Henrique Queiroga

Interactions between behaviour and physical forcing in the control of horizontal transport of decapod crustacean larvae

We summarize what is known of the biophysical interactions that control vertical migration and dispersal of decapod larvae, asking the following main questions: How common is vertical migration in decapod crustacean larvae? What is the vertical extent of the migrations? What are the behavioural mechanisms that control vertical migrations? How does vertical migration interact with the physics of the ocean to control the dispersal of larvae? These questions are analysed by first giving a synopsis of the physical processes that are believed to significantly affect horizontal transport, and then by describing migration patterns according to taxon, to ecological category based on the habitat of adults and larvae, and to stage within the larval series. Some kind of vertical migration has been found in larval stages of virtually all species that have been investigated, irrespective of taxonomic or ecological category. Most vertical migration schedules have a cyclic nature that is related to a major environmental cyclic factor. Tidal (ebb or flood) migration and daily (nocturnal and twilight) migration are the two types of cyclic migration that have been identified. In general, all species show some type of daily migration, with nocturnal migration being the most common, whereas tidal migrations have only been identified in species that use estuaries during part of their life cycle. Moreover, there are several examples indicating that the phasing and extent of migration both change throughout ontogeny. Reported ranges of vertical displacement vary between a few metres in estuaries and several tens of metres (sometimes more than 100 m) in shelf and oceanic waters. Vertical movements are controlled by behavioural responses to the main factors of the marine environment. The most important factors in this respect are light, pressure and gravity, but salinity, temperature, turbulence, current and other factors, also influence behaviour. Many of these factors change cyclically, and the larvae respond with cyclic behaviours. The type of response may be endogenous and regulated by an internal clock, as in the case of some tidally synchronised migrations, but in most cases it is a direct response to a change in an environmental variable, as in diel migration. The reaction of the larvae to exogenous cues depends both on the rate of change of the variable and on the absolute amount of change. A series of dispersal types, involving different spatial and temporal scales, have been identified in decapod larvae: retention of the larval series within estuaries; export from estuarine habitats, dispersal over the shelf, and reinvasion of estuaries by the last stage; hatching in shelf waters and immigration to estuaries by late larvae or postlarvae; complete development on the shelf; and hatching in shelf waters, long-range dispersal in the ocean, and return to the shelf by late stages. In all of these cases, vertical migration behaviour and changes of behaviour during the course of larval development have been related to particular physical processes, resulting in conceptual mechanisms that explain dispersal and recruitment. Most decapod larvae are capable of crossing the vertical temperature differences normally found across thermoclines in natural systems. This ability may have significant consequences for horizontal transport within shelf waters, because amplitude and phase differences of the tidal currents across the thermocline may be reflected in different trajectories of the migrating larvae.

Environmental gradients in a southern Europe estuarine system: Ria de Aveiro, Portugal implications for soft bottom macrofauna colonization

Four seasonal sampling surveys were carried out between December 1985 and September 1986 in Canal de Mira (Ria de Aveiro, Portugal). A total of 40 sampling stations, distributed over 13 transects, was used. Salinity, temperature, dissolved oxygen and pH of the water mass were measured. Sediment temperature, and salinity and pH of interstitial water were determined. Sediment variables also included granulometric composition and organic matter contents. Bottom macrofauna samples were collected at each station.Ordination (PCA and MDS) and classification of the sampling stations were performed, using the physicochemical and the biological data sets separately. Average linkage cluster analysis using the unweighted paired-group method, arithmetic averages, was used for both sets of data.With a salinity range from 35.1‰ to 0.0‰, Canal de Mira behaves like a tidally and seasonally poikilohaline estuary. Water temperature (8.5–24.7°C) decreased along the channel towards its inner part during the cold season; an inverse and more pronounced trend was observed during the hot season. Dissolved oxygen contents was generally high during the day (50% to 240% saturation). Oversaturation was observed throughout the growing season, with peaks in areas with large amounts of rooted vegetation. The pH values, largely correlated with dissolved oxygen, ranged from 6.8 to 8.9. Four types of sediment were present in Canal de Mira, medium and muddy sands being dominant.Two major gradients were identified: (i) a typical longitudinal estuarine gradient, associated with distance from the mouth, representing physicochemical variables such as tidal amplitude, salinity and temperature; this gradient was accompanied by an upstream increase in dominance; the community composition changes were mainly related to salinity; (ii) a lateral gradient, related to current velocity, depth and sediment composition; the subtidal community had a comparatively low species richness and abundance. Groups of stations could be recognized along the environmental gradients. Benthic community changes, however, appeared to be gradual rather than marked by abrupt transitions.

Vertical migration and selective tidal stream transport in the megalopa of the crab Carcinus maenas

Megalopae of Carcinus maenas (L.) were intensively sampled in the Canal de Mira (Ria de Aveiro, Portugal) during the years of 1990 and 1991, with the use of a pump and nets, respectively. Plankton sampling was carried out along 25 h cycles conducted at fixed stations, at pre-determined depths along the water column. In 1990, the average depth of distribution of megalopae throughout the water column was affected by tidal phase: the larvae were closer to the surface during flood than ebb. Stepwise linear regression showed that a shallower distribution of the larvae was also associated with higher salinity. Other hydrological variables did not account well for the vertical distribution of megalopae. Analysis of megalopal instantaneous transport velocity indicated that their horizontal velocity depended on phase-of-tide: during ebb megalopae were transported downstream at a lower velocity than the vertically integrated water column velocity; during flood, the vertically integrated velocity of the larvae and water column were similar. Thus, a shift of vertical position during the tidal cycle controlled the transport velocity of megalopae, which was due to vertical water velocity shear current differences. During the 1991 study, significantly higher densities of megalopae were collected during flood. Main effects of phase-of-day and depth of sampling on density were not significant. However, highest densities during flood were found at mid-water, in both day phases, whereas during ebb megalopae were evenly distributed throughout the water column during the day, with low densities, or showed increasing abundances towards the bottom during the night. These observations are consistent with the hypothesis that megalopae of C. maenas undergo active vertical migration synchronised with the tidal cycle, which can be classified as a selective tidal stream transport mechanism to travel up estuaries. A conceptual model for the reinvasion of estuaries by C. maenas megalopae is proposed. According to the model, vertical movements between the bottom and the water column are controlled by exogenous factors associated with the tidal cycle.

Model-derived dispersal pathways from multiple source populations explain variability of invertebrate larval supply.

Background Predicting the spatial and temporal patterns of marine larval dispersal and supply is a challenging task due to the small size of the larvae and the variability of oceanographic processes. Addressing this problem requires the use of novel approaches capable of capturing the inherent variability in the mechanisms involved. Methodology/Principal Findings In this study we test whether dispersal and connectivity patterns generated from a bio-physical model of larval dispersal of the crab Carcinus maenas, along the west coast of the Iberian Peninsula, can predict the highly variable daily pattern of wind-driven larval supply to an estuary observed during the peak reproductive season (March–June) in 2006 and 2007. Cross-correlations between observed and predicted supply were significant (p<0.05) and strong, ranging from 0.34 to 0.81 at time lags of −6 to +5 d. Importantly, the model correctly predicted observed cross-shelf distributions (Pearson r = 0.82, p<0.001, and r = 0.79, p<0.01, in 2006 and 2007) and indicated that all supply events were comprised of larvae that had been retained within the inner shelf; larvae transported to the outer shelf and beyond never recruited. Estimated average dispersal distances ranged from 57 to 198 km and were only marginally affected by mortality. Conclusions/Significance The high degree of predicted demographic connectivity over relatively large geographic scales is consistent with the lack of genetic structuring in C. maenas along the Iberian Peninsula. These findings indicate that the dynamic nature of larval dispersal can be captured by mechanistic biophysical models, which can be used to provide meaningful predictions of the patterns and causes of fine-scale variability in larval supply to marine populations.

Development and Application of Microsatellites in Carcinus maenas: Genetic Differentiation between Northern and Central Portuguese Populations

Carcinus maenas, the common shore crab of European coastal waters, has recently gained notoriety due to its globally invasive nature associated with drastic ecological and economic effects. The native ubiquity and worldwide importance of C. maenas has resulted in it becoming one of the best-studied estuarine crustacean species globally. Accordingly, there is significant interest in investigating the population genetic structure of this broadly distributed crab along European and invaded coastlines. Here, we developed polymerase chain reaction (PCR) primers for one dinucleotide and two trinucleotide microsatellite loci, resulting from an enrichment process based on Portuguese populations. Combining these three new markers with six existing markers, we examined levels of genetic diversity and population structure of C. maenas in two coastal regions from Northern and Central Portugal. Genotypes showed that locus polymorphism ranged from 10 to 42 alleles (N = 135) and observed heterozygosity per locus ranged from 0.745 to 0.987 with expected heterozygosity ranging from 0.711 to 0.960; values typical of marine decapods. The markers revealed weak, but significant structuring among populations (global FST = 0.004) across a 450 km (over-water distance) spatial scale. Combinations of these and existing markers will be useful for studying population genetic parameters at a range of spatial scales of C. maenas throughout its expanding species range.

Zooplankton abundance in a coastal station off the Ria de Aveiro inlet (north-western Portugal): relations with tidal and day/night cycles

Abstract Temporal and vertical variations of zooplankton at a station on the north-western Portuguese shelf, close to the Ria de Aveiro inlet, were studied during two periods of 25 h each in the summer of 1994. Zooplankton sampling was carried out every 2 h, using horizontal plankton tows (mesh size, 500 μm). Sampling was carried out in two depths, 4 and 12 m. The vertical profiles of salinity and temperature were obtained immediately before the plankton sampling. Higher zooplankton concentrations were usually observed during the night and at 4 m depth. Most taxa also occurred inside the Ria de Aveiro, indicating an exchange of planktonic forms between the Ria and the shelf. A classification analysis of the most abundant taxa suggests some groups, which differ according to taxonomic features and their origin. This was attributed to the high variability of the forcing agents that affect zooplankton abundance.

Flux of decapod larvae and juveniles at a station in the lower Canal de Mira (Ria de Aveiro, Portugal) during one lunar month

Summary Emigration and immigration of decapod larvae from estuaries depend on timing of larvae occurrence in the water column relative to the tidal, tidal amplitude and day cycles. The phase relation of these natural cycles varies with tidal regime and geographically, resulting in different time-patterns of hatching of first stage larvae and of presence of late stage larvae in the water column. Vertical migration behaviour according to phase of tide also controls transport inside estuaries. These mechanisms were investigated in a field study conducted on the northwest coast of Portugal where neap ebb tides occur during the night around the quarters of the moon. Flux of decapod larvae through one sampling station was measured during one lunar month at the Canal de Mira (Ria de Aveiro) in the spring of 1990. The sampling programme was comprised of a set of 25-h fixed station studies, separated by 25-h intervals during which no sampling took place. Plankton samples were collected with a pump every hour at three depths. Current velocity and direction at the standard depths, as well as height of the water column, were also measured every hour. Hourly instantaneous flux of larvae through a 1-m-wide vertical section of the Canal de Mira was calculated for the most abundant forms. A total number of 13 combinations of species and larval stages were analyzed, belonging to the families Atelecyclidae, Pirimelidae, Portunidae, Pilumnidae, Grapsidae, Palaemonidae, Crangonidae and Thalassinidae. Patterns of net larval flux along the lunar month could be grouped into three types. Type 1 includes first zoeas that were consistently exported to the sea. Type 2 comprises late zoeas, megalops and juveniles that were consistently imported into the estuary. First zoeas that were imported during some of the 25-h studies but were exported during the others were included in Type 3; in species of this type import periods appeared to alternate with export periods according to lunar phase. Flux of Type 1 larvae followed a semi-lunar pattern. Release activity of Type 1 zoeas took place during the night and started during neap tides around the quarters of the moon, but maximum releases occurred 3–4 h after high tide of average amplitude tides, 3–4 days after the quadratures. These observations agree with the hypothesis that hatching is timed to occur on ebb tides of the largest possible amplitude so that larvae are easily dispersed from areas with a high density of predator fishes. However, based on other observations on the Portuguese coast, it cannot be ruled out that hatching might depend on a minimum number of hours of darkness experienced by the females. Larvae included in Type 2 comprise forms that may have been retained inside the estuary for the entire larval phase, as well as one form that was imported from shelf waters. No semi-lunar pattern of import was detected in this last form. Fluctuations of net flux observed in Type 3 larvae, as well in other forms that were not included in any of the types, were more difficult to explain. These larvae were first zoeas of species belonging to different taxonomic, morphological and ecological groups and may show a diversity of adaptations to the way of life of the adults. Imports and exports of larvae depended not only on time-patterns of abundance, but also on time-patterns of larval vertical distribution. As a general rule, larval stages showed patterns of depth distribution that were consistent with vertical migration rhythmic behaviours synchronized with the tidal cycle. Though the effect was not always statistically significant, first-stage larvae were closer to the surface during ebb, especially during the night, enhancing seaward transport. On the contrary, later zoeal stages, megalops and juveniles were usually closer to the surface during flood, suggesting migration to the water column during this phase of the tide and landward transport.

Corophium multisetosum (Amphipoda: Corophiidae) in Canal de Mira, Portugal: Some factors that affect its distribution

The population ofCorophium multisetosum (L.) from Canal de Mira, Ria de Aveiro, Portugal, was sampled seasonally from December 1985 to September 1986, as part of a larger survey of the benthic invertebrate macrofauna. Its distribution along the channel exposes the species to a range of salinities from freshwater to above 30‰. A principal components analysis, using the physical and chemical parameters of the sediment as variables and sampling stations as operational taxonomic units, indicated that abundance is negatively correlated with salinity, depth, and the occurrence of sediments rich in particles below 125µm and rich in organic matter. Abundance is positively correlated with temperature. The distribution of the species does not seem to be affected by the occurrence of sediment grades between 125 and 1 000µm. Paired-choice salinity experiments indicated thatC. multisetosum prefers salinities within the range 2.5 to 10‰. In multi-choice experiments concerning sediment grade, amphipods did not show any significant preference within the 125 to 500µm range, although the 125µm grade was chosen less frequently. The influence of temperature on the overall distribution ofC. multisetosum is discussed.

Feeding ability of early zoeal stages of the Norway lobster Nephrops norvegicus (L.).

The wide geographical distribution of the Norway lobster, Nephrops norvegicus, results in a delay, with latitudinal decrease, in the larval season from spring to winter. Newly hatched larvae of the species may therefore be exposed to suboptimal levels or types of prey and face intermittent periods of starvation at low latitudes. This work investigated the feeding response of the first two zoeal stages of N. norvegicus under variable prey densities, prey types, feeding histories, and photoperiods. Both zoeae (Z) I and II increased the number of consumed prey with increasing food levels. ZI preferred Artemia sp. nauplii over larger metanauplii, while in ZII, higher ingestion was observed only for metanauplii at higher food concentrations. The number of prey ingested by larvae previously starved or under low food conditions was always higher than that of larvae exposed to high food levels. These findings seem to indicate that larvae may maximize prey ingestion in the presence of plankton patches with higher food abundance and minimize the deleterious effects induced by previous periods of intermittent starvation or unsuitable prey densities or types. Extreme photoperiods (24 and 0 h of light) did not improve larval feeding ability and are not a suitable option for larviculture.

Towards Operational Modeling and Forecasting of the Iberian Shelves Ecosystem

There is a growing interest on physical and biogeochemical oceanic hindcasts and forecasts from a wide range of users and businesses. In this contribution we present an operational biogeochemical forecast system for the Portuguese and Galician oceanographic regions, where atmospheric, hydrodynamic and biogeochemical variables are integrated. The ocean model ROMS, with a horizontal resolution of 3 km, is forced by the atmospheric model WRF and includes a Nutrients-Phytoplankton-Zooplankton-Detritus biogeochemical module (NPZD). In addition to oceanographic variables, the system predicts the concentration of nitrate, phytoplankton, zooplankton and detritus (mmol N m−3). Model results are compared against radar currents and remote sensed SST and chlorophyll. Quantitative skill assessment during a summer upwelling period shows that our modelling system adequately represents the surface circulation over the shelf including the observed spatial variability and trends of temperature and chlorophyll concentration. Additionally, the skill assessment also shows some deficiencies like the overestimation of upwelling circulation and consequently, of the duration and intensity of the phytoplankton blooms. These and other departures from the observations are discussed, their origins identified and future improvements suggested. The forecast system is the first of its kind in the region and provides free online distribution of model input and output, as well as comparisons of model results with satellite imagery for qualitative operational assessment of model skill.