Progress in Oceanography 97–100 (2012) 174–186

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Progress in Oceanography

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Zooplankton time series in the coastal zone off Chile: Variation in upwellingand responses of the copepod community

Ruben Escribano a,b,⇑, Pamela Hidalgo a,b, Marcelo Fuentes b, Katty Donoso a,b

a Center for Oceanographic Research in the Eastern South Pacific (COPAS), Universidad de Concepción, Chileb Department of Oceanography, Universidad de Concepción, Chile

a r t i c l e i n f o

Article history:Available online 3 December 2011

0079-6611/$ - see front matter � 2011 Elsevier Ltd. Adoi:10.1016/j.pocean.2011.11.006

⇑ Corresponding author at: Center for OceanograpSouth Pacific (COPAS), Universidad de Concepción, Ch

E-mail address: rescribano@udec.cl (R. Escribano).

a b s t r a c t

Two zooplankton time series from the coastal upwelling region off Chile were studied in terms of cope-pod biomass and abundance in relation with upwelling variation. The time series from Antofagasta (23�S)was collected between 1988 and 2008 and based on bi-annual sampling, whereas the time series fromConcepción (36�S) was based on monthly samples between 2002 and 2008. In both sites, Ekman trans-port was derived from local wind obtained at coastal stations as an upwelling index. At both sites Ekmantransport exhibited a seasonal patterns characterized by stronger upwelling during the spring–summer,although Ekman transport was stronger in northern Chile. Ekman transport also revealed three distinctperiods of upwelling intensity between 1988 and 2008 in northern Chile. Copepod biomass varied inassociation with these periods, as follows: (1) 1988–1997 with a positive linear trend, (2) an abruptdecline in 1998–2000 after the 1997–1998 El Niño, and (3) a negative trend associated with increasedupwelling from 2001 to 2008. A negative trend of zooplankton biomass and copepod abundance alsooccurred at Concepción during the period 2002–2008. Seasonal peaks in copepod biomass also coincidedwith the upwelling season (spring–summer). The correlation between variation in upwelling and cope-pod biomasses in northern Chile suggested that population dynamics of copepods may depend on inten-sity of upwelling. Although the underlying mechanisms are unclear, and several hypotheses dealing withbottom-up or top down factors can be put forth, our findings suggest that upwelling intensity operatesthrough an optimal window for copepod abundance and biomass and increasing upwelling in the lastdecade (2000–2008) may has been unfavorable for copepod populations.

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1. Introduction

Long-term studies of zooplankton are considered to be highlyrelevant to assess the variability of the marine ecosystem uponongoing climate change (e.g. Richardson and Schoeman, 2004;Mackas et al., 2007). Zooplankton mostly comprises a number ofshort-lived taxa that can rapidly respond to environmentalchanges because of the high sensitivity of their populations to var-iation in oceanographic conditions such as temperature, foodquantity and quality, oxygen levels, or other chemical and physicalfactors. The responses of zooplankton to long-term changes can bereflected in changes in species composition and diversity(Beaugrand et al., 2000), changes in biomass and abundance (e.g.Roemmich and McGowan, 1995), size structure spectra and phe-nology (Richardson, 2007). All these changes may act as indicatorsof ecosystem state (Hays et al., 2005).

There are number of important time series from differentregions of the world ocean (Perry et al., 2004). They may differ in

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hic Research in the Easternile.

terms of sampling resolution and gears, but they have still provencomparable to explore for more general patterns and synchronies(Perry et al., 2004). From the eastern South Pacific the most impor-tant zooplankton time series is that off the coast of Peru (Ayónet al., 2004). This time series covers nearly 40 years of zooplanktonvolumes and it has proven very useful to assess the impact of cli-mate variability and the El Niño on biological responses of lowertrophic levels. Farther south, off Chile, there have been no reportsdealing with existing zooplankton time series. The coastal upwell-ing zone off Chile has a latitudinal extent of nearly 24� (�2700 km),exhibits high levels of primary production (Daneri et al., 2000;Montero et al., 2007) and represents a large fraction of theHumboldt Current Large Marine Ecosystem (HCLME). Similar tothe Peruvian region, the Chilean upwelling zone sustains a strongfishery industry mostly based on small pelagic fishes (Alheit andBernal, 1993; Cushing, 1990).

From the Chilean upwelling region we know very little aboutthe long-term changes in the zooplankton community. In northernChile, the impact of the El Niño has been studied for some copepodpopulations (Hidalgo and Escribano, 2001; Ulloa et al., 2001). Thesestudies, however, are based on rather short time series (<2 years)and they mostly describe seasonal population responses (e.g.

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Hidalgo and Escribano, 2008), but they can hardly tell us aboutinterannual variation or longer-term responses of zooplankton. Itseems apparent that organized programs sponsored by national(usually governmental) institutions are necessary to maintainlong-term series, which does not appear to be the case in Chile.Although, the Chilean Fishery Institute (IFOP) is known to have car-ried out a long-term (>30 years) zooplankton survey in northernChile, data have not been made available to the scientificcommunity.

The upwelling zone of Chile can be divided into two majorregions on the basis of large scale oceanographic patterns andthe annual regime of upwelling (Escribano et al., 2004). The north-ern upwelling region (18–30�S) is subjected to permanent weak-to-intermittent upwelling year round (Thomas et al., 2001; Blancoet al., 2001), whereas the central/southern upwelling region exhib-its a strongly seasonal regime dominated by intense upwellingduring the austral spring/summer and downwelling conditions inthe autumn and winter (Sobarzo et al., 2007). In northern Chile,zooplankton sampling has been carried out at Antofagasta (23�S)at least twice a year between 1988 and 2008. In central/southernChile, the COPAS Oceanographic Center initiated a zooplanktontime series at Station 18 (36�S) in 2002 (Escribano et al., 2007).Although of rather low spatial resolution, these two time seriescould be useful to evaluate potential trends or changes of thezooplankton community on temporal scales longer than the sea-sonal cycle. From the taxonomic standpoint, copepods have beenthe target group for these two programs because most of the timethey are the dominant taxa in the zooplankton. In this study, weexamine the responses in copepod abundance, composition andbiomass to changes in upwelling at these two locations off theChilean coast. We aim to assess whether the changes in copepodcommunity structure and biomass car serve as potential indicatorsof environmental impacts on the marine system driven by variabil-ity in the intensity of upwelling.

2. Methods

2.1. The study region

The Chilean coastal upwelling region comprises the southernportion of the Humboldt Current system between 18�S and about42�S (Fig. 1). This large coastal system aligned nearly north–southis subjected to wind-driven upwelling along its entire length (Strubet al., 1998). Upwelling, however, may exhibit a different seasonalregime, depending on latitude, allowing the distinction betweentwo major upwelling regions: (1) the northern upwelling region(18–30�S), and (2) the central/southern upwelling region(30–42�S, Escribano et al., 2004).

In the northern region, upwelling occurs intermittently yearround and winds are moderate (5–10 m/s), with increased magni-tudes during the spring–summer period resulting in a weak sea-sonal signal of upwelling (Pizarro et al., 1994). In this region,upwelling induces the ascent of equatorial subsurface water inassociation with a persistent oxygen minimum zone OMZ(<0.5 mL O2 L�1) that may enter the euphotic layer (<50 m) in thecoastal band (<40 km) (Morales et al., 1999). The continental shelfis very narrow or almost non-existing (<20 km wide) and high lev-els of biomass and productivity appear to be well restricted to thecoastal band (Morales et al., 1996; Daneri et al., 2000). This systemsustains a strong pelagic fishery, at times reaching up to 5–6 millionmetric tonnes per year which accounts for about 40% of total annualChilean fish landings.

In the region off central/southern Chile, upwelling is stronglyseasonal with intensive events occurring during the spring/sum-mer period (Sobarzo et al., 2007; Escribano and Schneider, 2007).

The wider continental shelf (ca. 60 km) is interrupted by two sub-marine canyons (Figueroa and Moffat, 2000). River runoff and rain-fall are important in this area and low salinity waters (<33.8) mayextend far offshore (>30 km) during winter and early spring (Sob-arzo et al., 2007). The OMZ in this region is deeper (>100 m depth)and less intense (> 0.5 mL O2 L�1), although in the summer it canalso reach very shallow depths (<50 m) in the coastal zone (Sob-arzo et al., 2007). Very high values of primary production (>10 gC m�2 d�1) have been recorded here (Montero et al., 2007), sustain-ing the largest fisheries of jack mackerel in the eastern south Paci-fic, which reached 3 million tons between 1990 and 1996 (Arcoset al., 2001).

2.2. Zooplankton time series

There are few data for long-term studies of zooplankton in thenorthern and central/southern regions off Chile. At the northernregion a time series of zooplankton was initiated in 1988 at Antofag-asta in the Bay Mejillones (23�S) and maintained until 2008, but onlywith sampling twice a year (summer and winter). Bay Mejillones isunder the influence of a very active upwelling center (Marín et al.,2001), and several studies on zooplankton, focused on copepod dis-tribution and dynamics, have been carried out in the last decades(e.g. Escribano and McLaren, 1999; Hidalgo and Escribano, 2001;Giraldo et al., 2002, 2009). At this upwelling site, three sampling sta-tions have been used for zooplankton collections, representing theinshore, mid-bay and at the entrance of Bay Mejillones. Sampleswere obtained with a 200 lm, 0.5 m opening diameter WP2 net. Thisnet is towed vertically from depths between 50 m and 20 m to sur-face. Water volume filtered by the net was estimated from the depthof deployment. From these samples, dominant copepods were iden-tified and counted. All sampling was performed during daylighthours.

At the central/southern region off Chile, the COPAS oceano-graphic center initiated a time series study at Station 18 over thecontinental shelf (ca. 90 m depth) in August 2002. Zooplanktonhas been sampled since then on a nearly monthly basis. Samplesare obtained at Station 18 using a 1 m2 Tucker Trawl equipped with200 lm mesh-size nets. The net has a calibrated flowmeter to esti-mate the volume sampled. Oblique tows have been made from80 m to surface. All samplings were carried out between 12 PMand 4 PM (daylight hours). The net collect an integrated 0–80 mand two stratified samples, 80–50 m and 50–0 m. Copepods for thisstudy are those identified and counted from the 0–80 m integratedsample. Total zooplankton biomass and monthly abundance ofdominant copepods for the period 2002–2005 were reported inEscribano et al. (2007). For the present work, we use abundancesof copepods and biomass for the period 2002–2008.

2.3. Samples and data analysis

The analysis of copepod composition was carried out under ste-reo microscopes and in some cases sub-samples were obtainedusing a Folsom splitter. Once sorted, copepods were identifiedand counted to species level. All recognized copepodid stages werecounted for each of the most abundant species. At least 30 adultfemales of each species have been measured in length (totallength) using a 0.1 mm resolution micrometer. Because samplingdepths were variable we decided to standardize copepod abun-dances in numbers m�3.

Copepod biomasses were estimated for each species based onthe mean body length of adult females and weight–length relation-ships from published material. Estimated lengths and weight-specific dry weights are shown in Table 1.

In order to relate copepod abundances and biomass with varia-tions in upwelling intensity, we calculated an index of upwelling

Fig. 1. The coastal upwelling system off Chile in the eastern south Pacific basin, illustrating the locations of the zooplankton time series: at Antofagasta (northern Chile) in BayMejillones and off Concepción (central/southern Chile) at Station 18.

Table 1Body length (mean ± SD) and estimated dry weight (DW) of dominant copepod species in the coastal upwelling area offChile. DW was estimated from log–log weight–length regressions from previous studies. Both lengths and weightsrepresent mean values for copepodite stages C1–C6.

Species Body length (lm) DW (lg) Source

Acartia tonsa 1450.00 ± 39.00 13.30 Berggreen et al. (1988)Centropages brachiatus 2080.00 ± 87.00 12.62 Hay et al. (1991)Calanus chilensis 3229.00 ± 49.00 33.20 Escribano et al. (1997)Paracalanus cf. indicus 1060.00 ± 35.00 2.99 Chisholm and Roff (1990)Oithona similis 1120.00 ± 65.00 2.10 Chisholm and Roff (1990)Oncaea spp. 1090.00 ± 68.00 1.97 Chisholm and Roff (1990)Corycaeus typicus 1000.00 ± 108.00 1.82 Chisholm and Roff (1990)Eucalanus inermis 5730.00 ± 208.00 26.75 Hopcroft et al. (2002)Rhincalanus nasutus 5360.00 ± 214.00 33.30 Hopcroft et al. (2002)Pleurommama gracilis 2422.00 ± 37.00 4.70 Bennet and Hopkins (1989)

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using wind data from local meteorological stations located at thecoastal zone. At Antofagasta, wind data come from the meteorolog-ical station at Cerro Moreno Airport. These data are suitable to rep-resent upwelling conditions in the area of Mejillones, and show astrong correlation with sea surface temperature (Escribano,1998). In Concepción, we used data from a coastal meteorologicalstation located off Coliumo (36�300S). These data are also stronglycorrelated with sea surface temperature measured at the coast(Sobarzo et al., 2007). The upwelling index was estimated as Ek-man transport (Mann and Lazier, 1991):

Mx ¼ sy=f

where Mx = Ekman transport (km3 s�1 km�1), f the coriolis parame-ter and sy denotes the alongshore wind stress (pa). sy was estimatedas,

sy ¼ q� cd� Vi � jv ij

where q is the air density (1.2 kg m�3), cd is an empirical constant(0.0013), and Vi is the velocity of the alongshore component ofthe wind (m s�1). Ekman transport (Ek) was calculated daily usingthe wind measured at 14 h (local time). A time series of Ek withtime intervals of 1-month was then calculated, using integratedmonthly values of transport. Comparisons between regions consid-ered only the period 2003–2008 for which data were available. Inaddition to Ek, we also examined sea surface temperature (SST)and their monthly anomaly from both places. SST was availablefrom daily measurements made near-shore in Antofagasta duringthe entire time series. SST has routinely been measured three timesa day using standard thermometers (±0.1 �C), such that daily meansare obtained. Times series of SST and its monthly anomaly (based

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on 30 years data) were then constructed using monthly values. Thetime series in Antofagasta was between April 1988 and January2008 (n = 230).

Time series of Ek, SST and SST anomaly were assessed for peri-odicity and trends after application of an autocorrelation functionand linear regression for significant trends when monthly datawere available. The association between Ek and SST was examinedwith a cross-correlation function.

Time series de copepod abundances and biomass, and totalzooplankton biomass were available for different periods at bothplaces. For Antofagasta, data were available between 1988 and2008 every 6-months (n = 36), with a gap in 1991–1992. In Con-cepción, data were monthly between August 2002 and April2008. In both cases the linear trends were investigated with linearregressions and F-ratio tests of significance and the non-paramet-ric s-Kendall test was used to assess for correlation between Ek,SST and copepod biomass.

3. Results

3.1. Antofagasta time series

During the period 1988–2008, monthly integrated Ek was posi-tive throughout the year cycle, although with strong seasonal fluc-tuations (Fig. 2a). The autocorrelation was significant for lagsbetween 2 and 12 months (r > 0.6, p < 0.05) revealing significantperiodicity. During the entire time series, three different upwellingperiods can be distinguished. The first period was between 1988and April 1997 with moderate levels of upwelling (meanEk = 16,901 km�3 s�1 km�1), then a second period that started inMay 1997 under the influence of the 1997–1998 El Niño, andlasted until the end of 1999 with much lower upwelling intensity(mean Ek = 10,048 km�3 s�1 km�1), and a third period with in-creased upwelling starting in January 2000 until 2008 and havinghigher upwelling intensity (mean Ek = 18,200 km�3 s�1 km�1)(Fig. 2a). Sea surface temperature (SST) fluctuated strongly andcorrelated significantly and negatively with Ek in accordance withto the cross-correlation function, with lags between 1 and 5 month(r = �0.55, at lag = 2, p < 0.01). SST showed no significant trendduring the first period, increased substantially during the secondperiod, and exhibited a significant negative trend (F1,228 = 17.2,p < 0.05) during the third period (Fig. 2b). Monthly anomalies ofSST were consistent with SST variation, i.e. positive and negativevalues in the first period, positive anomaly during the secondwarm period, and prevalence of negative anomalies during thethird period (Fig. 2c).

From the entire time series of zooplankton collections, nine spe-cies of copepods dominated the community (Table 2). They weredefined as dominant because were the most abundant and fre-quent during all samplings with >1% of relative abundance. Takentogether, these nine species always represented more than 90%of the total copepod community. Rhincalanus nasutus having <1%in relative abundance was also included because of their large size(>4 mm), and therefore their potentially significant contribution tocopepod biomass. Paracalanus cf. indicus has clearly been the dom-inant copepod in this region with high levels of abundance andrepresenting almost half of the copepod community. This speciesis followed by Acartia tonsa and Oithona similis, which have previ-ously been reported as common copepods in the region, althoughP. cf. indicus was previously described as P. parvus (Hidalgo andEscribano, 2001). It is interesting to note that the greatest contribu-tion to copepod biomass comes from A. tonsa and important con-tributors also include Centropages brachiatus and Calanus chilensisbecause of their larger size (Table 2).

The semi-annual estimated copepod biomass remained at lowlevels (<30 mg DW m�3) during the first years of the series

(1988–1990), although no samples were available for 1991 and1992, followed by a steady increase until 1997 (El Niño) and a sud-den decrease after the El Niño to increase again in 2000 (Fig. 3a).Copepod abundance, however, did not clearly reflect these fluctu-ations in biomass (Fig. 3b). Annual means of biomasses, on theother hand, revealed important changes characterized by a positivelinear trend until 1997 (F1,6 = 5.38, p = 0.05), a sharp decrease after1997 (El Niño condition), an increase again and a linear negativetrend through the last decade (F1,8 = 4.50, p = 0.06) (Fig. 3c).

When examined in more detail, it is possible to assess which arethe species determining the patterns in total copepod biomass. Alldominant species showed low biomass (<10 mg m�3) prior to the1997–1998 El Niño, increasing during 1997 (El Niño onset), witha sharp decrease after the El Niño, and then increasing again shar-ply after which a negative trend followed from about 2000 through2008. Changes in biomasses of the dominant P. cf indicus and A. ton-sa appeared as major drivers of variations in total copepodbiomass, because their biomasses fluctuated in a very similar pat-tern to that of total biomass (Fig. 4). Grouped cyclopoid copepodsshowed a peak during the 1997–1998 El Niño, whereas C. chilensis,C. brachiatus and the two Eucalanidae species tended to increaseafter the 1997–1998 El Niño, but with a minor contribution to totalcopepod biomass (Fig. 4).

To assess the relationship between variation in upwelling andcopepod biomass, we estimated annual means of monthly accumu-lated Ekman transport, annual means of SST, and annual means ofcopepod biomass. The plot of the annual series is shown in Fig. 5.For the entire time series we found no significant correlationbetween copepod biomass and Ekman transport, or SST (s-Ken-dall < 0.10). However, prior to the 1997–1998 El Niño, copepodbiomass was negatively correlated to Ekman transport (s-Ken-dall = �0.76) and positively correlated to SST (s-Kendall = 0.84).During the El Niñoevent when upwelling decreased copepod bio-mass suddenly increased. After the 1997–1998 El Niño (1999through 2008) copepod biomass was again negatively correlatedto Ekman transport (s-Kendall = �0.39), but with no significantcorrelation to SST (s-Kendall = �0.17) when upwelling becamestronger (Fig. 5).

3.2. Concepción time series

At Concepción, the zooplankton time series considered themonthly estimate of total zooplankton biomass (methods inEscribano et al., 2007). The biomass of all zooplankton (copepodsand other taxa) during the 2002–2008 period fluctuated in therange of 2.34–542.5 mg DW m�3, with a mean value of86.08 mg DW m�3 (SE = 10.217). Highest values of biomass wereobserved during the spring–summer 2002–2003 mostly associatedwith presence of large-sized euphausiids (Escribano et al., 2007).Zooplankton biomass exhibited strong intra-annual fluctuations,which did not necessarily coincide with seasonal upwelling(spring–summer), although as previously described in Escribanoet al. (2007) positive and negative anomalies in biomass for theperiod 2002–2005 were present in the spring and winter,respectively. Nevertheless, the most remarkable feature for the2002–2008 period was a significant linear negative trend inzooplankton biomass (F1,69 = 6.48, p = 0.013) (Fig. 6).

When looking at the copepod community, eight species wereconsidered common and numerically dominant, representing morethan 90% of total copepods. They were present during the whole per-iod (2002–2008) and comparatively more abundant than the rest ofcopepods at Station 18 (Escribano et al., 2007). This copepod com-munity was similar to that of Antofagasta, although with some dif-ferences. For instance, Eucalanus inermis and Corycaeus typicuswere rarely present and not considered as dominant. Instead Pleuro-mamma gracilis was a common species and considered as dominant

Fig. 2. Time series of Ekman transport (a), sea surface temperature (b) and monthly anomalies of sea surface temperature (c) at Antofagasta between 1988 and 2008. Ekmantransport represents monthly integrated values and horizontal lines are mean values for each corresponding period. The horizontal line in panel (b) is the grand mean of theseries, whereas the broken line represents a linear significant-negative trend in the last decade.

Table 2Abundance and biomass (mean ± SE) of the dominant pelagic copepods from zooplanktoncollections at the Antofagasta location (23�S) during 1998–2008. RA = relative abundances.

Species Abundance(Number m�3)

Biomass(mg DW m�3)

RA (%)

Paracalanus cf. indicus 1846.4 ± 620.73 5.67 ± 1.901 43.14Acartia tonsa 845.7 ± 186.03 11.56 ± 2.524 31.77Oithona similis 800.6 ± 476.39 1.73 ± 1.029 8.54Centropages brachiatus 208.6 ± 60.47 2.71 ± 0.781 6.36Oncaea spp. 430.3 ± 234.73 0.87 ± 0.475 5.89Calanus chilensis 73.1 ± 40.79 2.49 ± 1.390 2.12Corycaeus typicus 108.7 ± 72.39 0.20 ± 0.136 2.02Eucalanus inermis 4.2 ± 1.43 0.11 ± 0.039 0.15Rhincalanus nasutus 0.9 ± 0.86 0.03 ± 0.029 0.01

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Fig. 3. Time series of copepods biomass and abundances at Antofagasta between 1988 and 2008. (a) Bi-annual data representing spring–summer and fall–winter samples, (b)bi-annual abundance of dominant copepods (log-scale), and (c) annual means of copepod biomass illustrating the positive linear trend (1988–1997) and the negative lineartrend (2000–2008) with broken lines.

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for this region. In general terms, all the species in Concepción wereabout one order of magnitude lower in abundance compared tothe Antofagasta time series, and the dominant species again was P.cf. indicus (Table 3), but A. tonsa was in much less abundant than inAntofagasta, and O. similis and C. chilensis were among the mostabundant species (Table 3). C. chilensis, P. cf. indicus and R. nasutuswere the most important species in terms of their contribution tototal biomass.

Total copepod biomass was in the range of 0.9–9.6 mg DW m�3,and its contribution to the bulk of zooplankton biomass varied inthe range of 5% to nearly 40%. Most of the variance in copepodsabundance in this zone is explained by seasonal upwelling (Escrib-ano et al., 2007). Therefore, to assess inter-annual variations, meanvalues of copepod biomass for upwelling (spring–summer) andnon-upwelling (fall–winter) periods were calculated. The trend of

copepod biomass reflected that of total zooplankton biomassshown in Fig. 6, indicating that the gradually decrease in zooplank-ton from 2002 to 2008 was also apparent and contributed to by adecrease in biomass of copepods (Fig. 7a). Interestingly, however,such negative trend in biomass is not reflected in numerical abun-dances of copepods (Fig. 7b). In this respect, and looking at in moredetail the changes in the copepod community, we observed that rel-atively larger-sized species, such as C. chilensis and R. nasutus,explain the negative trend of copepod biomass, while biomass ofthe numerically dominant P. cf. indicus and O. similis did not exhibitsuch a negative trend in their biomass (Fig. 8). Thus, total numericalabundance of copepods shown in Fig. 7b does not properly repre-sent copepod biomass without consideration of copepod body sizes.

The potential association between variations in upwelling andcopepod biomass for this region was assessed using monthly

Fig. 4. Time series of biomass (mg DW m�3) of dominant copepod species at Antofagasta off northern Chile between 1988 and 2008 based on bi-annual samples at threestations in Bay Mejillones.

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estimates of biomass and monthly accumulated Ekman transport.Wind data were only available for the period September 2003and December 2007. Monthly variability in copepod biomass andEkman transport is shown in Fig. 9. For this period the correlationbetween copepod biomass and Ekman transport was not signifi-cant (s-Kendall = �0.09).

Because of different sampling periods and potential biasesderived from distinct sampling methods, copepods series werenot compared between regions. However Ekman transportbehaved similarly in terms of its seasonal pattern at both sites,although with a much higher magnitude in northern Chile(Fig. 10).

Fig. 5. Time series of annual means of copepod biomass and annual means of Ekman transport at Antofagasta off northern Chile between 1988 and 2008. Annual means wereobtained from bi-annual samples at three stations in Bay Mejillones. Ekman transport was derived from wind data obtained at a coastal meteorological station.

Fig. 6. Time series of the bulk of zooplankton biomass off Concepción at Station 18 between 2002 and 2008 in central/southern Chile based on monthly samples. The brokenline shows a significant linear negative trend.

Table 3Abundances and biomass (mean ± SE) of dominant pelagic copepods found during the zooplanktontime series at Concepción location (36�300S) during 2002–2008. RA = relative abundances.

Species Abundance(Number m�3)

Biomass(mg DW m�3)

RA (%)

Paracalanus cf. indicus 142.1 ± 24.16 0.49 ± 0.141 45.0Oithona similis 84.0 ± 17.31 0.18 ± 0.044 28.4Calanus chilensis 38.4 ± 10.33 1.48 ± 0.548 12.0Oncaea spp. 10.6 ± 4.19 0.02 ± 0.013 2.4Rhincalanus nasutus 10.2 ± 4.05 0.26 ± 0.153 4.0Centropages brachiatus 9.2 ± 4.80 0.12 ± 0.048 1.9Acartia tonsa 8.7 ± 2.15 0.13 ± 0.046 4.6Pleuromamma gracilis 3.6 ± 1.80 0.02 ± 0.009 1.4

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Fig. 7. (a) Seasonal (upwelling and non-upwelling seasons) mean of estimated total copepod biomass and the proportion of copepod biomass to total zooplankton biomass,and (b) mean seasonal abundance of dominant species at Station 18 off central/southern Chile between 2002 and 2008. Means were obtained from monthly samplecollections and species biomass from weight–length relationships.

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4. Discussion

Various limitations can be ascribed to both time series. Firstly,they did not include the analysis of the whole zooplankton com-munity, but only copepods, and estimates of the bulk of zooplank-ton biomass were available only for Concepción. It was thusassumed that biomass and abundance of dominant copepod spe-cies may represent variation of the whole zooplankton assemblage.Off Concepción, it was possible to assess the contribution of cope-pods to total zooplankton biomass. On occasions, dominant cope-pods represented more than 30% of total zooplankton biomass,although for most of the time series their contribution wasbetween 5% and 10%. Possibly an important part of biomassaccounted by euphausiids could have been overlooked, becausethey may be abundant at times of the year in the Chilean upwellingregion (Escribano et al., 2007). However, the bulk of zooplanktonbiomass is comprised by a variety of taxa in this region. Some ofthem may not be numerically abundant, but can be important con-tributors to the dry mass, such as decapoda larvae and gelatinouszooplankton, such as siphonophora, appendicularian and chaetog-natha (Escribano et al., 2007). In any case, despite this apparentlysmall contribution to total zooplankton biomass, dominant cope-pods appear to reflect the temporal patterns of zooplankton varia-tion in this region.

Spatial coverage and replication (both in time and space) arecertainly further limitations in our data. For the Antofagasta series,

sampling was close to shore with a maximal depth of 130 m, cov-ering a limited area in Bay Mejillones. In this respect, it should bementioned that Bay Mejillones is strongly subjected to the upwell-ing center at the Mejillones Peninsula (Marín et al., 2001) and sincethe continental shelf in this area is very narrow (<20 km), the shelfbreak is close to shore, so that zooplankton widely distributed inthe coastal area is well represented in the inshore as well (Escrib-ano and Hidalgo, 2000). Therefore, we conclude that copepod spe-cies found in our sampling stations can properly represent thecopepod community of this upwelling zone, and dominant speciesare indeed the same as those reported by Escribano and Hidalgo(2000), who sampled the entire coastal zone around the MejillonesPeninsula. On the vertical plane, on the other hand, some speciesdistributed deeper in the water column may have been underesti-mated. The upper limit of the oxygen minimum zone (OMZ)(<0.5 mL O2 L�1) in Bay Mejillones may remain within the upper50 m most of the year (Escribano, 1998). Most of dominant cope-pods, however, are constrained to the upper 50 m in the coastalzone off northern Chile, and within the copepod community onlyE. inermis seem to persistently inhabit the OMZ (Escribano et al.,2009).

Only two samplings per year were available for Antofagasta, lim-iting the analysis of intra-annual variability, and also causing lessreplication of the year cycle. This limitation, however, can be min-imized given the weaker seasonal signal in copepod abundances inthis upwelling zone as a result of the continuous reproduction of

Fig. 8. Seasonal (upwelling and non-upwelling seasons) mean of biomass of dominant copepods at Station 18 off central/southern Chile between 2002 and 2008. Speciesbiomasses were obtained from their numerical abundance from monthly sample collections and species weight–length relationships.

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dominant species throughout the year (Escribano and McLaren,1999; Hidalgo and Escribano, 2008). For the Concepción series, asingle sampling point (Station 18) precludes any assessment of spa-tial variation, although in this case monthly samples provided us

information on intra-annual and even intra-seasonal variation(Escribano et al., 2007). In any case, all these limitations shouldbe kept on mind when inferring general patterns of zooplanktonvariation over seasonal, interannual or longer time scales.

Fig. 9. Total copepod biomass and Ekman transport at Station 18 off central/southern Chile between mid 2003 and beginning 2008, based on monthly samples. Copepodbiomass was derived from copepod abundance and weight–length relationships and Ekman transport from wind data from a coastal meteorological station.

Fig. 10. Comparison of Ekman transport between Antofagasta off northern Chile and Concepción off central/southern Chile for the period 2003 and 2007. Ekman transportwas accumulated monthly from daily estimates based on wind data obtained from a coastal meteorological station.

184 R. Escribano et al. / Progress in Oceanography 97–100 (2012) 174–186

Seasonal patterns of variation at both sites seem an importantfeature of these zooplankton series. The northern upwelling regionoff Chile has been considered as having intermittent and perma-nent upwelling throughout the year. Our data indeed show upwell-ing-favorable winds year round in Antofagasta, but there is also aclear seasonal patterns characterized by greatly increased intensityof upwelling in the summer. Seasonal patterns in copepods are alsopersistent with greater biomasses and abundances in the summerupwelling season. In central/south of Chile, upwelling is stronglyseasonal (Sobarzo et al., 2007) and here downwelling prevails inwinter, as shown by negative values of Ek. Copepods also exhibitgreater abundances during the upwelling season (spring–summer).Reproduction and production of copepods intensify in the spring–summer at both sites (Escribano and McLaren, 1999; Vargas et al.,2006) and thus populations aggregate in the food-rich upwellingcenters. However, the physical process of upwelling itself can help

concentrate zooplankton. Upon increased upwelling the presenceof coastal fronts may cause coastal aggregation of copepods(Giraldo et al., 2009), while the ascent of the OMZ may cause moreaggregation in the upper layer (Manríquez et al., 2009). If samplingtakes place in the upwelling zone, and usually in upper 100 m, in-creased concentration of populations is thus expected whenupwelling is more intense. Therefore, patterns of seasonal variabil-ity may be the result of changes driven by the annual life cycles ofpopulations (Hidalgo and Escribano, 2007; 2008), or spatial distri-bution forced by upwelling affected sampling.

When examining the 20 years time series from Antofagasta, adecadal pattern of variability became evident. Decadal periods,however, are better seen when examining annual means (Fig. 3c).The increase of copepod biomass between 1987 and 1997 was sud-denly interrupted by the 1997–1998 El Niño. During 1997, at the on-set of this El Niño event in May 1997 (Ulloa et al., 2001), copepods

R. Escribano et al. / Progress in Oceanography 97–100 (2012) 174–186 185

indeed increased in biomass and number, as previously reported forthe population of C. chilensis, whose production increased in thatyear due to the increase in temperature (Ulloa et al., 2001). Thisoccurred because the population was apparently growing with nofood limitation and growth was temperature-dependent. However,copepods abruptly decreased in numbers and biomass in 1998, theyear after the El Niño. Thereafter, copepods increased again by1999–2002 to gradually decrease until the end of the observationperiod (2008). Thus, the entire time series can be divided into threephases: (1) a positive trend (1988–1997), (2) an abrupt decline (ENperiod), and (3) a negative trend (2000–2008). It is interesting tonote that variation in upwelling also exhibited three phases coinci-dent with the patterns in copepod biomass. This coupling betweenupwelling and copepods can be summarized in three phases as well:(1) copepods tended to increase and seem favored with moderateupwelling intensity (1988–1997), (2) copepods abruptly declinewith strongly depleted upwelling (1997–1999, EN period), and (3)copepods gradually decrease when upwelling becomes too intense(2000–2008). These phases can also be inferred when looking at therelationship between upwelling variation and copepod biomass.This shows both series nearly in phase during 1988 and up to theEl Niño event (1997), but then they diverge and become negativelyrelated from 2000 to 2008 (Fig. 5).

In the 7-years series off Concepción we can assess both seasonalan interannual patterns of copepods and biomass. Clearly, most ofthe variability is concentrated in annual peaks in biomass, usuallytaking place during the upwelling season (spring–summer), butthere was also a significant negative trend reflected in both totalzooplankton and copepods biomasses when looking at interannualvariations, although this was not apparent in total copepod num-bers. This may be explained because larger-sized copepods, suchas C. chilensis and R. nasutus, decreased through time possibly caus-ing the decrease in biomass, but smaller-sized copepods, such as P.cf. indicus and Oithona spp. increased in number, thereby compen-sating numerical losses of the larger species. It should also be notedthat the negative trend of zooplankton biomass shown in Fig. 6may largely be explained by greater values of biomass in 2002and early 2003, the result of the high abundance of euphausiids(Escribano et al., 2007), although it also appears that copepod bio-mass was higher at that time (Fig. 7a). In any case, copepod bio-mass in this region did not show a clear or significant associationwith variations in upwelling strength. It may be that a longer timeseries is needed in order to assess the connection between upwell-ing and the copepod community.

Environmental variability in the Pacific basin has mostly beenviewed in terms of ENSO variation, based on interdecadal andinterannual changes (Enfield and Mestas-Nuñez, 2000). For in-stance, interdecadal regime-shifts are considered to impact smallpelagic fishes (Lluch-Belda et al., 1992; Chavez et al., 2003),whereas interannual changes are associated with cold and warmphases of ENSO (El Niño, La Niña) that cause drastic changes in pro-duction and biomass at low trophic levels, as well as abrupt alter-ations of the physical and chemical properties of the water column(Chavez et al., 2002; Escribano et al., 2004).

Long series of zooplankton in the Pacific basin, as that off Peru-vian waters (Ayón et al., 2004), may exhibit variation associatedwith interdecadal periods or regime shifts, reflected in increasedbiomass (as zooplankton volume) during cold regimes, and lowerbiomass upon warmer periods (Ayón et al., 2004). It is not clear,however, if such coupling to regime shifts results from bottom-up or top down regulation of zooplankton and this is certainly animportant question for understanding long-term trends (Perryet al., 2004).

In this context, the analysis of our time series may provide someinsights for understanding the relationship between the environ-ment and zooplankton variation. Firstly, we found evidence of a

link between upwelling intensity and copepod biomass, at leastin northern Chile. Nevertheless, the relationship between variationin upwelling and copepod biomass is not a simple one and it rathersuggests there exists an optimal range of upwelling intensity thatyields the greatest copepod biomass. Greatly depressed upwelling,like that after the 1997–1998 El Niño, might impact food resources.It may be not just quantity, as Ulloa et al. (2001) showed that Chlo-rophyll-a remained high during El Niño, but food quality. At leastthe microplankton fraction seems drastically modified during ElNiño (Iriarte et al., 2000), and it is known that microplankton com-position is a key issue affecting copepod growth and recruitment inthe Chilean upwelling system (Vargas et al., 2006). Strong upwell-ing on the other hand, may favor intense blooms of chain-formingdiatoms, whose quality value as copepod food is matter of debate(Vargas et al., 2006; Poulet et al., 2007). Strong upwelling also pro-motes an extremely shallow oxygen minimum zone (OMZ) whichmay constrain zooplankton in the upper layer (Manríquez et al.,2009) giving rise to increased predation and perhaps increasedcopepod mortality (Thiel et al., 2007; Manríquez et al., 2009).Another potential negative impact of strong upwelling on cope-pods populations is increased offshore advection (Peterson,1998). It may thus be possible that the gradual decline in copepodbiomass observed in northern Chile (2000–2008) has resulted froma greatly augmented upwelling intensity in the eastern south Paci-fic. In fact, the Humboldt Current System has been suggested asbeing dominated by La Niña during the last decade (2000–2008),with greater upwelling intensity and even becoming colder (ca.�0.1 �C) in the last two decades (Belkin, 2009). Recent work alsoshows that complete assemblages of copepods can be advected off-shore by mesoscale eddies originated in the upwelling zone offChile (Morales et al., 2010).

Acknowledgements

Time series work at Antofagasta has been supported by theInstituto de Investigaciones Oceanológicas of Universidad de Anto-fagasta and the times series off Concepción by FONDAP Program ofCONICYT, Chile. Students from Universidad of Antofagasta havecontributed to field work, among them M. Rojo, D. Fernándezshould be mentioned. At Station 18 a number of students of Uni-versity of Concepción have contributed to samplings, sample anal-yses and data processing. Three anonymous reviewers havesubstantially contributed to improve this work after many keycomments and suggestion. We are also thankful to Dave Mackasfor helping us clarify ideas and correct earlier versions of the paper.

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