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Fisheries Research

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Benefits of frontal waters for the growth of Engraulis anchoita larvae: The influence of food availability

Marina Do Soutoa,d,⁎, Mariela L. Spinellib,c, Daniel R. Browna, Marcelo Pájaroa, Marina V. Diaza,d, Fabiana L. Capitaniob,c

a Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo N°1, Escollera Norte, B7602HSA Mar del Plata, Argentina b Laboratorio de Zooplancton Marino, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (DBBE, FCEN, UBA), Intendente Güiraldes 2160, C1428EGA CABA, Argentina c Instituto de Biodiversidad y Biología Experimental y Aplicada, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas (IBBEA, UBA- CONICET), Argentina d Instituto de Investigaciones Marinas y Costeras, Consejo Nacional de Investigaciones Científicas y Técnicas (IIMyC-CONICET), Argentina

A R T I C L E I N F O

Handled by B. Morales-Nin

Keywords: Anchovy Ichthyoplankton Growth Zooplankton Tidal front

A B S T R A C T

We studied the abundance, size and growth rates of Engraulis anchoita larvae during the end of the species’ spawning season in relation to environmental variables. Two sampling transects, one in Península Valdés (northern transect: NT) and the other in Isla Escondida (southern transect: ST), with four stations each, were established in late summer. Both locations are characterized by high concentrations of E. anchoita larvae in spring, strongly associated with the presence of frontal waters, at the beginning of the species’ spawning season. Zooplankton and ichthyoplankton were sampled, and temperature profiles and chlorophyll-a satellite images were analyzed for each sampling station. Zooplankton samples were divided in size fractions, and composition and abundances were estimated. Standard length (SL), ontogenetic stages, and abundance (including eggs) were estimated. Additionally, age and growth rates were determined by otolith analysis. Two different scenarios were observed in both transects. In the NT, a frontal structure was found, while at the ST, the water column was completely homogeneous. Total zooplankton abundance was maximum at frontal waters, with 22,195 ind. m−3, being the small size fraction (< 200 μm) the most abundant, mainly composed of nauplii (9000 ind. m−3) and cyclopoid copepodites (4000 ind. m−3). The NT showed higher abundance (mean of 126.5 ind. m−2 per station in NT; 29.75 ind. m−2 in ST), faster growth rates of E. anchoita larvae (NT: 0.45 ± 0.04 mm day−1; ST: 0.34 ± 0.09 mm day−1; n = 90), and higher mean SL at frontal waters (7.57 ± 1.52 mm SL) than the ST. In the NT, E. anchoita growth rates were constant in time, whereas in the ST, they decreased with age. Our results support the classical theory, which states that frontal waters provide advantageous environmental conditions for fish larvae feeding, growth and, thus, survival.

1. Introduction

Frontal waters are characterized by circulations that are a con- sequence of differential densities between two water masses, which generate a convergence at the surface or bottom boundary (Largier, 1993; Mann and Lazier, 1996). Oceanographic characteristics of sea- sonal fronts such as nutrition enrichment and water stratification gen- erate favorable conditions for the development of phytoplankton, zooplankton, ichthyoplankton and top predators (Bakun et al., 2010; Mann and Lazier, 1996). According to the hypothesis of Bakun (1996), the “Bakun’s Fundamental Triad”, frontal areas have three essential

characteristics that enhance survival and recruitment of pelagic fish during their early stages: i) the enrichment of surface water layers caused by the rise of deeper water rich in nutrients; ii) the concentra- tion of planktonic organisms that constitute food items for fish larvae and iii) the retention of fish eggs and larvae in favorable areas.

A conspicuous feature in the Patagonian coastal area is the devel- opment of the tidal thermal front of Península Valdés during spring and summer (Fig. 1). When the frontal system is fully formed, it extends between 41° and 45°S, following the 75–80 m isobath (Sabatini et al., 2004). High tidal dissipation rates generate strong vertical mixing in near shore waters, which homogenizes the entire water column. Wind

https://doi.org/10.1016/j.fishres.2018.02.019 Received 12 June 2017; Received in revised form 19 February 2018; Accepted 20 February 2018

⁎ Corresponding author at: Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo N°1, Escollera Norte, B7602HSA Mar del Plata, Argentina. E-mail addresses: [email protected] (M. Do Souto), [email protected] (M.L. Spinelli), [email protected] (D.R. Brown), [email protected] (M. Pájaro),

[email protected] (M.V. Diaz), [email protected] (F.L. Capitanio).

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pressure on the surface layer also contributes to forming and main- taining the homogeneity near the shore. On the other hand, seasonal surface warming induces a strong stratification of the shelf waters. As a consequence, a clear separation can be observed between highly mixed coastal and stratified offshore waters (Tonini et al., 2013). Between the homogeneous and stratified waters, there is a transitional zone, with a weaker thermocline, which constitutes the frontal area (Carreto et al., 1986; Glorioso, 1987). This structure is maintained until autumn, when the stratification is weakened due to the wind effect and decreasing solar heating (Acha et al., 2004).

The Península Valdés tidal front is important to several fish re- sources that are subject to commercial fishery, e.g. the hake, the southern blue whiting, the Argentine shortfin squid, the mackerel and the patagonic Argentine anchovy (Alemany et al., 2014; Brunetti et al., 1998). The latter, Engraulis anchoita (Hubbs and Marini, 1935), is a small pelagic fish, important in the food web of the Argentine Sea, being in the dietary base of several commercially exploited species. Engraulis anchoita represents one of the most important fish resources in terms of biomass in the Southwest Atlantic Ocean (Hansen and Madirolas, 1996; Madureira et al., 2009; Pájaro et al., 2009). The

patagonic stock of E. anchoita spawns between 41° and 47°S from aus- tral spring to autumn, with a maximum spawning peak in December, from the coast to 150 km offshore. Each female lays eggs multiple times during the entire spawning season, forming areas with large con- centrations of larvae. Two main areas of larval concentration have been previously detected: one near Península Valdés and the other a few kilometers south, in the area of Isla Escondida (Sánchez, 1995; Sánchez and Ciechomski, 1995). Engraulis anchoita is a zooplanktivorous species throughout its life cycle, being a key component of the dynamics of pelagic ecosystems, performing a “wasp-waist” type control (Bakun, 2006; Cury et al., 2000; Hunt and McKinnell, 2006). Thus, variations in the adult biomass of E. anchoita could generate drastic changes at both higher and lower trophic levels.

Ciechomski (1966) and Ciechomski and Weiss (1974) reported that larval stages up to around 38 mm of standard length feed mainly on small organisms, mostly copepod eggs, nauplii and small copepodites (Sabatini, 2004; Sánchez and Manazza, 1994; Sato et al., 2011; Viñas and Ramírez, 1996). Copepod ontogenetic stages have been related to the degree of water stratification. Previous studies in the frontal system of Península Valdés have reported the highest abundance value of

Fig. 1. Position of transects and distribution of stations with mean surface chlorophyll-a values (mg C m−3) calculated as an average of eight days centered on April 3rd, 2013 (center). Detail of temperature profiles (°C) of the northern and southern transects (above and below, respectively). The purple arrow indicates the location of Isla Escondida.

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nauplii in the transitional area, in coincidence with the maximum trophic incidence of E. anchoita larvae (Derisio et al., 2014; Viñas and Ramírez, 1996). The prey of E. anchoita larvae is generally smaller than 500 μm, most commonly smaller than 300 μm (Sato et al., 2011; Spinelli et al., 2012; Viñas and Ramírez, 1996).

In clupeiform fishes as anchovy, environmental variability has a strong influence on early developmental stages (Sánchez, 1995), and larvae are subject to high mortality rates that could impact on the re- cruitment of adults. In particular, pelagic fish populations have de- monstrated to be variable and sensitive to various internal factors, such as the growth rate, natural mortality, predation mortality and nutri- tional condition; and external factors, such as the stability of the water column, temperature, upwelling periods and food availability. In ad- dition, each internal factor depends on the environmental conditions (Houde, 2008). Particularly, in several species of marine fish, larval growth influences the recruitment of adult stocks (Campana, 1996; García et al., 2003; Takasuka et al., 2007). Larval growth is commonly studied by the analysis of the otolith microstructure, a methodology that allows determining the age, growth rates and hatching date, by counting and measuring the otolith daily increments (Baumann et al., 2003; Brown et al., 2004). This methodology has been successfully applied to E. anchoita larvae and juveniles (Brown and Sánchez, 2010; Brown et al., 2013; Castello and Castello, 2003; Leonarduzzi et al., 2010).

The aim of this study was to study the growth of E. anchoita larvae through the analysis of the otolith microstructure in two different oceanographic scenarios at the end of the spawning season. Frontal waters are expected to favor higher chlorophyll-a concentration and zooplanktonic prey availability, resulting in faster growth rates. Thus, our work intends to reassert the importance of frontal systems as nur- sery areas.

2. Materials and methods

2.1. Study area and sample collection

Zooplankton samples were taken on board the oceanographic ship ARA Puerto Deseado, along two transects, a northern (NT) and a southern one (ST), with four stations each (stations 1–4 and 5–8 re- spectively), during March 2013 (29 and 30th). Both transects were planned considering two known major larval concentration areas: the area of Península Valdés and the proximities of Isla Escondida (Fig. 1).

At each station, zooplankton samples were collected with a MiniBongo net of 67 μm mesh size and 20 cm in mouth diameter, per- forming oblique hauls, from near the bottom to the surface, and then fixed in 5% formaldehyde. Ichthyoplankton samples were collected with a Bongo net of 300 μm mesh size and 60 cm in mouth diameter, also by oblique hauls. The ship moved at 2 knots during the trawls and a mechanical flowmeter was used in the mouth of each net to measure the volume of filtered water. A subsample of larvae (n = 90) was taken from each station and the individuals were frozen on board in liquid nitrogen at −196 °C; the rest of the samples were fixed in 5% for- maldehyde. Hydrographic conditions were determined by measuring temperature and conductivity at each station with a CTD Seabird 911. Satellite images of surface chlorophyll-a were obtained from MODIS Composite Software Giovanni System – Interactive Visualization and Analysis, with the mean values of eight days focused on April 3rd, 2013. Due to cloudiness, we chose the closer date to the sampling period showing a suitable image resolution.

2.2. Sample processing

The zooplankton obtained by using the MiniBongo net was divided into three size fractions through filters with appropriate mesh openings: larger than 500 μm (large fraction), between 200 and 500 μm (inter- mediate fraction), and smaller than 200 μm (small fraction). The large

fraction, although underrepresented by the MiniBongo net capture ca- pacity, was considered as a proxy of the abundance of larger zoo- plankton organisms. Each size fraction was filtered and resuspended in seawater (between 300 and 800 mL of total volume) and taxonomic groups (appendicularians, chaetognaths, copepods and their naupliar stages) were identified under a dissecting microscope. A variable number of 5-mL aliquots were taken from each size fraction, depending on the total abundance and composition of organisms found. In all cases, it was assured that the number of aliquots reached a stable proportion of zooplankton organisms. The total number of individuals counted was 11,261 in the NT and 10,731 in the ST. The abundance of specimens was calculated by analyzing fractions of the material in seawater (distilled water with 35 NaCl g L−1). Copepods in the inter- mediate and large size fractions were identified to species level (Bradford-Grieve et al., 1999), whereas those in the small fraction were identified only to Order level (Cyclopoida, Calanoida and Harpacti- coida).

Egg and larvae of E. anchoita collected with the Bongo net were separated from the rest of the sample, and their abundances (ind. m−2) were estimated. The standard length (SL) of each larva was measured under a binocular microscope equipped with a video camera. When larvae were curved due to fixation effects, SL was measured considering several straight sections. When there were less than 100 individuals per sample, all the individuals were measured, whereas when there were more than 100 individuals per sample, subsamples of about 100 an- chovy larvae were randomly selected. Larvae were classified according to the ontogenetic stages described by Alheit et al. (1991) as: preflexion (SL < 8.00 mm), flexion (8.00–12.90 mm SL) and postflexion (12.90–50.00 mm SL). As normality and homoscedasticity assumptions were not met, a Kruskal Wallis test was used to compare SL mean values among stations.

Heads of the frozen larvae were cut and preserved in 96% alcohol; head soft tissues were dissolved with sodium hypochlorite and cleaned with distilled water. Sagittal otoliths were removed under a binocular stereoscope. Otolith pairs were mounted on transparent medium (Protex-xylene) and dried for 48 h. The microstructure was analyzed with a Zeiss Axioscop binocular microscope at maximum magnification (×1000). Images were enhanced and analyzed using Kontron software (KS-300). The sagittal otolith radius (OR) and the number and width of daily increments were measured using a digital image processing soft- ware, considering the major axis of the otolith. Increments were counted in both otoliths of the pair and when there was at least 90% of coincidence between them (e.g. 10 and 11 increments), the number of increments of the otolith of the clearest image was assumed as the larval age in days. When only one otolith from the pair was available due to the loss of the other during the extraction, such information was considered (Brown et al., 2013).

2.3. Data analysis

Hatching dates were determined by subtracting the number of daily increments from the dates of capture. Power relationships between OR and SL and between OR and age (number of daily increments) were regressed. Larval growth was analyzed by back-calculation of past sizes at previous ages (growth trajectories). To obtain past size values, we used the methodology described by Watanabe and Kuroki (1997) and Watanabe and Nakamura (1998). After fitting SL and OR to a power relationship, the relationship of the ith otolith radius (ORi) and SL on the day of the ith increment (SLi) was considered to be expressed by this formula for each larva:

SLi = aORi b (1)

a b

SL1 = aOR1 b (2)

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SLcaptured b = aORcaptured

b (3)

where SL1 = standard length at first-increment deposition (4 mm;

Leonarduzzi et al., 2010); OR1 = measured otolith radius of the first daily increment (μm); SL captured = measured standard length at capture (mm); OR captured = otolith radius (μm) at capture. For the statistical analysis, we transformed the power relationships

(OR – age and SL – OR) applying natural logarithm (Ln). Then, we tested differences between the slopes of the linearized relationships obtained for larvae from the NT and the ST (Zar, 1996). Somatic growth rates of larvae were calculated as mean values of differences between two consecutive back-calculated sizes of the individuals: SLj (i + 1), SLj (i) (Leonarduzzi et al., 2010):

∑ + −

=

SLj i SLj i n

( ( 1) ( ) )

j

n

1 (4)

where n = number of individuals at age i; SLj (i) = standard length back-calculated for an individual j at age i; SLj (i + 1) = standard length back-calculated for an individual j at

age i + 1 To analyze the influence of spatial differences on larval growth,

growth rates per age from both transects were compared. After ver- ifying statistical assumptions (see Supplementary material 1 for de- tails), a General Linear Mixed Model was applied to analyze the dif- ferences between both transects, ages and individuals. The age-transect interaction was also tested and the model was expressed as:

∼ + + ×

+

Growth rate Transect Age Transect Age

Individual Transect( ) (5)

Growth rate = continuous numerical variable that represents the daily growth rate. Previous to the analysis, this variable was trans- formed by Box-Cox to achieve better normality and homoscedasticity of the data.

Transect = fixed factor that represents the transect analyzed; Age = fixed factor that represents the larval age in days; Transect × Age = interaction between both factors; Individual (Transect) = random factor representing each individual,

nested within each transect.

3. Results

The persistence of the tidal front was detected only in the NT, and stratified waters were observed in the offshore area (stations 3 and 4), as shown in the temperature profiles (Fig. 1). Transitional waters were detected in station 2. In station 4, which showed the greatest stratifi- cation degree, the thermocline was located between 40 and 50 m deep. Station 1 of the NT and all stations of the ST presented homogeneous waters. No strong halocline was detected in the NT or ST (see Supple- mentary material 2 for details). The values of chlorophyll-a con- centration were slightly higher in the ST than in the NT, and a patch of high chlorophyll-a concentration was observed at the coastal area around 43°S (Fig. 1).

Zooplankton abundance was markedly higher in the NT than in the ST (Fig. 2), with the maximum values located in transitional (13,327 ind. m−3 in station 2) and stratified waters (22,195 ind. m−3 in station 3). The maximum zooplankton abundance value in the ST was observed in station 5, with 4617 ind. m−3. Intermediate and small size fractions were the predominant ones in the entire area, with a max- imum abundance value of the small size fraction in station 3, mainly composed of nauplii (9000 ind. m−3) and cyclopoids (4000 ind. m−3). Appendicularians and cyclopoids occurred in the most offshore stations of the NT (stations 3 and 4), while calanoids were especially abundant

in transitional (station 2) and homogeneous waters (station 1). Ad- ditionally, a high abundance of the dinoflagellate Noctiluca scintillans was observed in the samples from transitional and frontal stations 2 and 3 (see Supplementary material 3 for details). The intermediate size fraction had a maximum abundance value in transitional waters (sta- tion 2) and was mainly composed of calanoids, both adults and cope- podites (Fig. 2). As expected due to the mesh size of the MiniBongo net, the large size fraction abundance was low, being mainly composed of calanoid adults. In the ST, unlike that recorded in the NT, the inter- mediate size fraction was the most abundant, followed by the large size fraction and finally by the small size fraction. This transect was mainly composed of large and intermediate sizes of calanoids, followed by small and intermediate sizes of cyclopoids. The calanoids Acartia tonsa and Paracalanus parvus and the cyclopoids Oithona similis and O. nana were the copepod species that dominated both transects. Furthermore, the calanoid Calanus australis was found in stratified (stations 3 and 4) and transitional waters (station 2) and only one harpacticoid, Euterpina acutifrons, occurred in the ST (see Supplementary material 4 and 5 for details). In all stations, the presence of other large zooplankton or- ganisms was recorded (see Supplementary material 3 for details).

Following the same trend as zooplankton prey, E. anchoita larvae were more abundant in the NT than in the ST, with a maximum value of 220 ind. m−2 in station 3. In the ST, a maximum abundance of 85 ind. m−2 was detected in station 8. Anchovy eggs mainly occurred in the most offshore station of the NT (175 eggs m−2 in station 4) and, when present in the remaining stations, did not exceed 1 egg m−2

(Fig. 3). Anchovy larvae from the NT hatched from February 26 to March 27, whereas those from the ST hatched from February 16 to March 27. In both transects, larvae hatching occurred mostly from March 18 to March 22. Older larvae were located in the most coastal stations, while younger ones were in a more offshore position. Pre- flexion larvae were the most abundant in all stations. Postflexion larvae occurred in low quantities and did not exceed 15.5 mm SL. The max- imum density of flexion larvae was observed in the NT, particularly in frontal waters (station 3). In this location, the mean SL value (mean SL: 7.57 ± 1.52 mm) was the highest of the whole transect (p < 0.05).

When OR/age values (Fig. 4A) were compared between transects (considering the same age range of 4–27 days), the slope of the line- arized relationship was significantly higher for the larvae from the NT (p < 0.001). The same occurred with the linearized relationships be- tween OR and SL (Fig. 4B), where a higher slope value was found for the larvae from the NT (p < 0.001). Therefore, when comparing larvae of the same age or SL, a faster otolith growth rate was detected in larvae from the NT.

The results of the General Linear Mixed Model showed significant differences between transects in larval growth per age (Table 1). Sta- tistical differences between individuals from each transect were also detected, demonstrating the existence of high variability between larval growth trajectories. Total mean growth rates (considering average va- lues per age) were 0.45 ± 0.04 mm day−1 for the NT and 0.34 ± 0.09 mm day−1 for the ST. When larval growth rates were plotted for each age and compared between transects, values of larvae of the NT were higher than the ones of the ST; the difference was more noticeable in older larvae (Fig. 5).

4. Discussion

4.1. Oceanography, zooplankton abundance and size composition

In the present study, we found two different oceanographic sce- narios across two known spawning and nursery grounds of E. anchoita larvae, with chlorophyll-a values at the coastal area in coincidence with the autumn pattern described by Paparazzo et al. (2010) and Rivas et al. (2006). Nevertheless, the maximum zooplankton abundance value was found at a low-concentration chlorophyll-a patch. This could have been caused by a large grazing effect, consequence of an active feeding of the

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abundant zooplankton organisms located there. We found that zoo- planktonic groups showed a differential spatial distribution in relation to water stratification, in agreement with that found by Sabatini and Martos (2002) in the same area during spring. These authors observed distinct physical environments characterizing the northern and southern boundaries of the tidal front (Península Valdés and Isla Es- condida respectively), mainly due to differential wind/tidal relative forcing, which led to the occurrence of different plankton assemblages. They also found that cyclopoids and appendicularians were con- spicuous toward the north (Península Valdés), and suggested that the microbial food web played an important role in the area, while in further south (Isla Escondida), where calanoid copepods were domi- nant, a classic herbivorous food web was probably the case. In our study, zooplankton groups in the northern and southern transects were distributed in a similar way to that described by these authors during spring. Total zooplankton abundances recorded in the NT were higher than or quite similar to the ones described during November/December (austral spring) blooms at the beginning of the anchovy spawning season (Sabatini et al., 2004; Spinelli et al., 2012). The great abundance

of the dinoflagellate N. scintillans found in our study suggests that transitional waters were enriched, supported by the high abundance of the small size zooplankton fraction (< 200 μm), mainly composed of copepod nauplii and small cyclopoids. The same happened with the intermediate zooplankton size fraction (200–500 μm) in the frontal position next to transitional waters, where both small and intermediate size fractions represented suitable prey for the E. anchoita larvae that were growing in the NT.

4.2. Engraulis anchoita eggs and larval distribution

Low abundance of anchovy eggs was expected, as the sampling took place at the end of the reproductive season, which has been established around April, in coincidence with the start of the austral autumn (Sánchez, 1995). Since eggs and newly hatched larvae were detected in the offshore station, and older larvae in postflexion stage were present in the coastal stations, a displacement of the spawning towards offshore waters could be occurring, a phenomenon previously observed by Brown et al. (2013) and Sánchez (1995). These authors described the

Fig. 2. Total zooplankton abundance (ind. m−3) in each station (center). Composition of zooplankton size fractions (small (< 200 μm), intermediate (200–500 μm) and large (> 500 μm)) of nauplii, calanoids, cyclopoids, harpacticoids and appendicularians from the northern and southern transects (above and below, respectively). Note the difference in the scale between both transects.

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displacement of the spawning area from coastal waters to outer waters as the reproductive season progresses. Hansen et al. (2001) detected that changes in the tidal front position were followed by similar changes in the location of the E. anchoita spawning adults. Such loca- tion of adults would determine the position of eggs and larvae, coin- ciding with stratified water masses.

4.3. Growth rates of E. anchoita larvae at the end of the spawning season

The growth rates of E. anchoita larvae (0.34–0.45 mm day−1) ob- tained in this work coincide with those reported for this species during spring time. Brown and Sánchez (2010) and Brown et al. (2013) re- corded values between 0.35 and 0.51 mm day−1. In another frontal area of the Southwestern Atlantic Ocean (near the Buenos Aires pro- vince), Leonarduzzi et al. (2010) detected larval growth rates between 0.41 and 0.51 mm day−1. Spatial differences in E. anchoita larval growth related to the presence of a frontal system were detected in this study for the first time. These growth differences were mainly observed for the older larvae, while younger individuals had similar growth rates in both areas. Probably, environmental conditions turn out to be more influent when larval feeding becomes active. Thus, the advantageous

environmental conditions of the NT would have influenced positively on older anchovy larvae.

The main external factors that affect fish larvae growth are tem- perature and food availability (Heath, 1992; Stevenson and Campana, 1992). Castello and Castello (2003) analyzed E. anchoita larval growth in Brazilian waters in winter and spring, and found growth rates from 0.40 to 0.50 mm day−1 in a thermal range of 17–25 °C. In another study performed in southern Brazil, where temperature values varied be- tween 20 and 22 °C, Ekau (1998) obtained a growth rate range of an- chovy larvae from 0.7 to 1 mm day−1. All these growth rate values were higher than those herein reported. Nevertheless, our temperature range was 12–16 °C, thus, the slower growth rates reported here could be the result of the lower mean temperature due to latitudinal effects.

Even so, in the present study, temperature differences between sampling stations did not exceed 1 °C, and such thermal variation could not lead to growth rate differences in a species that inhabits a broad latitudinal range. In contrast, food availability seems to have played a key role, while growth rates are driven mainly by early life trophic dynamics according to the results presented by Catalán et al. (2010) for E. encrasicolus in the Aegean Sea. Accordingly, while analyzing the in- fluence of seasonality on larval growth, Leonarduzzi et al. (2010) did

Fig. 3. Abundance (ind. m−2) of Engraulis anchoita larvae and eggs in each station (center). Hatching dates, ontogenetic stages (preflexion, flexion and postflexion) and mean standard length (SL) values of E. anchoita larvae from the northern and southern transects (above and below, respectively). * indicates a significant difference (p < 0.05) in mean SL values.

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not attribute differences in growth rate to temperature, but proposed that growth differences could be related to food availability. Taking into account the concept of Hjort’s critical period (Hjort, 1926), Houde

(2008) supported the existence of a positive relationship between prey availability and larval survival and stated that well-fed individuals would acquire a larger size in a shorter time, which would reduce the chances of mortality due to predation. Clemmesen (1994) stated that when prey availability is not a limiting factor for fish larvae in terms of quality or quantity, larval growth rates will increase and a better nu- tritional condition will be obtained. Moreover, Diaz et al. (2016) ana- lyzed the nutritional condition of anchovy larvae by means of the RNA/ DNA index, with specimens collected in the same oceanographic ship as the anchovy larvae analyzed in this study, and found that anchovy larvae from Península Valdés had a better condition than the ones from Isla Escondida area. These authors proposed that larvae in better nu- tritional condition are expected to have advantages in food competition and predator evasion.

An important issue studied in fisheries research is the mechanisms of population control. However, assessing which factors determine larval abundance is complex since many factors act simultaneously. Although the developmental stage at which recruitment is determined is under discussion, larval success is very important in this concern (Bailey and Houde, 1989). In our study, frontal waters with their en- richment and development of planktonic organisms fulfilled what was expected by Bakun’s theory. This fact could imply an impact on the survival and recruitment of E. anchoita larvae (García et al., 2003). The consequences of the variations in larval abundance, growth and con- dition herein reported on E. anchoita recruitment are yet to be under- stood.

Funding

This work was supported by the INIDEP, the CONICET [PIP CONICET 11220150100109CO] and UBA [UBACYT 20020160100045BA] to Dr. FC.

Acknowledgments

We would like to thank Carlos Balestrini and Martin Saraceno for providing the temperature and salinity profiles and useful bibliography, Daniel Hernández for statistical support, and INIDEP authorities and the crew of the oceanographic ship ARA Puerto Deseado for all the samples provided. Special thanks to the reviewers and the editor since their comments have substantially helped to improve our manuscript. This is INIDEP contribution N° 2105.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, in the online version, at https://doi.org/10.1016/j.fishres.2018.02.019.

References

Acha, E.M., Mianzan, H.W., Guerrero, R.A., Favero, M., Bava, J., 2004. Marine fronts at the continental shelves of austral South America: physical and ecological processes. J. Mar. Syst. 44, 83–105. http://dx.doi.org/10.1016/j.jmarsys.2003.09.005.

Alemany, D., Acha, E.M., Iribarne, O.O., 2014. Marine fronts are important fishing areas for demersal species at the Argentine Sea (Southwest Atlantic Ocean). J. Sea Res. 87, 56–67. http://dx.doi.org/10.1016/j.seares.2013.12.006.

Alheit, J., Ciechomski, J.D., Djurfeldt, L., Ebel, C., Ehrlich, M.D., Elgue, J.C., Viñas, M.D., 1991. SARP Studies on Southwest Atlantic anchovy, Engraulis anchoita, off Argentina, Uruguay and Brazil, vol. 46. ICES Biol. Oceanogr. Comm., Copenhagen, pp. 1–66.

Bailey, K.M., Houde, E.D., 1989. Predation on eggs and larvae of marine fishes and the recruitment problem. Adv. Mar. Biol. 25, 1–83. http://dx.doi.org/10.1016/S0065- 2881(08)60187-X.

Bakun, A., Field, D.B., Redondo-Rodriguez, A., Weeks, S.J., 2010. Greenhouse gas, up- welling-favorable winds, and the future of coastal ocean upwelling ecosystems. Global Change Biol. 16, 1213–1228. http://dx.doi.org/10.1111/j.1365-2486.2009. 02094.x.

Bakun, A., 1996. Patterns in the Ocean. Ocean Processes and Marine Population Dynamics. University of California Sea Grant, in cooperation with Centro de Investigaciones Biologicas de Noroeste, La Paz, México, California.

Bakun, A., 2006. Wasp-waist populations and marine ecosystem dynamics: navigating the

Fig. 4. Linearized logarithm (Ln) relationships between otolith radius (OR) and age (A) and between standard length (SL) and OR, (B) of Engraulis anchoita larvae from the northern and southern transects. Larvae from 0 to 27 days old were considered for sta- tistical comparison.

Table 1 GLM-ANOVA Univariate Tests of Significance for the growth rate (dependent variable) of Engraulis anchoita larvae, and potentially explanatory factors of Transect, Age, Individual and interactions.

Factor Degree of Freedom

Sum of Squares

Mean Squares

F statistic p value

Transect 1 0.0360 0.0360 6.803 0.0097 Age 26 0.1507 0.0060 2.182 0.0006 Transect × Age 26 0.1637 0.0063 2.370 0.0002 Individual

(Transect) 87 1.4684 0.0169 6.353 0.0000

Error 834 2.2157 0.0027

Fig. 5. Average growth rates (mm day−1) by age of Engraulis anchoita larvae from the northern (NT) and southern transects (ST) at the Península Valdés Frontal System.

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“predator pit” topographies. Prog. Oceanogr. 68, 271–288. http://dx.doi.org/10. 1016/j.pocean.2006.02.004.

Baumann, H., Pepin, P., Davidson, F., Mowbray, F., Schnack, D., Dower, J., 2003. Reconstruction of environmental histories to investigate patterns of larval radiated shanny (Ulvaria subbifurcata) growth and selective survival in a large bay of Newfoundland. ICES J. Mar. Sci. 60, 243–258. http://dx.doi.org/10.1016/S1054- 3139(03)00019-5.

Bradford-Grieve, J.M., Markhaseva, E.L., Rocha, C.E.F., Abiahy, B., 1999. Copepoda, In: D., Boltovskoy (Ed.), South Atlantic Zooplankton, Mar del Plata, pp. 869–1706.

Brown, D.R., Sánchez, R.P., 2010. Larval and juvenile growth of two Patagonian small pelagic fishes: Engraulis anchoita and Sprattus fuegensis. Rev. Invest. Desarro. Pesq. 20, 35–50.

Brown, D.R., Leonarduzzi, E., Machinandiarena, L., 2004. Age, growth and mortality of hake larvae (Merluccius hubbsi) in the north Patagonian shelf. Sci. Mar. 68, 273–283. http://dx.doi.org/10.3989/scimar.2004.68n2273.

Brown, D.R., Leonarduzzi, E., Averbuj, A., Livore, J.P., 2013. Temporal variation in Engraulis anchoita eggs and larvae abundance in northpatagonian littoral between January–April 2001. Larval growth and mortality. Rev. Invest. Desarro. Pesq. 23, 175–192.

Brunetti, N.E., Elena, B., Rossi, G.R., Ivanovic, M.L., Aubone, A., Guerrero, R., Benavides, H., 1998. Summer distribution, abundance and population structure of Illex argentinus on the Argentine shelf in relation to environmental features. Afr. J. Mar. Sci. 20, 175–186. http://dx.doi.org/10.2989/025776198784126386.

Campana, S.E., 1996. Year-class strength and growth rate in young Atlantic cod Gadus morhua. Mar. Ecol. Prog. Ser. 135, 21–26. http://dx.doi.org/10.3354/meps135021.

Carreto, J.I., Benavides, H.R., Negri, R.H., Glorioso, P.D., 1986. Toxic red tide in the Argentine Sea: phytoplankton distribution and survival of the toxic dinoflagellate Gonyaulax excavata in frontal area. J. Plankton Res. 8, 15–28. http://dx.doi.org/10. 1093/plankt/8.1.15.

Castello, L., Castello, J.P., 2003. Anchovy stocks (Engraulis anchoita) and larval growth in the SW Atlantic. Fish. Res. 59, 409–421. http://dx.doi.org/10.1016/S0165-7836(02) 00014-0.

Catalán, I.A., Folkvord, A., Palomera, I., Quílez-Badía, G., Kallianoti, F., Tselepides, A., Kallianotis, A., 2010. Growth and feeding patterns of European anchovy (Engraulis encrasicolus) early life stages in the Aegean Sea (NE Mediterranean). Estuar. Coast. Shelf Sci. 86, 299–312. http://dx.doi.org/10.1016/j.ecss.2009.11.033.

Ciechomski, J.D., Weiss, G., 1974. Estudios sobre la alimentación de larvas de la merluza, Merluccius hubbsi y de la anchoíta, Engraulis anchoita en el mar. Physis 33, 199–208.

Ciechomski, J.D., 1966. Development of the larvae and variations in the size of the eggs of the Argentine anchovy, Engraulis anchoita (Hubbs and Marini). ICES J. Mar. Sci.: J. Cons. 30, 281–290. http://dx.doi.org/10.1093/icesjms/30.3.281.

Clemmesen, C., 1994. The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Mar. Biol. 118, 377–382. http://dx.doi.org/10.1007/BF00350294.

Cury, P., Bakun, A., Crawford, R.J.M., Jarre, A., Quiñones, R.A., Shannon, L.J., Verheye, H.M., 2000. Small pelagics in upwelling systems: patterns of interaction and struc- tural changes in “wasp-waist” ecosystems. ICES J. Mar. Sci. 57, 603–618. http://dx. doi.org/10.1006/jmsc.2000.0712.

Derisio, C., Alemany, D., Acha, E.M., Mianzan, H., 2014. Influence of a tidal front on zooplankton abundance, assemblages and life histories in Península Valdés, Argentina. J. Mar. Syst. 139, 475–482. http://dx.doi.org/10.1016/j.jmarsys.2014.08. 019.

Diaz, M.V., Do Souto, M., Peralta, M., Pájaro, M., Spinelli, M., Saraceno, M., Balestrini, C., Capitanio, F., 2016. Comer o ser comido: factores que determinan la condición nu- tricional de larvas de Engraulis anchoita de la población patagónica de la especie. Ecol. Austral 26, 120–133.

Ekau, W., 1998. Comparative growth analysis of Engraulis anchoita larvae from southern Brazil. Arch. Fish. Mar. Res. 46, 1–17.

García, A., Cortés, D., Ramírez, T., Giráldez, A., Carpena, A., 2003. Contribution of larval growth rate vairability to the recruitment of the Bay of Málaga anchovy (SW Mediterranean) during 2000–2001 spawning seasons. Sci. Mar. 67, 477–490. http:// dx.doi.org/10.3989/scimar.2003.67n4477.

Glorioso, P.D., 1987. Temperature distribution related to shelf sea fronts on the Patagonian shelf. Cont. Shelf Res. 7, 27–34. http://dx.doi.org/10.1016/0278- 4343(87)90061-6.

Hansen, J.E., Madirolas, A., 1996. Anchovy distribution, acoustic assessment and popu- lation structure. Results from year 1993 surveys. Rev. Invest. Desarro. Pesq. 10, 5–21.

Hansen, J.E., Martos, P., Madirolas, A., 2001. Relationship between spatial distribution of the Patagonian stock of Argentine anchovy, Engraulis anchoita, and sea temperatures during late spring to early summer. Fish. Oceanogr. 10, 193–206. http://dx.doi.org/ 10.1046/j.1365-2419.2001.00166.x.

Heath, M.R., 1992. Field investigations of the early life stages of marine fish. Adv. Mar. Biol. 28, 1–174. http://dx.doi.org/10.1016/S0065-2881(08)60039-5.

Hjort, J., 1926. Fluctuations in the year classes of important food fishes. J. Cons. Int. Explor. Mer. 1, 5–38. http://dx.doi.org/10.1093/icesjms/1.1.5.

Houde, E.D., 2008. Emerging from Hjort’s shadow. J. Northwest Atl. Fish. Sci. 41, 53–70. http://dx.doi.org/10.2960/J.v41.m634.

Hunt Jr., G.L., McKinnell, S., 2006. Interplay between top-down, bottom-up, and wasp- waist control in marine ecosystems. Prog. Oceanogr. 68, 115–124. http://dx.doi.org/ 10.1016/j.pocean.2006.02.008.

Largier, J.L., 1993. Estuarine fronts: how important are they? Estuaries 16, 1–11. http:// dx.doi.org/10.2307/1352760.

Leonarduzzi, E., Brown, D.R., Sánchez, R., 2010. Seasonal variations in the growth of anchovy larvae (Engraulis anchoita) on the Argentine coastal shelf. Sci. Mar. 74, 267–274. http://dx.doi.org/10.3989/scimar.2010.74n1267.

Madureira, L.A.S.P., Castello, J.P., Hernandez, C.P., Queiroz, M.I., Espírito Santo, M.L.P., Ruiz, W.A., Abdallah, P.R., Hansen, J.E., Bertolotti, M.I., Manca, E.A., 2009. Current and potential alternative food uses of the Argentine anchoita (Engraulis anchoita) in Argentina, Uruguay and Brazil. FAO Fish. Aquac. Tech. Pap., vol. 518. pp. 269–288.

Mann, K.H., Lazier, J.R.N., 1996. Dynamics of Marine Ecosystems: Biological-Physical Interactions in the Oceans. Blackwell Publishing, Cambridge.

Pájaro, M., Macchi, G.J., Leonarduzzi, E., Hansen, J.E., 2009. Spawning biomass of Argentine anchovy (Engraulis anchoita) from 1996 to 2004 using the Daily Egg Production Method. J. Mar. Biol. Assoc. U. K. 89, 829–837. http://dx.doi.org/10. 1017/S0025315408003019.

Paparazzo, F.E., Bianucci, L., Schloss, I.R., Almandoz, G.O., Solís, M., Esteves, J.L., 2010. Cross-frontal distribution of inorganic nutrients and chlorophyll-a on the Patagonian Continental Shelf of Argentina during summer and fall. Rev. Biol. Mar. Oceanogr. 45, 107–119.

Rivas, A.L., Dogliotti, A.I., Gagliardini, D.A., 2006. Seasonal variability in satellite mea- sured surface chlorophyll in the Patagonian Shelf. Cont. Shelf Res. 26, 703–720. http://dx.doi.org/10.1016/j.csr.2006.01.013.

Sánchez, R.P., Ciechomski, J.D., 1995. Spawning and nursery grounds of pelagic fish species in the sea-shelf off Argentina and adjacent areas. Sci. Mar. 59, 455–478.

Sánchez, R.P., Manazza, G.O., 1994. Aspects of feeding ecology of larval anchovy, Engraulis anchoita, in relation with patagonian tidal frontal systems. Frente Marit. 15, 51–66.

Sánchez, R.P., 1995. Patrones de distribución espacio-temporal de los estadíos em- brionarios y larvales de la anchoíta (Engraulis anchoita Hubbs & Marini) a micro y macro-escala. Su relación con la supervivencia. PhD diss. Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Buenos Aires 630 pp.

Sabatini, M., Martos, P., 2002. Mesozooplankton features in a frontal area off northern Patagonia (Argentina) during spring 1995 and 1998. Sci. Mar. 66, 215–232. http:// dx.doi.org/10.3989/scimar.2002.66n3215.

Sabatini, M., Reta, R., Matano, R., 2004. Circulation and zooplankton biomass distribu- tion over the southern Patagonian shelf during late summer. Cont. Shelf Res. 24, 1359–1373. http://dx.doi.org/10.1016/j.csr.2004.03.014.

Sabatini, M., 2004. Environmental features, reproduction and feeding of hake (Merluccius hubbsi) and anchovy (Engraulis anchoita) in the Patagonian spawning ground. Synthesis and perspectives. Rev. Invest. Desarro. Pesq. 16, 5–25.

Sato, N.E., Hernández, D., Viñas, M.D., 2011. Hábitos alimentarios de las larvas de Engraulis anchoita (Hubbs & Marini, 1935) en las aguas costeras de la Provincia de Buenos Aires, Argentina. Lat. Am. J. Aquat. Res. 39, 16–24.

Spinelli, M.L., Pájaro, M., Martos, P., Esnal, G.B., Sabatini, M., Capitanio, F.L., 2012. Potential zooplankton preys (Copepoda and Appendicularia) for Engraulis anchoita in relation to early larval and spawning distributions in the Patagonian frontal system (SW Atlantic Ocean). Sci. Mar. 76, 39–47. http://dx.doi.org/10.3989/scimar.2012. 76n1039.

Stevenson, D.K., Campana, S.E., 1992. Otolith Microstructure Examination and Analysis, vol. 117. Canadian Special Publication of Fisheries and Aquatic Sciences, pp. 59–71.

Takasuka, A., Oozeki, Y., Aoki, I., 2007. Optimal growth temperature hypothesis: why do anchovy flourish and sardine collapse or vice versa under the same ocean regime? Can. J. Fish. Aquat. Sci. 64, 768–776. http://dx.doi.org/10.1139/f07-052.

Tonini, M.H., Palma, E.D., Piola, A.R., 2013. A numerical study of gyres, thermal fronts and seasonal circulation in austral semi-enclosed gulfs. Cont. Shelf Res. 65, 97–110. http://dx.doi.org/10.1016/j.csr.2013.06.011.

Viñas, M.D., Ramírez, F.C., 1996. Gut analysis of first-feeding anchovy larvae from Patagonian spawning area in relation to food availability. Arch. Fish. Mar. Res. 43, 231–256.

Watanabe, Y., Kuroki, T., 1997. Asymptotic growth trajectories of larval sardine (Sardinops melanostictus) in the coastal waters off western Japan. Mar. Biol. 127, 369–378. http://dx.doi.org/10.1007/s002270050023.

Watanabe, Y., Nakamura, M., 1998. Growth trajectory of the larval Japanese sardine, Sardinops melanostictus, transported into the Pacific coastal waters off central Japan. Fish. Bull. 96, 900–907.

Zar, J.H., 1996. Biostatistical Analysis, third ed. Prentice-Hall, Englewood Cliffs, NJ.

M. Do Souto et al. Fisheries Research 204 (2018) 181–188

188