Revista de Biología Marina y

Oceanografía
ISSN: 0717-3326
[email protected]
Universidad de Valparaíso
Chile

Abdelouahab, Hinde; Berraho, Amina; Ramzi, Azeddine; Ettahiri, Omar; Errhif, Ahmed;
Tojo, Naoki
Mortality of early life stages of European pilchard Sardina pilchardus along the Atlantic
Coast of Northwest Africa (22°30’N-26°N)
Revista de Biología Marina y Oceanografía, vol. 51, núm. 3, diciembre, 2016, pp. 483-492
Universidad de Valparaíso
Viña del Mar, Chile

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 Revista de Biología Marina y Oceanografía
Vol. 51, Nº3: 483-492, diciembre 2016
DOI 10.4067/S0718-19572016000300001

ARTICLE
Mortality of early life stages of European pilchard
Sardina pilchardus along the Atlantic Coast of
Northwest Africa (22°30’N-26°N)
Mortalidad en los primeros estadios de desarrollo de la sardina europea
Sardina pilchardus a lo largo de la Costa Atlántica del
Noroeste de África (22°30’N-26°N)

Hinde Abdelouahab1*, Amina Berraho2, Azeddine Ramzi2,

Omar Ettahiri2, Ahmed Errhif1** and Naoki Tojo3
1
University Hassan II, Faculty of Sciences Ain Chock, B.P 5366 Maarif 20000, Casablanca, Morocco. *Corresponding author:
[email protected]; **[email protected]
2
National Institute of Marine Research, 2 Sidi Abderrahmane, Casablanca, Morocco. [email protected],
[email protected], [email protected]
3
Japan International Cooperation Agency (JICA), Expert of Resource Dynamics Analyses and Monitoring, National Institute of
Marine Research, Casablanca, Morocco. [email protected]

Resumen.- El objetivo de este estudio fue estimar la mortalidad natural en los estados embrionarios y larvales de la sardina
europea Sardina pilchardus a largo de la Costa Atlántica del Noroeste de África entre el Cabo Barbas (22°30’N) y el Cabo Bojador
(26°N) durante noviembre de 2007. Se utilizaron datos planctónicos seleccionados de un estudio realizado en noviembre 2007 y
ajustados a un modelo exponencial; el índice de mortalidad de huevos de sardina (Z) fue estimado en 0,07 (por hora), siendo el
índice de mortalidad diario del 83,5%. Por otra parte, para larvas de sardina, Z fue estimada en 0,1 (por hora), correspondiente
a un índice de mortalidad diario igual al 21,4%. Migraciones hacia el sur y costa afuera pueden ser consideradas como una causa
de la variabilidad en la deriva y condiciones de sobrevivencia de larvas de sardina. Análisis adicionales de serie de tiempo de las
primeras etapas del ciclo vital de las sardinas y la futura supervisión con programas de monitoreo adaptativo deberían ser
conducidos para un mejor manejo de la industria pesquera de esta especie en Marruecos.

Palabras clave: Sardina, huevos, larvas, mortalidad, Noroeste África

Abstract.- The purpose of this study was to estimate the natural mortality of embryonic and larval stages of European pilchard
Sardina pilchardus along the Atlantic Coast of Northwest Africa between Cape Barbas (22°30’N) and Cape Bojador (26°N) during
November 2007. Using planktonic data that were fitted to an exponential model, sardine eggs hourly mortality rate (Z) was
estimated in 0.07 (per hour) corresponding to 83.5% of daily mortality rate. On the other hand, for sardine larvae, Z was estimated
in 0.01 (per hour), corresponding to a daily mortality rate of 21.4%. Southward and offshore transport can be considered as
causes of variability in drifting scenario and survival condition of sardine larvae. Additional analyses of time series of the early
life history data of sardines and future adaptive monitoring should be conducted to better manage sardine fisheries in Morocco.

Key words: Sardine, eggs, larvae, mortality, Northwest Africa

INTRODUCTION
European pilchard, Sardina pilchardus (Walbaum, 1792) is In northwest Africa, S. pilchardus spawning occurs
one of the most important and abundant forage fishes along the throughout the year, although seasonal peaks of spawning
northwest African Atlantic coast. In the regional ecosystem, it depend on time and location (Berraho 2007). In the coastal
plays a key role in the trophic web as the dominant forage fish. area off Northwest Africa, spawning peaks were found in winter/
Major S. pilchardus distribution in the northwestern African early spring between Cape Ghir (31°N) and Cape Bojador
coast extends from Cape Blanc (21°N) to Cape Spartel (32°N) (26°N). Between Cape Bojador (26°N) and Cape Blanc
(Kifani & Gohin 1992, Berraho 2007, Ettahiri et al. 2012). It (21°N), the principal spawning peaks were generally found in
is also one of the important fishing targets in this coastal area. winter (mainly between November and December) at the
In Morocco, small pelagic fishes represent more than 75% of northern part of Cintra Bay corresponding to temperatures
total landings dominated by S. pilchardus (INRH 2002). ranging from 16.5 to 17.5°C. In general, the temperature ranges

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Revista de Biología Marina y Oceanografía
 between 15.5 and 17.5°C were suggested as the preferable environmental factors (Houde 2008, Garrido et al. 2015). The
thermal range of spawning for sardine (Berraho 2007). These high mortality occurring at early life stages of fish is selective
temperature ranges are lower than the known thermal range of (Houde & Schekter 1980), usually influenced by individual’s
spawning windows for some species in similar ecological niches. phenotype (Johnson et al. 2014), and during larvae stage the
For example, spawning peak of Sardinops sagax occurs at mortality is highly size-dependent (Anderson 1988). Various
water temperatures between 18ºC and 22ºC in southern studies have suggested that lower growth rates during larval
Queensland (Staunton-Smith & Ward 2000). phase results in higher mortality (Wilson & Meekan 2002). The
‘growth-mortality’ hypotheses (Anderson 1988) have been
Most pelagic forage fishes over the world like sardines are
usually used to explain the recruitment variation of marine fish
known to have large biomass fluctuations. In response to the
populations. According to these hypotheses, faster growing
environmental variability, S. pilchardus population in the Atlantic
individuals have a higher probability of survival. Fast growing
Ocean of South African coast and Namibia collapsed during
larvae develop a strong swimming abilities comparing to small
1965-1966 (Crawford & Shannon 1988). Sudden population
larvae, and experience a shorter stage-duration increasing their
collapse of Japanese sardine (Sardinops melanostictus) in the
chance to survive and become less vulnerable to predation.
early 1990’s was most likely the result of the unsuccessful
Garrido et al. (2015) have concluded that survival probability
recruitment (Suda & Kishida 2003, Watanabe 2009). The
of European pilchard S. pilchardus larvae is linked to the larval
variability of recruitment success has been explained from the
size at hatch. Therefore, prey availability probably influence
survival during the critical pre-recruitment phase (Hjort 1914,
dynamics of early life stages of fish and the limited feeding
1926). In the match/mismatch hypothesis by Cushing (1975),
availability may be regulating year class success (Houde &
recruitment success depends on the timing of fish spawning and
Schekter 1980). Nevertheless, mortality during this critical
prey production. Ocean dynamics may influence the embryonic
period can be influenced by several factors such as temperature
and larval survival and growth. Lasker (1981) proposed that in
(Blaxter 1992), physical processes (Cushing 1975), nutritional
upwelling ecosystems the more stable ocean conditions are,
conditions, growth rates (Vigliola & Meekan, 2002), etc.
the better survival and growth of larval fish are.
Thus, mortality during the early life stages becomes an
S. pilchardus stock of Morocco also experienced dramatic
important research line for an adaptive monitoring and
changes in abundance, especially in the 1997/1998, period that
sustainable management of the European pilchard stock of
was characterized by a warming due to El Niño phenomena
Morocco. In this work, we aimed to discuss the early life
(INRH 2002). The population dynamics may have been
survival of S. pilchardus in relation to the environmental
impacted by the change in the early-life survival condition
conditions especially in the passive phase with estimation of the
associated to the regional oceanography (INRH 2002). In the
mortality in northwestern Atlantic coast of Africa between
southern area of the northwestern Atlantic coast of Africa (21-
22°30’N and 26°N.
26°N), the upwelling activity provides a considerable supply of
nutrients sustaining primary and secondary production in the
ecosystems (Somoue et al. 2013, Demarcq & Somoue 2015). MATERIALS AND METHODS
Upwelled waters lower the Sea Surface Temperature (SST)
and develop spatial heterogeneity in this area according to the STUDY AREA AND SURVEYS
variability of the upwelling center location and its intensity This study is based on data of a survey carried on board of the
(Benazzouz et al. 2014). Many research activities have focused R/V Al Amir Moulay Abdellah in the south zone of the African
on physical and biological oceanography in this area, specifically Atlantic coast between Cape Bojador (26°N) and Cape Blanc
spatio-temporal dynamics of the marine environment in relation (21°N), in autumn 2007, from November 21st to December
to the upwelling. However, there have not been sufficient 2nd (Fig. 1). A total of 40 stations were sampled extending
discussions in the population dynamics of S. pilchardus and over 12 transects, at a rate of 3 to 4 stations per transect. Eggs
observed oceanographic dynamics in this region in relation to and larvae were collected using a Bongo net (20 x 20 cm mouth
the early life survival. diameter, 300 µm mesh size) by oblique tows (3 min) with 2.5
Houde (1987) suggested that mortality is critical during the knots. The Bongo net was equipped with flowmeters to estimate
early larval stages of a fish. Hjort´s hypotheses constituted the the volume of filtered water. Samples were immediately
background for the recent recruitment studies, mainly focused preserved in 5% borax buffered formalin solution in filtered sea
on the Critical Period hypothesis (Houde 2008). Fish water.
recruitment success is associated to species/populations and

484 Abdelouahab et al.

Mortality of early life stages of Sardina pilchardus
Figure 1. Surve yed area curried out in
November 2007, along the Atlantic Coast of
Northwest Africa (22°30’N-26°N). Cross circles
indicate oceanographic sampling stations / Área
de prospección realizada en noviembre 2007,
a lo largo de la costa Atlántica del Noroeste de
África (22°30’N-26°N). Las cruces corresponden
a las estaciones de muestreo oceanográficos

Sea surface temperature was measured using a CTD S PATIAL D ISTR IB U TION OF B IO LO GIC AL AN D
(Seabird SBE-911+) and water samples were collected by ENVIRONMENTAL CONDITIONS
Niskin bottles to estimate chlorophyll a concentration. Spatial distribution maps of eggs and small larvae (sized less
At the laboratory, all sardine eggs and larvae were sorted than 7 mm) are presented separately in 3 maps: eggs, newly
from the rest of plankton in samples and counted. Sardine eggs hatched eggs (larvae aged < 4 days) and larvae aged between
were classified into 11 embryonic stages according to the growth 4 and 7 days. Here the threshold size of 7 mm corresponds to
criteria (Ahlstrom 1943) while sardine larvae were measured the dorsal fin apparition and is considered as a limit between
and classified into 1 mm standard length classes. The abundance small and large larvae (Berraho et al. 2012). Kernel density
of sardine eggs and larvae was expressed into number per 10 estimation (KDE) was used to show spatial distribution of both
m² (Smith & Richardson 1979). eggs and larvae. They were also statistically examined to
pinpoint eggs and larvae distribution using geostatistical analysis.
Due to the weak abundance of eggs and larvae found in the
two last transects at 21°N and 21°30’N, the study area was Related environmental conditions including sea surface
limited to the main spawning zone located between 22°30’N- temperature and chlorophyll a maps are showed. Average
26°N, composed of 33 stations to avoid bias in mortality rates temperature between surface and 10 m map distribution was
estimation. obtained by ordinary kriging and chlorophyll a interpolation was
performed by probability kriging after normalization.

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 ESTIMATION OF THE MORTALITY we obtain the linear equation:
Estimation of the mortality was done in 2 major steps. First LN(Nt)= LN(N0) – Zt (4)
step was devoted to age estimation of eggs and larvae. Then,
embryonic and larval mortality rates of S. pilchardus were Then, parameters N0 and Z can be estimated using a linear
estimated by applying an exponential decay model (eq. 3). regression of the above equation as following:

For sardine eggs age estimation, the model established by N0= exp(intercept); Z= -Coeff
Lo (1985) was used and adjusted as in Ettahiri (1996): where intercept and Coeff are the parameters of the linear
Yegg= 10.73 x e (-0.1612i-0.0924 x T) 1.955
xi (1) regression of equation (4).

where Based on the equation (3), daily percentage of death of egg

or larvae (%D) can be estimated by applying the equation (5):
Y: age of eggs per hour
%D= 100 x (1- e-Zt) (5)
i: embryonic stages (i= 1, 2,…11)
where t= 24 hours.
T: temperature (°C)
All statistical analyses were carried out using R 2. 15.2 (R
For larvae age estimation, the relationship between size and Core Team).
age was considered. The larvae growth rate considered for the
Moroccan S. pilchardus was 0.6 mm day-1 (Ettahiri 1996).
Larvae sorted from samples were measured and grouped by
RESULTS
size class of 1 mm. In the analysis, we focused on small larvae
(< 7 mm) because large larvae (>7 mm) develop stronger REVIEW OF THE ENVIRONMENTAL CONDITIONS DURING

swimming capabilities and present a high net avoidance which 2007

can bias the mortality rate estimation. Distribution of average sea surface temperature showed a
differentiation of two coastal patterns of low temperature near
The estimation of larvae age (Ylarv) is obtained from the
to the coast. First one was observed between Cape Bojador
following formula:
and north of Dakhla (24°30’N), while the second one was
Ylarv= (Lobs – L0) / G (2) located in the south of Cape Barbas. Differences in water
temperature were around 1.3°C. Relatively high temperatures
L0 : Standard length of newly hatched larvae approximately
were observed in the north part especially in the offshore and
equals 2.5 mm
low temperature in the southern part of the study area.
Lobs : observed length of larvae (in mm) Chlorophyll a probability of occurrence was higher in the
G : Growth rate of Sardine larvae (0.6 mm day-1) southern part of the study area than in the northern part (almost
two times higher). The spatial distribution of the interpolated
surface temperature (Fig. 2a) suggests an inshore-offshore and
EXPONENTIAL DECAY MODEL north-south gradient. Temperatures less than 19°C in the south
Mortality estimation of egg and larvae of S. pilchardus was part, probably due to the presence of an upwelling activity, were
calculated using an exponential decay model: observed between Cape Barbas and Cape Blanc area and
between Cape Bojador and Dakhla.
Nt= N0 x e-Zt (3)
Nt : Egg/Larvae density at time t (ind. per 10 m2) The surface concentrations of chlorophyll a in the study area
reached 4.68 µg L-1. Mean concentration recorded was about
N0 : Egg/Larvae density at time t= 0 0.6 µg L-1 and high concentrations were recorded south of Cape
Z : Instantaneous mortality rate (per hour) Barbas (Fig. 2b).

t : Time (hours)
EGGS AND LARVAE SARDINE DISTRIBUTION

Sardine eggs showed a heterogeneous spatial distribution

MODEL FITTING
along the study area where high abundance recorded
Assuming that the spawning patterns are the same during the essentially between 23°N and 25°N with a maximum of
sampling period and that the emigration/immigration in the area 48,884 ind 10 m-2 (off Dakhla).
is balanced, using a natural-log transformation of equation (3),

486 Abdelouahab et al.

Mortality of early life stages of Sardina pilchardus
Figure 2. Distribution maps of a) ave rage
temperature and b) probability of presence of
chlorophyll a. Interpolated of average temperature
(°C) was from surface to 10 m. Probability of
occurrence of sea surface chlorophyll a / Mapas de
distribución de a) temperatura media y b)
probabi lidad de presencia de clor ofila a.
Interpolación de la temperatura media (°C) desde
la superficie hasta 10 m de profundidad.
Probabilidad de ocurrencia de la concentración de
clorofila a en la superficie del mar

Table 1. Estimation of the parameters Z (instantaneous mortality rate) and N0 (density at time
t= 0) for eggs of Sardina pilchardus / Estimación de los parámetros Z (tasa instantánea de
mortalidad) y N0 (densidad en el tiempo t= 0) para los huevos de Sardina pilchardus

After hatching, the spatial distribution of larvae aged less lost for the > 4-days age phase and could not be well fitted,
than 4 days showed a clustered distribution over the study area. which means that there is no clear spatial correlations for the
Highest abundances were observed in the north and south of observed densities (Fig. 4).
the study area.
Larvae older than 4 days were distributed mainly in offshore EMBRYONIC MORTALITY OF SARDINE

suggesting a southward/offshore displacement. Relatively high The mortality rate of eggs (Z) was estimated to 0.075 (per
density (> 3rd quartile) was still observed in the extreme south hour) corresponding to a daily mortality rate approximately equal
part (Fig. 3). to 83.5% (Table 1). N0 was estimated to 1720 eggs per 10 m2.
Looking at the semivariograms, the relative density of sardine In some stations, abundance of eggs was extremely high and
for eggs and larvae aged less than 4 days, still show spatial the sensitivity to those extreme values was taken into
correlations up to some thresholds and the semivariograms can consideration by applying the CI (95%) (Fig. 5)
be fitted to a theoretical model. But, this spatial pattern was

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 Figure 3. Distribution map of the passive phase of
early-life stage of Sardina pilchardus. a) Eggs; b)
Larvae aged less than 4-days; c) Larvae aged
greater than 4-days). Size of circles indicates the
abundance in statistical quantiles, and cross marks
are where no eggs or larvae were captured.
Contours are based on best-fit probability kriging
/ Mapa de distribución de la fase pasiva en los
primer os estadios de desarroll o de Sardina
pilchardus. a) Huevos; b) Larvas con menos de 4
días; c) Larvas mayores de 4 días. El tamaño de
círculos indica la densidad relativa en cuantiles
estadísticos, y la cruz indica donde no hubo
huevos o larvas capturadas. Los contornos están
basados en la probabilidad mejor adaptada al
método kriging

Figure 4. Semivariograms of the transformed

density of passive phase of early-life stage of Sardina
pilchardus a) Egg; b) < 4-day age larvae; c) > 4-day
age larvae, over the study area. Densities were
transformed into normal scores between 0 and 1
before the calculation of the semivariograms. Black
dots are the empirical semivariograms. Lines are
the best-fit spherical semivariogram models /
Semivariogramas de la densidad transformada de
la fase pasiva en los primeros estadios de
desarrollo de Sardina pilchardus. a) Huevo; b) edad
de larvas < 4 días; c) edad de larvas > de 4 días
en el área del estudio. La densidad fue
transformada en puntuación normal entre 0 y 1
antes del cálculo del semivariograma. Puntos
negros son semivariogramas empíricos. Las líneas
son modelos de semivariogramas esféricos que
mejor se adaptan

488 Abdelouahab et al.

Mortality of early life stages of Sardina pilchardus
Figure 5. Representation of the linear regression model with natural-log transformed egg or larvae density relation to the age (hours). Black dots are
the natural-log transformed egg or larvae density. Black lines are linear regression. Dotted lines are the upper and lower limit of the Confidence
Interval (95%) / Representación del modelo de regresión lineal con el logaritmo natural truncado y transformado de la densidad de huevo o larvas
en relación a la edad (horas). Puntos negros serian el logaritmo natural truncado transformado de la densidad de huevos o larvas. Líneas negras
corresponden a la regresión lineal y líneas de puntos sería el límite superior e inferior del intervalo de confianza (95%)

Table 2. Estimation of the parameters Z (instantaneous mortality rate) and N0 (density at

time t= 0) for larvae of Sardina pilchardus / Estimación de los parámetros Z (tasa instantánea
de mortalidad) y N0 (densidad en el tiempo t= 0) para larvas de Sardina pilchardus

LARVAL MORTALITY OF THE SARDINE extending from 32°N to 26°N of Atlantic Moroccan coast for
the same species estimated to 84% (Ettahiri 1996). The daily
The mortality rate Z of sardine larvae in this study area was
mortality of eggs of the kin species, Sardinops sagax, was
estimated to 0.01 (per hour) corresponding to a daily mortality
88% of dead eggs per day in the central part of the Peruvian
rate of 21.4% and N0 was estimated to 159 larvae per 10 m2
waters and reached 98% in the northern region of Peru (Smith
(Table 2). A linear regression with natural-log transformed larvae
et al. 1989), while in the Pacific coast the egg mortality rate
density in relation to the age was established (Fig. 5).
estimated for Sardinops caerulea was 36% (Smith 1973).
However, in the Japanese coast, characterized by the presence
DISCUSSION of other oceanographic features (other than upwelling), the daily
Both embryonic and larval mortality of S. pilchardus in the egg mortality rate estimated for Sardinops melanostictus was
southern area of the northwest African coast was estimated based 40% (Tanaka 1974). Multiple causes influence the variability
on in situ samples collected in November 2007. The eggs were of the estimated daily embryonic mortality rate, including spatio-
observed near the main spawning grounds located around temporal changes of environmental conditions (temperature,
Dakhla (Berraho 2007). This region is characterized by a large, physical processes, etc), species feeding behavior (predation,
flat and not deep continental shelf which constitutes a favorable cannibalism) and even the sampling strategy. Larval mortality
place for retention of eggs and larvae and for their development of S. pilchardus (< 7 mm) was not as high as the embryonic
(Ettahiri et al. 2012). The estimated embryonic mortality was mortality. It suggests higher vulnerability of S. pilchardus in
comparable to the available past information in the area egg phase than in larval phase. Either on-site thermal condition

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Revista de Biología Marina y Oceanografía
 or ecological interactions such as predations upon eggs may and food availability. The variability of the mortality rate and
have driven the higher mortality rate (Santander et al. 1983, the hatching timing will be depending upon the extension of cold
Kucharczyk et al. 1997). The mortality experienced during and nutrient rich water from the upwelling in the area. Since we
larval stage is extensively due to the larvae size (Garrido et al. have only single survey information, the specific range of the
2015) where smaller larvae are more vulnerable to predators variability in the mortality rate and the hatching timing needs
than others. Therefore, negative size selection of prey by the further data and studies. The mortality in 2007 was comparable
potential predators is conditioned by the high presence prey of to the other years in this region in early 1990s’ (Ettahiri 1996).
smaller size and decreasing number of predators when the prey Upwelling in the region including the study area in autumn-
size increases (Takasuka et al. 2003). Then, size-selective winter is not extremely intense (Benazzouz et al. 2014) though
predation may cause high larvae mortality among other causes. the intensity is interannually variable. In 2007, relatively high
Optimum temperature with stability of water column enhance autumn-winter upwelling in the northern area from 24°N, resulted
embryonic growth, and sufficient availability of prey is required in the along-coast extension of the cold and productive water.
for the successful survival of the larvae (Riveiro et al. 2000, In this extension, nearshore eggs may have taken time for
Kucharczyk et al. 1997, Kujawa et al.1997). Thus, fairly embryonic growth comparing to the area > 50 m bottom depth.
consistent transport and associated successful retention of eggs Though the high primary production may be beneficial for the
and larvae over the large and productive coastal shelf in this larvae, it will be significant after the beginning of the active
area are probably advantageous for their growth and survival. feeding. Thus, offshore transports after observed early larval
The area around Dakhla (24°N), where the majority of eggs phase will be the key of the early-life survival. The growth rate
were observed, is characterized by a large and flat continental and retention success in the given environmental conditions
shelf, limiting the dispersal toward the offshore (Roy 1991). probably played the keys of the early-life survival in this region,
The observed extension of productive cold water along coast which can be confirmed by more investigations using times series
may have provided adequate environment for the larval growth. of eggs, larvae and environmental data. Furthermore, variability
The observed southward extension of larval distribution is in upwelling seems to be the major driver of the survival
probably consequence of a passive drift associated to the condition. Though the thermal condition derived from upwelling
may be preferable for spawning (Berraho et al. 2005), the
southward surface current (Mittelstaedt 1991, Ettahiri et al.
condition might have been disadvantageous for retention, growth
2003).
and survival of passive phase of S. pilchardus.
In November 2007 SST showed gradients that may have
To examine the hypothesized scenario, further analysis using
affected the survival of sardine eggs and larvae. Faster growth
time series is necessary. Improving the sampling design to study
of egg and larvae will be enhanced by warmer temperature in
the mortality of pre-recruitment stages will allow future research
the observed range of the temperature though effect of direct
to test previous assumptions and follow the dynamics of fish
thermal shock and associated infections is uncertain (Lo 1985,
population taking into account the transport effect. Considering
Miranda et al. 1990). Especially for eggs, the spread surface
the importance of quantitative information in the pre-recruitment
water with temperature higher than 20°C would have
survival and recruitment success in the resource management,
accelerated the growth in the study area in November 2007.
oceanographic monitoring to confirm presented mortality
On the other hand, the productive southern water extended
dynamics hypothesis will be essential to establish the sustainable
along the coastline in the area may be advantageous to the
S. pilchardus resource assessment and fisheries.
survival of larvae (Varela 1992).
As the discussion in the ‘Optimal Environment Window’ ACKNOWLEDGMENTS
hypothesis (Cury & Roy 1989) and ‘Stable Ocean’ (Lasker
The authors thank the entire scientific team involved in sampling
1981), nutrient inputs from upwelling and stability of water
on board the research vessel Al Amir Moulay Abdellah and the
column over the coastal shelf of the study area provide high
Moroccan-Japanese coordinators and scientific team who
production of primary producers and optimum habitat conditions
contributed in the present work.
for the survival of early life S. pilchardus. Depending upon the
balance of the southern productive water and > 20°C surface
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Received 8 October 2015 and accepted 1 June 2016

Editor: Claudia Bustos D.

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Mortality of early life stages of Sardina pilchardus