Cell size as driver and sentinel of phytoplankton community structure and functioning

Body size is a decisive functional trait in many organisms, especially for phytoplankton, which span several orders of magnitude in cell volume. Therefore, the analysis of size as a functional trait driving species’ performance has received wide attention in aquatic ecology, amended in recent decades by studies documenting changes in phytoplankton size in response to abiotic or biotic factors in the environment. We performed a systematic literature review to provide an overarching, partially quantitative synthesis of cell size as a driver and sentinel of phytoplankton ecology. We found consistent and significant allometric relationships between cell sizes and the functional performance of phytoplankton species (cellular rates of carbon fixation, respiration and exudation as well as resource affinities, uptake and content). Size scaling became weaker, absent or even negative when addressing C- or volume-specific rates or growth. C-specific photosynthesis and population growth rate peaked at intermediate cell sizes around 100 µm3. Additionally, we found a rich literature on sizes changing in response to warming, nutrients and pollutants. Whereas small cells tended to dominate under oligotrophic and warm conditions, there are a few notable exceptions, which indicates that other environmental or biotic constraints alter this general trend. Grazing seems a likely explanation, which we reviewed to understand both how size affects edibility and how size structure changes in response to grazing. Cell size also predisposes the strength and outcome of competitive interactions between algal species. Finally, we address size in a community context, where size-abundance scaling describes community composition and thereby the biodiversity in phytoplankton assemblages. We conclude that (a) size is a highly predictive trait for phytoplankton metabolism at the cellular scale, with less strong and nonlinear implications for growth and specific metabolism and (b) size structure is a highly suitable sentinel of phytoplankton responses to changing environments. A free Plain Language Summary can be found within the Supporting Information of this article

Filter-Feeding in Marine Invertebrates

Filter-feeding in marine invertebrates is a big and important research subject, which cannot be even approximately covered by the present six articles. But although these articles deal with a limited and rather random selection of both topics and filter-feeding species, they give an update of certain aspects of important ongoing research. The articles deal with many topics, such as: filtration rates, energy budgets, growth rates, bioenergetic modeling, filter-pump design, particle-capture mechanisms, functional morphology, and hydrodynamics studied in sponges, jellyfish, mussels, and other filter-feeding marine invertebrates. This makes the Special Issue relevant for all marine biologists

Temperature-dependence of minimum resource requirements alters competitive hierarchies in phytoplankton

Resource competition theory is a conceptual framework that provides mechanistic insights into competition and community assembly of species with different resource requirements. However, there has been little exploration of how resource requirements depend on other environmental factors, including temperature. Changes in resource requirements as influenced by environmental temperature would imply that climate warming can alter the outcomes of competition and community assembly

Understanding the responses of marine phytoplankton to experimental warming

Understanding how marine phytoplankton will fare in response to the expected increases in ocean temperature over the next century is crucial for improving their inclusion in models of ocean biogeochemistry. Marine phytoplankton plays an essential role for the global carbon cycle, accounting for approximately 50% of global primary production, and provides the base of all aquatic food webs. There is currently poor understanding of what sets the limits of thermal tolerance and how quickly different species of phytoplankton can adapt to changes in environmental temperature. Furthermore, models that have previously factored for the response of phytoplankton to warming have tended to generalise their inclusion by applying the Eppley coefficient to make predictions about future ocean productivity; this is an across-species characterisation of the thermal sensitivity of phytoplankton growth rates, which assumes a monotonic, exponential, increase in maximal growth rates with temperature. To enhance our understanding of the responses of marine phytoplankton to warming we first investigated the limits of thermal tolerance, as well as the thermal performance of both photosynthesis and respiration rates, for an array of phytoplankton taxa, representing key functional groups, including: cyanobacteria, diatoms, coccolithophores, dinoflagellates and chlorophytes. We identify, qualitatively, that the limits of thermal tolerance are likely to be underpinned by the thermal performance of metabolism, whereby across all taxa respiration was more temperature dependent, and generally had a higher optimal temperature, than photosynthesis. Next, using the understanding of thermal tolerance at the species level we estimated an across-species temperature dependence of maximal growth rates that was lower than the within-species average, supporting the “partial compensation” mechanism of thermal adaptation and highlighting that the canonical Eppley coefficient is likely to under or overestimate the temperature dependence in ocean regions where particular species, or phylogenetic groups, may dominate. With this finding we were also able to associate greater thermal tolerance with covariance of other ecologically important physiological and morphological traits, highlighting that the likely restructuring of phytoplankton communities in response to warming will have strong implications for ecosystem function and biogeochemical cycles. Lastly, we investigated the pace and magnitude of thermal adaptation to a stressful supra-optimal temperature across three very different but ecologically important phytoplankton species. We found that across the three taxa there was clear variance in the rate and magnitude of thermal adaptation, with the least complex and smallest of the three taxa showing the fastest rates of thermal adaptation and the greatest improvement in thermal tolerance. Underpinning thermal adaptation across the taxa were clear metabolic adjustments, likely to be associated with overcoming the constraints of carbon allocation to growth due to the differing thermal sensitivities of photosynthesis and respiration. We conclude that each of the main findings from this research can help improve the inclusion of marine phytoplankton in models of ocean biogeochemistry and as part of wider Earth systems models, thereby aiding predictions of the likely reorganisation of phytoplankton communities and the impact of warming on the critical ecosystem services and biogeochemical cycles that phytoplankton mediate

Five Years of Experimental Warming Increases the Biodiversity and Productivity of Phytoplankton

Phytoplankton are key components of aquatic ecosystems, fixing CO2 from the atmosphere through photosynthesis and supporting secondary production, yet relatively little is known about how future global warming might alter their biodiversity and associated ecosystem functioning. Here, we explore how the structure, function, and biodiversity of a planktonic metacommunity was altered after five years of experimental warming. Our outdoor mesocosm experiment was open to natural dispersal from the regional species pool, allowing us to explore the effects of experimental warming in the context of metacommunity dynamics. Warming of 4°C led to a 67% increase in the species richness of the phytoplankton, more evenly-distributed abundance, and higher rates of gross primary productivity. Warming elevated productivity indirectly, by increasing the biodiversity and biomass of the local phytoplankton communities. Warming also systematically shifted the taxonomic and functional trait composition of the phytoplankton, favoring large, colonial, inedible phytoplankton taxa, suggesting stronger top-down control, mediated by zooplankton grazing played an important role. Overall, our findings suggest that temperature can modulate species coexistence, and through such mechanisms, global warming could, in some cases, increase the species richness and productivity of phytoplankton communities

A phytoplankton model for the allocation of gross photosynthetic energy including the trade‐offs of diazotrophy

Author Posting. © American Geophysical Union, 2018. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Journal of Geophysical Research: Biogeosciences 123 (2018): 1796-1816, doi:10.1029/2017JG004263.Gross photosynthetic activity by phytoplankton is directed to linear and alternative electron pathways that generate ATP, reductant, and fix carbon. Ultimately less than half is directed to net growth. Here we present a phytoplankton cell allocation model that explicitly represents a number of cell metabolic processes and functional pools with the goal of evaluating ATP and reductant demands as a function of light, nitrate, iron, oxygen, and temperature for diazotrophic versus nondiazotrophic growth. We employ model analogues of Synechoccocus and Crocosphaera watsonii, to explore the trade‐offs of diazotrophy over a range of environmental conditions. Model analogues are identical in construction, except for an iron quota associated with nitrogenase, an additional respiratory demand to remove oxygen in order to protect nitrogenase and an additional ATP demand to split dinitrogen. We find that these changes explain observed differences in growth rate and iron limitation between diazotrophs and nondiazotrophs. Oxygen removal imparted a significantly larger metabolic cost to diazotrophs than ATP demand for fixing nitrogen. Results suggest that diazotrophs devote a much smaller fraction of gross photosynthetic energy to growth than nondiazotrophs. The phytoplankton cell allocation model model provides a predictive framework for how photosynthate allocation varies with environmental conditions in order to balance cellular demands for ATP and reductant across phytoplankton functional groups.DOC | NOAA | Climate Program Office (CPO) Grant Number: NA100AR4310093; National Science Foundation (NSF) Grant Number: EF‐0424599; Center for Microbial Oceanography Research and Education (CMORE) Grant Number: NSF EF‐0424599; NOAA Global Carbon Program Grant Number: NA100AR43100932018-11-0

Temporal declines in Wadden Sea phytoplankton cell volumes observed within and across species

Cell size is a master trait in the functional ecology of phytoplankton correlating with numerous morphological, physiological, and life-cycle characteristics of species that constrain their nutrient use, growth, and edibility. In contrast to well-known spatial patterns in cell size at macroecological scales or temporal changes in experimental contexts, few data sets allow testing temporal changes in cell sizes within ecosystems. To analyze the temporal changes of intraspecific and community-wide cell size, we use the phytoplankton data derived from the Lower Saxony Wadden Sea monitoring program, which comprises sample- and species-specific measurements of cell volume from 1710 samples collected over 14 yr. We find significant reductions in both the cell volume of most species and the weighted mean cell size of communities. Mainly diatoms showed this decline, whereas the size of dinoflagellates seemed to be less responsive. The magnitude of the trend indicates that cell volumes are about 30% smaller now than a decade ago. This interannual trend is overlayed by seasonal cycles with smaller cells typically observed in summer. In the subset of samples including environmental conditions, small community cell size was strongly related to high temperatures and low total phosphorus concentration. We conclude that cell size captures ongoing changes in phytoplankton communities beyond the changes in species composition. In addition, based on the changes in species biovolumes revealed by our analysis, we warn that using standard cell size values in phytoplankton assessment will not only miss temporal changes in size, but also lead to systematic errors in biomass estimates over time

Phytoplankton Dynamics and Harmful Algal Species in the Potomac River Estuary

Phytoplankton populations are a primary driver of chemical and biological dynamics and are therefore important sentinel organisms for monitoring environmental perturbations. Additionally, long term ecological monitoring in the Potomac River estuary provides opportunities to examine phytoplankton dynamics. Annual blooms of the cyanoHAB Microcystis were observed in the 1970’s and 80’s, and since declined in frequency. A large Microcystis aeruginosa bloom occurred, summer 2011, prompting investigation of forecasting efforts for harmful algal species. Three prediction methods were investigated, with binary linear regression identified as the most appropriate forecasting tool. Coastal marine ecosystems are also at risk from climate change and phytoplankton provide a crucial monitoring tool. Extensive time series analysis revealed changes in phytoplankton phenology in response to climate indicators, mainly a shift in the timing of maximum abundance of diatoms and cryptophytes. It is likely that this change in phenology has an effect on energy transfer to higher trophic levels

Limits to thermal adaptation in ectotherms

Climate change is expected to affect biological systems across multiple scales through its direct effects on the physiology of individual organisms. Therefore, to predict how communities and ecosystems will be impacted by changes in climate, it is key to understand the extent to which ectotherm physiology can change through thermal adaptation. In this thesis, we examine the influence of possible constraints on thermal adaptation, as predicted by the Metabolic Theory of Ecology. In Chapter 2 we describe the consequences of violating a key assumption of a model used for quantifying the thermal performance curve, i.e., the relationship of biological rates with temperature. We then proceed in Chapter 3 to evaluate the impact of thermodynamic constraints on the evolution of the thermal performance curves of phytoplankton. We show that thermodynamic constraints have a very weak effect on thermal adaptation, with phylogenetically structured variation being present across the entire thermal performance curve. Further support for such a conclusion is obtained in Chapter 4 through a phylogenetic comparative analysis of the evolution of thermal sensitivity across prokaryotes, phytoplankton, and plants. This reveals that thermal sensitivity is much more variable than expected, as it can change drastically within short amounts of evolutionary time. In Chapter 5, we finally investigate thermal adaptation at the molecular level, examining if changes in temperature can alter the effects of nonsynonymous mutations. We show that across prokaryotes, mutations become increasingly detrimental to the stability of proteins with temperature. In response, thermophile species evolve enzymes that are more robust to mutations and exhibit low substitution rates. Overall, these results further our understanding of how thermal physiology evolves and indicate areas where the theory – as it currently stands – may need to be modified.Open Acces

From Land to Lake: Contrasting Microbial Processes Across a Great Lakes Gradient of Organic Carbon and Inorganic Nutrient Inventories

Freshwater ecosystems have strong linkages to the terrestrial landscapes that surround them, and contributions of carbon and inorganic nutrients from soil, vegetation and anthropogenic sources subsidize autochthonous water body productivity to varying degrees. Abundant freshwater phytoplankton and bacterioplankton are key to linking the planet\u27s geosphere and atmosphere to the food webs in the hydrosphere through their growth and respiration. Rich resources that move through land margin waterways make them active sites for cycling organic carbon and thus important, but understudied, contributors to global climate. During 2010-2011, we examined seasonal changes in carbon and nutrient inventories, plankton community composition and metabolism along a land-to-lake gradient in a major West Michigan watershed at four interconnected habitats ranging from a small creek to offshore Lake Michigan. In all seasons Lake Michigan had significantly lower concentrations of CDOM and DOC than any of the other sites. Lake levels of NO3 were not significantly lower than tributaries other than Cedar Creek, and SRP was not measurable in any of the sites other than Cedar Creek. Bacterial production as % of GPP revealed a distinct land-to-lake gradient from an average of 448% in Cedar creek to 5% in Lake Michigan. Microbial activity in Cedar Creek (bacterial production 3- 93 μg C/L/d, and plankton respiration 9-193 μg C/L/d) was generally higher than all other sites. Muskegon Lake dominated GPP among the sites reaching a peak of \u3e1000 μg carbon/L/d during a large fall Microcystis bloom. Offshore Lake Michigan had less variation in GPP and R than the other sites with GPP:R ratio close to 1 in all seasons but spring. Metabolism appears to be substantially subsidized by terrigenous inputs in the creek/river ecosystem with heterotrophy dominant over autotrophy. Autotrophy was maximized in the coastal/estuary, whereas both autotrophy and heterotrophy were minimal but in near-balance in offshore waters receiving little subsidy from the land. Along this land-to-lake gradient terrestrial subsidies combined with a host of other factors making conditions “just right” for a hot-spot to emerge, highlighting Muskegon Lake estuary a “Goldilocks Zone” of net biological productivity