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Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.44 no.1 Valparaíso mar. 2016

http://dx.doi.org/10.3856/vol44-issue1-fulltext-7 

 

Research Article

Distribution and abundance of Engraulis ringens eggs along the north-central Chilean coastline (25.0-31.5°S) during February 2008 to 2014

Distribución y abundancia de huevos de Engraulis ringens en la zona centro-norte de Chile (25,0°-31,5°S) en febrero 2008-2014

 

Armando Mujica1, María Luisa Nava1, Ken Matsuda2 & Alejandra Vargas1

1Departamento de Acuicultura, Universidad Católica del Norte, Coquimbo, Chile.
2Departamento de Matemáticas, Universidad de La Serena, La Serena, Chile.

 Corresponding author: Armando Mujica (amujica@ucn.cl)
Corresponding editor: Guido Plaza


ABSTRACT. In the north-central Chilean coast (25.5-31.5°S), zooplankton samples were analyzed in 100 oceanographic stations from six oceanographic cruises made in February of 2008, 2009, 2010, 2011, 2013 and 2014. Engraulis ringens eggs were separated and counted, thus providing data on distribution, abundance, interannual variation, and relationships with ocean surface temperature and chlorophyll-a. The egg distribution was preferentially coastal, with maximum concentrations at stations next to Esmeralda Cove (26°S) and Chañaral Cove (29°S). In this time series, which includes cold and warm periods, it was established the relationship of these biological variables with defined ranges of temperature (16,1°-18,0°C).

Keywords: Engraulis ringens, eggs, temperature, interannual distribution, north-central Chile.


RESUMEN. En la zona centro-norte de Chile (25,0°- 31,5°S), se analizaron muestras de zooplancton en 100 estaciones oceanográficas de seis cruceros oceanográficos efectuados en febrero de los años 2008, 2009, 2010, 2011, 2013 y 2014. De las muestras se separaron y contabilizaron los huevos de Engraulis ringens, para determinar su distribución, abundancia, variación interanual y la relación con la temperatura superficial del mar y concentración de clorofila-a. La distribución de los huevos fue preferentemente costera, con máximas concentraciones en estaciones ubicadas próximo a Caleta Esmeralda (26°S) y Caleta Chañaral (29°S). En esta serie de tiempo, que incluye periodos fríos y cálidos, se estableció la relación de estas variables biológicas con rangos definidos de temperatura (16,1°-18,0°C).

Palabras clave: Engraulis ringens, huevos, temperatura, distribución interanual, centro-norte de Chile.


 

INTRODUCTION

Engraulis ringens is an anchovy species with a wide latitudinal distribution across the southwestern Pacific and an important standing in the regional fishing industry (Castro et al., 2000; Canales & Leal, 2009; Soto-Mendoza et al., 2010). Three E. ringens populations have been found, with the distribution of these populations being 1) northern and central Peru, 2) southern Peru, and 3) northern and south-central Chile (Canales & Leal, 2009). Canales & Leal (2009) also found a fishing stock of this species in north-central Chile (25 and 32°S) that has an independent population unit that recruits, grows, and reproduces in the area.

This species spawns near the ocean surface (0-40 m). Maximum spawning for E. ringens primarily occurs along the coastline at a depth of 20 m (Lett et al., 2007; Braun et al., 2007, 2008, 2009) between August and March, with peaks occurring at the end of the Austral winter (August-September) and during the Austral summer (February-March) (Cubillos et al., 1999; Perea et al., 2011; Hernández-Santoro et al., 2013). The spawning, abundance, and egg distribution in plankton of E. ringens have been related to a number of environmental variables, including temperature, salinity, chlorophyll-a levels, and upwelling (Escribano et al., 1996; Braun et al., 2007; Tarifeño et al., 2008; Soto-Mendoza et al., 2010; Claramunt et al., 2012).

Nevertheless, spawning has not been uniquely associated with any of these or other environmental variables, which is a product of this species wide latitudinal distribution, broad spawning period, and the existence of discrete populations within the distribution area. These variances, in turn, are the result of the diverse range of environmental variables existing within the geographical areas of this species.

Among the determined environmental variables, the temperature at which spawning occurs has evidenced recurring patterns, with spawning in northern Chile occurring between 15 and 18°C and in south-central Chile, between 12 and 15°C (Tarifeño et al., 2008). Tarifeño et al. (2008) additionally linked spawning with the lower temperatures that occur in upwelling zones, which are also nutrient rich.

By evaluating the second spawning (February) of E. ringens over a number of years, the present study associated E. ringens egg abundances and distributions with ocean surface temperature and chlorophyll-a concentration.

MATERIALS AND METHODS

Zooplankton samples were taken onboard the research vessel B/C Abate Molina of the Instituto de Fomento Pesquero (IFOP) in February 2008, 2009, 2010, 2011, 2013, and 2014 (Fishery Improvement Project [FIP]: Evaluación hidroacústica del reclutamiento de anchoveta entre la III y IV Regiones). Samples were collected at 80 oceanographic stations located 1, 5, 10 and 20 nm (nautical miles) from the coast and at an additional 20 oceanographic stations located 1 nm from the coast. All stations were distributed within 20 transects perpendicular to the coast between Paposo (25.0°S) and Puerto Oscuro (31.5°S), Chile (Fig. 1). The stations were always sampled from north to south during the first and last days of February each year (25 consecutive days).



Figure 1. Sampling stations location. Samples were taken during February 2008, 2009, 2010, 2011, 2013, and 2014.

 

Bongo nets (59 cm diameter, 300 pm mesh) equipped with flowmeters were used to collect zooplankton between the surface and a depth of 70 m, or 10 m from the bottom at sites with a lesser depth. The samples were preserved with a formalin solution in 5% seawater, from which E. ringens eggs were separated and quantified (number of eggs 100 m "3). The abundance, dominance, and frequency of E. ringens eggs were determined overall and in regards to site distance from the coast (1, 5, 10, and 20 nm).

Ocean surface temperature and integrated chlorophyll-a (chl-a) levels (0-100 m), obtained from Castillo et al. (2009a, 2009b, 2010, 2012, 2013) and Leiva et al., (2014), were related to E. ringens egg abundances, distributions, and frequencies through Q coefficient analysis (Van der Lingen et al., 2001; Bernal et al., 2007; Claramunt et al., 2012). For this, five temperature ranges (≤14; 14.1-16; 16.1-18; 18.120; and >20°C) and six chl-a ranges (≤20; 20.1-40; 40.1-60; 60.1-80; 80.1-100; and > 100 mg m-2) were established.

where n° hr: number of eggs in the r range (temperature or chlorophyll-a), n° ht: total number of eggs, n° estr: number of sampling stations in the r range, and n°estt: total number of sampling stations.

To determine statistically significant differences of Q within the distinct temperature ranges, chl-a ranges, and sampling years, the normal distribution of the dependent variable (Q) was confirmed by the Kolmogorov-Smirnov test while homoscedasticity was verified by the Lavene test (P < 0.05).

Following this, randomized blocks of the sampling years (2008, 2009, 2010, 2011, 2013, and 2014) were tested with an analysis of variance, using years, temperature range, chl-a, and the variable response to Q as factors. Significantly different variables were later analyzed by a Tukey test.

Since the maximum values of the Q coefficient were found within different chl-a range in different sampling years, Bootstrap analysis was used to confirm randomization and to verify if the maximum Q value was significant for each year.

RESULTS

The greatest total abundance of E. ringens eggs (>150,000 eggs 100 m-3) was found during February 2010, reaching an order of magnitude greater than the other years (Table 1). Egg frequency was within 15 and 32% at each sampling station. Egg distributions showed similar patterns for all years, with preferential distri-bution towards coastal sites. The dominance at stations 1 nm from the coast was always greater than 94%.

Table 1. E. ringens egg abundance (number of eggs 100 m-3), dominance (%), and frequency (%) at the sampling stations, grouped by distance from the coast.


Engraulis ringens eggs were collected along the coastline from the extreme northern zone of the study area (25°S) to the Bay of Tongoy (30°10’S). Only in February 2008 were eggs collected south of the Bay of Tongoy, and the distribution of eggs at these sites was notably different than at more northern sites, evidencing the minimum recorded values of abundance and frequency found over the years studied (Fig. 2). The zone between Caldera and Chañaral Cove (27-29°S) generally showed low egg abundances, and in February 2008, no E. ringens eggs were found. However, in February 2010, 2013, and 2014, eggs were found in these zone even at the most coastally distant stations (Fig. 2).



Figure 2. Engraulis ringens egg distribution and abundance within the Samplingarea. Samples were taken during February 2008, 2009, 2010, 2011, and 2014)

The maximum egg abundances were always recorded at stations 25 and 70, both of which were coastal and located south of Esmeralda Cove (26°S) and Chañaral Cove (29°S), respectively. Only in February 2013 were eggs not collected from station 70 (Figs. 1-2).

The surface temperature at the different stations was between 13 and 24°C, with a clear north-to-s|outh gradient and extreme values in February 2013 (Castillo et al., 2009a, 2009b, 2010, 2012, 2013; Leiva et al., 2014) (Fig. 3). Regarding integrated chl-a, maximum values (>400 mg m-2) were recorded in February 2013. In the first three years of study (2008, 2009, and 2010), chl-a values were between 20 and 100 mg m-2 (Fig. 4). In general, the lowest ocean surface temperatures and highest integrated chl-a were related to a greater upwelling index (Castillo et al., 2009a, 2009b, 2010, 2012, 2013; Leiva et al, 2014).


 


 

The Q coefficient was established between temperature ranges and the presence of E. ringens eggs over the years at all stations and at stations 1 nm from the coast. Values greater than 1 (greater affinity between variables) were found for temperature ranges between 16 and 18°C, with the exception of February 2013, where a greater association was established with a range of 18-20°C (Table 2).


Table 2. Q coefficient values presented for all sampling stations and those 1 nm from the coast, grouped by temperature range (°C).

 

On the other hand, the relationship established by the Q coefficient between the presence of eggs and the ranges of integrated chl-a levels (0-100 m), for all stations and for those located 1 nm from the coast, generated values higher than those established for the temperature ranges. This was especially notable for 2009 and 2010 (60-80 mg m-2). In these years, the majority of the eggs (65 and 44%) were found at stations 4 and 3, respectively (Table 3).


Table 3. Q coefficient values presented for all sampling stations and those 1 nm from the coast, grouped by integrated chlorophyll-a levels (0-100 m; mg m-2).


When using randomized blocks in the analysis of variance, statistically significant differences were established between the values of the Q coefficient and the temperature ranges for all years and in an integrated time-series, results which are contrary to that established for the ranges of chl-a (Table 4). After applying the Tukey test to the integrated time-series, it was possible to establish that the greatest affinities occurred between the temperature ranges 16-18°C and 18-20°C (Table 5). In contrast, the chl-a ranges did not evidence significant differences, with the highest affinities found for all ranges >3 (>40 mg m-2).


Table 4. Randomized blocks in analysis of variance applied to the Q coefficient values for temperature and chlorophyll-a.

 


Table 5. Affinity and significance (Tukey test, P < 0.05) between the temperature ranges of the Q coefficient values in the time-integrated series.



Given that the maximum values of the Q coefficient were found within different chl-a range over the studied years, a Bootstrap analysis was used to verify that the maximum Q value was significant for each year, in addition to confirming randomization. For this, 1000 bootstrap replications were performed, from which the maximum Q values were determined for each study year and for both the range of total chl-a for all stations and for stations 1 nm from the coast. This also indicated the respective frequency (F), probability (P), and 5% confidence interval for the estimated proportion of Q values (Tables 6-7).


Table 6. Bootstrap analysis between the Q coefficient values of chlorophyll-a range in the time-integrated series for all stations.


The occurrence probabilities for each Q value were found greater than 5% for all stations and for those located 1 nm from the coast. The maximum Q of the information for each sampling year was estimated by 1000 bootstrap replications, and, for 2008, 694 were found to be greater than or equal to 9,801. This result indicates that the occurrence probability of this value is 694/1000, or, in other words, that 69.4% of the iterations of the Q values were equal to 9,801. These calculations determined that the Q value was significant for 2008 and that this depended on the distribution of environmental and biological variables. Similar observations were made for the remaining sample years (Tables 6-7).


Table 7. Bootstrap analysis between Q coefficient values of the chlorophyll-a range in the time-integrated series for stations at 1 nm.


DISCUSSION

The sampling period (February) of E. ringens coincided with the second spawning of this species (Cubillos et al., 1999; Perea et al., 2011; Hernández-Santoro et al., 2013). Due to this, the obtained data regarding distribution, abundance, and interannual variation of the number of eggs collected are representative of the second spawning period.

The primarily coastal distribution of E. ringens eggs found by this study is consistent with Braun et al. (2007, 2008, 2009) and Soto-Mendoza et al. (2010). These authors reported the presence of E. ringens eggs near the ocean surface along the coastal zone within the entire distribution area of this species, with maximum presence found in northern Chile and southern Peru. In turn, the similar interannual distribution pattern of eggs corresponded with those areas showing greater adult abundances of this species, with two coastal sites (25-27°40’ and 29-30°10’S) consistently found as focal points for E. ringens (Castillo et al., 2009a, 2009b, 2010, 2012, 2013; Leiva et al, 2014).

The highest concentration of eggs was found in February 2010, coinciding with the lowest total abundance acoustically detected for this species, although the total biomass was the highest found over the sampling years (Castillo et al., 2010). A similar tendency was found in February 2013 (Castillo et al., 2013), thus involving the greatest proportion of adults in the biomass, which would explain the abundance of eggs. Regarding this, the distributions and abundances of the eggs collected over the different years of study were related to the highest proportions of adults, as acoustically detected over the same sampling periods (Castillo et al., 2009a, 2009b, 2010, 2012, 2013, Leiva et al., 2014). Moreover, the adult distribution of this species is in line with the sites that had the highest egg concentrations; the coast south of Esmeralda Cove (26°S) and Chañaral Cove (29°40’S), corresponding to stations 25 and 70, respectively. The exception to this tendency, in February 2013 at station 70, could be a result of the predominance of juvenile recruits acoustically detected during this year (Castillo et al., 2013).

A number of authors have related spawning and the abundance of E. ringens eggs with environmental variables and oceanographic events. Escribano et al. (1996) found that in northern Chile, E. ringens spawning is associated with lower seawater temperatures related to upwelling events. In contrast, Claramunt et al. (2012) indicates that temperature is not a relevant variable for determining the geographic position of spawning sites for E. ringens and that high chlorophyll-a concentration is the variable that determines changes in the spawning site. On the other hand, in the zone between Constitución (35°20’S) and Talcahuano (36°42’), Soto-Mendoza et al. (2010) did not find a relationship between salinity and the abundance of E. ringens eggs and larvae, observing instead that greater egg concentrations can be found outside of the continental water plumes.

Within the period assessed by the present study, Castillo et al. (2013) detected colder (February 2008, 2009, and 2011) and warmer (February 2010 and 2013) years, which can be related to the interannual variation of the Humboldt current (Escribano et al., 2002). Associated with this, greater abundances of E. ringens eggs were found during the warmer years within the evaluated time period.

The integrated chl-a value generally followed the previously indicated interannual ocean surface tempe-rature variations. However, some latitudinal variations were found for chl-a level that did not align with egg distributions and abundances in the evaluated years. Regarding this, Claramunt et al. (2012) found wide variations between temperature and chl-a ranges and the spawning sites of this species, in relation to both the zones analyzed (northern and southern Chile) and whether the studied year evidenced the El Niño phenomenon or not.

The wide latitudinal distribution of this species along the coasts of the south Pacific (Castro et al., 2000; Canales & Leal, 2009; Soto-Mendoza et al., 2010; Medina et al., 2015), the two reported spawning periods (August-September and February-March) (Perea et al., 2011), and the association of spawning with different temperatures (Escribano et al., 1996; Claramut et al., 2007; Soto-Mendoza et al., 2010) indicate that different fractions of the E. ringens stock spawn under different environmental conditions. During the assessed period, which covered a wide area of distribution (25-31°S) in February (summer spawning) of consecutive years, use of the Q coefficient established that the abundance of eggs was related to ocean surface temperature (16.1-18.0°C in February 2008, 2009, 2010, 2011, and 2014), as well as to the total number of stations and those located 1 nm from the coast. In February 2013, abundance was related to a temperature range of 18.1-20.0°C.

The relationship between egg abundances and the indicated temperature ranges, as supported by the Q coefficient and statistical analyses, is consistent with previous studies, where during the same study period Castillo et al. (2013) identified hotter and colder years.

ACKNOWLEDGEMENTS

This study was funded by projects awarded by the Fondo de Investigación Pesquera (FIP) 2007-03; 200802; 2009-03; 2010-03; 2012-13; and 2013-04 (Evaluación hidroacústica del reclutamiento de anchoveta entre la III y IV Regiones). The authors would also like to thank the support provided by the Instituto de Fomento Pesquero (IFOP) that, in partnership with the Universidad Católica del Norte, permitted us to obtain the information used as a starting point for this study. We would also like to thank the crew of the IFOP research vessel B/C Abate Molina and the personnel who aided in sample collection.

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Received: 3 March 2014; Accepted: 26 October 2015.

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