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Revista de biología marina y oceanografía

On-line version ISSN 0718-1957

Rev. biol. mar. oceanogr. vol.51 no.2 Valparaíso Aug. 2016 



Seasonal dynamics of zooplankton in a northern Chile bay exposed to upwelling conditions

Dinámicas estacionales del zooplancton en una bahía de la zona norte de Chile expuesta a condiciones de surgencias


M. Loreto Torreblanca1,Iván Pérez-Santos1,2,3, Bruno San Martín1, Eduardo Varas1, Rodrigo Zilleruelo1, Ramiro Riquelme-Bugueño1,4,5 and Álvaro T. Palma1,6,7*

1Fisioaqua, Avenida Vitacura 2909, oficina 717, Las Condes, Santiago, Chile. *
2Centro i~mar, Universidad de Los Lagos, camino a Chinquihue km 6, Puerto Montt, Chile
3Programa COPAS Sur-Austral, Universidad de Concepción, Campus Concepción, Victor Lamas 1290, Concepción, Chile
4Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
5Instituto Milenio de Oceanografía, Universidad de Concepción, Concepción, Chile
6Universidad Gabriela Mistral, Ricardo Lyon 1177, Providencia, Santiago, Chile
7Programa CAPES, Pontificia Universidad Católica de Chile, Av. Libertador Bernardo O'Higgins 340, Santiago, Chile


Debido al creciente uso del borde costero con fines industriales, particularmente aquellas actividades que utilizan cantidades importantes de agua de mar, es fundamental entender la composición de la fauna planctónica junto con reconocer su variabilidad espacial y temporal en función de variables hidrográficas relevantes. Totoralillo Norte (~30°S) es un bahía localizada dentro de un área comúnmente afectada por eventos de surgencia, así como una zona que se proyecta relevante para el desarrollo industrial. Aquí se realizaron muestreos estacionales (varios días en cada estación) durante 2013 y 2014 donde se pudo reconocer una comunidad zooplanctónica abundante con una buena representación de los principales taxa, conformada por al menos 166 especies. Los copépodos dominaron en términos numéricos el holoplancton (91,7%), mientras que el meroplancton estuvo compuesto principalmente por estadios larvales de cirripedios, moluscos, decápodos, briozoos y peces. A pesar de ser una zona de la costa normalmente afectada por eventos de surgencia, la abundancia del zooplancton fue elevada durante todo el año, incluso durante períodos dominados por vientos débiles y condiciones de hundimiento. Estudios como este ayudan a develar patrones ecológicos relevantes así como procesos que los afectan; información vital y que debe ser considerada al momento de evaluar impactos ambientales.

Palabras clave: Bahía, surgencia, holoplancton, meroplancton, diversidad del zooplancton


Due to the ever-increasing use of the coastline for industrial purposes, particularly by those activities that take up great amounts of sea water, it is fundamental to understand the composition of the planktonic fauna and its natural spatial and temporal variability in relation to hydrographic variables, in order to understand the potential impact of such undertakings. Totoralillo Norte (~30°S) is an embayment located within a well-known area of recurring upwelling events, as well as a zone with projection for industrial development. Here we performed seasonal surveys (several days sampling within each season) during 2013 and 2014 recognizing an abundant zooplanktonic community with a good representation of the main taxa comprised by at least 166 species. In terms of numbers, copepods dominated the holoplankton (91.7%), whereas meroplankton was mainly composed of larval stages of barnacles, mollusks, decapods, bryozoans and fish. In spite this being a coastal zone normally affected by upwelling events, zooplankton abundance was high throughout the year, even during periods dominated by weak winds and downwelling conditions. Studies such as this can help unveil relevant ecological patterns and their related processes; vital information that must be considered during an environmental impact assessments.

Key words: Bay, upwelling, holoplankton, meroplankton, zooplankton diversity


The increasing pressure on coastlines for all sorts of human development imposes the need for a detailed understanding of the ecological patterns of the organisms that inhabit these environments, as well as the processes involved. Many of these organisms either undergo a dispersive larval phase (meroplankton) or live throughout their ontogeny in the water column (holoplankton) near the coast. This diversity in life history strategies poses an additional challenge to the understanding of the characteristics and determinants that affect their distribution and abundance.

The zooplankton community includes larval stages of organisms that become benthic after recruiting, whose population dynamics and community structure is directly determined by a variety of transport mechanisms (Morgan & Fisher 2010). In coastal areas transport mechanisms can intimately be related to: the dynamics of the Ekman layer during upwelling events (e.g., Poulin et al. 2002 a, b), the effect of wind over surface layers (e.g., Tapia et al. 2004), the presence of upwelling shadows (e.g., Marín et al. 2003, Roughan et al. 2005), occurrence of internal waves (Pineda 1994, 2000) or vertical migration of organisms (e.g., Marta-Almeida et al. 2006, Palma et al. 2011). Within this wide array of processes, upwelling events are among the principal determinants of advection or larval positioning, being both frequent and intense, and affecting the coastal dynamics in the north, north-central and south-central areas of Chile (Montecino & Quiroz 2000, Moraga et al. 2001, Poulin et al. 2002a, Rutllant et al. 2004, Montecino et al. 2005, Marín et al. 2007).

In north-central coastal Chile, the Coquimbo area (~30°S) represents a well-known area of coastal upwelling (Montecino & Quiroz 2000, Moraga et al. 2001, Montecino et al. 2005), where filaments of sub-superficial waters frequently form due to wind as well as `jet' type flows that contribute to an increased availability of nutrients in the coastal area (Marín et al. 2003a, 2007). In contrast, during periods of calm [from wind intensity] an increase in residence time of dominant currents occurs (Marín et al. 2007). These dynamics represent the main physical factors that affect the circulation patterns on the Chilean coastal zones, and that are thus of potential impact to the planktonic communities therein.

Several studies in northern Chilean coastal areas discuss overall aspects of regional oceanography (e.g., Escribano et al. 2004, Thiel et al. 2007), others emphasize the relationship between zooplankton and conditions associated to upwelling episodes (i.e., Escribano & Hidalgo 2000, Escribano et al. 2001, Giraldo et al. 2002). Regardless of these generalized studies, basic and detailed information regarding local circulation patterns, as well as descriptions of planktonic communities in coastal areas (i.e., bays and headlands), are scarce (i.e., Palma et al. 2006). Semi-protected embayment systems can display characteristic circulation patterns that have as defining factors the degree of exposure to general oceanographic conditions (Acuña et al. 1989, Palma et al. 2006, 2009). Fairly recent studies describe the effect that smaller bays and geographic barriers have over local circulation and/or planktonic distribution patterns along the coastline (Mace & Morgan 2006a, b; Palma et al. 2006, Vander Woude et al. 2006, Henríquez et al. 2007, Palma et al. 2009, Morgan & Fisher 2010).

Given the above background information and the importance that embayments represent for new investment projects along the coast in general, our primary objective is to provide a seasonal description of the zooplanktonic community present in a semi-protected bay in the north of Chile along with the variability of hydrographic patterns at the same scales. To ensure this, the focus was placed on identifying spatial distribution and abundance patterns of planktonic organisms, as well as their relationships to relevant environmental variables (i.e. water column thermal structure, wind patterns). The underlying hypothesis being that an important part of the observed variance in the zooplanktonic community is related to major hydrographic forcing such as upwelling events. To date there are no comprehensive studies that describe the high diversity of the zooplankton present in smaller embayment systems and the related processes that could affect their spatial and temporal patterns of distribution and abundance. Furthermore, such information may deem relevant when decision regarding the implementation of man-made developmental projects (i.e. desalination plants, thermal power plants) could be guided/improved in order to minimize their environmental impact.



Study area and sampling procedures

Totoralillo Norte (29°45'S, 71°35'W; 29°49'S-71°35'W) is a semi-exposed embayment located in north-central Chile that was sampled every season in 2013: austral summer (15-20 January), fall (8-14 June), winter (14-19 August) and spring (November 30-December 8) as well as winter 2014 (10-13 July). We sampled several days within each season in order to capture as much of the inherent variability of the zooplankton distribution and abundance patterns. The bay was divided in several distinct zones with several sampling points within each one: 6 sampling transects at the northern bay, 5 sampling transects at the southern bay, 2 sampling transects outside the southern end of the bay, as well as 4 transects approximately 2 nautical miles offshore (Fig. 1). Only during fall and winter 2013 all the points were visited while fewer were considered during the reminding seasons (although the within-bay points were always sampled). In addition to the zooplankton samples, temperature, salinity and dissolved oxygen profiles were recorded by means of a Hydrolab DS-5 CTD, allowing for an accurate water column characterization of each point down to the maximum possible depth at each coastal point and reaching down to 50 m at the outer coastal points.


Figure 1. Area and location of the sampling stations indicating the bathymetry (m).
Depths from 0 to 60 m
Figura 1. Área y localización de las estaciones de muestreo indicando la batimetría (m).
Profundidades de 0 a 60 m


Wind data and derived variables

Wind data were obtained from a coastal meteorological station installed in Totoralillo Norte (29°29'30''S-71°19´16''W). Data were recorded every 5 minutes from January 2013 through November 2014. Original data were averaged on an hourly basis to calculate the wind-derived variables. A cumulative upwelling index was also considered here since it represents the summation of the daily mean upwelling indices that further highlights its potential relevance having local impact (Bograd et al. 2009).

The components of the zonal (τu) and meridional (τv ) wind stress were computed as follows:

where ρa is air density (1.2 kg m-3), Cd is a dimensionless drag coefficient, u and v are the zonal and meridional wind components, respectively, and U10 is the magnitude of the wind vector 10 m above sea level.

The drag coefficient was calculated using the formula proposed by Yelland & Taylor (1996), in which the coefficient varies as a function of the wind velocity. The average wind speed was 2.92 m s-1, with an absolute maximum of 11.1 m s-1.

Finally, the upwelling index, Mx (m3 s-1× 100 m), was calculated for the complete time series using the equation (Bakun 1975):

where τv is the meridional wind stress vector, ρw is the water density (1025 kg m-3), and f is the Coriolis parameter.

Temperature time series

A mooring with a thermistor chain of 5 Hobo Tid bits (Onset Computers) positioned at 4, 11, 16, 19 and 25 m was installed in a central part of the bay at a depth of ~30 m (Fig. 1). Temperature was recorded every 15 min from October 2012 to October 2014, with a resolution of 0.02°C and accuracy of ± 0.21°C.

Zooplankton abundance and distribution

In each sampling point, zooplankton was collected by means of 3 distinct nets, all of them having the same mesh size (210 µm).The surface layer (0-5 m) was sampled by use of an epineustonic net, towed along a transect of approximately 150 m in length. The subsurface layer (5-10 m) was sampled by use of a bongo net, towed along the same transects. At the end of each transect, a WP-2 net was vertically trawled to capture zooplankton from the bottom layers (>10 m). Each net was equipped with a Hydrobios flowmeter to estimate the volume of water filtered during each tow.

All samples were maintained at constant temperature until preserved in a solution of formaldehyde (10%) 24 h after collection and then transferred to a solution of alcohol for a better handling while identifying and quantifying organisms. Once in the laboratory, plankton samples were identified and quantified following the methodology proposed by Boltovskoy (1981), Olivar & Fortuño (1991) and Palma & Kaiser (1993). All zooplankton specimens were counted and identified using Olympus series SZ stereomicroscopes. Each individual was identified and counted with exception of copepods and sometimes decapod crustacean zoea larvae where a Folsom splitter was used, counting the fraction range of 1/2-1/64, depending upon the abundance of individuals in a single sample. Abundances were standardized to 100 m-3. Abundance of all 3 nets used was added in order to obtain the integrated abundance of zooplankton throughout the water column. Total abundance in the water column was then averaged by the number of days surveyed during each seasonal sampling, thus allowing comparisons between seasons.

Statistical analysis

All datasets were examined for normality using the Kolmorogov-Smirnov test. Abundance datasets were non-normal distributed and therefore non-parametric statistical analyses were applied. We assessed seasonal and upwelling-related changes in the community structure and the abundances by zooplankton group. For community structure analyses, a classical approach from Field et al. (1982) and Clarke & Warwick (2001) using PRIMER v6 software (Clarke & Gorley 2006) was used. Prior to the analyses, samples from the stations common to all the sampling times were selected in order to obtain results consistent and statistically comparable. After that, the data were fourth root transformed to normalize the variance while preserving distances among low values (Field et al. 1982). To test the hypothesis for differences in the community structure among samples from different time periods (seasons) and upwelling regimes, we applied a similarity analysis (ANOSIM test). ANOSIM is a permutation-based nonparametric test (analogue to a one-way analysis of variance), which performs average ranked values of Bray-Curtis measures of dissimilarity in abundances among and within samples. The R statistic is scaled to lie between -1 and +1, where zero represents the null hypothesis of no differences among a set of samples (Clarke 1993). For abundances of zooplankton groups, statistical differences were assessed with the Kruskal-Wallis test. The descriptive statistical summary presents the median and quartiles (25 and 75%) as central tendency and deviation measures, respectively.

Cumulated Ekman transport was computed as described previously where negative values represent offshore transport or coastal upwelling. Average values were used for each sampling season. Cumulated Ekman transport values were categorized as downwelling (DWN, ≈14,000 m2 s-1), weak upwelling (LUP, ≈ -20,000 m2 s-1), moderate upwelling (MUP, ≈ -40,000 m2 s-1) and strong upwelling (HUP, ≈ -80,000 m2 s-1).

The BEST analysis (in Primer software) was applied in order to select the taxa (zooplankton groups) that best correlate with the Cumulated Ekman transport. The BVSTEP stepwise algorithm was used to search the zooplankton groups (best subset) with >0.95 and <0.001 P-values as removal and addition criterions, respectively.



Physical setting characterization

The thermal structure of the water column in Totoralillo Norte presented a clear pattern of higher stratification during the warmer months while during the cooler months there was a higher degree of mixing (Figs. 2a-f). During spring and summer frequent periods of warming and cooling were detected, the highest temperatures were recorded during the summer period (18°C) and spring only presented moderate warming of the water column (~14°C) (Figs. 2b, e). A Fourier analysis of the temperature data collected showed that the fluctuations corresponded mostly to daily cycles, particularly evident from the 4 and 16 m signals (Fig. 2g). The wind stress data exhibited a defined seasonal pattern with periods of high winds (especially zonal) with peaks of intensity during the spring and summer seasons (Figs. 3a, b). Although the upwelling index during these periods was high (Fig. 3c), wind stress averaged during other seasons was not markedly lower. Spectral analysis of the complete wind series recorded at this location revealed prevalence of diurnal and semi-diurnal frequencies (Fig. 3d).


Figure 2. (a) Thermistor chain time series obtained in Totoralillo Norte bay from October 2012 through October 2014. Dots represent the vertical position of the temperature sensors and triangles represent the dates of the different campaigns. (b-f) Daily vertical temperature records obtained during each seasonal campaign. (g) The Fourier spectral analysis to the surface (4 m), middle (16 m) and bottom (25 m) time series
Figura 2. Series de tiempo de la cadena de termistores obtenidos en la bahía Totoralillo Norte desde octubre 2012 a octubre 2014. Los puntos negros representan la posición vertical de los sensores de temperatura y los triángulos representan los datos de las diferentes campañas. (b-f) Registros verticales diarios de la temperatura obtenida durante cada campaña estacional. (g) Series de tiempo del análisis espectral de Fourier en la superficie (4 m), capa media (16 m) y fondo (25 m)


Figure 3. Monthly mean of the (a) zonal and (b) meridional wind stress obtained from the coastal meteorological station in period January 2013 to January 2014. (c) Monthly mean of upwelling index and (d) Fourier spectral analysis to the zonal and meridional wind stress
Figura 3. Promedio mensual de (a) estrés de viento zonal y (b) meridional obtenido de la estación metereológica costera durante Enero 2013 a Enero 2014. (c) Promedio mensual del índice de surgencia y (d) análisis espectral de Fourier del estrés del viento zonal y meridional


During summer 2013 there was a dominance of winds favorable to the occurrence of upwelling events, and during the sampling period (15-20 January) there were 3 distinguishable upwelling events episodes (Fig. 4a). On the other hand, during fall 2013, winds with weaker characteristics for producing upwelling events alternated with downwelling conditions, albeit during the sampling period (8-14 June) the upwelling index was noticeably at least in 4 opportunities (Fig. 4b). During the winter season of 2013 a scenario similar to the one described for the previous fall was observed, although during August upwelling favorable winds were more dominant, and in at least 3 occasions this occurred during the sampling period (14-19 August, Fig. 4c). During spring, as in summer, there was a predominance of upwelling favorable winds, however during the sampling period diurnal cycles of strong upwelling (7 such events) alternated with downwelling conditions (Fig. 4d). During winter 2014 downwelling conditions predominated, although 2 consecutive days (12-13 July) of upwelling conditions were registered during the sampling period (Fig. 4e).


Figure 4. (a-e) Hourly upwelling index (black lines) derived from in-situ wind data (grey lines). Arrows indicate the starting and ending dates, respectively, for the sampling period within each season. Right panels depict the average wind direction during the month of the respective surveys
Figura 4. (a-e) Índice de surgencia por hora (líneas negras) derivado de los datos de viento in-situ (líneas grises). Las flechas indican los datos iniciales y finales, respectivamente, para el periodo de muestreo dentro de cada estación del año. Paneles a la derecha representan la dirección promedio del viento durante el mes de las mediciones respectivas


The above patterns are further examined and corroborated following the approach proposed by Bograd et al. (2009), whereby the cumulative upwelling index allows for a sounder distinction of the upwelling favorable periods with summer, winter 2013 and spring being the clearest ones (Fig. 5).


Figure 5. Cumulative upwelling index for the surveyed periods. The sampling period are marked with arrows. Black/grey shaded areas denote favorable upwelling/downwelling conditions
Figura 5. Índice de surgencia acumulado para los períodos analizados. Los períodos de muestreo se marcan con flechas. Áreas negro/gris indican condiciones de surgencia/ hundimiento


Zooplankton community composition

From a total of 166 taxa that were encountered, 123 (74.1%) were identified at the species level, 39 (23.5%) at the level of genera and 4 (2.4%) at other lower taxonomic levels, and categorized as follows: 48 holoplankton taxa, 8 meroplankton taxa, 51 copepods (separated from the rest of the holoplankton due to their high abundance), 35 decapods larvae, and 24 taxa of ichthyoplankton (eggs and larvae). Throughout the study period, a total of 55 taxa (33.5% of the total) of the above mentioned were present in every season (Table 1).

Zooplankton distribution and abundance

The abundance of the principal groups occurring within Totoralillo bay as well as outside its boundaries varied greatly throughout the study period. Summer 2013 registered the lowest overall abundance of zooplankton (< 490000 ind. 100 m-3), while the highest was observed during winter 2014 (< 5950000 ind. 100 m-3) (Fig. 6). Copepods were always the most abundant group over the study period (65.3%) mainly represented by Acartia tonsa and Paracalanus cf. indicus, followed by meroplankton (17.6%), independently from where samples were collected.


Figure 6. Average abundance (individual 100 m-3) for each zooplankton category from summer 2013 to winter 2014 in Totoralillo Norte Bay. Letters identify position of the different sampling points. E= Exterior, S-E= Southern exterior, S-B= Southern bay, N-B = Northern bay (see Fig. 1 for details)
Figura 6. Abundancia promedio (individuos 100 m-3) para cada categoría de zooplancton desde verano 2013 hasta invierno 2014 en la bahía Totoralillo Norte. Letras identifican la posición de los diferentes puntos de muestreo. E= Exterior, S-E= Exterior sur, S-B= Bahía sur, N-B= Bahía norte (ver Fig. 1 para detalles)


These patterns can be graphically appreciated when reviewed as total abundance at each of the sampling points over each of the sampling periods (Fig. 7). Noteworthy is the high abundance of zooplankton within the bay of Totoralillo Norte during winter 2014, although no sampling was conducted outside of the bay during that period. When samples were taken from all points, including those outside the bay, highest abundances were always recorded in the points closest to the coast, regardless of seasonality. From a seasonal perspective, copepods were numerically dominant throughout the study, although exhibited greater abundance during fall and winter periods of each year. The holoplankton, meroplankton and fish eggs did not show marked differences among seasons, although their abundance was higher during the winter 2014. Decapods exhibited a remarkable higher abundance during the winter 2014 season while fish larvae were fairly well represented during all seasons except spring, and fish larvae exhibited some abundance peaks during winter 2013 (Fig. 7).

Zooplankton community structure and abundance dynamics

Numerically the zooplankton was more abundant in samples collected during the winter 2014 than during the remaining seasons. A descriptive statistical summary for zooplankton group abundances is shown in Table 2. Throughout this study zooplankton abundance was highly variable in the study area, ranging from 0 in the case of fish larvae to >1 million of individuals per 100 m3 in the case of copepods. The latter group accounts for 64% of the overall zooplankton abundance followed by meroplankton which accounted for 22% in abundance. Differences in the community structure between seasons were statistically significant (ANOSIM test, Global R= 0.249, P < 0.0001) as well as among different wind regimes (ANOSIM test, Global R= 0.194, P < 0.0001) (Table 3).


Table 2. Statistical summary for zooplankton abundance by category (Individuals 100 m-3) in relation to seasons and wind regimes (cumulated Ekman transport, CET) in Totoralillo Norte Bay, northern Chile. CET values were categorized as downwelling (DWN,14,000 m2 s-1), weak upwelling (LUP, -20,000 m2 s-1), moderate upwelling (MUP, -40,000 m2 s-1) and strong upwelling (HUP, -80,000 m2 s-1). Q25 and Q75 indicate 25 and 75% quartiles, respectively
Tabla 2. Resumen estadístico de la abundancia de zooplancton por categoría (Individuos 100 m-3) en relación a estaciones del año y regímenes de viento (Transporte de Ekman acumulado, CET) en bahía Totoralillo Norte, Norte de Chile. Valores CET fueron categorizados como convergencia (DWN,
14,000 m2 s-1), surgencia débil (LUP, -20,000 m2 s-1), surgencia moderada (MUP, -40,000 m2 s-1) y surgencia fuerte (HUP, -80,000 m2 s-1). Q25 y Q75 indican los cuartiles 25 y 75% respectivamente


Table 3. Analysis of similarity (ANOSIM) showing Global R and pairwise test for differences among seasons and wind regimes (cumulated Ekman transport, CET) in Totoralillo Bay, northern Chile. CET values were categorized as downwelling (DWN,14,000 m2 s-1), weak upwelling (LUP, -20,000 m2 s-1), moderate upwelling (MUP,-40,000 m2 s-1) and strong upwelling (HUP,-80,000 m2 s-1)
Tabla 3 Análisis de similitud (ANOSIM) que muestra el R global y comparaciones pareadas para diferentes estaciones del año y regímenes de viento (Transporte de Ekman acumulado, CET) en bahía Totoralillo Norte, norte de Chile. Valores de CET fueron categorizados como convergencia (DWN,
14,000 m2 s-1), surgencia débil (LUP, -20,000 m2 s-1), surgencia moderada (MUP, -40,000 m2 s-1) y surgencia fuerte (HUP, -80,000 m2 s-1)


In relation to the changes observed in the zooplankton abundances, the Kruskal-Wallis test (multiple comparisons) showed statistical differences between seasons and upwelling regimes (Table 4). Strongest statistical differences (P < 0.00001) were observed between contrasting seasons (e.g., summer versus winter) and a higher influence of moderate and weak upwelling events than strong Ekman transport (Table 4).


Table 4. Kruskal-Wallis test of multiple comparisons for statistical differences in the zooplankton abundances between seasons and upwelling regimes in Totoralillo Norte Bay, northern Chile. CET values were categorized as downwelling (DWN, 14,000 m2 s-1), weak upwelling (LUP, -20,000 m2 s-1), moderate upwelling (MUP, -40,000 m2 s-1) and strong upwelling (HUP, -80,000 m2 s-1). NS, no significant
Tabla 4. Test de Kruskal-Wallis con comparaciones múltiples para diferencias estadísticas en las abundancias del zooplancton entre estaciones y regímenes de surgencia en bahía Totoralillo Norte, Norte de Chile. Valores de CET fueron categorizados como convergencia (DWN,
14,000 m2 s-1), surgencia débil (LUP, -20,000 m2 s-1), surgencia moderada (MUP, -40,000 m2 s-1) y surgencia fuerte (HUP, -80,000 m2 s-1). NS, valor no significativo


The non-parametric stepwise multiple regression (BEST analysis) indicates that holoplankton, meroplankton, decapods, fish eggs and copepods were the groups that best correlated with the Ekman transport (Global R= 0.99; correlation= 0.990; P-value= 0.001), which confirms the influence of coastal upwelling regime on the zooplankton community.



The present study not only provides a detailed and exhaustive list of zooplankton species present in the bay of Totoralillo Norte, but also describes its variability at different spatial (bay-scale) and temporal (seasonal) scales. Similar studies exist along the coast of Chile, where detailed patterns of distribution and abundance together with related forcing factors (i.e., wind-driven currents) are provided, although they are generally restricted to a specific group within the zooplanktonic community (i.e., copepods, Escribano & Hidalgo 2000; gelatinous zooplankton, Palma & Apablaza 2004; decapod, meroplankton, Palma et al. 2006). Similar such efforts have also been carried out at other latitudes (i.e., California). However, only patterns of distribution and abundance and related processes for single or reduced groups of species were described (i.e. Roughan et al. 2005, Mace & Morgan 2006a). Seasonal differences in plankton composition and biomass have been described from a variety of marine environments. In high latitudes like the Barents Sea this is mainly related to water mass circulation and bottom topography (Araskkevich et al. 2002) and in a tropical estuarine system in the Persian Gulf the observed changes were mainly related to salinity, chlorophyll a, temperature and pH differences (Farhadian & Pouladi 2014). Other examples of changes in plankton composition and abundance along coastal settings include a strong human-related pollution/eutrophication that alters natural seasonal changes (Kwang-Hyeon et al. 2009). Here, we describe the seasonal dynamics of the entire zooplankton community for an important spatial span of the coastal area, including sites close to shore (~200 m) to points well outside the bay of Totoralillo Norte (several km offshore) stressing on the relevance of hydrographic processes that not necessarily operate with similar strength on a seasonal basis. Such basic understanding of how a wide variety of zooplankton behaves both spatially and temporally is fundamental given the degree of anthropic intervention over coastal environments (Viles & Spencer 2014).

From October 2012 through November 2014, we uncovered a seasonal pattern regarding the thermal structure of the water column and prevailing winds of Totoralillo Norte Bay consistent with patterns of seasonal occurrence of upwelling conditions (i.e. peak upwelling typically observed during the Spring-Summer seasons) that have been described for this area of the Chilean coastline (Montecino & Quiroz 2000, Montecino et al. 2005, Letelier et al. 2009, Tapia et al. 2009). Moreover, the high temporal sampling frequency used in this study revealed that upwelling events can be frequent in this bay even in seasons (i.e., winter 2013) when they are least expected.

These wind stress patterns were integrated with zooplankton abundance data in order to assess how upwelling may determine the distribution and abundance patterns of zooplankton at these specific spatial (bay) and temporal (seasonal) scales (Tapia et al. 2004, Daneri et al. 2012). Generally, upwelling events result in higher plankton abundance towards the interior parts of bays (Mace & Morgan 2006a, b; Palma et al. 2006, Vander Woude et al. 2006, Morgan & Fisher 2010). The mechanisms by which this occurs are not evident, since superficial plankton should be transported off-shore by advection (Wing et al. 1995, Miller & Emlet 1997, Morgan & Fisher 2010, Morgan et al. 2012), but may be associated with the high retention rates at protected systems (Roughan et al. 2005, Mace & Morgan 2006a) or alternatively with the ability of certain groups within the zooplankton to move throughout the water column (i.e., daily vertical migration) and thus avoid being advected offshore (Poulin et al. 2002b, Sponaugle et al. 2002). For instance, in upwelling regions, upwelling shadows form in the lee of large headlands and are characterized by reduced local wind forcing, localized reversal of alongshore flow, and warm surface waters (Graham & Largier 1997). When the wind is not sufficiently diminished by a small headland (which is the case of Totoralillo) alongshore transport of surface water into the bay with recirculation at depth can occur, more so during upwelling events, and can promote retention of plankton, particularly the type capable of daily vertical migration (Roughan et al. 2005). Our results are coherent with such previous studies showing increased abundance in the inner part of Totoralillo bay. However, the novelty found here is that this pattern emerges not only on an annual basis, but during all seasons studied.

In this study, we found higher abundance of zooplankton in winter 2014 that were concomitant with downwelling prevailing conditions, particularly during the sampling period (i.e., 10-13 July 2014). Such an association between local wind patterns and zooplankton abundance may indicate that stronger winds do not necessarily imply higher zooplankton abundances, but rather calm or variable periods promote higher concentration of pelagic organisms by influencing (increasing) the retention times within bays like Totoralillo. Similarly, Cury & Roy (1989) demonstrated that fish larvae recruitment was highest at intermediate, rather than strong upwelling intensity in the Peruvian, California, Moroccon, and Senegalese upwelling systems.

We identified 166 taxa, highlighting the importance that these environments have for holoplanktonic species, and the role of such species in coastal trophic webs (Escribano 1998, Vargas et al. 2006, El-Sabaawi et al. 2010). This is also true for meroplankton, and emphasis should be placed in realizing how these coastal environments serve as breeding/nursery grounds for pelagic species (i.e., anchovies and sardines Hernández-Miranda et al. 2003) or nurseries for benthic species (i.e., decapod crustaceans Palma et al. 2006, mollusks Poulin et al. 2002a, b). If the prevailing physical conditions (i.e., occurrence of upwelling or downwelling favorable events) alongside other mechanisms -that determine the patterns of zooplankton distribution and abundance- are recurring; then it becomes of utmost importance to recognize that embayment systems, such as Totoralillo Norte, represent discrete, yet complex environments along the Chilean coast and their conservation should be a priority that future sustainable endeavors should embrace.



We are grateful to the colleagues and students that contributed to this study. Special thanks to the editorial committee of RBM&O and the comments provided by two anonymous reviewers for critical reviews of earlier drafts. During this research IP-S was funded by the FONDECYT grant 11140161 and COPAS SUR-AUSTRAL grant PFB-31. This study was supported by AndesIron Spa.



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Received 4 May 2015 and accepted 22 March 2016
Editor: Claudia Bustos D.

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