Modelling potential spawning habitat of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus) in the Bay of Biscay

Large amplitude variations in recruitment of small pelagic fish result from interactions between a fluctuating environment and population dynamics processes such as spawning. The spatial extent and location of spawning, which is critical to the fate of eggs and larvae, can vary strongly from year to year, as a result of changing population structure and environmental conditions. Spawning habitat can be divided into ‘potential spawning habitat’, defined as habitat where the hydrographic conditions are suitable for spawning, ‘realized spawning habitat’, defined as habitat where spawning actually occurs, and ‘successful spawning habitat’, defined as habitat from where successful recruitment has resulted. Using biological data collected during the period 2000–2004, as well as hydrographic data, we investigate the role of environmental parameters in controlling the potential spawning habitat of anchovy and sardine in the Bay of Biscay. Anchovy potential spawning habitat appears to be primarily related to bottom temperature followed by surface temperature and mixed‐layer depth, whilst surface and bottom salinity appear to play a lesser role. The possible influence of hydrographic factors on the spawning habitat of sardine seems less clear than for anchovy. Modelled relationships between anchovy and sardine spawning are used to predict potential spawning habitat from hydrodynamical simulations. The results show that the seasonal patterns in spawning are well reproduced by the model, indicating that hydrographic changes may explain a large fraction of spawning spatial dynamics. Such models may prove useful in the context of forecasting potential impacts of future environmental changes on sardine and anchovy reproductive strategy in the north‐east Atlantic.     

Relationships between anchovy (Engraulis encrasicolus) recruitment and environment in the Bay of Biscay (1967–1996)

Various hypotheses have been put forward to explain the mechanisms leading to recruitment variability in fish populations. These have been based on either physical (wind stress, upwelling) or biological (food and predation) processes. In the Bay of Biscay, the hypothesis of a physical influence on anchovy recruitment has been confirmed. Oceanographic conditions in the Bay of Biscay in the spring and summer, influenced by north-easterly winds of medium and low intensity, seem to induce good levels of recruitment to the anchovy ( Engraulis encrasicolus ) population. An index of upwelling was significantly correlated with annual recruitment of anchovy ( P  < 0.0001) for the period 1967–1996. This physical parameter explains about 59% of the variability in the recruitment of the Bay of Biscay anchovy. Two factors affecting productivity in the Bay of Biscay may be linked to north-easterly winds, namely weak upwelling and an extension of the area influenced by river outflows. Both of these factors, together with low turbulence and stability, may act to enhance survival of the early life-history stages of anchovy by increasing food availability. The potential use of this upwelling index to forecast the recruitment of the Bay of Biscay anchovy offers possibilities for improving the management of this population.     

Size,permeability and buoyancy of anchovy (Engraulis Encrasicolus) and sardine (Sardina Pilchardus) eggs in relation to their physical environment in the Bay of Biscay

The size and specific gravity of eggs of marine pelagic fish partly determine their dispersal and survival. Using an original dataset of anchovy and sardine eggs, sampled in spring over the last decade in the Bay of Biscay, we provide a parameterization of these properties on ambient water temperature and salinity. We used the density gradient column for measurement of egg specific gravity. The column was also filled with homogeneous water for sinking velocity experiments. For anchovy, these experiments confirm that the effect of egg permeability through the chorion could be neglected when modelling sinking, while it has to be considered for sardine, its perivitelline space representing 78.6% (±6.2%) of the total egg volume, as opposed to 5–10% for most teleosts species. We estimated a coefficient of permeability of the chorion of 0.0038 mm s^?1. However, permeability should not affect the measurement of sardine egg specific gravity in a gradient column, provided a minimum duration before reading is respected for equilibrium to be reached. In relation to their environment, we found that the egg specific gravity is largely determined by sea surface salinity for both species, whereas egg size is weakly but significantly impacted by temperature, for sardine only. On average, the estimated difference in specific gravity between egg and surface water is ?0.92 σ_T for anchovy and ?1.06 σ_T for sardine. The detailed parameterization of the relationship between eggs and water properties should prove useful, in particular to modellers dealing with the dispersal of fish early life stages.     

Climate,oceanography, and recruitment: the case of the Bay of Biscay anchovy (Engraulis encrasicolus)

The Bay of Biscay anchovy has experienced, since 2001, a succession of low recruitments, resulting in the collapse of the stock in 2005; this has led to successive closures of the fishery. This study investigates the possible impact of different controlling factors [North Atlantic Oscillation (NAO), East Atlantic (EA) pattern, turbulence, upwelling, and river flow] upon anchovy recruitment and fishery catches. Fifty‐five percent of the recruitment variability of this fishery can be explained by upwelling over the spawning area; this is related, in turn, to the EA pattern. The conceptual understanding of the system proposed for the Bay of Biscay anchovy suggests that negative EA periods are associated with northeasterly wind circulation, which produces weak upwelling over the continental shelf. This pattern results in hydrodynamic stability over the area, leading, probably, to adequate food availability. A positive EA (which extends onwards, from 1998) is associated with southwesterly winds and downwelling over the continental shelf; this leads, probably, to the dispersion of anchovy food and larvae, together with increasing mortality.     

Growth and movement patterns of early juvenile European anchovy (Engraulis encrasicolus L.) in the Bay of Biscay based on otolith microstructure and chemistry

Various hypotheses have been put forward to explain the mechanisms in the Bay of Biscay that result in a good recruitment of European anchovy. Anchovy larvae from the spawning area in the Gironde River plume are advected towards off-shelf waters, where juveniles are commonly observed. Otolith microstructural and chemical analysis were combined to assess the importance of this off-shelf transport and to determine the relative contribution of these areas for anchovy survival. Chemical analysis of otoliths showed that anchovy juveniles in the Bay of Biscay can be divided into two groups: a group that drifts towards off-shelf waters early in their life and returns later, and a group that remains in the low salinity waters of the coastal area. The first group presents significantly faster growth rates (0.88 mm day⁻¹) than those remaining in the coastal waters (0.32 mm day⁻¹). This may be due to off-shelf waters being warmer in spring/summer, and to the fact that the lower food concentration is compensated for by higher prey visibility. Furthermore, the group of juveniles that drifted off the spawning area and had faster growth rates represents 99% of the juvenile population. These findings support the hypothesis that anchovy in the Bay of Biscay may use off-shelf waters as a spatio-temporal loophole, suggesting that transport off the shelf may be favourable for recruitment.     

The influence of environment and spawning distribution on the survival of anchovy (Engraulis encrasicolus) larvae in the Bay of Biscay (NE Atlantic) investigated by biophysical simulations

A growth and survival model of the early life stages was run along virtual drift trajectories tracked in a hydrodynamic model to simulate the annual recruitment process of anchovy (Engraulis encrasicolus) in the Bay of Biscay (NE Atlantic). These biophysical simulations concerning three different years were analysed in order to investigate the influence of environment and spawning dynamics on the survival of larvae and juveniles. The location of space–time survival windows suggested major environmental mechanisms involved in simulated recruitment variability at the different scales – retention of larvae and juveniles in favourable habitats over the shelf margins and turbulence effects. These small‐scale and meso‐scale mechanisms were related to the variations in wind direction and intensity during spring and summer. Survival was also variable according to the origin of the drift trajectories, that is spawning distribution in space and time. The observed spawning distribution (according to field surveys) was compared with the spawning distribution that would maximize survival (according to the biophysical model) on a seasonal scale, which revealed factors not considered in the biophysical model (e.g. spawning behaviour of the different age classes). The variation of simulated survival according to spawning distribution was examined on a multi‐annual scale and showed a coherent pattern with past and present stock structures. The interaction processes between the population (influence on spawning) and its environment (influence on survival) and its implications on recruitment and stock dynamics are discussed.     

Biophysical modelling of larval drift, growth and survival for the prediction of anchovy (Engraulis encrasicolus) recruitment in the Bay of Biscay (NE Atlantic)

Fish recruitment is the result of the integration of small‐scale processes affecting larval survival over a season and large oceanic areas. A hydrodynamic model was used to explore and model these physical–biological interaction mechanisms and then to perform the integration from individual to population scales in order to provide recruitment predictions for fisheries management. This method was applied to the case of anchovy (Engraulis encrasicolus) in the Bay of Biscay (NE Atlantic). The main data available to investigate survival mechanisms were past growth (otolith) records of larvae and juveniles sampled at sea. The drift history of these individuals was reconstructed by a backtracking procedure using hydrodynamic simulations. The relationships between (real) growth variation and variations in physical parameters (estimated by hydrodynamic simulations) were explored along the individual trajectories obtained. These relationships were then used to build and adjust individual‐based growth and survival models. Thousands of virtual buoys were released in the hydrodynamic model in order to reproduce the space–time spawning dynamics. Along the buoy trajectories (representative of sub‐cohorts), the biophysical model was run to simulate growth and survival as a function of the environment encountered. The survival rate after 3 months of drift was estimated for each sub‐cohort. The sum of all these survival rates over the season constituted an annual recruitment index. This index was validated over a series of recruitment estimations. The modelling choices, model results and the potential use of the recruitment index for fisheries management are discussed.     

Remotely sensed spawning habitat of Pacific sardine (Sardinops sagax) and Northern anchovy (Engraulis mordax) within the California Current

We use trivariate kernel density estimation to define spawning habitat of northern anchovy ( Engraulis mordax ) and Pacific sardine ( Sardinops sagax ) in the California Current using satellite data and in situ egg samples from the Continuous Underway Fish Egg Sampler (CUFES) deployed during surveys in April by the California Cooperative Oceanic Fisheries Investigations (CalCOFI). Observed egg distributions were compared with monthly composite satellite sea surface temperature (SST) and surface chlorophyll a (chl a ) data. Based on the preferred spawning habitat, as defined in SST and chl a space, the satellite data were used to predict potential spawning habitat along two areas of the west coast of North America. Data from the southern area (21.5 to 39°N) were compared to observations from the CUFES data for the period 1998–2005. Northern anchovy and Pacific sardine exhibited distinctly different spawning habitat distributions. A significant relationship was found between satellite-based spawning area and that measured during surveys for sardine. CUFES area estimated for sardine was similar in magnitude to that estimated from satellite data (∼60 000 km²). In contrast, spawning habitat of anchovy averaged between 1000 and 200 000 km² for the period 1998–2005, for CUFES and satellite estimates, respectively. Interannual variability in the area (km²) and duration (months) of estimates of suitable habitat varied between species and between the northern (39 to 50.5°N) and southern portions of the California Current. Long-term monitoring of habitat variability using remote sensing data is possible in the southern portion of the California Current, and could be improved upon in the northern area with the addition of surveys better timed to describe relationships between observed and estimated spawning habitats.     

Fine scale spatial pattern of Pacific sardine (Sardinops sagax) and northern anchovy (Engraulis mordax) eggs

Pacific sardine (Sardinops sagax) and northern anchovy (Engraulis mordax) eggs exhibited different spatial structure on the scale of 0.75–2.5 km in two egg patches sampled in the Southern California Bight in April 2000. Plankton samples were collected at 4‐min intervals with a Continuous Underway Fish Egg Sampler (CUFES) on 5 × 5 km grids centered on surface drifters. Variograms were calculated for sardine and anchovy eggs in Lagrangian coordinates, using abundances of individual developmental stages grouped into daily cohorts. Model variograms for sardine eggs have a low nugget effect, about 10% of the total variance, indicating high autocorrelation between adjacent samples. In contrast, model variograms for anchovy eggs have a high nugget effect of 50–100%, indicating that most of the variance at the scales sampled is spatially unstructured. The difference between observed spatial patterns of sardine and anchovy eggs on this scale may reflect the behavior of the spawning adults: larger, faster, more abundant fish may organize into larger schools with greater structure and mobility that create smoother egg distributions. Size and mobility vary with population size in clupeoids. The current high abundance of sardines and low abundance of anchovy off California agree with the greater autocorrelation of sardine egg samples and the observed tendency for locations of anchovy spawning to be more persistent on the temporal scale of days to weeks. Thus the spatial pattern of eggs and the persistence of spawning areas are suggested to depend on species, population size and age structure, spawning intensity and characteristic physical scales of the spawning habitat.     

Spawning site selection by European anchovy (Engraulis encrasicolus) in relation to oceanographic conditions in the Strait of Sicily

European anchovy egg occurrence and density data from summer surveys (1998–2007) and oceanographic data were examined to study the mechanisms that control the spatial distribution of anchovy spawning habitat in the Strait of Sicily. Quotient analysis indicated habitat preference for temperature (18–19°C), bottom depth (50–100 m), water column stability (13–14 cycle h^?1), fluorescence (0.10–0.15 μg m^?3 Chl a), salinity (37.5–37.6 PSU), current speed (0.20–0.25 m s^?1) and density (26.7–26.8 kg m^?3, σ_t). Canonical discriminant analysis identified temperature, column stability and fluorescence as major drivers of anchovy spawning habitat. Three of the 4 years which had lower egg abundance were warmer years, with low values of primary productivity. A geostrophic current flowing through the Strait (the Atlantic Ionic Stream, AIS) was confirmed as the main source of environmental variability in structuring the anchovy spawning ground by its influence on both the oceanography and distribution of anchovy eggs. This 10‐yr data series demonstrates recurrent but also variable patterns of oceanographic flows and egg distribution. A lack of freshwater flow in this area appears to depress productivity in the region, but certain and variable combinations of environmental conditions can elevate production in some sub‐areas in most years or other sub‐areas in fewer years. These temporal and spatial patterns are consistent with an ocean triad theory postulating that processes of oceanographic enrichment, concentration, and retention may help predict fishery yields.     

From egg to juvenile in the Bay of Biscay: spatial patterns of anchovy (Engraulis encrasicolus) recruitment in a non‐upwelling region

In this study the spatial distribution of eggs, larvae and juveniles of European anchovy (Engraulis encrasicolus) was followed in 2004 and 2005 during three consecutive cruises each year in spring–summer to test what the limits of retention are in a non‐upwelling area. Eggs, small larvae and large juveniles were mainly distributed over the shelf, whereas large larvae and small juveniles were found mainly off the shelf. Although overall distributions were similar, the 2 yr differed in that there was more of a coastal distribution of individuals in 2004, whereas in 2005 more individuals were found off the shelf. There were no significant differences in the length–weight relationships for individuals found on and off the shelf or between years. The correspondence in circulation patterns and the lack of difference in the length–weight relationships suggest that a single population is present, larvae drifting off the shelf due to currents and returning as mobile juveniles. Quantile regression analysis of the long‐term recruitment index suggests that transport off the shelf may favour good recruitments. This would suggest that in non‐upwelling regions the retention area resulting in good recruitment may not be restricted to the shelf.     

The influence of mesoscale ocean processes on anchovy (Engraulis encrasicolus) recruitment in the Bay of Biscay estimated with a three-dimensional hydrodynamic mode

The relationship between anchovy ( Engraulis encrasicolus ) recruitment in the Bay of Biscay and environmental variables during their planktonic phase (March to July) was investigated from 1986 to 1997. Meteorological variables (wind and temperature) are forcing effects on the sea, but they are not thought to be processes that govern larval survival directly. Food-web dynamics are believed to be more closely linked to larval survival and are related to the physical vertical water column structure. Therefore, we used a three-dimensional (3D) hydrodynamic model to characterize three major physical mesoscale processes affecting vertical structure in south-east Biscay: stratification, upwelling and river plume extent. Indices were estimated from the model outputs to characterize and quantify the space/time evolution of these structures during the period March to July. A multiple linear regression analysis was then used to analyse hierarchy in the explanatory power of the physical indices. Coastal upwelling and shelf stratification breakdown indices were the most significant explanatory variables, with positive and negative effect on recruitment, respectively. A model with these two indices explains 75% of the recruitment variability of anchovy observed in the period 1987–96.     

Transport and environmental temperature variability of eggs and larvae of the Japanese anchovy (Engraulis japonicus) and Japanese sardine (Sardinops melanostictus) in the western North Pacific estimated via numerical particle-tracking experiments

Numerical particle-tracking experiments were performed to investigate the transport and variability in environmental temperature experienced by eggs and larvae of Pacific stocks of the Japanese anchovy ( Engraulis japonicus ) and Japanese sardine ( Sardinops melanostictus ) using high-resolution outputs of the Ocean General Circulation Model for the Earth Simulator (OFES) and the observed distributions of eggs collected from 1978 to 2004. The modeled anchovy individuals tend to be trapped in coastal waters or transported to the Kuroshio–Oyashio transition region. In contrast, a large proportion of the sardines are transported to the Kuroshio Extension. The egg density-weighted mean environmental temperature until day 30 of the experiment was 20–24°C for the anchovy and 17–20°C for the sardine, which can be explained by spawning areas and seasons, and interannual oceanic variability. Regression analyses revealed that the contribution of environmental temperature to the logarithm of recruitment per spawning (expected to have a negative relationship with the mean mortality coefficient) was significant for both the anchovy and sardine, especially until day 30, which can be regarded as the initial stages of their life cycles. The relationship was quadratic for the anchovy, with an optimal temperature of 21–22°C, and linear for the sardine, with a negative coefficient. Differences in habitat areas and temperature responses between the sardine and anchovy are suggested to be important factors in controlling the dramatic out-of-phase fluctuations of these species.     

Predicting the vertical profiles of anchovy (Engraulis mordax) and sardine (Sardinops sagax) eggs in the California Current System

Several published models exist for simulating vertical profiles of pelagic fish eggs, but no one has rigorously assessed their capacity to explain observed variability. In this study, we applied a steady‐state model, with four different formulations for vertical diffusivity, to northern anchovy (Engraulis mordax) and Pacific sardine (Sardinops sagax) eggs in the California Current region. Vertical mixing profiles, based on wind speed and hydrography, were combined with estimated terminal ascent velocities of the eggs based on measurements of egg buoyancy and size, to simulate the vertical profiles of the eggs. We evaluated model performance with two data sets: (1) vertically stratified tows for both species and (2) paired samples for sardine eggs from 3‐m depth and in vertically integrated tows. We used two criteria: whether the model predicted individual observed vertical profiles (1) as well as the observed mean and (2) better than the observed mean. Model predictions made with the formulation producing the most gradual profile of vertical diffusivity provided the best match to observations from both data sets and for both species. Addition of a random error term to the terminal ascent velocity further improved prediction for anchovy eggs, but not sardine. For the paired data, model prediction of integrated abundance from abundance at 3‐m depth had significantly lower mean square error than prediction based on a linear regression of 3 m on integrated abundance. Our results support the feasibility of using data from the Continuous Underway Fish Egg Sampler quantitatively as well as qualitatively in stock assessments.     

Spawning habitat and daily egg production of sardine (Sardina pilchardus) in the eastern Mediterranean

Spawning habitats of two eastern Mediterranean sardine, Sardina pilchardus (Walbaum, 1792), stocks (coastal waters of central Aegean and Ionian Seas) are characterized from daily egg production method (DEPM) surveys conducted during the peak of the spawning period. The latter occurs earlier in the Aegean Sea (December) than in the less‐productive Ionian Sea (February). Single‐parameter quotient analysis showed that the preferred bottom depth for spawning was 40–90 m in both areas but sardine selected sites of increased zooplankton in the Aegean Sea during December and increased fluorescence in the Ionian Sea during February. Estimates of daily egg production (P) and spawning stock biomass (B) were about four times lower for the Ionian Sea (P = 7.81 eggs m^?2, B = 3652 tonnes) than the Aegean Sea (P = 27.52 eggs m^?2, B = 16 174 tonnes). We suggest that zooplankton biomass might not be sufficient to support sardine reproduction in the highly oligotrophic Ionian Sea where the very small sardine stock may rely on the late‐winter phytoplankton bloom. Actively selecting sites with increased zooplankton or phytoplankton and feeding plasticity (the well‐known switching from selective particle feeding to non‐selective filter feeding in sardines) are interpreted as adaptations to grow and reproduce optimally at varying prey conditions. Despite differences in temperature and productivity regimes, reproductive performance of sardine in the Ionian Sea was very similar to that in the Aegean Sea during the peak of the spawning period. In comparing adult parameters from DEPM applications to Sardina and Sardinops stocks around the world, a highly significant linear relation emerged between mean batch fecundity (F) and mean weight of mature female (W, g) (F = 0.364W, r² = 0.98). The latter implies that, during the peak of the spawning period, mean relative batch fecundity (eggs g^?1) of sardine is fairly constant in contrasting ecosystems around the world.     

Importance of the Shatsky Rise Area in the Kuroshio Extension as an offshore nursery ground for Japanese anchovy (Engraulis japonicus) and sardine (Sardinops melanostictus)

Recent findings suggest that recruitment of Japanese anchovy (Engraulis japonicus) and sardine (Sardinops melanostictus) depends on survival during not only the first feeding larval stage in the Japanese coastal waters and the Kuroshio front but also during the post‐larval and juvenile stages in the Kuroshio Extension. Spatial distributions of juvenile anchovy and sardine around the Shatsky Rise area in the Kuroshio Extension region and the Kuroshio–Oyashio transition region are described, based on a field survey in the late spring using a newly developed mid‐water trawl for sampling juveniles. All stages of anchovy from post‐larvae to juveniles were obtained in the northern Shatsky Rise area. The Kuroshio Extension bifurcates west of the Shatsky Rise area and eddies are generated, leading to higher chlorophyll concentrations than in the surrounding regions in April and May. When Japanese anchovy and sardine spawn near the Kuroshio front or the coastal waters south‐east of Japan, their larvae are transported by the Kuroshio Extension and are retained in the Shatsky Rise area, which forms an important offshore nursery ground, especially during periods of high stock abundance.     

Anchovy (Engraulis ringens) and sardine (Sardinops sagax) spatial dynamics and aggregation patterns in the Humboldt Current ecosystem, Peru, from 1983–2003

Three indexes of spatial aggregation are developed and used to examine the aggregation pattern of sardine (Sardinops sagax) and anchovy (Engraulis ringens) in the Peruvian Humboldt Current System, determined from 36 acoustic surveys conducted from 1983 through 2003 by the Peruvian Marine Institute (IMARPE). Each index assesses a different aspect of aggregation: the concentration, the percent occupancy of space and the clustering of high‐fish abundance. Both time‐series correlation and tree‐based clustering‐regression method, classification and regression trees (CART), were used to relate each of the indexes to environmental variables (season, temperature anomaly and year). Additionally, a measure of onshore–offshore distribution, the average distance from the coast, and abundance variables (the average acoustic backscatter per occupied sampling unit, and the acoustically estimated total abundance of sardine and anchovy from IMARPE) were related to environmental factors by using CART. We show that the 1983–2003 time series can be divided into three different periods: with shifts in 1992 and in 1997–98. Sardine and anchovy showed large differences in both abundance and aggregation among these periods. Although upwelling ecosystems support dramatic and sudden changes in environmental conditions, fish responses are sometimes smoother than usually suggested and there are transition periods with concomitant high biomasses of anchovy and sardine, but with different spatial aggregation patterns. Observed relationships between environmental proxies and aggregation patterns support the habitat‐based hypothesis that environmentally mediated alterations in range lead to population changes.     

Impact of freshwater input and wind on landings of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) in shelf waters surrounding the Ebre (Ebro) River delta (north-western Mediterranean)

Time series analyses (Box–Jenkins models) were used to study the influence of river runoff and wind mixing index on the productivity of the two most abundant species of small pelagic fish exploited in waters surrounding the Ebre (Ebro) River continental shelf (north‐western Mediterranean): anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus). River flow and wind were selected because they are known to enhance fertilization and local planktonic production, thus being crucial for the survival of fish larvae. Time series of the two environmental variables and landings of the two species were analysed to extract the trend and seasonality. All series displayed important seasonal and interannual fluctuations. In the long term, landings of anchovy declined while those of sardine increased. At the seasonal scale, landings of anchovy peaked during spring/summer while those of sardine peaked during spring and autumn. Seasonality in landings of anchovy was stronger than in sardine. Concerning the environmental series, monthly average Ebre runoff showed a progressive decline from 1960 until the late 1980s, and the wind mixing index was highest during 1994–96. Within the annual cycle, the minimum river flow occurs from July to October and the wind mixing peaks in winter (December–April, excluding January). The results of the analyses showed a significant correlation between monthly landings of anchovy and freshwater input of the Ebre River during the spawning season of this species (April–August), with a time lag of 12 months. In contrast, monthly landings of sardine were significantly positively correlated with the wind mixing index during the spawning season of this species (November–March), with a lag of 18 months. The results provide evidence of the influence of riverine inputs and wind mixing on the productivity of small pelagic fish in the north‐western Mediterranean. The time lags obtained in the relationships stress the importance of river runoff and wind mixing for the early stages of anchovy and sardine, respectively, and their impact on recruitment.