High frequency responses of nanoplankton and microplankton to wind-driven upwelling off northern Chile

Journal of Marine Systems 78 (2009) 124–135

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Journal of Marine Systems j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j m a r s y s

High frequency responses of nanoplankton and microplankton to wind-driven upwelling off northern Chile Victor Aguilera a,b,⁎, Ruben Escribano b, Liliana Herrera c a b c

Programa de Doctorado en Oceanografía, Departamento de Oceanografía, Universidad de Concepción, Chile Center for Oceanographic Research in the Eastern South Pacific (COPAS), Departamento de Oceanografía, Universidad de Concepción, Chile Departamento de Ciencias del Mar, Universidad Arturo Prat, Chile

a r t i c l e

i n f o

Article history: Received 22 August 2008 Received in revised form 18 April 2009 Accepted 27 April 2009 Available online 5 May 2009 Keywords: Community structure Nanoplankton Phytoplankton Inter-daily variability Northern Chile Upwelling Chile (21°–23° latitude south)

a b s t r a c t Autotrophic and heterotrophic nanoplankton and microplankton vary widely in quantity and composition in coastal upwelling zones, causing a highly heterogeneous distribution of food resources for higher trophic levels. Here, we assessed daily changes in size-fractioned biomass and community structure of nanoplankton and microplankton at two upwelling sites off northern Chile, Mejillones (23°S) and Chipana (21°S), during summer 2006, winter 2006 and summer 2007 as related to changes in oceanographic conditions upon upwelling variation. We found highly-significant changes in quantity and community structure (species diversity and richness) of both nanoplankton and microplankton fractions after 3–5 days of observations. These changes were coupled to an intermittent upwelling regime reflected in the alongshore component of the wind. After a few days the whole community was modified in terms of species and size structure. Overimposing this variability, during winter 2006 there was a strong perturbation of remote origin that substantially impacted temperature, oxygenation and stratification of the water column. This “abnormal” warming event altered the upwelling regime, but its impact on abundance and composition of the nanoplankton and microplankton fractions was uncertain. Over the short-time scale however, we found a strong coupling between daily changes in the alongshore component of wind and nanoplankton and microplankton abundances and their structure. All these findings indicate that despite the high biological productivity of this upwelling region, high frequency variation induced by wind forcing may be a major regulator of food resources (quantity and quality) for primary consumers, such as zooplankton, fish larvae and benthic organisms in the near-shore area. This high frequency variation may also impose a key constrain for prey–predator encounter rates and survival of short-lived zooplankton and invertebrate and fish larvae in the upwelling zone. © 2009 Elsevier B.V. All rights reserved.

1. Introduction Upwelling zones play a crucial role for the global climate system promoting not only a considerable biological capture of atmospheric carbon, but also constituting the main regions for marine productivity. One of these large marine ecosystems, the Humboldt Current System (HCS), has received increased scientific attention in the last decade (e.g. Thiel et al., 2007). In this region, much research effort has been devoted to oceanic circulation and water masses (Strub et al., 1998; Blanco et al., 2001, 2002), spatial–temporal variability of the upwelling process (Mesias et al., 2001; Silva and Valdenegro, 2003; Sobarzo and Djurfeldt, 2004), primary producers' successions (Herrera and Labbé, 1990; Herrera and Merino, 1992; Herrera and Escribano, 2006), effects on primary production (Daneri et al., 2000), secondary production and zooplankton biomass variability ⁎ Corresponding author. Departamento de Oceanografía, Universidad de Concepción, Casilla 160 C, Concepción, Chile. Tel.: +56 41 2204239; fax: +56 41 2256571. E-mail addresses: [email protected] (V. Aguilera), [email protected] (R. Escribano). 0924-7963/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.jmarsys.2009.04.005

(Escribano, 1998; Escribano and McLaren, 1999; Escribano and Hidalgo, 2000; Escribano et al., 2001, 2004). All this research represents a very complete and highly relevant body of basic environmental information for the Eastern South Pacific region. In the HCS at northern Chile the influence of the South Pacific Anticyclone generates permanent equatorward winds (Rutllant and Montecino, 2002) and primary production and the dynamics of the phytoplankton is largely governed by successive upwelling events, leading to dominance of chain-forming diatoms, interrupted by small size and flagellated cells during warm conditions of the water column (Herrera and Escribano, 2006). There are physical processes affecting the dynamics of autotrophic components, such as local wind pulses (Fonseca, 1989), the influence of oceanic currents on the near shore (Strub et al., 1998), remote forcing as coastal-trapped waves (Shaffer et al., 1997), or the El Niño Southern Oscillation over a larger scale (Ulloa et al., 2001; Escribano et al., 2004; Thiel et al., 2007). All these processes cause large variation in the distribution of autotrophic and heterotrophic components of plankton, giving rise to a strongly heterogeneous food resource for subsequent trophic levels, and

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explaining the pulsed productivity in the upwelling areas, as stressed by Peterson (1988), Pitcher et al. (1991) and Gómez-Gutiérrez and Peterson (1999). Among the processes controlling plankton dynamics, high frequency variability of the environment has not been studied in the upwelling zone off Chile. In the classical model of the upwelling process, the spin-up and spin-down phases of upwelling could be characterized by two kinds of autotrophic and heterotrophic assemblages. One specialized in exploiting conditions under turbulent and reduced nutrient conditions of the initial phase and another which is able to prevail in a more stable and productive water column (relaxation phase) (Hutchings et al., 1995). These upwelling phases may act as environmental disturbances which can cause rapid responses of the autotrophic and heterotrophic components of nanoplankton and microplankton, promoting fast changes in community descriptors as diversity, species richness and species abundances. The resulting pattern is a highly patchy and erratic food resource for primary consumers, such as zooplankton, meroplankton and fish larvae of the upwelling zone. The magnitude of this high frequency variation and its connection to the physical environment and has not been well studied in upwelling habitats. This information can prove as highly valuable for modeling the dynamics of the plankton compartment in the upwelling system. In this work, we assessed daily changes in sized-fractioned biomass and community structure of nanoplankton and microplankton size fractions from two upwelling sites off northern Chile. The study aims at testing the hypothesis that high frequency changes in community structure at low trophic levels of the planktonic system respond to physical forcing driven by upwelling variability. 2. Methods 2.1. The study area This study was conducted at two upwelling sites in the Chilean northern coast: Mejillones (23°S, 70.30°W) and Chipana (21°S,

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70.18°W) (Fig. 1). These localities are currently target sites for process-oriented studies under variable upwelling conditions carried out by the Climate Variability and the El Niño Southern Oscillation project (CENSOR, www.censor.name). At these places, four seasonal surveys were performed during 2006 and 2007. These are summarized as: 6 days of observations in Mejillones during summer 2006 (MESU06) with sampling at 0, 5 and 15 m depth; 8 days in Chipana during summer 2006 (CHSU06) with sampling at 0, 10 and 20 m depth; 8 days in Chipana during winter 2006 (CHWN06) with sampling at 0, 10, 20 and 45 m depth, and 8 days in Chipana during summer 2007 (CHWN07) with sampling at 5, 10 and 20 m depth. 2.2. Sampling and methods Samplings at each site were carried out at fixed stations in the near shore (ca. 5 km from the shoreline) at about 90 m depth. Oceanographic conditions were daily assessed with a SeaBird SBE19 Plus CTD equipped with oxygen sensor and a WetStar fluorometer. Temperature, salinity, dissolved oxygen and fluorescence profiles were daily recorded from near the bottom to surface. Water samples were obtained with 10 L Niskin bottles. Sized fractioned chlorophyll-a (Chl) b20 µm and N20 µm was measured with a TD Turner fluorometer after 300 mL subsamples was sieved with a 20 µm mesh and filtered onto GF/F filter. Chl was extracted in the dark for 24 h in 90% acetone v/v (Strickland and Parsons, 1972). For cell count and identification 125 mL of subsamples were preserved with acid Lugol's solution 2% (final concentration) and maintained in darkness; 50 mL aliquots were settled for 24 h in sedimentation chambers (Utermöhl, 1958), then cells were counted and identified under an inverted microscope Leica Leitz DMIL. This analysis included the identification of genera and specie level whenever possible. Nanoplankton composition (heterotrophic and autotrophic components) and its concentration were estimated from 20 mL subsamples, preserved with glutaraldehyde and stained with proflavine (Haas,

Fig. 1. The northern coastal upwelling region off Chile in the eastern South Pacific illustrating the location of Chipana and Mejillones, where nano- and microplankton studies were performed at the indicated fixed stations. The Chipana area constitutes the target upwelling site of the Climate Variability and the El Niño Southern Oscillation (CENSOR) Project.

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Fig. 2. Daily time series of temperature and dissolved oxygen at two locations, Chipana and Mejillones, off northern Chile for 4 seasonal surveys. A) Mejillones in summer 2006, B) Chipana in summer 2006, C) Chipana in winter 2006, D) Chipana in summer 2007. Contours were constructed from daily 1 m resolution CTDO profiles. Bold isolines represent depth of the 15 °C isotherm and depth of the oxygen minimum zone (1 ml O2 L− 1), respectively.

1982), then they were filtered onto 0.8 mm filters and cells were counted with a Zeiss A 100× microscope. Autotrophic and heterotrophic flagellates were distinguished and counted by means of their autofluorescence, although heterotrophs also included some mixotrophic cells. Phosphate (PO4) levels were determined following the Murphy and Riley's method modified by Koroleff (1983) using a HP 8453 spectrophotometer. Method 353.2 (EPA-600/4-79-020 Environmental Monitoring and Support Laboratory: Cincinnati) was considered using colorimetric detection for Nitrite (NO2) determination. Nitrate (NO3) and Silicate (SiO) determinations were made in according to Strickland and Parsons (1968) using a HP 8453 spectrophotometer. Hourly data of winds were obtained from two meteorological stations located in the area of each sampling site: Cerro Moreno (at 23°26′S–70°26′W) and Diego Aracena (at 20°32′S/70°11′W).

2.3. Data analysis Water column conditions, as influenced by upwelling variation, were assessed by using temperature, salinity and oxygen data from daily CTD profiles. Water density was derived from salinity and temperature as Sigma T. All CTD data were processed and illustrated through vertical profiles and contours made using 1 m bins for vertical resolution. Upwelling variation was also assessed with wind data. For this, the northern component of the wind (ty) was obtained from hourly winds. This component represents the alongshore wind favorable for upwelling. An index of net upwelling transport was estimated from daily integrated values of this north component of the wind. The impact of wind forcing causing upwelling and water column variation was also examined by estimating daily changes in depth of the 15 °C isotherm, which was located near the base of the thermocline in most situations. In order to better

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Fig. 3. Vertical profiles of temperature and water density (Sigma T) at 4 different surveys: MESU06 = Mejillones summer 2006, CHSU06 = Chipana summer 2006, CHWN06 = Chipana winter 2006, CHSU07 = Chipana summer 2007. Profiles are from 5 to 7 days averaged data at each survey.

quantify the stability of the water column an index of the intensity of the stratification was calculated as suggested by Bowden (1983) as,

3. Results 3.1. Oceanographic variability

Φ=

g H

Z

0

−H

ðρm − ρÞzdz

where Φ is an index of potential energy anomaly (J m− 3), H is the water column height (m), ρ is the density at any depth z, and rm is the mean density of the water column. This index estimates the deficit in potential energy due to a density gradient. A highly mixed water column will present small values of Φ. Water density was derived from temperature–salinity measurements. Integrated values of Φ were obtained for the 0–50 m layer for all stations having this depth or greater. Flagellate cells included silicoflagellates, dinoflagellates and nanoflagellates smaller than 20 µm, but for this size fraction only total abundance was considered in analysis, because data on species was not available. Diatoms and autotrophic/heterotrophic flagellate species (micro-nanoplankton assemblage hereby) were considered together to compare ecosystem descriptors. With daily phytoplankton assemblages, including data of cell mL− 1, the Shannon diversity index was computed as:

H V= −

n X

Daily variability in temperature and dissolved oxygen for both locations and seasons are shown in Fig. 2. Mean temperatures in the upper 40 m were between 15 °C and 19 °C and the coldest condition was observed during the summer in Mejillones (Fig. 2A). Deepening of the thermocline and the mixed layer were remarkable during winter 2006 in Chipana as reflected in the 15 °C isotherm (Fig. 2C). The upper boundary of the Oxygen Minimum Zone (OMZ) (1 mL O2 L− 1) was permanently within the upper 20 m (Fig. 2), possibly constraining the distribution of plankton near the surface layer, except during the

pi lnðpi Þ

i

where n is the number of species and pi is the abundance of each specie. Information on species composition was used to generate the Bray–Curtis similarity matrices for cluster analysis and also to obtain values for species richness (S) and total abundance (n). Oceanographic changes, as well as variability on a day-to-day scale in the biological communities were assessed by ANOVA when normality conditions could be met (Barlett test), and otherwise the non-parametric Kruskal–Wallis ANOVA was applied. To assess correlations between biological or community descriptors and environmental factors, multiple Spearman correlations, and regression analysis were performed in attention to variance distribution. Finally as to assess multiple effects of the oceanographic environment on day-to-day variability of the micro-nanoplankton community the exploratory, multivariate, Principal Component Analysis (PCA) was applied to non-transformed variables using the correlation matrix and without rotation. PCA was performed with the software STATISTICA version 8.0.

Fig. 4. The relationship between the daily accumulated alongshore wind and water column stratification (A) and depth of the 15 °C isotherm (B) from all pooled data after 4 seasonal surveys at Chipana and Mejillones (northern Chile). Dashed lines represent 95% confidence limits of the regression fittings.

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Fig. 5. Vertical distribution of macronutrients (in µM) at two locations, Mejillones and Chipana, off northern Chile. A) Mejillones in summer 2006, B) Chipana in summer 2006, C) Chipana in winter 2006, D) Chipana in summer 2007. Profiles are from 5 to 7 days averaged data at each survey.

CHWN06 period when the OMZ was the deepest (Fig. 2C). Daily changes in sea surface temperature (SST) within samplings were significant (Kruskal–Wallis, p b 0.05) during two conditions at Chipana location, summer 2006 (Fig. 2B) and winter 2006 (Fig. 2C). Minimum values of salinity were observed during MESU06 (34.2) whereas a higher salinity was measured during CHWN06 and CHSU07 (N34.9). These ranges of temperature and salinity suggested that Subtropical Surface Water (SSW) and Subantarctic Water (SAAW) were mainly found on the upper 40 m (Strub et al., 1998), although different proportions of these water masses could have prevailed during CHWN06 and CHSU07. Shallow thermoclines and picnoclines (b20 m) were also evident from the averaged vertical profiles of temperature and water density (Fig. 3). However, this pattern was notably altered in winter 2006 when a sharp deepening of the thermocline and picnocline took place, reaching almost 40 m depth (Fig. 3). This winter anomaly was accompanied by a subsurface warming of the water column (Fig. 3A) and less stratified condition (Fig. 3B), coinciding with a highly oxygenated water column upon an abrupt descent of the OMZ down to N40 m (shown in Fig. 2C).

It became clear that observed oceanographic variability, both among and within sampling periods, was associated with wind-driven upwelling. This is because, the daily cumulated alongshore wind correlated positively with water column stratification (Fig. 4A), and negatively with depth of the 15 °C isotherm (Fig. 4B). These correlations were both highly significant (F1, 21 N4, p b 0.01) and suggested that increases in daily wind forcing did not cause strong turbulence,

Table 1 Macronutrients concentrations observed at 4 different surveys in two upwelling sites of northern Chile: MESU06 = Mejillones summer 2006, CHSU06 = Chipana summer 2006, CHWN06 = Chipana winter 2006, CHSU07 = Chipana summer 2007. Nutrients

CHWN06

CHSU06

CHSU07

MESU06

NO3 NO2 PO4 SiO

6.07 ± 2.841 0.20 ± 0.114 0.93 ± 0.271 6.91 ± 2.182

0.50 ± 0.493 0.53 ± 0.870 1.53 ± 0.833 5.36 ± 3.212

5.34 ± 5.958 3.39 ± 3.666 1.47 ± 0.544 18.16 ± 11.814

0.20 ± 0.059 14.74 ± 12.463 1.51 ± 0.103 14.03 ± 2.375

Values are mean ± SD from integrated data over the photic layer obtained after 5–7 days of measurements.

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Fig. 6. Daily time series of two size fractions of Chlorophyll-a concentration at two locations, Chipana and Mejillones, off northern Chile during 4 seasonal surveys. A) Mejillones in summer 2006, B) Chipana in summer 2006, C) Chipana in winter 2006, D) Chipana in summer 2007. Values are integrated over the photic layer after 2–3 variable depths of measurements.

but instead resulted in the ascent of the thermocline and consequently a more stratified condition upon a warmer surface water. Another potential source of variation for short-term oceanographic conditions is tidal forcing. Tides can have effects on properties of the water column over short-term scales (b24 h). In our data we found a nonsignificant (r2 = 0.26, p N 0.05, n = 8) correlation between tides and depth of the 15 °C isotherm. Tidal effects were only detected during the CHSU06 period when a significant relationship was found between low tide and the 15 °C isotherm (r2 = 0.64, p b 0.05, n = 8). The patterns of vertical distribution of macronutrients were characterized by low levels at surface and a maximum near the thermocline or below (Fig. 5). These patterns were similar among sampling periods, although mean concentrations of nutrients integrated over the photic zone varied considerably among seasons and locations (Table 1). For example, NO3 levels were significantly

lower in the photic zone during summer 2006 in Chipana (F3,16 = 12.2, p b 0.01) compared to winter 2006 and summer 2007, possibly because of more utilization of NO3 by autotrophic components during spring–summer 2006. On the contrary, PO4 was much lower in winter 2006 conditions (F3,61 = 4.49, p b 0.01), suggesting a much less vertical influx of PO4 perhaps due to a depressed upwelling situation during this sampling as shown in Fig. 3. Meantime, day-to-day changes in nutrient concentrations within sampling locations were not significant at any season, possibly due to the high variation among depths within periods (Kruskal–Wallis, p N 0.05). Negative and significant correlations were found between nutrients and temperature during winter 2006 (n = 19, r2 = 0.6, p b 0.01 for NO3; r2 = 0.7, p b 0.001 for PO4 and r2 = 0.7, p b 0.001) for SiO. A similar pattern between nutrients and temperature was observed in Chipana during summer 2007 (n=24,

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r2 =0.7, pb 0.0001 for PO4; n=24, r2 =0.6, pb 0.0004 for NO2 and n=24, r2 =0.6, pb 0.0005 for NO3; n=24, r2 =0.6, pb 0.003 for SiO). Total Chla and fractioned Chla b20 µm varied widely in the photic zone while sampling at each location and Chla b20 µm did not substantially contribute to total Chla in most cases, with the exception of winter 2006 at Chipana when both fractions exhibited similar levels (Fig. 6). The lowest values of total Chla (mean b1.5 mg m− 3) were found at Chipana during winter 2006 (Fig. 6C), whereas the highest concentrations (mean N14 mg Chla m−3) were observed during summer 2007 at Chipana (Fig. 6D). A significant and positive correlation (n = 9, r2 = 0.8, p b 0.009) was found between temperature and Chl at MESU06. These variables were also significantly correlated during summer in Chipana, but the correlation was negative (n = 13, r2 = 0.6, p b 0.02). In this period phytoplankton biomass was also positively correlated with NO2 (n = 13, r2 = 0.5, p b 0.03). 3.2. Community structure responses The microplankton fraction of phytoplankton was identified at the species level and all the species found are shown in Table 2. Species assemblages varied among samplings, although some of the species were common across samplings. Total abundance of diatoms and flagellates, including both micro- and nanoplankton fractions, integrated over the upper 20 m, also varied widely among samplings (Fig. 7), and there were also strong variations on a daily basis within periods (Fig. 7). The greatest concentrations of total diatoms reached 3 × 107 while the lowest ones were about 1 × 105 cells m− 2. It is important to note that short-term changes were not abrupt, but they occurred gradually during each sampling period, such that substantial and significant changes took about 3–4 days to develop. For instance, in Mejillones location a marked decreased in cell concentration occurred between the 1st and 2nd days (24-01 and 25-01), and then it dropped again on the 5th day (28-01). At this place, flagellated cells were predominant over diatoms and they steadily decreased from the first to the last day of sampling (Fig. 7A), although as shown in Fig. 6A total Chla increased during the last 2 days. We have no clear explanation for this, but changes in species of autotrophic flagellates with different Chla contents, or strong spatial–temporal variation not fully covered by our sampling may be considered. Lack of daily sampling in this location did not allow us to examine such possibilities. Meantime, in Chipana during summer 2006, abundances alternate (Fig. 7B), steadily increase (Fig. 7C), or exhibit a dome-type variation with scarce contribution of diatoms during CHSU07 (Fig. 7D). Daily changes in relative abundance of the numerically dominant species of diatoms and flagellates for Chipana location are shown in Fig. 8. Mejillones was not included because of too few samples. Only five dominant species were considered which altogether contributed to more than 90% of total phytoplankton abundance. Changes in the descriptors of the community structure, diversity (H′), species richness (S) and numerical abundance (n) for each sampling are also shown in Fig. 8 as to describe the day-to-day variability in the community. Similarly to total abundances, substantial changes in H′ and S took place after 3–4 days (Fig. 8). After that time, variation in H′ and S became significant in all cases at Chipana (Table 3), even when changes in cell abundance were not significant (Table 3). Therefore, this short-term variation (3–4 days) occurred from changes in dominance or co-dominance among different algae classes. For example, after a shift of dominance from Bacillarophyceae to Dinophyceae had taken place. In understanding the factors influencing variation in H′ and S, we found that H′ was significant and negatively correlated with logtransformed values of dissolved oxygen (r2 = 0.15, p b 0.05, n = 25), whereas with temperature H′ was negatively correlated without logtransformation (r2 = 0.26, p b 0.05, n = 25). These negative relation-

Table 2 Species composition of phytoplankton assemblages found during 4 seasonal surveys in two upwelling sites of northern Chile, Mejillones and Chipana. Phytoplankton group Diatoms

Flagellates

Actinoptychus senarius (1, 2) Asteromphalus arachne (1, 2, 4) Asterionellopsis glacialis (2, 3) Asteromphalus heptactis (2) Bacteriastrum delicatulum (2, 3) Cerataulina pelagica (2) Chaetoceros affinis (2) Chaetoceros compressus (2, 3) Chaetoceros curvisetus (2) Chaetoceros lorenzianus (2, 3) Chaetoceros protuberans (2, 4) Chaetoceros peruvianus (3) Corethron criophillum (3) Coscinodiscus centralis (1, 2, 4) Coscinodiscus concinnus (1, 3) Coscinodiscus curvatulus (1, 2, 3) Coscinodiscus wailessii (1, 2) Cylindroteca closterium (3) Dactilyosolen fragilissimus (2) Detonula pumila (2, 3) Ditylum brightwellii (2, 4) Eucampia cornuta (1, 2, 3) Eucampia zodiacus (1, 2) Fragilariopsis doliolus (1, 4) Guinardia delicatula (2) Guinardia striata (2) Hemiaulus sinensis (2) Leptocylindrus danicus (1, 2) Leptocylindrus mediterraneus (1, 3, 4) Lioloma pacificum (1, 2) Lithodesmium undulatum (3) Odontella longicruris (2) Nitzschia longissima (1, 2, 3, 4) Planktoniella sol (1) Proboscia indica (2) Pseudonitzschia australis (2, 3) Pseudonitzschia pungens (2) Pseudosolenia calcaravis (2) Pseudonitzschia multiseries (3) Rhizosolenia setigera (1, 2, 3) Rhizosolenia imbricata (3) Stephanopyxis turris (1) Thalassionema bacillare (1, 2) Thalassiosira aestivalis (1) Thalassiosira minuscula (1, 2) Thalassionema nitzschioides (2) Thalassiosira rotula (2) Thalassiosira decipiens (3) Skeletonema japonica (2, 3, 4)

Ceratium azoricum (1, 2, 4) Ceratium breve var. paralellum (2) Ceratium furca var. berghii (1, 2, 3, 4) Ceratium furca var. eugrammun (1, 4) Ceratium massiliense (1, 2, 4) Ceratium fusus var. seta (2, 4) Ceratium lineatum (3) Ceratium inflatum (3) Ceratium pulchellum (1, 3) Ceratium tripos var. pulchellum (3) Corythodinium tesselatum (4) Dictyocha fibula (1, 2, 3) Dinophysis acuminata (1, 2, 4) Dinophysis caudata (1, 2, 4) Dinophysis tripos (1, 2) Distephanus speculum (1) Distephanus sp.var. octonarius (1, 2) Goniodoma polyedricum (4) Gonyaulax polygramma (1) Gonyaulax grindleyi (4) Gymnodinium sp. (3, 4) Gyrodinium sp. (1, 2) Kofoidinium splendens (4) Lingulodinium polyedrum (4) Oxytoxum scolopax (2, 4) Podolampas palmipes (2, 4) Podolampas bipes (3) Polykrikos kofoidii (4) Pronoctiluca sp. (4) Prorocentrum gracile (1) Prorocentrum micans (1, 2, 3, 4) Protoperidinium claudicans (1, 3) Protoperidinium conicum (1, 2, 4) Protoperidinium depressum (1, 2, 4) Protoperidinium divergens (1, 3, 4) Protoperidinium leonis (1, 2) Protoperidinium oceanicum (1) Protoperidinium pellucidum (1, 2, 4) Protoperidinium pyrum (4) Protoperidinium tenuissimum (4) Protoperidinium steinii (2)

MESU06 (1), CHSU06 (2), CHWN (3) and CHSU07 (4).

ships between diversity and environmental variables are shown in Fig. 9, and they indicate that diversity was greater upon low oxygen and low temperature which is the condition when upwelling prevails. Because of expected serial correlation within each sampling series, it was not advisable to apply day-to-day statistical comparisons in the community descriptors. Thus, in order to assess how significant variations took place, we performed a cluster analysis on the species composition by grouping in according to date of sampling. To do that the Bray–Curtis Similarity Matrix was constructed for clustering. As expected consecutive days are very close to each other, but then 2–3 days apart became joined at maximal distances (Fig. 10 left panel). As to better illustrate this temporal divergence we applied Principal Component Analysis (PCA) to same data (Fig. 10 right panel). These analyses included data representing all species sampled in both places and seasons and

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Fig. 7. Daily time series of nano- and microplankton represented by diatoms and flagellates (autotrophic and heterotrophic included) at two locations, Chipana and Mejillones, off northern Chile during 4 seasonal surveys. A) Mejillones in summer 2006, B) Chipana in summer 2006, C) Chipana in winter 2006, D) Chipana in summer 2007. Values are integrated over the photic layer after 2–3 variable depths of measurements. Arrows indicate significant changes on abundance.

were located in the sub-space of maximal inertia of these multivariate tests. PCA for 2 components was highly significant, explaining N68% of total variance. The graphic representation of the two factors clearly shows how distant days fall in different planes, while consecutive days are close to each other (Fig. 10 right panel).

4. Discussion Upwelling conditions may vary on a wide range of spatial and temporal scales. Off the Chilean coast, most temporal variability has been examined for monthly, seasonal and inter-annual comparisons (Strub et al., 1998; Blanco et al., 2001). Variability in a higher frequency (daily or weekly) has not received much attention (Hidalgo and Escribano, 2008). This kind of variation may prove highly relevant in the context of food supply for short-lived zooplankton, or even for invertebrate and fish larvae, whose survival depends on encounter rates with their prey. For example, young copepods (nauplii and early copepodids) may develop into 2–3 stages in 3–4 days (Escribano and McLaren, 1999) and larvae of anchovy, the most important fishery in northern Chile, require successful encounters with their food in no longer than 3–4 days which is the time known as the “critical period” (sensu Hunter, 1981). In both cases, substantial variation in the nanoplankton and microplankton community over this time scale may be considered critical for sustaining either copepod recruitment or cohort strength, respectively. We indeed showed that such drastic variation do occur in the upwelling zone, even in a system where upwelling is active all year round (Rutllant and Montecino, 2002; Blanco et al., 2002; Herrera and Escribano, 2006). This high frequency variation should therefore be an important component in modeling population dynamics of short-lived or transient organisms in the water column.

Our daily time series may not be sufficiently long (b8 days) as to test for cross-correlation and eventual time lags in responses of the planktonic system to the high frequency variation of the physical environment. However, the cluster analysis and PCA suggested that changes in planktonic descriptors and environmental variables are not randomly distributed over the time scale, but they vary associated to each other and with strong serial correlation, i.e. changes occur gradually, since consecutive days were close to each other, whereas days separated in time were distant in clustering and fell apart when plotting the PCA components (Fig. 10). The short-term temporal variation found in this study was apparently transferred to the phytoplankton assemblages, and this was reflected in drastic changes in species composition, abundance and ecological descriptors of the community. The underlying mechanisms causing these changes can be understood considering: 1) fast generation times of phytoplankton ranging from hours to a few days (Carpenter et al., 1985); 2) distribution and growth rates of marine phytoplankton are chiefly governed by variable nutrients and radiant energy availability (Bidigare et al., 1990); and 3) also patterns of planktonic associations will respond to different interactions between 1) and 2). Furthermore, in according to the Intermediate Disturbance Hypothesis (IDH) (Connell, 1978; Padisak et al., 1993), which establishes that the frequency of disturbances from external forces has an effect on the diversity of a biotic community, the continuous and simultaneous action of multiple forces, superimposed over upwelling events, could respond to high frequency disturbances promoting continuous changes of the community's properties of planktonic assemblages. In fact, alternate shifts from autotrophy to heterotrophy or diatoms to flagellates dominance, with a mean period of about 3 days, or co-dominance, were observed in the surveys. Likewise, these changes promoted significant variability in H′, S and n. This can be explained from,

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Fig. 8. Daily time series of dominant species of nano- and microplankton and community structure descriptors (biodiversity = H′, species richness and abundance = n) at two locations, Chipana and Mejillones, off northern Chile during 3 surveys. A) Chipana in summer 2006, B) Chipana in winter 2006, C) Chipana in summer 2007. Values are integrated over the photic layer from 3 to 4 depths estimates of cellular abundances. Diversity and species richness were estimated from the total number of species found (see Table 2).

either replacement or co-existence of organism K-strategists (with low loss rates and able to prevail in nearly-stable systems even for short times) and smaller r-strategists with high specific growth rates but high mortality as well (Sommer, 1981; Lindenschmidt and Chorus, 1997). Genera such as Leptocylindrus, Skeletonema, Thalassiosira and Rhizosolenia, along with flagellates, such as Ceratium, Distephanus and Gymnodinium, which have small sizes and high growth rates (r-strategists, sensu Margaleff, 1963, 1967), were highly conspicuous but also variables, inducing the observed changes on the community structure. In understanding the physical factors controlling the high frequency variation upon upwelling conditions, thermal and stability conditions of the water column should be considered as important. Thermal and stability conditions are mainly related to the sea– atmosphere interaction (Sobarzo and Figueroa, 2001). In this context, the impact of increased wind stress on water column

conditions was clear in our study, causing changes in stratification and the rise in the 15 °C isotherm (see Fig. 4). However, it should be noted that the increase in wind stress did not cause more turbulence or deepening of the mixing layer, but instead the water column became more stratified. This occurred because the alongshore winds were in most cases steady and slight (b10 knots) causing the rise of the thermocline, i.e. producing more upwelling, and cooling the subsurface layer below a warm surface heated by strong solar radiation at northern Chile and hence promoting thermal stratification. Tidal forcing can also cause high frequency variation in the water column in near-shore areas, mostly by modulating internal waves, which are usually in phase with the tidal cycle (ca. 12 h) (Federiuk and Allen, 1996). Our daily measurements cannot examine such potential source of variation for water column changes. The non-significant correlation between tides and the 15°°C isotherm suggested that, at least for day-to-day variation in the physical and

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chemical conditions of the water column, tidal forcing may not be the key factor. However, a further examination of tidal effects may require a longer time series, or a shorter (b24 h) sampling. By contrast, as shown by our results wind forcing, which is the energy source for upwelling, seemed the key factor influencing water column changes. Now the question is, whether this high frequency variation of upwelling, forced by wind variation, was the main factor causing variation in the nano- and microplankton communities. To assess such connection we added the total abundance of nanoplankton and microplankton for each sampling series and plotted them as a function of the daily accumulated alongshore wind. The patterns linking wind forcing and nano- and microplankton responses (Fig. 11) suggest a connection between high frequency upwelling variation and a surprisingly fast response of the autotrophic/heterotrophic components at lower trophic level. Certainly, there is much variation between and within the shorttime series as to attempt the application of any correlation test with too few degrees of freedom, but the trends in day-to-day fluctuations of the planktonic system and those of the wind stress were similar at most situations (Fig. 11). Superimposing the seasonal changes observed in oceanographic conditions and nano- and microplankton, the observations obtained in winter 2006 deserve special attention. The greatly depleted upwelling, warmer and well oxygenated water column altogether resemble the El Niño like conditions, such as those observed in 1997–98 at northern Chile (Ulloa et al., 2001). This abnormal winter warming was also observed at the El Callao off coast of Peru (Gutierrez, unpublished) suggesting that this was a large-scale and not a simple local event. Another possibility is the presence of coastal-trapped waves (CTWs) which are remotely (equatorial) forced and propagate towards the south. These waves are responsible for most of the variability of coastal currents, sea-level and mass fields near shore (Shaffer et al., 1997; Pizarro, 1999; Hormazabal et al., 2001). This CTW may have affected the distributions of oxygen levels and thermal and stability conditions at Chipana. However, the dramatic deepening of the oxycline and subsurface warming seemed a more intense an extensive event than a CTW, which may occur a few times during the year cycle (Pizarro, 1999). Thus, conditions found in winter 2006 are more likely attributed to a weak El Niño (EN) of rather short duration and generated by an equatorial Kelvin wave. The biological response of the nano- and microplankton community to this weak EN was not clear. Variability of both components was coupled to upwelling variation in the high frequency domain (see Fig. 11). Nutrients were not considerably depleted (Fig. 5) and the alongshore wind was positive and hence favorable to upwelling (Fig. 11). Chla had the lowest value observed in our study however (b1.5 mg m− 3)

Table 3 Kruskal–Wallis (K–W) test performed to assess changes in the structure of the nanoand microplankton community sampled on a day-to-day scale at Chipana (northern Chile) during 3 seasonal surveys. Place

Period

Variable

d.f

K–W

N

p

Chipana

CHSU06

Chipana

CHWN06

Chipana

CHSU07

H S n H S n H S n

4 4 4 6 6 6 7 7 7

3.48 4.65 1.51 6.81 6.69 16.46 9.94 9.29 3.63

13 13 13 19 19 19 24 24 24

b 0.05 b 0.05 N 0.05 b 0.05 b 0.05 b 0.01 b 0.05 b 0.05 N 0.05

Comparisons were made using the abundance (cell mL− 1) of species. Community structure descriptors were: Diversity (H), species richness (S) total abundance (n). d.f = degrees of freedom.

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Fig. 9. The relationship between species diversity (H′) and dissolved oxygen (Lntransformed) in the photic layer (A) and temperature (B). The regressions were constructed from pooled data after 4 seasonal surveys at Chipana and Mejillones (northern Chile) during summer–winter 2006–2007. Dashed lines represent 95% confidence limits of the regression fittings.

(Fig. 6A), although cell abundance was not substantially reduced, and even increased cellular abundance was observed by the end of the series (Fig. 7C). Meantime, diversity and species richness remained similar with the other surveys. Small diatoms and flagellates dominated the water column during this weak EN, as found during the 1997–98 EN (Iriarte et al., 2000). Nevertheless, seasonal (winter) effects cannot be discarded and no other winter situation was sampled for comparison. In any case, the observed anomalous situation in winter 2006 in the physical and chemical environments did not seem to greatly impact the nanoand microplankton community, both in terms of abundance and structure. Therefore, as Escribano et al. (2004) concluded, major impacts of the El Niño on the physical and chemical environments do not necessarily imply a drastic biological response, but high resilience seems a regular character of highly productive upwelling systems. 5. Conclusions The northern Chile upwelling region is highly productive and known to be subjected to strong variation over the inter-annual (EN), seasonal and intra-seasonal (CTW) time scales. Much less is known about variability over weekly or day-to-day time scale. We found significant variation in the physical environment on a daily basis triggered by local changes in the wind forcing. This variation significantly impacted the nano- and microplankton community in terms of abundance, species composition and diversity. We thus established a connection between wind-driven upwelling and autotrophic/heterotrophic community responses of the planktonic system. This short-term variability may certainly impose crucial constraints for pelagic heterotrophs whose survival depend on nano- and microplankton distribution and quality. On the other hand, we

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Fig. 10. Cluster analysis and Principal Components (PCA) analysis on the nano- and microplankton species composition from 4 seasonal surveys at Chipana and Mejillones (northern Chile) during 2006–2007. A) Mejillones in summer 2006, B) Chipana in summer 2006, C) Chipana in winter 2006, D) Chipana in summer 2007. Bray–Curtis distance was estimated for clustering the days of sampling as a function of species composition and two significant components were derived from PCA analysis explaining N 68% of total variance.

observed a weak El Niño condition during winter 2006 reflected in an abnormally warm and well oxygenated water column. This situation apparently did not cause a major impact on the pelagic communities at lower trophic levels.

Acknowledgements Authors are very grateful to the scientists and crew of the Universidad Arturo Prat headed by Gabriel Claramunt for their

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Fig. 11. The coupling between upwelling and nano- and microplankton responses (total abundances) at two locations off northern Chile (Mejillones and Chipana) during 4 seasonal time series studies on a daily basis. Upwelling is represented by variability in the daily cumulated alongshore wind.

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