Increasing picocyanobacteria success in shelf waters contributes to long‐term food web degradation

Abstract

Continental margins are disproportionally important for global primary production, fisheries and CO2 uptake. However, across the Northeast Atlantic shelves, there has been an ongoing summertime decline of key biota—large diatoms, dinoflagellates and copepods—that traditionally fuel higher tropic levels such as fish, sea birds and marine mammals. Here, we combine multiple time series with in situ process studies to link these declines to summer nutrient stress and increasing proportions of picophytoplankton that can comprise up to 90% of the combined pico‐ and nanophytoplankton biomass in coastal areas. Among the pico‐fraction, it is the cyanobacterium Synechococcus that flourishes when iron and nitrogen resupply to surface waters are diminished. Our field data show how traits beyond small size give Synechococcus a competitive edge over pico‐ and nanoeukaryotes. Key is their ability to grow at low irradiances near the nutricline, which is aided by their superior light‐harvesting system and high affinity to iron. However, minute size and lack of essential biomolecules (e.g. omega‐3 polyunsaturated fatty acids and sterols) render Synechococcus poor primary producers to sustain shelf sea food webs efficiently. The combination of earlier spring blooms and lower summer food quantity and quality creates an increasing period of suboptimal feeding conditions for zooplankton at a time of year when their metabolic demand is highest. We suggest that this nutrition‐related mismatch has contributed to the widespread, ~50% decline in summer copepod abundance we observe over the last 60 years. With Synechococcus clades being prominent from the tropics to the Arctic and their abundances increasing worldwide, our study informs projections of future food web dynamics in coastal and shelf areas where droughts and stratification lead to increasing nutrient starvation of surface waters.

Effect of temperature on the unimodal size scaling of phytoplankton growth

“…At the level of functional groups, there is also evidence that diatoms sustain faster growth rates in conditions when they contribute most to the community biomass [41][42][43] . In this connection, the association between a higher ability to sustain fast growth rates and an enhanced contribution to total biomass agrees with the observation that picoeukaryotes tend to become dominant over the picocyanobacteria Synechococcus and Prochlorococcus as conditions become less oligotrophic 31,44,45 . A similar result has been described also for phytoplankton of larger cell sizes, whereby the size distribution of pico-and nanoeukaryotes in the Atlantic Ocean shifted from a biomass dominance of picoeukaryotes in oligotrophic regions towards a dominance by nanoeukaryotes in more nutrient-rich waters 46 .…”

Synergic Effects of Temperature and Irradiance on the Physiology of the Marine Synechococcus Strain WH7803

“…The observed synergic effect between LT and HL might have important implications for the dynamics of natural Synechococcus populations in the field, where cells are often subjected to concomitant variations of temperature and irradiance, notably in upwelling areas or during seasonal mixing events. In these circumstances, this effect could negatively impact the competitiveness of Synechococcus cells with regard to other phytoplanktonic groups, such as picoeukaryotes or diatoms that often predominate in cold mixed waters (Uysal and Köksalan, 2006;Schmidt et al, 2020).…”

Increasing nutrient stress reduces the efficiency of energy transfer through planktonic size spectra

“…(Li et al 2009;Morán et al 2010). Such changes are already being observed (Schmidt et al 2020) and are concomitant with changing human nutrient inputs to inshore eutrophic waters (Capuzzo et al 2018). Such shifts underline the need to better understand how pelagic food web efficiency relates to nutrient status.…”

“…Clearly, size spectrum approaches have limitations. They cannot resolve important species-specific detail, for example on changing distribution patterns or replacement of nutritious taxa with those of similar size, but which are non-nutritious or harmful (Schmidt et al 2020). Their key advantage is that, when based on time averaging measurements, and across a sufficiently large range of body mass, they provide insights into some key properties of the system.…”