Net effect of environmental fluctuations in multiple global-change drivers across the tree of life

Jensen’s inequality predicts that the response of any given system to average constant conditions is different from its average response to varying ones. Environmental fluctuations in abiotic conditions are pervasive on Earth; yet until recently, most ecological research has addressed the effects of multiple environmental drivers by assuming constant conditions. One could thus expect to find significant deviations in the magnitude of their effects on ecosystems when environmental fluctuations are considered. Drawing on experimental studies published during the last 30 years reporting more than 950 response ratios ( n = 5,700), we present a comprehensive analysis of the role that environmental fluctuations play across the tree of life. In contrast to the predominance of interactive effects of global-change drivers reported in the literature, our results show that their cumulative effects were additive (58%), synergistic (26%), and antagonistic (16%) when environmental fluctuations were present. However, the dominant type of interaction varied by trophic level (autotrophs: interactive; heterotrophs: additive) and phylogenetic group (additive in Animalia; additive and positive antagonism in Chromista; negative antagonism and synergism in Plantae). In addition, we identify the need to tackle how complex communities respond to fluctuating environments, widening the phylogenetic and biogeographic ranges considered, and to consider other drivers beyond warming and acidification as well as longer timescales. Environmental fluctuations must be taken into account in experimental and modeling studies as well as conservation plans to better predict the nature, magnitude, and direction of the impacts of global change on organisms and ecosystems.Agencia Estatal de Investigación | Ref. PGC2018-094553B-I00Agencia Estatal de Investigación | Ref. FJCI2017-32318Agencia Estatal de Investigación | Ref. IJC2019-040850-IJunta de Andalucía | Ref. POSTDOC-21-0004

Nutrient limitation suppresses the temperature dependence of phytoplankton metabolic rates

Climate warming has the potential to alter ecosystem function through temperature-dependent changes in individual metabolic rates. The temperature sensitivity of phytoplankton metabolism is especially relevant, since these microorganisms sustain marine food webs and are major drivers of biogeochemical cycling. Phytoplankton metabolic rates increase with temperature when nutrients are abundant, but it is unknown if the same pattern applies under nutrient-limited growth conditions, which prevail over most of the ocean. Here we use continuous cultures of three cosmopolitan and biogeochemically relevant species (Synechococcus sp., Skeletonema costatum and Emiliania huxleyi) to determine the temperature dependence (activation energy, Ea) of metabolism under different degrees of nitrogen (N) limitation. We show that both CO2 fixation and respiration rates increase with N supply but are largely insensitive to temperature. Ea of photosynthesis (0.11 ± 0.06 eV, mean ± SE) and respiration (0.04 ± 0.17 eV) under N-limited growth is significantly smaller than Ea of growth rate under nutrient-replete conditions (0.77 ± 0.06 eV). The reduced temperature dependence of metabolic rates under nutrient limitation can be explained in terms of enzyme kinetics, because both maximum reaction rates and half-saturation constants increase with temperature. Our results suggest that the direct, stimulating effect of rising temperatures upon phytoplankton metabolic rates will be circumscribed to ecosystems with high-nutrient availabilityMinisterio de Economía y Competitividad | Ref. CTM2014-53582-

Effects of temperature and nutrient supply on resource allocation, photosynthetic strategy, and metabolic rates of Synechococcus sp.

Temperature and nutrient supply are key factors that control phytoplankton ecophysiology, but their role is commonly investigated in isolation. Their combined effect on resource allocation, photosynthetic strategy, and metabolism remains poorly understood. To characterize the photosynthetic strategy and resource allocation under different conditions, we analyzed the responses of a marine cyanobacterium ( Synechococcus PCC 7002) to multiple combinations of temperature and nutrient supply. We measured the abundance of proteins involved in the dark (RuBis CO , rbc L) and light (Photosystem II , psbA) photosynthetic reactions, the content of chlorophyll a , carbon and nitrogen, and the rates of photosynthesis, respiration, and growth. We found that rbc L and psbA abundance increased with nutrient supply, whereas a temperature‐induced increase in psbA occurred only in nutrient‐replete treatments. Low temperature and abundant nutrients caused increased RuBis CO abundance, a pattern we observed also in natural phytoplankton assemblages across a wide latitudinal range. Photosynthesis and respiration increased with temperature only under nutrient‐sufficient conditions. These results suggest that nutrient supply exerts a stronger effect than temperature upon both photosynthetic protein abundance and metabolic rates in Synechococcus sp. and that the temperature effect on photosynthetic physiology and metabolism is nutrient dependent. The preferential resource allocation into the light instead of the dark reactions of photosynthesis as temperature rises is likely related to the different temperature dependence of dark‐reaction enzymatic rates versus photochemistry. These findings contribute to our understanding of the strategies for photosynthetic energy allocation in phytoplankton inhabiting contrasting environments.Agencia Estatal de Investigación | Ref. PGC2018‐094553‐B‐I00National Science Foundation (USA) | Ref. ANT‐0944254National Environmental Research Council (UK) | Ref. NE/F019254/1National Environmental Research Council (UK) | Ref. NE/G009155/1Xunta de Galici

Temporal variability of diazotroph community composition in the upwelling region off NW Iberia

Knowledge of the ecology of N 2 -fixing (diazotrophic) plankton is mainly limited to oligotrophic (sub)tropical oceans. However, diazotrophs are widely distributed and active throughout the global ocean. Likewise, relatively little is known about the temporal dynamics of diazotrophs in productive areas. Between February 2014 and December 2015, we carried out 9 one-day samplings in the temperate northwestern Iberian upwelling system to investigate the temporal and vertical variability of the diazotrophic community and its relationship with hydrodynamic forcing. In downwelling conditions, characterized by deeper mixed layers and a homogeneous water column, non-cyanobacterial diazotrophs belonging mainly to nifH clusters 1G (Gammaproteobacteria) and 3 (putative anaerobes) dominated the diazotrophic community. In upwelling and relaxation conditions, affected by enhanced vertical stratification and hydrographic variability, the community was more heterogeneous vertically but less diverse, with prevalence of UCYN-A (unicellular cyanobacteria, subcluster 1B) and non-cyanobacterial diazotrophs from clusters 1G and 3. Oligotyping analysis of UCYN-A phylotype showed that UCYN-A2 sublineage was the most abundant (74%), followed by UCYN-A1 (23%) and UCYN-A4 (2%). UCYN-A1 oligotypes exhibited relatively low frequencies during the three hydrographic conditions, whereas UCYN-A2 showed higher abundances during upwelling and relaxation. Our findings show the presence of a diverse and temporally variable diazotrophic community driven by hydrodynamic forcing in an upwelling system.Xunta de Galicia | Ref. EM2013/021Ministerio de Economía, Industria y Competitividad | Ref. CTM2016-75451-C2-1-RMinisterio de Educación, Cultura y Deporte | Ref. FPU13/01674Ministerio de Educación, Cultura y Deporte | Ref. EST16/00142Universidad de Vigo | Ref. Axudas á investigación 201

The CIM-UVigo plug-in hybrid propulsion vessel for coastal oceanographic research: a tool for the ecological transition

Peer Reviewe

Factors controlling the community structure of picoplankton in contrasting marine environments

The effect of inorganic nutrients on planktonic assemblages has traditionally relied on concentrations rather than estimates of nutrient supply. We combined a novel dataset of hydrographic properties, turbulent mixing, nutrient concentration, and picoplankton community composition with the aims of (i) quantifying the role of temperature, light, and nitrate fluxes as factors controlling the distribution of autotrophic and heterotrophic picoplankton subgroups, as determined by flow cytometry, and (ii) describing the ecological niches of the various components of the picoplankton community. Data were collected at 97 stations in the Atlantic Ocean, including tropical and subtropical open-ocean waters, the northwestern Mediterranean Sea, and the Galician coastal upwelling system of the northwest Iberian Peninsula. A generalized additive model (GAM) approach was used to predict depth-integrated biomass of each picoplankton subgroup based on three niche predictors: sea surface temperature, averaged daily surface irradiance, and the transport of nitrate into the euphotic zone, through both diffusion and advection. In addition, niche overlap among different picoplankton subgroups was computed using nonparametric kernel density functions. Temperature and nitrate supply were more relevant than light in predicting the biomass of most picoplankton subgroups, except for Prochlorococcus and low-nucleic-acid (LNA) prokaryotes, for which irradiance also played a significant role. Nitrate supply was the only factor that allowed the distinction among the ecological niches of all autotrophic and heterotrophic picoplankton subgroups. Prochlorococcus and LNA prokaryotes were more abundant in warmer waters (>20 ∘C) where the nitrate fluxes were low, whereas Synechococcus and high-nucleic-acid (HNA) prokaryotes prevailed mainly in cooler environments characterized by intermediate or high levels of nitrate supply. Finally, the niche of picoeukaryotes was defined by low temperatures and high nitrate supply. These results support the key role of nitrate supply, as it not only promotes the growth of large phytoplankton, but it also controls the structure of marine picoplankton communities.Ministerio de Economía y Competitividad | Ref. CTM2012-30680Ministerio de Economía y Competitividad | Ref. CTM2008-0626I-C03-01Ministerio de Economía y Competitividad | Ref. REN2003-09532-C03-01Ministerio de Economía y Competitividad | Ref. CTM2004-05174 -C02Ministerio de Economía y Competitividad | Ref. CTM2011-25035Xunta de Galicia | Ref. 09MMA027604PRXunta de Galicia | Ref. EM2013/021European Commission | Ref. FP7, n. 261860Ministerio de Economía y Competitividad | Ref. FJCI-641 2015-2571

A global compilation of coccolithophore calcification rates

The biological production of calcium carbonate (CaCO3), a process termed calcification, is a key term in the marine carbon cycle. A major planktonic group responsible for such pelagic CaCO3 production (CP) is the coccolithophores, single-celled haptophytes that inhabit the euphotic zone of the ocean. Satellite-based estimates of areal CP are limited to surface waters and open-ocean areas, with current algorithms utilising the unique optical properties of the cosmopolitan bloom-forming species Emiliania huxleyi, whereas little understanding of deep-water ecology, optical properties or environmental responses by species other than E. huxleyi is currently available to parameterise algorithms or models. To aid future areal estimations and validate future modelling efforts we have constructed a database of 2765 CP measurements, the majority of which were measured using 12 to 24 h incorporation of radioactive carbon (14C) into acid-labile inorganic carbon (CaCO3). We present data collated from over 30 studies covering the period from 1991 to 2015, sampling the Atlantic, Pacific, Indian, Arctic and Southern oceans. Globally, CP in surface waters ( < 20 m) ranged from 0.01 to 8398 µmol C m−3 d−1 (with a geometric mean of 16.1 µmol C m−3 d−1). An integral value for the upper euphotic zone (herein surface to the depth of 1 % surface irradiance) ranged from  < 0.1 to 6 mmol C m−2 d−1 (geometric mean 1.19 mmol C m−2 d−1). The full database is available for download from PANGAEA at https://doi.org/10.1594/PANGAEA.888182

Effect of temperature on the unimodal size scaling of phytoplankton growth

Contrary to predictions by the allometric theory, there is evidence that phytoplankton growth rates peak at intermediate cell sizes. However, it is still unknown if this pattern may result from the effect of experimental temperature. Here we test whether temperature affects the unimodal size scaling pattern of phytoplankton growth by (1) growing Synechococcus sp., Ostreococcus tauri, Micromonas commoda and Pavlova lutheri at 18 °C and 25 °C, and (2) using thermal response curves available in the literature to estimate the growth rate at 25 °C as well as the maximum growth rate at optimal temperature for 22 species assayed previously at 18 °C. We also assess the sensitivity of growth rate estimates to the metric employed for measuring standing stocks, by calculating growth rates based on in vivo fluorescence, chlorophyll a concentration, cell abundance and biomass (particulate organic carbon and nitrogen content). Our results show that the unimodal size scaling pattern of phytoplankton growth, with a peak at intermediate cell sizes, is observed at 18 °C, 25 °C and at the optimal temperature for growth, and that it prevails irrespective of the standing-stock metric used. The unimodal size scaling pattern of phytoplankton growth is supported by two independent field observations reported in the literature: (i) a positive relationship between cell size and metabolic rate in the picophytoplankton size range and (ii) the dominance of intermediate-size cells in nutrient-rich waters during bloomsMinisterio de Ciencia e Innovación | Ref. CTM2007-28925-E / MARMinisterio de Ciencia e Innovación | Ref. CTM2014-53582-RMinisterio de Ciencia e Innovación | Ref. PGC2018-094553-B-I00Xunta de Galicia | Ref. ED481-2017 / 34

A pseudo‐lagrangian transformation to study a chlorophyll‐a patch in the Ría de Vigo (NW Iberian Peninsula)

Financiado para publicación en acceso aberto: Universidade de Vigo/CISUGBecause of the difficulties in tracking a water mass over time and conducting synoptic surveys over large spatial scales, measurements of biological variables in the ocean are often restricted to isolated Eulerian observations. Here a proof-of-concept of a pseudo-Lagrangian transformation was applied to a time series of chlorophyll-a profiles acquired at a single fixed station to diagnose the shape of a phytoplankton patch, and its physical-biological rates of transformation. During August 2013, a 27-hr time series of observations of horizontal currents, hydrographic properties, turbulent mixing and chlorophyll-a was acquired at a central station of the Ría de Vigo (NW Iberian Peninsula). A chlorophyll-a patch, tilted upward toward the inner part of the Ría, was observed moving back and forth past the sampling station. Its shape and position during the sampling period were modulated by the semi-diurnal (M2) tidal currents and the vertically sheared upwelling circulation. The pseudo-Lagrangian transformation allowed estimation of chlorophyll-a net rates of change. These rates were positive between 12 and 14 m depth, and negative elsewhere, with a mean value of −0.001 ± 0.449 days−1 within the patch maximum. After accounting for the effects of diffusion and sinking, the mean net biological production rate in the upper 15 m (0.53 ± 0.25 days−1) was comparable with in vitro estimates of the balance between phytoplankton growth and mortality obtained from dilution experiments carried out under similar conditions (0.2 ± 0.7 days−1). This pseudo-Lagrangian transformation is complementary to traditional analyses for the quantification of ecological processes and biogeochemical budgets.Ministerio de Economía y Competitividad | Ref. CTM2012-35155Ministerio de Economía, Industria y Competitividad | Ref. CTM2016-75451- C2-1-RMinisterio de Educación, Cultura y Deporte | Ref. FPU014/0538

Characterizing the surface microlayer in the Mediterranean Sea: trace metal concentrations and microbial plankton abundance

The Sea Surface Microlayer (SML) is known to be enriched by trace metals relative to the underlying water and harbor diverse microbial communities (i.e., neuston). However, the processes linking metals and biota in the SML are not yet fully understood. The metal (Cd, Co, Cu, Fe, Ni, Mo, V, Zn and Pb) concentrations in aerosol samples in the SML (dissolved and total fractions) and in subsurface waters (SSWs; dissolved fraction at ∼1 m depth) from the western Mediterranean Sea were analyzed in this study during a cruise in May–June 2017. The composition and abundance of the bacterial community in the SML and SSW, the primary production, and Chl a in the SSW were measured simultaneously at all stations during the cruise. Residence times in the SML of metals derived from aerosol depositions were highly variable and ranged from minutes for Fe (3.6±6.0 min) to a few hours for Cu (5.8±6.2 h). Concentrations of most of the dissolved metals in both the SML and SSW were positively correlated with the salinity gradient and showed the characteristic eastward increase in the surface waters of the Mediterranean Sea (MS). In contrast, the total fraction of some reactive metals in the SML (i.e., Cu, Fe, Pb and Zn) showed a negative correlation with salinity and a positive correlation with microbial abundance, which might be associated with microbial uptake. Our results show a strong negative correlation between the dissolved and total Ni concentration and heterotrophic bacterial abundance in the SML and SSW, but we cannot ascertain whether this correlation reflects a toxicity effect or is the result of some other process.Ministerio de Economía y Competitividad | Ref. CTM2014-59244-C3-3-RMinisterio de Ciencia, Innovación y Universidades | Ref. IJC2018-037545-IMinisterio de Economía y Competitividad | Ref. JCI-2015-2687