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The impact of the occurrence of the non-indigenous species (NIS) Acartia tonsa, Oithona davisae, and Pseudodiaptomus marinus and of the range-expanding copepods Acartia bifilosa and Calanipeda aquaedulcis on the structure and diversity of zooplankton communities was analyzed using 18 years (1998-2015) time series from the contrasting estuaries of Bilbao and Urdaibai (Basque coast, Bay of Biscay). Changes in the structure of communities were assessed by using multivariate analyses of taxa abundances and changes in diversity by using descriptors of alpha, beta, and gamma diversity. The most evident changes occurred at the upper reaches of the estuary of Bilbao, where an abundant and less diverse brackish community, dominated by the NIS, A. tonsa and O. davisae, succeeded a low abundance and more diverse community of neritic origin. The later establishment of C. aquaedulcis was linked to further changes in the structure of the community and a progressive increase in diversity. The seasonal pattern of diversity at the inner estuary and the beta diversity in the estuary were also significantly affected by the arrival of the NIS and C. aquaedulcis. In contrast, the original low diversity brackish community of the estuary of Urdaibai, clearly dominated by A. bifilosa, was far less affected by the arrival of the same copepod NIS, and A. bifilosa remained as the species best related to the changes in zooplankton structure and diversity in the brackish habitats of the estuary. Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This work was supported by the University of the Basque Country (UPV/EHU) (UPV/EHU, GIU19/059) and the Basque Government (PIBA2020-1-0028 & IT1723-22) and through a grant to Z. Barroeta to carry out her PhD (UPV/EHUn Ikertzaileak Prestatzeko Kontratazio Deialdia 2016).

The interannual variations in absolute and relative densities of copepods from the neritic waters of the southeastern Bay of Biscay and their relationship to climate teleconnections and local environmental factors were assessed using time series for the 1998–2015 period. Opposite patterns of variation of the absolute densities of spring Acartia clausi and Centropages typicusspecies vs. summer/autumn species, mainly Oncaea media, but also Ditrichocorycaeus anglicus, Oithona nana, Temora stylifera, and Oithona plumifera were detected. This type of opposite patterns were also observed between the relative densities of the spring A. clausi and summer Paracalanus parvus species. These opposite density patterns were positively correlated to all seasons North Atlantic Oscillation (NAO), spring East Atlantic pattern (EA), summer and autumn water temperature and summer chlorophyll a. They were negatively correlated to summer EA pattern, the winter and spring Atlantic Multidecadal Oscillation (AMO) and water temperature, and the upwelling index of all seasons. In these patterns of copepod variation two regime shifts were detected, one in 2008 towards an increase in the spring species and the other one in 2014–2015 towards an increase of summer species. This latter regime shift coincides in time with the abrupt community shifts predicted in the literature for 2014.

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Zooplankton phenological shifts may affect energy transfer through pelagic food web and up to fisheries, but few studies have compared zooplankton phenology across a wide latitudinal range of water temperatures. We examined the phenological variations of zooplankton at four sites along a latitudinal gradient from the Bay of Biscay [Bilbao and Urdaibai (BU)], the English Channel (Plymouth; L4), and the North Sea [Stonehaven (SH)] from 1999 to 2013. Zooplankton taxa showed interannual phenological variations that were opposite in direction between the southernmost BU and the northernmost SH sites. The East Atlantic pattern was the climate teleconnection best related to zooplankton phenological variations. Among local variables , salinity at BU was best related to phenological changes at BU as opposed to those at SH. Locally, chlorophyll a was most relevant at SH and temperature at L4. While we did see some imprints of temperature in causing expected directions of phenology shifts, i.e. towards earlier appearance of spring taxa and later appearance of autumn taxa in warm years, these patterns were by no means clear-cut. The dominant role of temperature in driving phenological variation suggested by some studies seems to be obscured by biotic and climatic controls acting differently along our environmental gradient.

The colonization success of non-indigenous species (NIS) of copepods that arrived in the estuaries of Bilbao and Urdaibai (Bay of Biscay) and other expanding species (OES) of copepods that arrived in the former estuary during the 1998–2015 period, as well as the impact of such species on the density and seasonal patterns of congeneric species, total copepods and total zooplankton have been analysed. The estuary of Bilbao was successfully colonized by the NIS Acartia tonsa and Oithona davisae (since 2003) and by the NIS Pseudodiaptomus marinus and the OES Calanipeda aquaedulcis (since 2010), coinciding with the progressive improvement of environmental conditions in the rehabilitation process of this estuary. The three NIS species also arrived in the estuary of Urdaibai during the same time period, but only A. tonsa became abundant, likely due to inherent natural constraints for the other two species. A. tonsa in both estuaries, and O. davisae and C. aquaedulcis in the estuary of Bilbao became influential in the density, composition and dynamics of total copepods and zooplankton in water-masses of 33 or lower salinity. The highest impact was found in the inner estuary of Bilbao, where total copepods and zooplankton reached densities comparable to those of the outer estuary and copepod maxima moved from spring to summer due to the contribution of the colonizing copepod species. The congeneric species most affected by the NIS were the neritic species Acartia clausi and Oithona nana in the estuary of Bilbao, and the brackish species Acartia bifilosa in the estuary of Urdaibai.

The realized ecological niches of native zooplankton and non-indigenous species (NIS) were analysed in the contrasting estuaries of Bilbao and Urdaibai from 1998 to 2015 in order to study their responses to the particular features of each estuary and the biotic and abiotic changes along the study period. The marginality and tolerance of zooplankton taxa was estimated for the two estuaries together using the OMI analysis, whilst, by means of the WitOMI analysis, niches were differentiated into spatial subniches to assess the differences between estuaries and into temporal subniches to determine the variations in time within each estuary. The changes in the niche overlap of the main native and NIS species were calculated with the D-metric. Results showed that the combined effect of salinity gradients and seasonal variations, linked to temperature, defined the main spatio-temporal niches of zooplankton taxa in the overall environmental scenario of both estuaries. Thus, those factors separated winter-spring neritic, summer-autumn neritic, warm water affinity brackish and limnetic species. Secondarily, river discharge and hydrological stability accounted for the higher presence of freshwater and some brackish species in the estuary of Bilbao and tychoplanktonic organisms in the estuary of Urdaibai. At the regional scale the marginality and tolerance of zooplankton taxa reflected a combination of spatial and seasonal niche breadth and difference of abundance between estuaries. The number of taxa with niches not clearly explained by the environmental variables studied was higher in the estuary of Urdaibai, whilst the new arriving species occupied realized niches well defined by the environmental variables and overall zooplankton taxa showed a better discrimination from generalist to specialist behaviours in the estuary of Bilbao. This was related to inherent abiotic and biotic features of each estuary, which make the estuary of Urdaibai more refractory to the settlement of NIS species. Moreover, in the estuary of Bilbao, several neritic and brackish species experienced temporal changes in niche breadth and overlap that was attributed both to the environmental improvement related to rehabilitation plans in the system and the impact of the species that arrived during the study period. In the estuary of Urdaibai only small changes attributable to the limited impact of NIS were inferred, since no meaningful changes in environmental conditions were perceived. This work was supported by the University of the Basque Country through research funds to Consolidated Research Groups (GIU16/69) and through a grant to Z. Barroeta. The authors thank the WGEUROBUS of the International Council for the Exploration of the Sea (ICES) for facilitating research on P. marinus.

Since 2007, the non-indigenous calanoid copepod Pseudodiaptomus marinus Sato, 1913 has been increasingly recorded in numerous European sites, spreading at an unexpectedly fast pace over a short time-span. This species presents specific biological and behavioural traits which make it of particular interest for ecological and applied research topics. On 29–30 January 2018, 29 scientists from nine European Countries established the EUROBUS (Towards a EURopean OBservatory of the nonindigenous calanoid copepod Pseudodiaptomus marinUS) Working Group (WG). This WG aimed at creating a European network of institutions and researchers working on the various aspects of the biology and ecology of P. marinus, with an open forum where sharing experience and know-how among WG participants. This brought to an updated distribution map of P. marinus in European waters, as well as to the identification of priority research lines and potential joint initiatives under the WGEUROBUS umbrella. This contribution, stemming from the experts participating at the WG, represents the manifesto of the current and future initiatives developed within WGEUROBUS. info:eu-repo/semantics/publishedVersion

Zooplankton seasonality and its environmental drivers were studied at four coastal sites within the Northeast Atlantic Shelves Province (Bilbao35 (B35) and Urdaibai35 (U35) in the Bay of Biscay, Plymouth L4 (L4) in the English Channel and Stonehaven (SH) in the North Sea) using time series spanning 1999–2013. Seasonal community patterns were extracted at the level of broad zooplankton groups and copepod and cladoceran genera using redundancy analysis. Temperature was generally the environmental factor that explained most of the taxa seasonal variations at the four sites. However, between-site differences related to latitude and trophic status (i.e. from oligotrophic to mesotrophic) were observed in the seasonality of zooplankton community, mainly in the pattern of taxa that peaked in spring-summer as opposed to late autumn-winter zooplankton, which were linked primarily to differences in the seasonal pattern of phytoplankton. The percentage of taxa variations explained by environmental factors increased with latitude and trophic status likely related to the increase in the co-variation of temperature and chlorophyll a, as well as in the increase in regularity of the seasonal patterns of both temperature and chlorophyll a from south to north, and of chlorophyll a with trophic status. Cladocerans and cirripede larvae at B35 and U35, echinoderm larvae at L4 and decapod larvae at SH made the highest contribution to shape the main mode of seasonal pattern of zooplankton community, which showed a seasonal delay with latitude, as well as with the increase in trophic status.

Contribution of latitude, distance offshore and environmental factors to variations in zooplankton assemblages across the Northeast Atlantic Shelves Province, from the Bay of Biscay [Bilbao 35 (B35) and Urdaibai 35 (U35)] to the English Channel (Plymouth L4; L4) and the North Sea (Stonehaven; SH), were assessed mainly by redundancy analysis. For coarse zooplankton groups latitude explained the main between-site differences, and meroplankton contributed more than holoplankton. Latitudinal differences were best indicated by contrasting abundances of cirripede larvae and doliolids (most abundant at the lowest latitude sites) and bryozoan and polychaete larvae (most abundant at the highest latitude site). Doliolids were best indicators of temperature-mediated latitudinal differences. The interaction between latitude and distance offshore or salinity and phytoplankton biomass explained smaller percentages of the variability. The main differences in copepod and cladoceran genera reflected the oceanic influence, with highest presence of Corycaeus and Oncaea at L4, likely related to the higher influence of off-shelf water intrusions, and neritic Acartia dominating at SH, U35 and B35. Podon and Evadne, which decreased from south to north, reflected latitude-related differences driven more by salinity than by temperature. Instances where a single species (e.g. Acartia clausi) dominated showed common relationships with temperature, consistent with a common thermal niche. Differences in co-generic species dominance between sites depicted the latitudinal gradient.

Seasonal and interannual variations of total mesozooplankton abundance and community variability were assessed for the period 1998–2005 at 3 salinity sites (35, 33 and 30) of the estuaries of Bilbao and Urdaibai (southeast Bay of Biscay). Spatial differences in mesozooplankton seasonality were recognized, both within and between estuaries, related to differences between sites in hydrodynamic features and anthropogenic nutrient enrichment that drive phytoplankton biomass seasonal cycles. The within estuary seasonal differences in mesozooplankton community were mainly shown through seaward time-advances in the seasonal peak from summer to spring along the salinity gradient, linked to differences in phytoplankton availability during the summer, in turn, related to nutrient availability. These differences were most marked in the estuary of Urdaibai, where zooplankton seasonal pattern at 35 salinity (high tidal flushing) resembled that of shelf waters, while at 35 of the estuary of Bilbao zooplankton showed an estuarine seasonal pattern due to the influence of the estuarine plume. Cirripede larvae contributed most to the mesozooplankton seasonal variability, except at the outer estuary of Bilbao, where cladocerans and fish eggs and larvae were the major contributors, and the inner estuary of Urdaibai, where gastropod larvae contributed most. Total mesozooplankton increased at 30 salinity of the estuary of Bilbao and 35 salinity of the estuary of Urdaibai. Interannual variability of mesozooplankton at the lowest salinity of the estuary of Bilbao was mainly accounted for by copepods due to the introduction of non-indigenous species during estuarine rehabilitation from intense pollution. However, bivalve larvae and gastropod larvae showed the highest contributions at 35 salinity of the estuary of Urdaibai. At the rest of sites, the opposite interannual trends of polychaete larvae and hydromedusae generally made the highest contribution.

Zooplankton abundance series (1999–2013) from the coastal sites of Bilbao 35 (B35), Urdaibai 35 (U35), Plymouth L4 (L4) and Stonehaven (SH), in the Northeast Atlantic were compared to assess differences in the magnitude of seasonal, interannual and residual scales of variability, and in patterns of seasonal and interannual variation in relation to latitudinal location and trophic status. Results showed highest seasonal variability at SH consistent with its northernmost location, highest interannual variability at U35 associated to an atypical event identified in 2012 in the Bay of Biscay, and highest residual variability at U35 and B35 likely related to lower sampling frequency and higher natural and anthropogenic stress. Interannual zooplankton variations were not coherent across sites, suggesting the dominance of local influences over large scale environmental drivers. For most taxa the seasonal pattern showed coherent differences across sites, the northward delay of the annual peak being the most common feature. The between-site seasonal differences in spring–summer zooplankton taxa were related mainly to phytoplankton biomass, in turn, related to differences in latitude or anthropogenic nutrient enrichment. The northward delay in water cooling likely accounted for between-site seasonal differences in taxa that increase in the second half of the year.

The rapid warming of the wolrd’s oceans during the last few decades has affected distributional patterns of marine planktonic communities. Here, we analyse links between sea warming and changes in copepod community composition over the last 3 decades (1980−2012). We used zooplankton time-series data which included 79 species of copepods collected at 3 sites in the eastern North Atlantic (Bay of Biscay and the Kattegat Sea) and the Mediterranean Sea (Gulf of Saronikos). First, using community β-diversity metrics, we analysed temporal patterns of copepod community composition changes over time and its relation to local environmental conditions. Second, to test whether the changes in copepod community composition correspond to community thermal preferences, we used the community temperature index (CTI) and compared CTI interannual changes with local temperature trends. The β-diversity analysis reveals a high temporal turnover in the copepod community composition at the 3 sites (30−45%), with a significant similarity decrease over time (‘decay’) associated with both niche descriptors and demographic stochastic processes. CTI results reveal that both in the Kattegat and Saronikos, where the ocean warming rate was the highest amongst sites, copepod community changes are linked to temperature variability, suggesting that the community is tracking their thermal niche over time. Our findings unveil the fundamental role of abiotic factors structuring copepod biodiversity over time and reveal that the local velocity of ocean warming and the species thermal thresholds are key to rearranging copepod community composition in coastal ecosystems.

The effect of climate variability on estuarine water environments was assessed in two systems of the Bay of Biscay, the estuaries of Bilbao and Urdaibai, with contrasting morphology, hydrodynamic features and anthropogenic influence. To that purpose, the main time scales of variability in relevant environmental factors were established along spatial salinity gradients and, using a combination of multivariate and regression analyses, the contribution of each factor to the total variability, as well as the influence of climate factors in the seasonal and inter-annual estuarine environment variations were assessed. The major seasonal modes of variability in the water environments of both estuaries were accounted for by water temperature together with salinity stratification and/or chlorophyll a. This seasonal variability was associated with climate variability, as shown by the relationship with air temperature and river flow. The major inter-annual modes of variability were also accounted for by water temperature, along with dissolved oxygen and/or chlorophyll a in Bilbao, and chlorophyll a and/or transparency in Urdaibai. These were also associated with climate variability, in this case summer air temperatures. Water quality variables, such as dissolved oxygen and transparency, were found to be sensitive to reveal the effect of long term anthropogenic activities.

Feeding is critical for larval survival and it becomes a determining factor in the annual recruitment in species such as European anchovy Engraulis encrasicolus. Additionally, since differences in the plankton community may affect the larval feeding patterns, an interregional comparative study may contribute to understand these patterns concerning larval development and environmental features. The diet, feeding pattern and prey selectivity in relation to the ontogeny of the larval anchovy in the Cantabrian Sea (inner Bay of Biscay) and the Catalan Sea (NW Mediterranean) were compared in this study. Larvae fed preferentially on copepod eggs, nauplii and calanoid postnauplii, selecting them actively. Larval diet was similar before notochord flexion in the two areas. Nonetheless, for larvae of comparable size, prey preferences skewed towards small preys in the Cantabrian Sea, and towards large preys in the Catalan Sea. Differences appeared in the middle-sized larvae (6.5–9 mm) due to prey size and type. Diet differences were attributable (a) to the ability of the Catalan Sea larvae to capture bigger preys at a smaller individual size; and (b) to differences in prey preferences and availability. Therefore, geographic variety in larval populations and food environment features may promote variability in the larval anchovy diet.

Estuarine and marine ecosystems are subject to different sources of stress including changes in environmental physicochemical variables (nutrients, oxygen availability, temperature, salinity, pH) or exposure to a large cocktail of environmental pollutants. In the estuary of Bilbao, despite the improvement in environmental quality due to replacement of most polluting industries and the progressive implementation of an integrated sewage treatment plan, chronic pollution by metals and hydrocarbons still remains, together with eutrophication and pollution by emerging contaminants. The Unit of Formation and Research “Protection of Ecosystem Health” was created in 2012 through the strategic aggregation of three consolidated research groups: Cell Biology in Environmental Toxicology (CBET), Phytoplankton of estuaries and coastal areas (FITEAC) and Research on marine and estuarine pelagic environment and planktonic communities (MarEsPlank). The three groups have a long tradition in studying the health of marine and estuarine ecosystems from different perspectives, focusing in the Bay of Biscay and especially in the estuary of Bilbao. In this work we review data on the health status of the Bilbao estuary using early warning tools at the cell and tissue levels, phytoplankton assemblages and zooplankton ecology. In spite of the seasonal and interannual variability recorded for some parameters, a general recovery trend was observed for the health status in the estuary of Bilbao, with sporadic critical events such as the Prestige oil spill.

Variations in mesozooplankton abundance and community structure in response to water quality improvement and to variations in hydro-climatic conditions were studied in the inner estuary of Bilbao from 1998 to 2011. A process of recolonization was observed with a marked increase in copepod abundance and a smaller increase in the abundances of appendicularians, meroplanktonic bivalves and gastropods, at the expense of the decrease in groups of gelatinous predators. Within the copepods, an initial phase in this recolonization occurred through an increase in neritic copepods. However, in a second phase, the non-indigenous species Acartia tonsa and Oithona davisae increased and became dominant. In the last 2 years, a third non-indigenous species Pseudodiaptomus marinus was observed in lower densities, and Calanipeda aquaedulcis abundance increased becoming co-dominant with A. tonsa. All non-indigenous copepod species had summer/autumn peaks and were characteristic of brackish conditions, which suggests that unsaturated ecological niches in brackish waters were important for the settlement of non-indigenous species. Pollution abatement allowed for zooplankton recolonization, but variations in community structure, both at the broad taxonomic group and at the copepod species level, were greatly influenced by hydro-climatic factors, temperature being the single best explanatory variable of zooplankton variations.

A two-layer box model based on salinity and freshwater inflow data was developed and used to estimate net water circulation, contributions of gravitational circulation exchange and tide-driven exchange, and turnover times for the estuary of Bilbao, a small estuary of the Basque coast (Bay of Biscay). Average monthly estimations for the 2001–2010 period were made and related to river discharge and saltwater inflow. Seasonal variations of surface-layer outflows were strongly related to the river discharge regime, even in the lower estuary (inner Abra harbour). Bottom-layer salt-water inflow from the outer Abra was the main driver of bottom landward flow, vertical advection and surface-layer outflow in the inner Abra, but not in the channelized zone that extends from the inner limit of the Abra harbour to the tidal limit. Gravitational circulation exchange dominated in the entire estuary over the annual cycle. Tide-driven exchange proportionately increased in summer and showed the highest contribution (42%) in the lower estuary in August. Flushing and residence times increased in summer in relation with the decrease of freshwater discharge, although in the innermost zone of the estuary they were also high in winter due to the retention of freshwater at the inner estuary under extremely high discharge conditions. Flushing and residence time maxima of 21.5 and 28.6 days respectively were obtained for the entire studied zone in August. It is of note that turnover times differed largely between the upper (flushing time of 0.4–2.4 days) and bottom (flushing time of 2–10 days) layers in the channelized zone. Results supported intuitive conclusions drawn in previous studies about the spatio-temporal dynamics of dissolved oxygen, chlorophyll and zooplankton populations in the estuary of Bilbao, in relation to the effect of water circulation and turnover.

Dissolved oxygen dynamics in estuarine and coastal environments are complex and highly variable, which highlight the need to compile information from many different types of estuaries. Small estuaries where euhaline habitats dominate are particularly ill represented in the literature. As a contribution to fill this gap, a study on dissolved oxygen dynamics was conducted in the small estuary of Urdaibai (inner Bay of Biscay). Spatial and temporal variations in the percentage saturation of dissolved oxygen (DO-saturation) along the salinity gradient of the estuary and the role of hydro-climatic factors and eutrophication as drivers of those variations at seasonal and inter-annual time scales were analyzed (period 1998–2008). DO-saturation showed an inner to outer estuary increasing gradient. DO-saturation below the salinity gradient layer was either significantly higher than or not significantly different from that in the salinity gradient layer. DO-saturation showed summer minima, but hypoxia was rarely observed. At the outermost estuary, seasonal variations of DO were small and it is hypothesized that DO dynamics were governed mainly by tidal exchange and turbulence. In the intermediate and inner estuary, seasonal variations of DO-saturation were best explained by river discharge, and to a lesser extent by chlorophyll a and temperature, each factor gaining relevance in different periods of the year. In intermediate and inner zones, river discharge exerted a positive effect on DO-saturation, likely via an increase in the renewal rate of DO. At the inter-annual time scale, unlike at the seasonal scale, temperature did not show a significant negative relationship with DO-saturation.

Background: The introduction of NIS to estuaries and coastal embayment is of great concern. Commercial ships’ ballast water discharge and the northwards progression of species due to the ongoing climate change arise as the main factors explaining the rising occurrence of NIS species in Northern Atlantic waters. In this regard, regular monitoring of the plankton communities is paramount as to be able to respond properly to this potential issue. Results: While monitoring the invasive copepod Acartia tonsa populations in the estuaries of Bilbao and Urdaibai (Basque country, Spain), we report here the Asian copepod Pseudodiaptomus marinus for the first time in the Iberian Peninsula waters. Individuals from both species were collected from July to October, 2013 for DNA sequencing of mitochondrial cytochrome c oxidase subunit I gene (MT-CO1). Phylogenetic analysis of MT-CO1 confirmed P. marinus identity. Conclusions: Phylogeographic distribution of A. tonsa haplotypes in Europe along with the Bilbao port traffic patterns suggested a secondary invasion from an European source to Basque estuaries. The successful establishment of the A. tonsa population and the appearance of Pseudodiaptomus marinus confirm the need for regular plankton monitoring of estuarine and port waters. This applies also to nearby systems as these populations could represent a source of future dispersal. DA’s work was supported by the ZabaldUz Program (PhD fellowship). SGIker technical and human support (UPV/EHU) is gratefully acknowledged. Thanks to T. Matellanes (Bilbao Port Authority) for providing maritime traffic data. Special thanks to the anonymous reviewers that greatly improved the different manuscript versions. The sampling program received funds from the University of the Basque Country (UFI11/37) and the Basque Government (GIC10/168).

Metabarcoding is becoming an increasingly valuable alternative approach to biodiversity assessment, due to the combination of extreme sensitivity and potential for the highest taxonomic resolution in a cost- and time-effective methodology. To evaluate the capacity of metabarcoding for estuarine plankton monitoring, a comparison between the results obtained with this approach were compared with those based on traditional taxonomic analysis (microscopy). Database incompleteness, one of the main limitations of metabarcoding, was somewhat overcome by the addition of DNA sequences for local species, which increased the taxonomic assignment success from 23.7 to 50.5 %. When the communities were studied along with environmental variables, similar spatial and temporal trends of taxonomic diversity were observed for metabarcoding and microscopic studies of zooplankton, but not for phytoplankton. This is most likely attributable to the lack of representative sequences for phytoplankton species in current databases. In addition, there was high correspondence in community composition when comparing abundances estimated from metabarcoding and microscopy, suggesting semiquantitative potential for metabarcoding. Furthermore, metabarcoding allowed the detection and identification of two non-indigenous species (NIS) found in the study area at abundances hardly detectable by microscopy. Overall, our results indicate that metabarcoding is a powerful approach with excellent possibilities for use in plankton monitoring, early detection of NIS and plankton biodiversity shifts.

Seasonal, interannual and spatial variabilities were analysed for the > 100 μm and > 200 μm zooplankton assemblages in the estuary of Bilbao throughout 1997–2000, and related to hydroclimatic and water-quality factors. Seasonal and interannual patterns of abundance differed between assemblages, and only the abundance of the > 100 μm zooplankton was correlated with temperature. The large-sized zooplankton decreased more drastically than the small-sized zooplankton with decreasing salinity, and showed highest correlations with dissolved oxygen and water transparency. Seasonal changes were the major variability mode of zooplankton composition in both assemblages. Interannual changes associated to phytoplankton biomass and temperature were more evident in the small-sized zooplankton, whilst spatial differences related to oxygen depletion were more evident in the large-sized zooplankton. This indicates that small zooplankton was more sensitive to climate-related factors, while large zooplankton was more sensitive to water quality. Small copepods, cirriped larvae, appendicularians and Noctiluca were the main taxa responsible for the interannual variations in the > 100 μm assemblage. In the > 200 μm assemblage, large copepods were the main zooplankton responsible for the spatial variability related to oxygen depletion. Cnidarians and cladocerans responded mainly to decreases in salinity, and polychaete larvae were found to be unaffected by the decrease in dissolved oxygen and salinity. Results suggest that size-related differential responses of zooplankton should be considered when zooplankton monitoring is performed to assess the effect of climate forcing and pollution in coastal and estuarine environments.

The effect of environmental factors (river discharge, water temperature and dissolved oxygen saturation) on the abundance and distribution of Acartia populations and the interactions between their congenerics was evaluated by means of transfer function (TF) models in the estuary of Bilbao during the period 1998–2005. The recorded species were Acartia clausi, Acartia tonsa, Acartia margalefi and Acartia discaudata. Acartia clausi dominated in the entire euhaline region of this estuary until 2003 when it was displaced from the inner part by A. tonsa. This invasive species (A. tonsa) was found for the first time in 2001 and colonized successfully the inner (salinity 30) and intermediate (salinity 33) waters of this estuary since 2003. The TF models revealed an immediate and negative effect of A. tonsa on A. clausi in the intermediate salinity (33) waters, where these species showed the highest spatial overlap. The results indicate that environmental changes from 2003 influenced the abundance of Acartia species, being unfavourable for A. clausi. The decrease of A. clausi abundance in low salinity waters was related to a significant decrease of dissolved oxygen saturation levels, whereas the increase of temperature was linked to a significant increase of A. tonsa. Acartia margalefi and A. discaudata were scarce over the entire period, but they were found to be valuable indicators of hydrological changes, which were associated to climate factors. These two latter species increased in abundance and expanded their seasonal distribution, and in the case of A. margalefi also its spatial distribution, in 2002, coinciding with the period in the time-series when autumn–winter rainfall and summer temperatures were lowest, and dissolved oxygen saturation levels were highest.

The seasonal pattern of size-fractionated phytoplankton biomass, primary production and respiration was investigated along the longitudinal axis of the Nervion–Ibaizabal estuary (Bay of Biscay) from April 2003 to September 2004. Environmental factors influencing phytoplankton dynamics were also studied. Chlorophyll a biomass showed a longitudinal pattern of increase from the outer Abra bay to the inner estuary. On a seasonal scale, in the intermediate and inner estuary phytoplankton biomass maxima were registered in summer, the warmest and driest season, whereas in the outer bay chlorophyll a peaks occurred in May 2004, but were delayed to August 2003, likely due to a very rainy spring. Data suggest that river flow exerts a marked influence on the timing of phytoplankton biomass maxima in this estuary, decreased river flows providing a lowering of turbidity and an increase in water residence time needed for chlorophyll a to build up. Nutrient concentrations were high enough not to limit phytoplankton growth throughout the annual cycle, except silicate and occasionally phosphate in the outer bay during summer. Silicate concentration correlated positively with river flow, whereas ammonium and phosphate maximum values were generally measured in the mid-estuary, suggesting the importance of allochthonous anthropogenic sources. In the intermediate and inner estuary phytoplankton biomass was generally dominated by >8 μm size-fraction (ca. 60%), but in August 2003 −3 d −1 and were comparable to those measured in nearby small estuaries of the Basque coast and other larger estuaries on the Bay of Biscay. Surface plankton community respiration rate maxima were measured during the spring 2004 chlorophyll a peak in the Abra bay and in summer months at the mid and inner estuary, coinciding with chlorophyll a biomass and primary production maxima. In general, respiration rates showed a positive correlation with temperature. In order to compare results from the Nervion–Ibaizabal estuary with other nearshore coastal and estuarine ecosystems within the Bay of Biscay a review of existing information on phytoplankton biomass and primary production dynamics was performed.

The effect of the North Atlantic Oscillation (NAO) indices on climatic conditions and their subsequent influence on water temperature of two Basque estuaries (estuary of Bilbao and estuary of Urdaibai) were assessed by transfer function (TF) models for the period 1997–2006. Results showed that air temperature had an immediate (lag=0) and significant negative response to the NAO, whereas rainfall was not correlated with this climate index. The negative correlation between NAO and air temperature was found to be stronger with the seasonal indices derived from the differences in surface pressure between Iceland and Azores than with that derived from the principal component time-series of the leading eigenvector of the sea-level pressure in an Atlantic sector. The correlations between rainfall and river discharge, and between air temperature and water temperature were positive and highly significant in both estuaries. The response of water temperature to air temperature was immediate in both estuaries, whereas one-quarter lagged responses were also observed in the estuary of Bilbao, which is deeper and more stratified than the estuary of Urdaibai. Our study provides evidence that on the Basque coast the NAO plays an important role in climate variations, which in turn affect estuarine water temperature.

Seasonal variations in abundance of heterotrophic bacteria, small (1-8 µm) heterotro- phic nanoflagellates (HNF), and ciliates, as well as bacterial production (BP) and bacterivory (PB) rates were investigated from May 1998 to May 1999 in the lower Urdaibai estuary (Bay of Biscay). Abundances ranged from 2.6 × 10 8 to 1.3 × 10 9 cells l -1 , 0.65 × 10 6 to 3.00 × 10 6 cells l -1 , and 12 to 436 cells l -1 for bacteria, HNF and ciliates, respectively. BP varied between 0.9 and 18.5 × 10 8 cells l -1 d -1 . Bacteria seemed to be more limited by food supply than by temperature. The major bacterivores were small HNF, but they could not satisfy their carbon demand only through bacterivory. Bacterivory rate per small HNF varied between 2.7 and 28.2 bacteria flagellate -1 h -1 . This rate showed seasonal vari- ations and was higher during late winter/early spring than during summer/early autumn. This pat- tern is probably due to the greater dependence of small HNF on bacteria during late winter/early spring, when the availability of food sources other than bacteria, e.g. autotrophic picoplankton, was low. This led to seasonal variations in the degree of grazing control on the bacterial standing stock, this control being tighter during late winter/early spring. Bacterivory rate was substantially higher than BP in many months, i.e. bacteria showed a negative growth, and this was paralleled by reduc- tion in bacterial abundance. The relationship between log bacterial abundance and log small HNF abundance suggested that small HNF were largely under a substrate supply (bottom-up) control.

The relationships between chlorophyll a concentration and environmental (climatic and associated hydrographical) factors were investigated in the estuary of Urdaibai (Bay of Biscay) in different salinity zones of the euhaline region, using time-series for the period 1997–2006. Transfer function (TF) models were used on quarterly data (3 month mean values) to establish possible relationships between time-series. In the non-nutrient limited waters with salinities of 30 and 33 PSU, a chain of effects from the North Atlantic Oscillation (NAO) to chlorophyll a was established, where air temperature followed inversely the NAO index, water temperature followed air temperature and chlorophyll a followed water temperature. Each of the steps occurred with a lag of 0 (within the 3 month period); however, the effect from NAO to chlorophyll a showed a lag of 1 (a mean of 3 months delay). Consistent with this result, annual mean chlorophyll a biomass in the 30 and 33 PSU salinity zones showed a significant positive relationship with annual mean water temperature and a significant negative relationship with the 12 month mean NAO index from October of the previous year to September. In the 35 PSU salinity zone, no significant relationship between chlorophyll a and NAO or water temperature was observed. It is suggested that nutrient limitation distorts the effect of temperature on phytoplankton biomass enhancement in the outer estuary (35 PSU salinity zone).

Slope Water anticyclonic Oceanic eDDIES (SWODDIES) are typical mesoscale features of open-ocean waters of the southern Bay of Biscay which usually develop in winter by shedding from the seasonal poleward current flowing along the northern Spanish slope. These eddies have been intensively studied from the physical perspective. However, their effect on the distribution of biological properties and on the functioning of the pelagic ecosystem has not been assessed so far. To this aim, a sea-truth, multidisciplinary and comprehensive study of a SWODDY was carried out in summer 1998. The eddy, radius of ≈50 km, was initially centred at 45·5°N 6·0°W, being characterized by a relatively homogeneous core of water in the centre of the eddy extending from 80 to about 200 dbar. In the central region of the core, temperature (12·55–12·75°C) and salinity (≈35·70) values were higher than outside the eddy. The optical properties of the eddy also differed from those of the surrounding waters. A distinct biological signature was found associated with the eddy. Depth-integrated chlorophyll-a concentrations were 25% higher at the eddy centre where upward doming of the seasonal pycnocline (up to 30 dbar) occurred. Enhanced phytoplankton biomass was related to a higher contribution of >10 μm cells, mainly represented by diatoms and chrysophyceans. Phytoplankton and mesozooplankton species composition in and outside the eddy differed significantly reflecting the coastal origin of the water parcel trapped by the eddy. The sharp modification of the planktonic community composition, biomass and associated size-structure caused by slope water oceanic eddies are likely to exert a significant effect upon the upper trophic levels of the pelagic ecosystem of the southern Bay of Biscay.

Heterotrophic bacterial and phytoplankton biomass, production, specific growth rates and growth efficiencies were studied from June to October in 1996 and from February to May in 1997 along the longitudinal axis of the Urdaibai Estuary, a shallow temperate tidal estuary. Both phytoplankton and bacterial biomass showed a distinct lower to upper estuary increasing gradient. Longitudinal variations of phytoplankton biomass were controlled mainly by inorganic nutrient availability and tidal flushing. Longitudinal variations of bacterial biomass were further influenced by allochthonous inputs of organic carbon from a wastewater treatment plant located at the upper estuary. On a temporal scale, the dilution and washout effect of river discharge was a major controlling factor of both bacterial and phytoplankton biomass in the upper estuary. In this zone there were no indications that bacteria were resource limited, and temperature was the variable that explained most of the variability in bacterial specific growth rates. In the lower estuary, however, data suggested bacteria were nitrogen limited. Likewise, phytoplankton growth rates also showed a positive correlation with inorganic nutrients in this area. Free-living bacteria were generally more abundant than attached ones all along the estuary. However, following the longitudinal gradient of turbidity, the proportion of attached bacteria increased from the lower to the upper estuary. Rates of thymidine incorporation per cell were generally higher for particle-attached bacteria than for free-living bacteria. On average, bacteria contributed only 23% of the phytoplankton plus bacterial carbon biomass. Bacterial contribution to total (bacterial plus phytoplankton) net production of organic carbon was on average 17% for surface samples and 39% for bottom samples. Average phytoplankton growth efficiency in the euphotic zone was estimated to be higher (85%) than bacterial growth efficiency (46%).

Patterns of longitudinal and temporal variation in rates of primary production, respiration and nitrification were investigated in the Urdaibai estuary during August 1994. Rates of primary production, as measured with the 14C technique, varied between 0.002 and 2.828 mg C l−1 d−1. 14C and oxygen based rates of primary production showed a good correlation, but photosynthetic quotients (mean PQ of 2.2) were higher than expected from considerations of the N source used by the algae. Chlorophyll a biomass showed an inverse correlation with salinity and tidal flushing is hypothesized to be a major controlling factor of its spatial variability. Temporal variations in chlorophyll a concentration were associated primarily to changes in the lunar cycle and following rain events. Rates of community respiration varied between 0.154 and 6.857 mg O2 l−1 d−1 and were significantly and positively correlated with both bacterial abundance and chlorophyll a concentration. The relationship between respiration and primary production suggested that respiration rates based on substrates not associated with the autochthonous pelagic primary production increased greatly from the outer to the inner estuary and that the consumption of autotrophic production by heterotrophs in the water column was higher in the less productive outer estuary than in highly productive intermediate and inner areas. Except at the innermost station, temporal variations in respiration rates followed variations in temperature. The ratio of gross primary production to respiration ( GP R ) showed marked spatial and temporal variations, ranging from 0.24 to 17.94. Rates of nitrification, measured as allylthiourea sensitive rates of CO2 fixation, varied from undetectable levels to 9.3 μg C l−1 d−1.In general, highest rates of nitrification were observed at the inner estuary under conditions of elevated ammonia concentration, high bacterial abundance and high turbidity. Rates of nitrification were frequently associated with the > 3 μm size fraction. Oxygen consumed in nitrification was estimated to account on average for 4.7 ± 8.3% of total oxygen consumption.

The rates of water column nitrification measured as nitrapyrin-sensitive rates of bicarbonate assimilation were monitoredalong the salinity gradient of the estuary of the RiverNervion (Bay of Biscay) from January to November 1993.Highest nitrapyrin-sensitive rates of bicarbonate assimilationwere found in the deep layer at stations located in the innerestuary during summer and autumn, coinciding with dissolvedoxygen concentrations generally lower than 1 mg O2 l−1. Possible explanation for this spatial distributionpattern are discussed. Axial and depth distribution of ammonia,nitrite and nitrate suggests that in the deep layer of theinner zone of the estuary nitrification and nitrate and nitritereduction are occurring concurrently. Nitrification showed asignificant positive correlation with temperature, but thiscorrelation was not very strong. It is argued that the wash outof nitrifying bacteria by rainfalls also plays a role in theseasonal variation of nitrification rates.

Seasonal and inter-annual variations of dissolved oxygen (DO) along the estuary of Bilbao were investigated from 1998 to 2008, during its rehabilitation phase from pollution, to determine whether anthropogenic or natural forcings or both govern DO dynamics and hypoxia. Both seasonal and inter-annual variations of DO were best explained by hydro-climatic factors, sewage pollution and phytoplankton dynamics in the inner, intermediate and outer estuary respectively. The most remarkable intra-decadal improvement in DO occurred in the halocline layer of the intermediate estuary, where the factor that best explained these changes was sewage pollution abatement. However, in the estuarine hotspot for hypoxia, i.e. inner estuary bottom waters, no parallel response to sewage pollution abatement was observed and hydro-climatic factors were the main drivers of inter-annual DO variations. Differences in the degree of stratification and flushing accounted for this differential response of DO to anthropogenic and climate-related forcings at both axial and vertical scales.

The spatial and vertical distribution of phycoerythrin(PE)-containing chroococcoid cyanobacteria and the contribution of the

The effects of environmental factors on variations of dissolved oxygen (DO) saturation was assessed in 2 estuaries (Bilbao and Urdaibai) in the Bay of Biscay with contrasting hydrography and anthropogenic impact, for the period 1997 to 2006, using generalised additive models (GAMs) and generalised additive mixed models (GAMMs). Spatial and temporal variations in DO saturation and the current severity and extent of hypoxia were higher in the culturally eutrophicated and stratified Bilbao estuary. Seasonal patterns of DO saturation and the hierarchy of factors controlling them differed both between estuaries and between salinity zones. In the inner Bilbao estuary, the main factor explaining DO-saturation variations was temperature, with a dominant effect on oxygen consumption processes. In contrast, in the outer Bilbao estuary, the main factor explaining DO-saturation variations was chlorophyll a, suggesting that the effect of oxygen production through photosynthesis was stronger than that of oxygen consumption. In the inner Urdaibai estuary, both a negative relationship with temperature and a positive relationship with chlorophyll a were detected. The outer Urdaibai estuary showed strong water-column mixing and very high tidal flushing, and ventilation processes were more important than oxygen production or consumption processes. River discharge affected DO saturation only at the inner waters, but when the effects of several variables on DO-saturation variability were tested in an additive model, river discharge was excluded from the models. The effects of temperature-dependent processes on DO-saturation dynamics decreased from the inner to the outer zones of both estuaries., Sí

Respiration rates normalized to chlorophyll a of laboratory cultures of Brachiomonas sp., Gyrodinium aureolum, Synechococcus sp. (clone WH 7803), Pycnococcus provasolii (clone W48–23) and Phaeocystis sp. showed a positive relationship with growth photon flux density (Ig). It is argued that this constitutes an energy conserving strategy of adaptation to conditions of low irradiance. The ratio of respiration to light-saturated rate of photosynthesis (R/Pmax) also showed a decrease with decreasing I. Algal cell size, within the investigated range (0·2 to 1380 pg C cell-1), showed little influence on biomass-specific respiration rates.

In the Urdaibai estuary, despite its small volume in relation to the tidal prism, phytoplankton grows massively in the upper and intermediate zones of the estuary during summer when rainfall is low to moderate. Data obtained in 23 sampling transects along the longitudinal axis of the estuary, undertaken in July 1993 and August 1994, showed three distinct zones in terms of the phytoplankton species composition: in the upper zone the phytoplankton assemblage was dominated by the diatoms Cyclotella spp., the dinoflagellate Glenodinium foliaceum, cryptophytes and euglenophytes; in the intermediate zone the diatom Chaetoceros ceratosporus, the dinoflagellates Peridinium quinquecorne and Prorocentrum minimum and cryptophytes were the most abundant; in the lower zone diatoms such as Leptocylindricus danicus and Skeletonema costatum together with the dinoflagellates Prorocentrum spp. were dominant. The distribution and abundance of these phytoplankton forms is discussed in relation to variations in salinity, water column stratification, nutrients and temperature, which in turn vary mainly as a function of meteorological conditions (i.e. rainfall, irradiance) and tidal amplitude. The longitudinal distribution of phytoplankton cells suggests that the diatoms Cyclotella spp. and Chaetoceros ceratosporus undergo a greater dispersion along the estuary during rain events than the flagellates, thus contributing to the transport of silica to the outer areas of the estuary., L'Estuaire de Guernica dans le pays basque, est de faible volume en comparaison avec les caux déplacées par la marée; pourtant en été, lorsque les précipitations sont faibles à modérées, le phytoplancton s'y développe en abondance dans les secteurs amont et intermédiaire. La composition taxonomique des prélèvements effectués en juillet 1993 et août 1994, suivant l'axe longitudinal de l'estuaire, révèle trois secteurs. L'amont est dominé par la diatomée du genre Cyclotalla spp., le dinoflagellé Glenodinium foliaceum, les cryptophycées et les euglenophycées. Dans le secteur intermédiaire, la diatomée Chaetoceros ceratosporus est en abondance, avec les dinoglagellés Peridinium quinquecorne et prorocentrum minimum et les cryptophycées. En aval, les diatomées telles que Leptocylindrus danicus et Skeletonema costatum sont dominantes, associées au dinoflagelléProrocentrum spp. La répartition et l'abondance de ces espèces est discutée en relation avec la salinité, la stratification des eaux, les nutriments et la température, paramètres qui varient eux-mêmes avec les conditions météorologiques (précipitations, éclairement) et l'amplitude de la marée. La répartition longitudinale du phytoplancton suggère que, pendant les précipitations, les diatomées de Cyclotella spp. et Chaetoceros ceratosporus sont soumises à une plus grande dispersion que les dinoflagellés, contribuant ainsi au transfert de silice en dehors de l'estuaire.

Microplankton metabolism was studied in the Urdaibai estuary from June 1996 to May 1997 to investigate the factors that control the autotrophic-heterotrophic balance in three zones of contrasting trophic status. Gross primary production (GPP) and dark oxygen consumption (R) were measured from the upper eutrophic reaches to the lower marine segment for unfractionated samples as well as for nanoplankton ( 1 only during peak values of production, whilst in the middle estuary they were almost always ≥1. Ultraplankton was generally heterotrophic in the three zones. The relative importance of the

Short-term variability in microbial food web dynamics was investigated from 3 to 17 May 2001 at 2 contrasting sites in the Urdaibai estuary (Bay of Biscay). The lower site is located in an area where tidal advection exerts a major influence, whereas the upper site is located in area where the influence of the tide is much lower and that of river runoff is markedly higher than at the lower site. The biomass of microbial plankton (phytoplankton, bacteria, non-pigmented flagellates [NPF] and ciliates) and their rates of activities (primary production, bacterial production, herbivory, bacterivory and microbial community respiration) were markedly higher at the upper site, thus showing that tidal flushing is a key factor controlling these spatial differences along the longitudinal axis of the estuary, rendering the upper channel a high productivity zone and the lower euhaline area a less productive one. Water residence time also exerted an overriding effect on chlorophyll a distribution on a temporal basis, with drastic increases in river runoff, due to heavy rain pulses, being responsible for immediate bloom dispersion in the upper channel. Bacterial density was less affected than phytoplankton biomass by increased river flow. It is hypothesised that detrital material increases caused by increases in river runoff provided an extra source of carbon for bacterial growth. On average, microbial herbivory was responsible for the fate of ca. 50% of chlorophyll a standing stock. Herbivory rates were not significantly different on phytoplankton 0.2 µm and on those 8 µm in size and grazing pressure on phytoplankton was lower in the more productive site. Protists 1 to 8 µm in size were the main bacterivores. No synchrony was observed between bacterial and NPF abundances. Instead a lag phase was observed between the peak densities of bacteria and NPF, which was larger at the more productive upper site than in the lower estuary and allowed bacteria in the former zone to exploit substrate availability without significant grazing control for several days. Microbial community rate of respiration was significantly correlated with bacterivory rates and NPF abundance in the upper estuary, but not in the lower zone. The median of the proportion of bacterial production removed by bacterivory was 64% at the lower estuary station and 17% in the upper estuary. A possible explanation for this difference could be that attached bacteria (abundant in the upper reaches of the estuary) are less accessible for protistan grazing. Bacterivory by protists accounted for a mean of 14 and 7% of protistan herbivory at the lower and upper sites respectively.