Thermal performance of planktonic ciliates differs between marine and freshwaters: A case study providing guidance for climate change studies

Predicting the performance of aquatic organisms in a future warmer climate depends critically on understanding how current temperature regimes affect the organisms’ growth rates. Using a meta-analysis for published experimental data, we calculated the activation energy (Ea) to parameterize the thermal sensitivity of marine and freshwater ciliates, major players in marine and freshwater food webs. We hypothesized that their growth rates increase with temperature but that ciliates dwelling in the immense, thermally stable ocean are closely adapted to their ambient temperature and have lower Ea than ciliates living in smaller, thermally more variable freshwater environments. The Ea was in the range known from other taxa but significantly lower for marine ciliates (0.390 ± 0.105 eV) than for freshwater ciliates (0.633 ± 0.060 eV), supporting our hypothesis. Accordingly, models aiming to predict the ciliate response to increasing water temperature should apply the environment-specific activation energies provided in this study

Insights on Short-term Blooms of Planktonic Ciliates, Provided by an Easily Recognised Genus: Cyrtostrombidium

Planktonic ciliates occasionally form brief rapid increases in numbers (blooms) that can be trophically important. Although model simulations and mesocosm studies indicate that blooms occur over 10 to 20 days, field data are rarely suffi ciently detailed to reveal their occurrence and demise. Our data (collected over 57 weeks across a coastal lagoon) offer insights into the population dynamics of a single species, place these in the context of the entire ciliate assemblage, and provide guidance on what should continue to be examined. Specifically, to evaluate population dynamics we examine two species of Cyrtostrombidium, characterise temporal and spatial variation of their abundance, and relate these to abiotic phenomena and biological factors. This is also the first report of Cyrtostrombidium in a tropical coastal lagoon. Collectively our analysis reveals key aspects of the dynamics of this genus: 1) small-scale peaks in abundance are ~30 m in size and can persist for ~10–30 days, reaching a maximum of 100 cells ml–1; 2) these increases are driven by biotic factors (revealed through autocorrelation analysis); 3) long-term trends are driven by the shift between dry and rainy seasons and by the periods of isolation of lagoon from the sea (revealed through multiple regression analysis); 4) blooms may at times control primary production; 5) conjugation, an ecologically important event, may be associated with blooms (at times 9% of population was conjugating); and 6) dinoflagellate parasitism, poorly described in oligotrichs, is potentially important in population demise. These results both reflect on how ciliates may behave in short-term events and should encourage the continued need for detailed observations of field samples at a high taxonomic resolution

An evidence-based framework for predicting the impact of differing autotroph-heterotroph thermal sensitivities on consumer-prey dynamics

Increased temperature accelerates vital rates, influencing microbial population and wider ecosystem dynamics, for example, the predicted increases in cyanobacterial blooms associated with global warming. However, heterotrophic and mixotrophic protists, which are dominant grazers of microalgae, may be more thermally sensitive than autotrophs, and thus prey could be suppressed as temperature rises. Theoretical and meta-analyses have begun to address this issue, but an appropriate framework linking experimental data with theory is lacking. Using ecophysiological data to develop a novel model structure, we provide the first validation of this thermal sensitivity hypothesis: increased temperature improves the consumer’s ability to control the autotrophic prey. Specifically, the model accounts for temperature effects on auto- and mixotrophs and ingestion, growth and mortality rates, using an ecologically and economically important system (cyanobacteria grazed by a mixotrophic flagellate). Once established, we show the model to be a good predictor of temperature impacts on consumer–prey dynamics by comparing simulations with microcosm observations. Then, through simulations, we indicate our conclusions remain valid, even with large changes in bottom-up factors (prey growth and carrying capacity). In conclusion, we show that rising temperature could, counterintuitively, reduce the propensity for microalgal blooms to occur and, critically, provide a novel model framework for needed, continued assessment

Do marine planktonic ciliates follow Bergmann's rule?

Body size is a fundamental trait determining individual fitness and ecological processes. Reduction in body size with increasing temperature has been widely observed in most ectotherms and endotherms, known as Bergmann's rule. However, we lack data to assess if ciliates, the major consumers of marine primary production, follow Bergmann's rule and what drives the distributions of their cell size. Here, we examined a data set (287 samples) collected across the global oceans to investigate biogeographic patterns in the mean cell-size of ciliate communities. By measuring the sizes of every ciliate cell ( 300 per sample), we found that community cell-size increased with increasing latitude, conforming to Bergmann's rule. We then addressed the cause. Temperature was a main driver of the trend. Ciliate community mean cell-size decreased 34% when temperature increased from 3.5 to 31°C, implying that temperature may be a direct physiological driver. In addition, prey (phytoplankton) size also influenced the trend, with ciliate size increasing by 35% across the gradient of phytoplankton size (0.6–15.5 μm). Generally, these findings emphasized the importance of how both biotic and abiotic factors affect size distribution of marine ciliates, a key component of pelagic ecosystems. Our novel, extensive dataset and the predictive trends arising from them contribute to understanding how climate change will influence pelagic ecosystem functions

High Genetic Diversity and Fine-Scale Spatial Structure in the Marine Flagellate Oxyrrhis marina (Dinophyceae) Uncovered by Microsatellite Loci

Free-living marine protists are often assumed to be broadly distributed and genetically homogeneous on large spatial scales. However, an increasing application of highly polymorphic genetic markers (e.g., microsatellites) has provided evidence for high genetic diversity and population structuring on small spatial scales in many free-living protists. Here we characterise a panel of new microsatellite markers for the common marine flagellate Oxyrrhis marina. Nine microsatellite loci were used to assess genotypic diversity at two spatial scales by genotyping 200 isolates of O. marina from 6 broad geographic regions around Great Britain and Ireland; in one region, a single 2 km shore line was sampled intensively to assess fine-scale genetic diversity. Microsatellite loci resolved between 1–6 and 7–23 distinct alleles per region in the least and most variable loci respectively, with corresponding variation in expected heterozygosities (He) of 0.00–0.30 and 0.81–0.93. Across the dataset, genotypic diversity was high with 183 genotypes detected from 200 isolates. Bayesian analysis of population structure supported two model populations. One population was distributed across all sampled regions; the other was confined to the intensively sampled shore, and thus two distinct populations co-occurred at this site. Whilst model-based analysis inferred a single UK-wide population, pairwise regional FST values indicated weak to moderate population sub-division (0.01–0.12), but no clear correlation between spatial and genetic distance was evident. Data presented in this study highlight extensive genetic diversity for O. marina; however, it remains a substantial challenge to uncover the mechanisms that drive genetic diversity in free-living microorganisms

The Interactive Effects of Ammonia and Microcystin on Life-History Traits of the Cladoceran Daphnia magna: Synergistic or Antagonistic?

The occurrence of Microcystis blooms is a worldwide concern that has caused numerous adverse effects on water quality and lake ecology. Elevated ammonia and microcystin concentrations co-occur during the degradation of Microcystis blooms and are toxic to aquatic organisms; we studied the relative and combined effects of these on the life history of the model organism Daphnia magna. Ammonia and microcystin-LR treatments were: 0, 0.366, 0.581 mg L−1 and 0, 10, 30, 100 µg L−1, respectively. Experiments followed a fully factorial design. Incubations were 14 d and recorded the following life-history traits: number of moults, time to first batch of eggs, time to first clutch, size at first batch of eggs, size at first clutch, number of clutches per female, number of offspring per clutch, and total offspring per female. Both ammonia and microcystin were detrimental to most life-history traits. Interactive effects of the toxins occurred for five traits: the time to first batch of eggs appearing in the brood pouch, time to first clutch, size at first clutch, number of clutches, and total offspring per female. The interactive effects of ammonia and microcystin appeared to be synergistic on some parameters (e.g., time to first eggs) and antagonistic on others (e.g., total offspring per female). In conclusion, the released toxins during the degradation of Microcystis blooms would result, according to our data, in substantially negative effect on D. magna

Molecular biogeography of planktonic and benthic diatoms in the Yangtze River

Background: Diatoms are of great significance to primary productivity in oceans, yet little is known about their biogeographic distribution in oligotrophic rivers. Results: With the help of metabarcoding analysis of 279 samples from the Yangtze River, we provided the first integral biogeographic pattern of planktonic and benthic diatoms over a 6030 km continuum along the world's third largest river. Our study revealed spatial dissimilarity of diatoms under varying landforms, including plateau, mountain, foothill, basin, foothill-mountain, and plain regions, from the river source to the estuary. Environmental drivers of diatom communities were interpreted in terms of photosynthetically active radiation, temperature, channel slope and nutrients, and human interference. Typical benthic diatoms, such as Pinnularia, Paralia, and Aulacoseira, experienced considerable reduction in relative abundance downstream of the Three Gorges Dam and the Xiluodu Dam, two of the world's largest dams. Conclusions: Our study revealed that benthic diatoms are of particular significance in characterizing motile guild in riverine environments, which provides insights into diatom biogeography and biogeochemical cycles in large river ecosystems

An investigation of the growth and feeding responses of oligotrich ciliates to food types and concentrations : an approach to assessing the potential of marine planktonic ciliate blooms

Planktonic ciliates consume small phytoplankton and can be important in the transfer of carbon through food webs. This study examined the impact of clonal ciliate populations on short term algal blooms. Numerical and functional responses (growth and grazing rates with varied food concentration)were established for 5 marine planktonic ciliates and were used in a model to examine predator-prey dynamics of ciliates and 8 Am algae. The ciliates Strombidinopsis acuminatum, Strobilidium spiralis, Strobilidium sp., Strombiclium acuminatum, and Strombiclium capitatum were isolated from British Columbian waters and maintained in culture. Ciliates were fed the flagellates Isochrysis galbana, Chroomonas sauna, Rhodomonas lens, and the diatom 7halassiosira pseudonana, individually or in combinations. Numerical responses were obtained by keeping ciliates in semi-continuous culture, measuring growth rates and fitting them to a modified Michaelis-Menten function; this provided both growth and mortality rates. Species specific differences existed in numerical response parameters. Functional responses were measured by observing the uptake of fluorescently labeled C. sauna or 5 it m beads. This was a poor method: when measured grazing rates were compared to those predicted by a bioenergetic formula, the measured rates either over or underestimated predicted rates by several fold. Functional responses were determined using 1) the bioenergetic formula Ingestion =(growth+respiration)/assimilation efficiency, and 2) volume specific respiration rates. Ciliate functional and numerical responses from this and other studies were compared, and 3responses were established. These were used in a model which simulated ciliate-algal population dynamics in a non-steady state, where ciliates and copepods encountered a patch of water with a defined initial algal concentration. The model indicated: 1) ciliates bloom over 10-20 d, when copepods are rare (103 mL4); 2) ciliate blooms can provide 40-50% of the carbon available to copepods, but when copepods are abundant and initial algal levels low, ciliates are not an important carbon source; 3) under "typical" conditions (103 algae mL4,1 copepod L4), ciliates are a link to copepods, but primary production is low; 4) bloom dynamics and carbon flow through the food web are dependent on the ciliate species present. In general, ciliates maybe, under transient conditions, important as both links and sinks of carbon, but under "typical" coastal conditions, ciliates are not important components of food webs.Science, Faculty ofEarth, Ocean and Atmospheric Sciences, Department ofGraduat