furcoides, an exotic species, in the Furnas Reservoir. Samples were taken at 36 points in the reservoir, during the months of March, June, September and December, 2007. Measurements of some physical and chemical variables were simultaneously performed at each site. The occurrence of C. furcoides was registered at 20 sites, with densities varying between 0.57 and 28,564,913.0 ind.m-3. Blooms of this species were recorded in points which were classified as mesotrophic, coinciding with the places receiving high amounts of untreated domestic sewage. C. furcoides density was correlated with temperature, nutrients (nitrate and nitrite) and water electric conductivity. The highest density was recorded in June when temperature was low. The presence of Ceratium furcoides in the reservoir apparently has not yet affected the reservoir water quality or other plankton communities. However, if it becomes fully established it could perhaps become a problem in the reservoir or even to spread out to other reservoirs in Rio Grande basin.

Data base on pelagic ciliates grazing and growth rate as a function of size, prey size and type compiled from the literature

Microzooplankton (the 20 to 200 µm size class of zooplankton) is recognised as an important part of marine pelagic ecosystems. In terms of biomass and abundance pelagic ciliates are one of the important groups of organism in microzooplankton. However, their rates - grazing and growth - , feeding behaviour and prey preferences are poorly known and understood. A set of data was assembled in order to derive a better understanding of pelagic ciliates rates, in response to parameters such as prey concentration, prey type (size and species), temperature and their own size. With these objectives, literature was searched for laboratory experiments with information on one or more of these parameters effect studied. The criteria for selection and inclusion in the database included: (i) controlled laboratory experiment with a known ciliates feeding on a known prey; (ii) presence of ancillary information about experimental conditions, used organisms - cell volume, cell dimensions, and carbon content. Rates and ancillary information were measured in units that meet the experimenter need, creating a need to harmonize the data units after collection. In addition different units can link to different mechanisms (carbon to nutritive quality of the prey, volume to size limits). As a result, grazing rates are thus available as pg C/(ciliate*h), µm**3/(ciliate*h) and prey cell/(ciliate*h); clearance rate was calculated if not given and growth rate is expressed as the growth rate per day.

A molecular basis for polyketide biosynthesis in marine dinoflagellates with emphasis on Karenia brevis

Polyketides derived from dinoflagellates are among the most complex and unique structures identified to date. The carbon framework of all polyketides is assembled by a polyketide synthase (PKS). No studies of the biosynthesis of dinoflagellate derived polyketides at the genomic level have been reported to date. Nine strains representing seven different species of dinoflagellates were screened for the presence of type I and type II polyketide synthases (PKS) by PCR and RT-PCR. Seven of the nine strains yielded products that were homologous with known and putative type I polyketide synthases. In each case, the presence of a PKS gene was correlated with the presence of bacteria in the cultures as identified by amplification of the bacterial 16S rRNA gene. However, residual phylogenetic signals, resistance to methylation sensitive restriction enzymes and the lack of hybridization to bacterial isolates support a dinoflagellate origin for most of these genes. ^ A more detailed analysis of Karenia brevis, a toxic marine dinoflagellate endemic to the Gulf of Mexico, also supports the hypothesis that dinoflagellates have polyketide synthase genes. Blooms of this harmful alga cause fish kills, marine mammal mortalities and neurotoxic shellfish poisonings. These harmful effects are attributed to a suite of polyketide secondary metabolites known as the brevetoxins. PKS encoding genes amplified from K. brevis culture were found to be similar to PKS genes from the closely related protist, Cryptosporidium parvum. This suggested that these genes originate from the dinoflagellate. However, K. brevis has not been grown axenically. The associated bacteria might be the source of the toxins or the PKS genes. This dissertation reports the localization of these PKS encoding genes by a combination of flow cytometry/PCR and fluorescence in situ hybridization (FISH). Two genes localized exclusively to K. brevis cells while a third localized to both K. brevis and associated bacteria. While these genes have not yet been linked to toxin production, the work describes the first definitive evidence of resident PKS genes in any dinoflagellate. ^

The role of dissolved organic matter bioavailability in promoting phytoplankton blooms in Florida Bay

The clear, shallow, oligotrophic waters of Florida Bay are characterized by low phytoplankton biomass, yet periodic cyanobacteria and diatom blooms do occur. We hypothesized that allochthonous dissolved organic matter (DOM) was providing a subsidy to the system in the form of bound nutrients. Water from four bay sites was incubated under natural light and dark conditions with enrichments of either DOM ( > 1 kD, 2×DOM) or inorganic nutrients (N+P). Samples were analyzed for bacterial numbers, bacterial production, phytoplankton biomass, phytoplankton community structure, and production, nutrients, and alkaline phosphatase (AP) activity. The influence of 2×DOM enrichment on phytoplankton biomass developed slowly during the incubations and was relatively small compared to nutrient additions. Inorganic nutrient additions resulted in an ephemeral bloom characterized initially as cyanobacterial and brown algae but which changed to dinoflagellate and/or brown algae by day six. The DIN:TP ratio decreased 10-fold in the N+P treatments as the system progressed towards N limitation. This ratio did not change significantly for 2×DOM treatments. In addition, these experiments indicated that both autotrophic and heterotrophic microbial populations in Florida Bay may fluctuate in their limitation by organic and inorganic nutrient availability. Both N+P and 2×DOM enrichments revealed significant and positive response in bioavailability of dissolved organic carbon (BDOC). Potential BDOC ranged from 1.1 to 35.5%, with the most labile forms occurring in Whipray Basin. BDOC at all sites was stimulated by the 2×DOM addition. Except for Duck Key, BDOC at all sites was also stimulated by the addition of N+P. BDOC was lower in the dry season than in the wet season (5.56% vs. 16.86%). This may be explained by the distinct chemical characteristics of the DOM produced at different times of year. Thus, both the heterotrophic and autotrophic microbial communities in Florida Bay are modulated by bioavailability of DOM. This has ramifications for the fate of DOM from the Everglades inputs, implicating DOM bioavailability as a contributing factor in regulating the onset, persistence, and composition of phytoplankton blooms.

Potential role of sponge communities in controlling phytoplankton blooms in Florida Bay

An unprecedented series of ecological disturbances have been recurring within Florida Bay since the summer of 1987. Persistent and widespread phytoplankton and cyanobacteria blooms have coincided with the large scale decimation of sponge communities. One hypothesis is that the large scale loss of suspension-feeding sponges has rendered the Florida Bay ecosystem susceptible to these recurring blooms. The primary objective of this study was to experimentally evaluate the potential for suspension-feeding sponges to control nuisance phytoplankton blooms within Florida Bay prior to a large sponge die-off event. To achieve this objective, we determined the extent and biomass of the surviving sponge community in the different basins of Florida Bay. Many areas within Florida Bay possessed sponge densities and biomasses of 1 to 3 ind. m–2 or 100 to 300 g m–2 respectively. The dominant species includedSpheciospongia vesparia, Chondrilla nucula, Cinachyra alloclada, Tedania ignis and Ircinia sp., which accounted for 68% of individual sponges observed and 88% of sponge biomass. Laboratory grazing rates of these dominant sponges were experimentally determined on 4 different algal food treatments: a monoculture of cyanobacteria Synechococcus elongatus, a monoculture of the diatom Cyclotella choctawhatcheeana, a monoculture of the dinoflagellate Prorocentrum hoffmanianum, and an equal volume of the 3 monocultures combined. To estimate the impact of a mass sponge mortality event on the system-wide filtration rate of Florida Bay, we combined estimates of the current sponge biomass and laboratory sponge filtration rates with estimates of mean volumes of the sub-basins of Florida Bay. This study implies that the current blooms occurring within the central region of Florida Bay can be explained by the loss of the dominant suspension feeder in this system, and there is no need to invoke a new addition of nutrients within this region for the blooms to occur.

Data compilation on the biological response to ocean acidification: environmental and experimental context of data sets and related literature

The exponential growth of studies on the biological response to ocean acidification over the last few decades has generated a large amount of data. To facilitate data comparison, a data compilation hosted at the data publisher PANGAEA was initiated in 2008 and is updated on a regular basis (doi:10.1594/PANGAEA.149999). By January 2015, a total of 581 data sets (over 4 000 000 data points) from 539 papers had been archived. Here we present the developments of this data compilation five years since its first description by Nisumaa et al. (2010). Most of study sites from which data archived are still in the Northern Hemisphere and the number of archived data from studies from the Southern Hemisphere and polar oceans are still relatively low. Data from 60 studies that investigated the response of a mix of organisms or natural communities were all added after 2010, indicating a welcomed shift from the study of individual organisms to communities and ecosystems. The initial imbalance of considerably more data archived on calcification and primary production than on other processes has improved. There is also a clear tendency towards more data archived from multifactorial studies after 2010. For easier and more effective access to ocean acidification data, the ocean acidification community is strongly encouraged to contribute to the data archiving effort, and help develop standard vocabularies describing the variables and define best practices for archiving ocean acidification data.

Individual-based modelling of the development and transport of a Karenia mikimotoi bloom on the North-West European continental shelf

In 2006, a large and prolonged bloom of the dinoflagellate Karenia mikimotoi occurred in Scottish coastal waters, causing extensive mortalities of benthic organisms including annelids and molluscs and some species of fish ( Davidson et al., 2009). A coupled hydrodynamic-algal transport model was developed to track the progression of the bloom around the Scottish coast during June–September 2006 and hence investigate the processes controlling the bloom dynamics. Within this individual-based model, cells were capable of growth, mortality and phototaxis and were transported by physical processes of advection and turbulent diffusion, using current velocities extracted from operational simulations of the MRCS ocean circulation model of the North-west European continental shelf. Vertical and horizontal turbulent diffusion of cells are treated using a random walk approach. Comparison of model output with remotely sensed chlorophyll concentrations and cell counts from coastal monitoring stations indicated that it was necessary to include multiple spatially distinct seed populations of K. mikimotoi at separate locations on the shelf edge to capture the qualitative pattern of bloom transport and development. We interpret this as indicating that the source population was being transported northwards by the Hebridean slope current from where colonies of K. mikimotoi were injected onto the continental shelf by eddies or other transient exchange processes. The model was used to investigate the effects on simulated K. mikimotoi transport and dispersal of: (1) the distribution of the initial seed population; (2) algal growth and mortality; (3) water temperature; (4) the vertical movement of particles by diurnal migration and eddy diffusion; (5) the relative role of the shelf edge and coastal currents; (6) the role of wind forcing. The numerical experiments emphasized the requirement for a physiologically based biological model and indicated that improved modelling of future blooms will potentially benefit from better parameterisation of temperature dependence of both growth and mortality and finer spatial and temporal hydrodynamic resolution.

Individual-based modelling of the development and transport of a Karenia mikimotoi bloom on the North-West European continental shelf

In 2006, a large and prolonged bloom of the dinoflagellate Karenia mikimotoi occurred in Scottish coastal waters, causing extensive mortalities of benthic organisms including annelids and molluscs and some species of fish ( Davidson et al., 2009). A coupled hydrodynamic-algal transport model was developed to track the progression of the bloom around the Scottish coast during June–September 2006 and hence investigate the processes controlling the bloom dynamics. Within this individual-based model, cells were capable of growth, mortality and phototaxis and were transported by physical processes of advection and turbulent diffusion, using current velocities extracted from operational simulations of the MRCS ocean circulation model of the North-west European continental shelf. Vertical and horizontal turbulent diffusion of cells are treated using a random walk approach. Comparison of model output with remotely sensed chlorophyll concentrations and cell counts from coastal monitoring stations indicated that it was necessary to include multiple spatially distinct seed populations of K. mikimotoi at separate locations on the shelf edge to capture the qualitative pattern of bloom transport and development. We interpret this as indicating that the source population was being transported northwards by the Hebridean slope current from where colonies of K. mikimotoi were injected onto the continental shelf by eddies or other transient exchange processes. The model was used to investigate the effects on simulated K. mikimotoi transport and dispersal of: (1) the distribution of the initial seed population; (2) algal growth and mortality; (3) water temperature; (4) the vertical movement of particles by diurnal migration and eddy diffusion; (5) the relative role of the shelf edge and coastal currents; (6) the role of wind forcing. The numerical experiments emphasized the requirement for a physiologically based biological model and indicated that improved modelling of future blooms will potentially benefit from better parameterisation of temperature dependence of both growth and mortality and finer spatial and temporal hydrodynamic resolution.

Toxin and Growth Responses of the Neurotoxic Dinoflagellate Vulcanodinium rugosum to Varying Temperature and Salinity

Vulcanodinium rugosum, a recently described species, produces pinnatoxins. The IFR-VRU-01 strain, isolated from a French Mediterranean lagoon in 2010 and identified as the causative dinoflagellate contaminating mussels in the Ingril Lagoon (French Mediterranean) with pinnatoxin-G, was grown in an enriched natural seawater medium. We tested the effect of temperature and salinity on growth, pinnatoxin-G production and chlorophyll a levels of this dinoflagellate. These factors were tested in combinations of five temperatures (15, 20, 25, 30 and 35 °C) and five salinities (20, 25, 30, 35 and 40) at an irradiance of 100 µmol photon m−2 s−1. V. rugosum can grow at temperatures and salinities ranging from 20 °C to 30 °C and 20 to 40, respectively. The optimal combination for growth (0.39 ± 0.11 d−1) was a temperature of 25 °C and a salinity of 40. Results suggest that V. rugosum is euryhaline and thermophile which could explain why this dinoflagellate develops in situ only from June to September. V. rugosum growth rate and pinnatoxin-G production were highest at temperatures ranging between 25 and 30 °C. This suggests that the dinoflagellate may give rise to extensive blooms in the coming decades caused by the climate change-related increases in temperature expected in the Mediterranean coasts.

Weather variability, sunspots, and the blooms of cyanobacteria

The roles of weather variability and sunspots in the occurrence of cyanobacteria blooms, were investigated using cyanobacteria cell data collected from the Fred Haigh Dam, Queensland, Australia. Time series generalized linear model and classification and regression (CART) model were used in the analysis. Data on notified cell numbers of cyanobacteria and weather variables over the periods 2001 and 2005 were provided by the Australian Department of Natural Resources and Water, and Australian Bureau of Meteorology, respectively. The results indicate that monthly minimum temperature (relative risk [RR]: 1.13, 95% confidence interval [CI]: 1.02-1.25) and rainfall (RR: 1.11; 95% CI: 1.03-1.20) had a positive association, but relative humidity (RR: 0.94; 95% CI: 0.91-0.98) and wind speed (RR:0.90; 95% CI: 0.82-0.98) were negatively associated with the cyanobacterial numbers, after adjustment for seasonality and auto-correlation. The CART model showed that the cyanobacteria numbers were best described by an interaction between minimum temperature, relative humidity, and sunspot numbers. When minimum temperature exceeded 18%C and relative humidity was under 66%, the number of cyanobacterial cells rose by 2.15-fold. We conclude that the weather variability and sunspot activity may affect cyanobacterial blooms in dams.

Integrated Bayesian network frameworks for modelling complex ecological issues

Ecological problems are typically multi faceted and need to be addressed from a scientific and a management perspective. There is a wealth of modelling and simulation software available, each designed to address a particular aspect of the issue of concern. Choosing the appropriate tool, making sense of the disparate outputs, and taking decisions when little or no empirical data is available, are everyday challenges facing the ecologist and environmental manager. Bayesian Networks provide a statistical modelling framework that enables analysis and integration of information in its own right as well as integration of a variety of models addressing different aspects of a common overall problem. There has been increased interest in the use of BNs to model environmental systems and issues of concern. However, the development of more sophisticated BNs, utilising dynamic and object oriented (OO) features, is still at the frontier of ecological research. Such features are particularly appealing in an ecological context, since the underlying facts are often spatial and temporal in nature. This thesis focuses on an integrated BN approach which facilitates OO modelling. Our research devises a new heuristic method, the Iterative Bayesian Network Development Cycle (IBNDC), for the development of BN models within a multi-field and multi-expert context. Expert elicitation is a popular method used to quantify BNs when data is sparse, but expert knowledge is abundant. The resulting BNs need to be substantiated and validated taking this uncertainty into account. Our research demonstrates the application of the IBNDC approach to support these aspects of BN modelling. The complex nature of environmental issues makes them ideal case studies for the proposed integrated approach to modelling. Moreover, they lend themselves to a series of integrated sub-networks describing different scientific components, combining scientific and management perspectives, or pooling similar contributions developed in different locations by different research groups. In southern Africa the two largest free-ranging cheetah (Acinonyx jubatus) populations are in Namibia and Botswana, where the majority of cheetahs are located outside protected areas. Consequently, cheetah conservation in these two countries is focussed primarily on the free-ranging populations as well as the mitigation of conflict between humans and cheetahs. In contrast, in neighbouring South Africa, the majority of cheetahs are found in fenced reserves. Nonetheless, conflict between humans and cheetahs remains an issue here. Conservation effort in South Africa is also focussed on managing the geographically isolated cheetah populations as one large meta-population. Relocation is one option among a suite of tools used to resolve human-cheetah conflict in southern Africa. Successfully relocating captured problem cheetahs, and maintaining a viable free-ranging cheetah population, are two environmental issues in cheetah conservation forming the first case study in this thesis. The second case study involves the initiation of blooms of Lyngbya majuscula, a blue-green algae, in Deception Bay, Australia. L. majuscula is a toxic algal bloom which has severe health, ecological and economic impacts on the community located in the vicinity of this algal bloom. Deception Bay is an important tourist destination with its proximity to Brisbane, Australia’s third largest city. Lyngbya is one of several algae considered to be a Harmful Algal Bloom (HAB). This group of algae includes other widespread blooms such as red tides. The occurrence of Lyngbya blooms is not a local phenomenon, but blooms of this toxic weed occur in coastal waters worldwide. With the increase in frequency and extent of these HAB blooms, it is important to gain a better understanding of the underlying factors contributing to the initiation and sustenance of these blooms. This knowledge will contribute to better management practices and the identification of those management actions which could prevent or diminish the severity of these blooms.

Cooperative multi-AUV tracking of phytoplankton blooms based on ocean model predictions

In recent years, ocean scientists have started to employ many new forms of technology as integral pieces in oceanographic data collection for the study and prediction of complex and dynamic ocean phenomena. One area of technological advancement in ocean sampling if the use of Autonomous Underwater Vehicles (AUVs) as mobile sensor plat- forms. Currently, most AUV deployments execute a lawnmower- type pattern or repeated transects for surveys and sampling missions. An advantage of these missions is that the regularity of the trajectory design generally makes it easier to extract the exact path of the vehicle via post-processing. However, if the deployment region for the pattern is poorly selected, the AUV can entirely miss collecting data during an event of specific interest. Here, we consider an innovative technology toolchain to assist in determining the deployment location and executed paths for AUVs to maximize scientific information gain about dynamically evolving ocean phenomena. In particular, we provide an assessment of computed paths based on ocean model predictions designed to put AUVs in the right place at the right time to gather data related to the understanding of algal and phytoplankton blooms.