Cell size trade-offs govern light exploitation strategies in marine phytoplankton

Marine phytoplankton show complex community structures and biogeographic distributions, the net results of physiological and ecological trade-offs of species responses to fluctuating, heterogeneous environments. We analysed photosynthesis, responses to variable light and macromolecular allocations across a size panel of marine centric diatoms. The diatoms have strong capacities to withstand and exploit fluctuating light, when compared with picophytoplankton. Within marine diatoms, small species show larger effective cross-sections for photochemistry, and fast metabolic repair of photosystem II after photoinactivation. In contrast, large diatoms show lower susceptibility to photoinactivation, and therefore incur lower costs to endure short-term exposures to high light, especially under conditions that limit metabolic rates. This size scaling of key photophysiological parameters thus helps explain the relative competitive advantages of larger versus smaller species under different environmental regimes, with implications for the function of the biogenic carbon pump. These results provide a mechanistic framework to explain and predict shifts in marine phytoplankton community size structure with changes in surface irradiance and mixed layer depth.     

Mix and match: how climate selects phytoplankton

Climate strongly influences the distribution and diversity of animals and plants, but its affect on microbial communities is poorly understood. By using resource competition theory, fundamental physical principles and the fossil record we review how climate selects marine eukaryotic phytoplankton taxa. We suggest that climate determines the equator-to-pole and continent-to-land thermal gradients that provide energy for the wind-driven turbulent mixing in the upper ocean. This mixing, in turn, controls the nutrient fluxes that determine cell size and taxa-level distributions. Understanding this chain of linked processes will allow informed predictions to be made about how phytoplankton communities will change in the future.     

Application of a new multi-metric phytoplankton index to the assessment of ecological status in marine and transitional waters

Patterns of phytoplankton size spectra variation with gradients of environmental stress have been observed in freshwater, transitional waters and marine ecosystems, driving the development of size spectra based assessment tools.In this study, we have tested on transitional and coastal waters a new Index of Size spectra Sensitivity of Phytoplankton (ISS-Phyto), which integrates simple size spectra metrics, size class sensitivity to anthropogenic disturbance, phytoplankton biomass (chlorophyll a) and taxonomic richness thresholds. ISS-Phyto has been tested both among and within ecosystems along pressure gradients based on expert view assessment; the adequacy of symmetric and both left and right asymmetric models of phytoplankton size class sensitivity have been compared.The results showed that ISS-Phyto consistently discriminated between anthropogenic and natural disturbance conditions. Left asymmetric models of size spectra sensitivity, assuming greater disturbance tolerance with respect to eutrophication and organic enrichment of increasingly large size classes, showed the best fit comparing all ecosystems; in three of the four considered ecosystems (Varna, Helsinki, Mompás-Pasaia), they seemed to discriminate best between different levels of disturbance also within ecosystems. Moreover, they demonstrated significant and inverse patterns of variation along the overall pressure gradient as well as along the inorganic phosphorus (DIP), chlorophyll a and trophic index (TRIX) gradients.Therefore, ISS-Phyto, originally developed for transitional waters, seems to be an adequate assessment tool of ecological status also in coastal marine waters; moreover, it seems adequate to describe within ecosystem disturbance gradients. Hence, ISS-Phyto helps to understand the relationships between anthropogenic impact and ecosystem response from the individual point of view, with reference to the simple parameter of body size.     

The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level

Trait-based approaches to community structure are increasingly used in terrestrial ecology. We show that such an approach, augmented by a mechanistic analysis of trade-offs among functional traits, can be successfully used to explain community composition of marine phytoplankton along environmental gradients. Our analysis of literature on major functional traits in phytoplankton, such as parameters of nutrient-dependent growth and uptake, reveals physiological trade-offs in species abilities to acquire and utilize resources. These trade-offs, arising from fundamental relations such as cellular scaling laws and enzyme kinetics, define contrasting ecological strategies of nutrient acquisition. Major groups of marine eukaryotic phytoplankton have adopted distinct strategies with associated traits. These diverse strategies of nutrient utilization can explain the distribution patterns of major functional groups and size classes along nutrient availability gradients.     

The vertical distribution of phytoplankton in stratified water columns

What determines the vertical distribution of phytoplankton in different aquatic environments remains an open question. To address this question, we develop a model to explore how phytoplankton respond through growth and movement to opposing resource gradients and different mixing conditions. We assume stratification creates a well-mixed surface layer on top of a poorly mixed deep layer and nutrients are supplied from multiple depth-dependent sources. Intraspecific competition leads to a unique strategic equilibrium for phytoplankton, which allows us to classify the distinct vertical distributions that can exist. Biomass can occur as a benthic layer (BL), a deep chlorophyll maximum (DCM), or in the mixed layer (ML), or as a combination of BL+ML or DCM+ML. The ML biomass can be limited by nutrients, light, or both. We predict how the vertical distribution, relative resource limitation, and biomass of phytoplankton will change across environmental gradients. We parameterized our model to represent potentially light and phosphorus limited freshwater lakes, but the model is applicable to a broad range of vertically stratified systems. Increasing nutrient input from the sediments or to the mixed layer increases light limitation, shifts phytoplankton towards the surface, and increases total biomass. Increasing background light attenuation increases light limitation, shifts the phytoplankton towards the surface, and generally decreases total biomass. Increasing mixed layer depth increases, decreases, or has no effect on light limitation and total biomass. Our model is able to replicate the diverse vertical distributions observed in nature and explain what underlying mechanisms drive these distributions.     

Invariant scaling of phytoplankton abundance and cell size in contrasting marine environments

Scaling relationships such as the variation of population abundance with body size provide links between individual organisms and ecosystem functioning. Previous work, in marine pelagic ecosystems, has focused on the relationship between total phytoplankton abundance and the assemblage mean cell size. However, the relationship between specific population abundance and cell size in marine phytoplankton has received little attention. Here, we show that cell size accounts for a significant amount of variability in the population abundance of phytoplankton species across a cell volume range spanning seven orders of magnitude. The interspecific scaling of population abundance and cell size takes a power exponent near −3/4. Unexpectedly, despite the constraints imposed on large phytoplankton by limited resource acquisition, the size scaling exponent does not differ between contrasting marine environments such as coastal and subtropical regions. These findings highlight the adaptive abilities of individual species to cope with different environmental conditions and suggest that a general rule such as the 'energetic equivalence' constrains the abundance of phytoplankton populations in marine pelagic ecosystems.     

Linking traits to species diversity and community structure in phytoplankton

In addition to answering Hutchinson’s question “Why are there so many species?”, we need to understand why certain species are found only under certain environmental conditions and not others. Trait-based approaches are being increasingly used in ecology to do just that: explain and predict species distributions along environmental gradients. These approaches can be successful in understanding the diversity and community structure of phytoplankton. Among major traits shaping phytoplankton distributions are resource utilization traits, morphological traits (with size being probably the most influential), grazer resistance traits, and temperature responses. We review these trait-based approaches and give examples of how trait data can explain species distributions in both freshwater and marine systems. We also outline new directions in trait-based approaches applied to phytoplankton such as looking simultaneously at trait and phylogenetic structure of phytoplankton communities and using adaptive dynamics models to predict trait evolution.     

Cryptophytes: An emerging algal group in the rapidly changing Antarctic Peninsula marine environments

The western Antarctic Peninsula (WAP) is a climatically sensitive region where foundational changes at the basis of the food web have been recorded; cryptophytes are gradually outgrowing diatoms together with a decreased size spectrum of the phytoplankton community. Based on a 11-year (2008–2018) in-situ dataset, we demonstrate a strong coupling between biomass accumulation of cryptophytes, summer upper ocean stability, and the mixed layer depth. Our results shed light on the environmental conditions favoring the cryptophyte success in coastal regions of the WAP, especially during situations of shallower mixed layers associated with lower diatom biomass, which evidences a clear competition or niche segregation between diatoms and cryptophytes. We also unravel the cryptophyte photo-physiological niche by exploring its capacity to thrive under high light stress normally found in confined stratified upper layers. Such conditions are becoming more frequent in the Antarctic coastal waters and will likely have significant future implications at various levels of the marine food web. The competitive advantage of cryptophytes in environments with significant light level fluctuations was supported by laboratory experiments that revealed a high flexibility of cryptophytes to grow in different light conditions driven by a fast photo-regulating response. All tested physiological parameters support the hypothesis that cryptophytes are highly flexible regarding their growing light conditions and extremely efficient in rapidly photo-regulating changes to environmental light levels. This plasticity would give them a competitive advantage in exploiting an ecological niche where light levels fluctuate quickly. These findings provide new insights on niche separation between diatoms and cryptophytes, which is vital for a thorough understanding of the WAP marine ecosystem.     

Shining Light on Benthic Macroalgae: Mechanisms of Complementarity in Layered Macroalgal Assemblages

Phototrophs underpin most ecosystem processes, but to do this they need sufficient light. This critical resource, however, is compromised along many marine shores by increased loads of sediments and nutrients from degraded inland habitats. Increased attenuation of total irradiance within coastal water columns due to turbidity is known to reduce species'' depth limits and affect the taxonomic structure and architecture of algal-dominated assemblages, but virtually no attention has been paid to the potential for changes in spectral quality of light energy to impact production dynamics. Pioneering studies over 70 years ago showed how different pigmentation of red, green and brown algae affected absorption spectra, action spectra, and photosynthetic efficiency across the PAR (photosynthetically active radiation) spectrum. Little of this, however, has found its way into ecological syntheses of the impacts of optically active contaminants on coastal macroalgal communities. Here we test the ability of macroalgal assemblages composed of multiple functional groups (including representatives from the chlorophyta, rhodophyta and phaeophyta) to use the total light resource, including different light wavelengths and examine the effects of suspended sediments on the penetration and spectral quality of light in coastal waters. We show that assemblages composed of multiple functional groups are better able to use light throughout the PAR spectrum. Macroalgal assemblages with four sub-canopy species were between 50–75% more productive than assemblages with only one or two sub-canopy species. Furthermore, attenuation of the PAR spectrum showed both a loss of quanta and a shift in spectral distribution with depth across coastal waters of different clarity, with consequences to productivity dynamics of diverse layered assemblages. The processes of light complementarity may help provide a mechanistic understanding of how altered turbidity affects macroalgal assemblages in coastal waters, which are increasingly threatened by diminishing light quantity and altered spectral distributions through sedimentation and eutrophication.     

Spatial and temporal patterns of pioneer macrofauna in recently created ponds: taxonomic and functional approaches

The present study was carried out in Faxinal Reservoir, a warm monomictic, meso-eutrophic reservoir in subtropical southern Brazil, with a long-standing, well-stratified condition, low epilimnetic nutrient concentrations, and a relatively clear epilimnion. In this study, we analyzed the dynamics of the phytoplankton functional groups, recognizing their driving forces in Faxinal Reservoir. Samples were taken at monthly intervals from January 2004 to January 2005 in surface waters. According to the reservoir’s mixing regime, three periods were identified during the study: stratification 1 (January–May 2004); mixing period (June–August 2004); and stratification 2 (September 2004–January 2005). The nutrient dynamics were driven by the mixing regime. The H1, F, and C phytoplankton functional groups were the most important in biomass, mainly represented by the N-fixing cyanobacterium Anabaena crassa, the colonial green alga with thick mucilaginous sheaths Nephrocytium sp., and the diatom Asterionella formosa, respectively. Tendencies pointed out by redundancy analysis (RDA) indicated that the mixing regime was the main determining factor of the seasonal dynamics of the phytoplankton community. The dominant functional groups showed a close relationship with the relative water-column stability (RWCS), and also, as a consequence of the mixing regime, with nutrient availability. The study also revealed the important role of physical processes in the seasonal gradient, in selecting for phytoplankton functional groups and, consequently, in the assessment of ecological status. Q index (assemblage index) of water quality based on functional groups revealed ecological status varying from very poor to tolerable in the stratification 1 period and from tolerable to medium in the mixing and stratification 2 periods. Handling editor: Judit Padisak     

Environmental control of phytoplankton productivity in turbulent turbid systems

Factors affecting phytoplankton productivity are analysed in turbid systems, such as shallow lakes and rivers. When resuspension from the sediment or loading from the catchment significantly increases inorganic (non-algal) turbidity and hence light attenuation potentials for high production are not realised. Energy available for phytoplankton growth is strongly regulated by underwater light availability which depends on the critical mixing depth, fluctuating light intensities and algal circulation patterns. Higher production rates in shallow waters are often compensated by greater algal respiration due to higher water temperatures when compared to deeper lakes.Total daily integral production of turbulent, turbid environments can be predicted from a combination of easily measured variables such as maximum photosynthetic rates, algal biomass, surface irradiance and some measure of underwater light attenuation.     

典型低纬度海区(南海、孟加拉湾)初级生产力比较

南海和孟加拉湾有着相似的纬度范围,均处于低纬度季风区,但环境的开放性和水体交换特征有所不同。将南海和孟加拉湾的初级生产力进行对比,有助于加深人们对低纬度海区生物生产过程的认识。南海有着复杂的物理过程,存在涡旋、上升流、黑潮、台风和冲淡水等多种现象,显著地影响着初级生产力大小和时空分布。南海初级生产力有以下几个特点:(1)受冲淡水和沿岸上升流的影响,沿岸海域常常高于开阔海区;(2)初级生产力的高值通常不出现在表层,大都出现在次表层;(3)在开阔海区受水体交换(黑潮等)和中尺度现象影响(涡旋)显著。此外,南海初级生产力的季节变化也比较明显,但季度变化规律有较强的区域性。孟加拉湾物理环境与南海差别明显,初级生产力主要受淡水输入、涡旋和光照的影响,受台风和上升流影响不如南海明显。在沿岸区,高温低盐水覆盖了沿岸上层水体,使得混合层较稳定,抑制了深层富含营养盐水体的涌升补充,导致初级生产力下降;光强(悬浮物多、多云天气多)也限制了初级生产力。孟加拉湾开阔海区常常有涡旋形成,也对初级生产力有一定影响。沿岸区初级生产力南海高于孟加拉湾,而在开阔海区两者差别不大,因此整体上南海初级生产力水平高于孟加拉湾。     

Tight spatial coupling of a marine predator with soniferous fishes: Using joint modelling to aid in ecosystem approaches to management

Aim

Understanding the distribution of marine organisms is essential for effective management of highly mobile marine predators that face a variety of anthropogenic threats. Recent work has largely focused on modelling the distribution and abundance of marine mammals in relation to a suite of environmental variables. However, biotic interactions can largely drive distributions of these predators. We aim to identify how biotic and abiotic variables influence the distribution and abundance of a particular marine predator, the bottlenose dolphin (Tursiops truncatus), using multiple modelling approaches and conducting an extensive literature review.

Location

Western North Atlantic continental shelf.

Methods

We combined widespread marine mammal and fish and invertebrate surveys in an ensemble modelling approach to assess the relative importance and capacity of the environment and other marine species to predict the distribution of both coastal and offshore bottlenose dolphin ecotypes. We corroborate the modelled results with a systematic literature review on the prey of dolphins throughout the region to help explain patterns driven by prey availability, as well as reveal new ones that may not necessarily be a predator–prey relationship.

Results

We find that coastal bottlenose dolphin distributions are associated with one family of fishes, the Sciaenidae, or drum family, and predictions slightly improve when using only fish versus only environmental variables. The literature review suggests that this tight coupling is likely a predator–prey relationship. Comparatively, offshore dolphin distributions are more strongly related to environmental variables, and predictions are better for environmental-only models. As revealed by the literature review, this may be due to a mismatch between the animals caught in the fish and invertebrate surveys and the predominant prey of offshore dolphins, notably squid.

Main Conclusions

Incorporating prey species into distribution models, especially for coastal bottlenose dolphins, can help inform ecological relationships and predict marine predator distributions.     

The species composition of Antarctic phytoplankton interpreted in terms of Tilman's competition theory

Summary An attempt was made, to test for the impact of resource competition on Antarctic marine phytoplankton. According to theory, species composition near competitive equilibrium should be determined by the ratios of limiting resources. Enrichment bioassays identified silicon and nitrogen as limiting nutrients for some of the most important phytoplankton species during early austral summer in the region near the Antarctic Peninsula. Together with the generally acknowledged limiting resource light, this gave three meaningful ratios of essential resources (Si:N, Si:light, N:light) and one ratio of substitutable resources (NO₃:NH₄). Phytoplankton species assemblages were found to be well separated by the ratios of the essential resources and by mixing depth. Nine out of 12 individual species were found to be separated along at least one of the gradients of resource ratios. Where comparison with competition experiments was available, predicted and realized distributions of species were compatible.     

Phytoplankton Fluctuations during an Annual Cycle in the Coastal Lagoon of Cullera (Spain)

The seasonal variation and the vertical distribution of the phytoplanktonic population of the lagoon of Cullera, an elongated coastal lagoon with estuarine circulation of water, has been studied in three sampling stations: mouth, centre and source. Seasonal variation is determined by a marine-freshwater interaction. In winter, the sea influence is important, a marine water wedge of anoxic water arrives at the sampling station located at the source and marine and brackish water species dominate the phytoplankton. Also marine species of zooplankton and fish enter the system, which may then be considered as exploited by the sea. In spring the marine wedge retreats from the source but remains in the centre and mouth, salinity diminishes, vertical mixing persists and phytoplankton is dominated by Cyclotella species. From late spring to autumn the freshwater influence prevails and a sharp stratification of the water is produced in the stations at the mouth and the centre, by means of a steep halocline coincident with an oxycline. The phytoplankton in this period follows a typical succession like those described in freshwater eutrophic lakes. Vertical distribution of phytoplankton is determined by the presence of the oxycline, originated by the marine water wedge, whose depth varies seasonally but which is always present in the mouth and centre of the lagoon; only few species of algae can be found below its level.     

Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton

Phosphorus (P) is an essential nutrient for marine phytoplankton and indeed all life forms. Current data show that P availability is growth‐limiting in certain marine systems and can impact algal species composition. Available P occurs in marine waters as dissolved inorganic phosphate (primarily orthophosphate [Pi]) or as a myriad of dissolved organic phosphorus (DOP) compounds. Despite numerous studies on P physiology and ecology and increasing research on genomics in marine phytoplankton, there have been few attempts to synthesize information from these different disciplines. This paper is aimed to integrate the physiological and molecular information on the acquisition, utilization, and storage of P in marine phytoplankton and the strategies used by these organisms to acclimate and adapt to variations in P availability. Where applicable, we attempt to identify gaps in our current knowledge that warrant further research and examine possible metabolic pathways that might occur in phytoplankton from well‐studied bacterial models. Physical and chemical limitations governing cellular P uptake are explored along with physiological and molecular mechanisms to adapt and acclimate to temporally and spatially varying P nutrient regimes. Topics covered include cellular Pi uptake and feedback regulation of uptake systems, enzymatic utilization of DOP, P acquisition by phagotrophy, P‐limitation of phytoplankton growth in oceanic and coastal waters, and the role of P‐limitation in regulating cell size and toxin levels in phytoplankton. Finally, we examine the role of P and other nutrients in the transition of phytoplankton communities from early succession species (diatoms) to late succession ones (e.g., dinoflagellates and haptophytes).     

Interannual variability in the distribution of the phytoplankton standing stock across the seasonal sea-ice zone west of the Antarctic Peninsula

The spatial distribution of phytoplankton cell abundance, carbon(C) biomass and chlorophyll a (Chl a) concentration was analysedduring three summers (1996, 1997 and 1999) in a seasonal sea-icearea, west of the Antarctic Peninsula. The objective of thestudy was to assess interannual variability in phytoplanktonspatial distribution and the mechanisms that regulate phytoplanktonaccumulation in the water column. Phytoplankton C biomass andChl a distributions were consistent from year to year, exhibitinga negative on/offshore gradient. The variations in C concentrationhad a close and non-linear relationship with the upper mixedlayer depth, suggesting that the vertical mixing of the watercolumn is the main factor regulating phytoplankton stock. Themagnitude of C gradients was 5-fold higher during 1996 thanduring 1997 and 1999. This was ascribed to interannual variationsin the concentration of diatom blooms in the region influencedby sea-ice melting. Vertical distribution of the phytoplankton,as estimated from Chl a profiles, also varied along an on/offshoregradient: Chl a was distributed homogeneously in the upper mixedlayer in coastal and mid-shelf stations and concentrated inthe deep layer (40–100 m) occupied by the winter waters(WW, remnants of the Antarctic surface waters during summer)in more offshore stations. The region with a deep Chl a maximumlayer (DCM layer) was dominated by a phytoplankton assemblagecharacterized by a relatively high concentration of diatoms.The extent of this region varied from year to year: it was restrictedto pelagic waters during 1996, extended to the shelf slope during1997 and occupied a major portion of the area during 1999. Itis hypothesized that iron depletion in near surface waters dueto phytoplankton consumption, and a higher concentration inWW, regulated this vertical phytoplankton distribution pattern.Furthermore, we postulate that year-to-year variations in thespatial distribution of the DCM layer were related to interannualvariations in the timing of the sea-ice retreat. The similaritybetween our results and those reported in literature for otherareas of the Southern Ocean allows us to suggest that the mechanismsproposed here as regulating phytoplankton stock in our areamay be applicable elsewhere.     

Redistribution of the lizardfish Harpadon nehereus in coastal waters of China due to climate change

Climate change has the potential to greatly alter species distributions and threatens biodiversity in marine ecosystems. Mapping changes in species distribution patterns under climate change will help facilitate management strategies to maintain ecosystem structure and function. The lizardfish Harpadon nehereus is an aggressive predator that has experienced rapid population growth along the coast of China in recent decades, compressing the ecological niches of other marine species and disrupting food webs. If this species’ range is shifting due to climate change, it could further impact the integrity of ecological communities. To map the distribution of H. nehereus, we developed an ensemble species distribution model and projected the present and future habitat suitability in Chinese coastal waters. Annual mean benthic water temperature was identified as the most important variable affecting the projected distribution of H. nehereus, followed by water depth and salinity. Currently suitable habitats are along the coast from Guangxi Province to the southern Jiangsu Province. As climate changes, the southern portion of its distribution is predicted to recede with habitat losses, and the overall suitable habitat will shift northward. To avoid the potential impacts of H. nehereus redistribution, precautionary management based on species distribution modeling would help to maintain healthy marine ecosystems in the newly invaded areas.