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Coastal upwelling circulation and its influence on the population dynamics ofCalanus chilensis (Brodski, 1959) off northern Chile (23°S)Alan Giraldo a; Ruben Escribano b; Victor Marín c; Pamela Hidalgo b

a Grupo de Investigación en Ecología Animal, Departamento de Biología, Universidad del Valle, Cali,Colombia b Center for Oceanographic Research in the South-Eastern Pacific (COPAS), Departamento deOceanografía, Universidad de Concepción, Chile c Departamento de Ciencias Ecológicas, Facultad deCiencias, Universidad de Chile, Santiago, Chile

Online Publication Date: 01 May 2009

To cite this Article Giraldo, Alan, Escribano, Ruben, Marín, Victor and Hidalgo, Pamela(2009)'Coastal upwelling circulation and itsinfluence on the population dynamics of Calanus chilensis (Brodski, 1959) off northern Chile (23°S)',Marine Biology Research,5:3,244— 256

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ORIGINAL ARTICLE

Coastal upwelling circulation and its influence on the populationdynamics of Calanus chilensis (Brodski, 1959) off northernChile (238S)

ALAN GIRALDO*1, RUBEN ESCRIBANO2, VICTOR MARIN3 & PAMELA HIDALGO2

1Grupo de Investigacion en Ecologıa Animal, Departamento de Biologıa, Universidad del Valle, Cali, Colombia; 2Center

for Oceanographic Research in the South-Eastern Pacific (COPAS), Departamento de Oceanografıa, Universidad de

Concepcion, Chile; 3Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile, Santiago, Chile

AbstractMarine pelagic copepods must cope with a highly heterogeneous environment in coastal upwelling systems. In addition tospatial and temporal heterogeneity in temperature and food supply, advective forces may strongly influence theirpopulations. Off northern Chile, the population of Calanus chilensis, a dominant copepod associated with upwelling centres,is subjected to large interannual variations in abundance, not explained by changing temperature regimes occurring uponcold and warm phases of the ENSO (El Nino Southern Oscillation) cycle. During two spring and two summer periods(1998�2000), we studied the abundance, distribution and growth of the copepodids of C. chilensis. The instantaneous meanweight-specific growth rate was estimated as 0.29 day�1 and was not significantly different among cruises. Weights of latestages did not differ either. However, the numerical abundance and biomass substantially differed among cruises, such thatdaily production of copepodids increased with greater biomasses. Chlorophyll-a was significantly greater in spring 1999 andsummer 2000, as compared to spring 1998 and summer 1999, coinciding with greater abundances of copepodids andstronger upwelling. The current field in the upper 200 m indicated that strong upwelling favoured nearshore waterretention, whereas weak or moderate upwelling caused more offshore advection. This finding is opposite to the usual viewthat strong upwelling favours offshore advection. We further concluded that neither food or temperature had muchinfluence on growth, abundance and production of C. chilensis, but instead seasonal and interannual variation in upwellingcaused by changes in local winds may be the primary cause for the observed fluctuations in population abundance.

Key words: Calanus, coastal upwelling, copepodid growth, Humboldt current, Chile, Antofagasta, 238 00?S, 708 30?W

Introduction

Advection is one of the environment factors

that exert important effects on the success of

zooplanktonic cohorts (Peterson 1998). For exam-

ple, if water circulation generates the conditions for

intense expatriation (e.g. high offshore advection)

from a retention area (e.g. near the upwelling focus),

then it can indeed play a major role in population

dynamics. Advective patterns depend upon the

interaction between local (e.g. winds) and remote

(e.g. coastally trapped waves) forcing, bottom topo-

graphy, coastline geometry and the physical struc-

ture (density) of the water column. Off northern

Chile, Shaffer et al. (1997) have concluded that

currents in the upper 300 m strongly depend upon

local wind forcing. Marın et al. (1993) and Marın

and Olivares (1999), studying Mejillones Bay (238S), have pointed out that local wind events explain

much of the biological variability both at daily and

seasonal scales. Marın et al. (2001) have also

suggested that currents in the upper 200 m in the

coastal zone can be explained as an Ekman dynamics

occurring on top of a poleward flow.

At the upwelling site off Mejillones Peninsula, the

calanoid copepod Calanus chilensis Brodsky, 1959 is a

key herbivore species. It is highly abundant and well

aggregated in the coastal upwelling zone (Escribano

1998). Spatial heterogeneity of temperature during

*Correspondence: Alan Giraldo, Grupo de Investigacion en Ecologıa Animal, Departamento de Biologıa, Universidad del Valle. A.A.

25360, Cali � Colombia. Email: agiraldo@univalle.edu.co

Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory,

University of Copenhagen, Denmark

Marine Biology Research, 2009; 5: 244�256

(Accepted 24 June 2008; Printed 19 May 2009)

ISSN 1745-1000 print/ISSN 1745-1019 online # 2009 Taylor & Francis

DOI: 10.1080/17451000802425635

Downloaded By: [Giraldo, Alan] At: 17:38 13 May 2009

active upwelling can have important influences in its

physiological responses, mainly on the development

rate, giving rise to variability in growth and reproduc-

tion success (Giraldo et al. 2002). Spatial hetero-

geneity during upwelling is also reflected in the

distribution of food resources for this species, at least

in terms of chlorophyll-a (Escribano 1998), although

Escribano and McLaren (1999) and Giraldo et al.

(2002) have pointed out that food is not a limiting

factor for population growth of this copepod, and that

individuals may grow at temperature-dependent

rates.

The northern area of Chile may also be subjected

to strong interannual variability, mostly derived from

the alternate phases of the ENSO (El Nino Southern

Oscillation) cycle. During the cold phase of ENSO

coastal upwelling seems more intense and primary

production might be higher, whereas under the

warm phase of ENSO upwelling appears as depleted

and productivity reduced (see Arntz & Fahrbach

1996 for a review). In other words, there seem to be

years with high productivity and others with low

productivity. It is not known if such year-to-year

variation in productivity affects the population

growth of copepods, like Calanus chilensis. In fact,

Escribano & Hidalgo (2000) found a high and

unexplained interannual variability in Calanus abun-

dances in the area from 1991 to 1999. These authors

suggested that interannual changes in mortality rates

may have produced such variation, because neither

temperature nor food showed any association with

copepod abundance.

Variability in mortality may be caused by

increased predation, but as stated by Peterson

(1998) advection might be the key factor regulating

mortality of pelagic copepods in coastal upwelling

systems. The current view states that upon strong

upwelling, offshore advection may increase losses of

copepodids remaining in the upper Ekman layer

(Peterson 1998). Off the Mejillones Peninsula,

however, increased upwelling may give rise to the

existence of retention zones near the coast, which

might prevent offshore advection of copepodids

(Giraldo et al. 2002) and fish larvae (Rojas et al.

2002). These retention areas will allow copepods

cohorts to fully develop, aggregated in the rich

upwellling centres. Conversely, if upwelling is

weak, the cohorts become dispersed, along with

their food, which is then more diluted. Under this

condition, individuals may be more exposed to be

advected away from the nearshore zone. Therefore

variation in upwelling intensity modifying the ad-

vective environment may strongly influence copepod

populations, such as that of C. chilensis. To examine

this hypothesis, in this work we used information

from four cruises performed during the spring/

summer period in 1998, 1999 and 2000. We aimed

at evaluating the effects of changing upwelling

intensity on population abundance, growth and

production of Calanus chilensis, over a seasonal and

interannual scale.

Methods and materials

Sampling methods

Four cruises were carried out: spring 1998 (October

1998), summer 1999 (January 1999), spring 1999

(November 1999) and summer 2000 (January 2000)

in the northern area off Mejillones Peninsula

(238 01’ 40.45’ S�708 30’ 45.32’ W), where a nearly

permanent upwelling plume can be observed.

Because this plume may change in position and

extension, a different oceanographic grid was sur-

veyed at each cruise (Figure 1), in order to adjust it

to the position of the upwelling plume, such that a

nearly equal number of sampling stations were inside

and outside of the cold upwelled waters. At

each station, direct current profiling in the upper

200 m was carried out using an Acoustic Doppler

current meter, Aanderaa RCM-9. Conductivity�temperature�depth�oxygen, and fluorescence pro-

files were also obtained with a SeaBird-SBE-19

CTD, and Wetstar fluorometer. Fluorescence units

were later converted to Chlorophyll-a concentration

(mg m�3) through an in situ calibration described in

Escribano & McLaren (1999). The sampling grid

was completed in about 30 h on each occasion to

obtain a synoptic description of the physical envir-

onment during upwelling. Further details on meth-

ods for oceanographic and current profiling were

provided in Marın et al. (2001).

A day after the oceanographic grid was finished,

zooplankton samples were obtained from four sta-

tions (Figure 1) in three depth strata: 0�20 m, 20�80 m and 80�200 m, using a Hensen type net with

0.5 m opening, 200 mm mesh, equipped with a

double opening�closing system and a calibrated

General Oceanic flowmeter. The stations were

chosen such that two were inside and two outside

of the cold upwelling plume, although sufficiently

close to each other so that they could be all sampled

during a single daytime or nighttime period to avoid

any diel change in vertical distribution of copepods.

Sampling was replicated during two consecutive

days at both daytime and nighttime periods, to yield

a total number of 48 samples per cruise. This design

was applied in October 1998, January 1999, and

November 1999. In the last cruise, during January

2000, we sampled the whole oceanographic grid

through integrated (0�80 m) net tows to better

examine the spatial distribution of copepods. On

Calanus chilensis and coastal upwelling circulation 245

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this occasion, 27 stations were thus sampled,

coinciding with the oceanographic grid (Figure 1).

Zooplankton analysis

Individual Calanus chilensis were sorted from the

samples after one week of preservation. All copepo-

did stages were identified and counted. Nauplii were

not analysed presuming that the 200 mm net could

not properly sample them. Depending on abun-

dance, about 10 individual copepodite stages C5,

and 10 adult females were chosen from all the

samples of the upper 20 m layer and from integrated

samples of the January 2000 cruise. The prosome

lengths of all individuals were measured. These

individuals were quickly rinsed in distilled water,

NorthernChile

EasternSouthPacific

23.5S

23.3S

23.1S

22.9S

22.7S

Antofagasta

Mejillones

Meteorologicalstation

Lat

tiud

e

Oceanographic grids

PuntaAngamos

Oct 1998Jan 1999Nov 1999Jan 2000

71.0W 70.8W 70.6W 70.4W 70.2WLongitude

23.5S

23.3S

23.1S

22.9S

22.7S

Oct 1998, Jan 1999, Nov 1999Jan 2000

Zooplankton Stations

Antofagasta

Mejillones

PuntaAngamos

November

Figure 1. The Mejillones Peninsula upwelling site at northern Chile in the Eastern South Pacific, illustrating the sampling grids for the four

oceanographic cruises and the zooplankton stations.

246 A. Giraldo et al.

Downloaded By: [Giraldo, Alan] At: 17:38 13 May 2009

placed in pre-weighed aluminium pans and dried to

constant weight (�12 h) at 708C. Dry weight

was recorded to the nearest 10 mg with a Denver

microbalance. Dry weights were corrected for losses

from preservation by increasing them in 30% as in

Escribano & McLaren (1999) and carbon content

was assumed as 40% of dry weight (Omori & Ikeda

1984; Bamstedt 1986). Dry weight of early copepo-

dids (C1 to C4) were estimated from their prosome

lengths and applying the weight-length regression

given by Escribano & McLaren (1999).

Weight-specific growth rate (gi) of the i-stage was

estimated according to Escribano & McLaren

(1999) as follows:

gi � ln (Wi�1=Wi)=Di; (1)

where Wi�1 and Wi are the weights of two sub-

sequent stages and Di the development time between

these stages. Temperature-dependent stage duration

between C1 and adult females was estimated from

the equation given by Escribano & McLaren (1999)

as:

Di � pi [5887 (T�11:0)�2:05]; (2)

where pi is the proportion of time occupied by each

copepodite stage, relative to the time from hatching

to CI, and assuming the ‘equiproportional rule’ of

Corkett et al. (1986), and T is the temperature

measured in the field at 10 m depth.

The physical environment

We characterized the advective environment for each

sampling period based on the analysis of three types

of variables: wind records, satellite images and direct

current measurements. Wind data were obtained

from the meteorological station at the local airport

(Figure 1) and satellite data from NOAA, AVHRR

images. For wind data we defined three parameters:

(1) upwelling phase (Up-phase): an upwelling event

can be split into three phases � spin-up, max-wind

and spin-down. Studying the wind records, we

recorded the phase of upwelling at the time of

sampling; (2) days from a large upwelling event

(LUE): large upwelling event (LUE) was defined as

a period of alongshore speeds ]5 m s�1. We used

the wind records to determine the time lapsed

between a previous LUE and each sampling date;

(3) Ekman transport, estimated from the alongshore

component of wind, as Mx�ty/f, where Mx repre-

sent Ekman transport (m3 s�1 km�1), f is the

Coriolis parameter and t the wind stress estimated

in according to Bowden (1983). Accumulated Mx

during the seven days prior sampling was used to

characterize prevailing upwelling conditions during

each period.

Upwelling filaments are advected in different

directions depending upon wind conditions.

Filaments can be advected equatorward and offshore

(458 left of the prevailing wind), or equatorward

along the coast (Marın et al. 2001). Therefore, in

order to characterize the advective environment, we

defined two parameters easily obtained from recti-

fied satellite images, (1) length of the filament

(LOF), defined as the total length of the filament,

in km, from the upwelling focus (Punta Angamos),

and (2) maximum offshore extension (MOE), de-

fined as maximum offshore distance, in km, using

the longitude of Punta Angamos as reference.

Finally, we used direct current measurements to

characterize the advective environment. We selected

five depths (5 m, 10 m, 20 m, 50 m and 75 m) in the

0�80 m depth range and computed spatially aver-

aged u and v components. All physical measure-

ments of upwelling filament were carried out follow

Marin et al. (2001). Statistics were calculated using

ARCWIEW Gis 3.1.

Results

The physical and biological environment

Satellite data and in situ measurements showed well-

developed upwelling plumes during the four cruises,

as illustrated by sea surface temperature (SST)

(Figure 2). The spring 1998 and spring 1999 were

much colder than both summers. During the spring

condition the mean SST was 14.58C and 14.78C for

1998 and 1999, respectively. In the summer mean

SST was 18.28C and 18.58C for 1999 and 2000.

Surface (mean concentration in the upper 5 m)

chlorophyll-a (Chl a) was higher near the coast

and showed substantial variation among the cruises.

In the spring 1998 surface Chl a was low and

averaged 2 mg l�1, while in the summer 2000 the

highest values were found averaging 10 mg l�1. In all

cases Chl a appeared aggregated inside the upwelling

plume judging by its greater values associated with

upwelled water exhibiting higher density (Figure 3).

From the wind and satellite data the values for all

derived parameters are shown in Table I. Time series

of wind records are shown in Figure 4. From current

measurements 2D current vectors were constructed

(depth�5 m) and they are shown in Figure 5. In

October 1998 our sampling took place 6 days after a

large upwelling event occurred during a spin-down

phase (Table I; Figure 4). Indeed, wind had

been spinning-up four days prior to our sampling.

Accordingly, we found the largest filament (91 km)

reaching to the maximum offshore distance (50 km).

If we assume that a 4-day steady current generated

the filament, it would require an equatorward speed

Calanus chilensis and coastal upwelling circulation 247

Downloaded By: [Giraldo, Alan] At: 17:38 13 May 2009

of 0.3 m s�1 (u��0.14 m s�1, v��0.26 m s�1)

which is within the measured range (see November

1999 below). However, at the time of sampling wind

was already in the spin-down phase and the 0�75 m

water column was moving southward at an average

speed of 0.2 m s�1. The fastest near-surface velocities

(Figure 5) (0.3 m s�1, 2108) occurred close to the

shoreline, whereas the slowest (0.1 m s�1, 1608) at

71.0ºW 70.5º W23.3ºS

23.0ºS

22.7ºS

SST (ºC)Jan. 2000

19.0

19.0

18.0

19.0

18.0

71.0ºW 70.0º W

23.5ºS

22.5º S

23.0º S

Jan 14 2000

N

Nubes14.0 - 14.514.5 - 15.015.0 - 15.515.5 - 16.016.0 - 16.516.5 - 17.017.0 - 17.517.5 - 18.0

Tierra

18.0 - 19.019.0 - 20.0

23.0º S

22.5º S

23.5ºS

N

Nubes14.0 - 14.514.5 - 15.015.0 - 15.515.5 - 16.016.0 - 16.516.5 - 17.017.0 - 17.517.5 - 18.0

Tierra

18.0 - 19.019.0 - 20.0

Jan 17 1999

23.5ºS

22.5º S

23.0º S

Nov 07 1999

N

Oct 01 1998

N

71.0ºW 70.5ºW23.3ºS

23.0ºS

22.7ºS

SST (ºC)Nov. 1999

17.0 16.016.0

15.0

71.0ºW 70.5ºW23.3ºS

23.0ºS

22.7ºS

SST (ºC)Jan. 1999

18.0 17

.0

18.019.0

20.0

71.0ºW 70.5ºW23.3ºS

23.0ºS

22.7ºS

SST (ºC)Oct. 1998

15.0

16.0

16.0

Figure 2. Distribution of sea surface temperature (SST) measured in situ (left panels) and through satellite images from NOAA (right

panels) in the upwelling site off Mejillones Peninsula for four occasions.

248 A. Giraldo et al.

Downloaded By: [Giraldo, Alan] At: 17:38 13 May 2009

23.3ºS

23.0ºS

22.7ºS

23.3ºS

23.0ºS

22.7ºS

23.3ºS

23.0ºS

22.7ºS

23.3ºS

23.0ºS

22.7ºS

Jan. 2000

Nov. 1999

Jan. 1999

Oct.1998

71.0ºW 70.5ºW

Nov. 1999

Jan. 1999

Oct. 1998

Jan. 2000

Chl-a Sigma-T

1.6

1.6

1.61.6

2.2

2.2

25.6

25.8

25.8

25.9

24.4

24.6

24.825.0

25.0

26.2

26.4

1.5

2.0

2.0

1.5

2.5

2.02.02.5

Chl-a Sigma-T

3.0 25.6

Chl-a Sigma-T

Chl-a Sigma-T

4.0

3.04.0

4.0

3.0

4.0

25.8

25.626.0

25.8

26.025.8

25.025.2 25.2

25.0

25.3

25.0

24.8

25.225.3 25

.4

3.05.0

9.0

3.0

3.0 5.0 7.0

11.0

5.0

71.0ºW 70.5ºW

Figure 3. Distribution of surface Chlorophyll-a (Chl a) (mg m�3) and water density (Sigma-T) at surface, during four oceanographic

surveys off Mejillones Peninsula during active coastal upwelling.

Calanus chilensis and coastal upwelling circulation 249

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locations where satellite images showed the presence

of cold temperature filaments.

In January 1999 the sampling occurred during a

low wind period, with alongshore wind speed less

than 4 m s�1. Although the wind was at its max-

imum during sampling, it had been spinning-down

for more than 12 days and the last large upwelling

event had occurred 10 days previously (Figure 4).

Thus, contrary to what we observed on October

1998, the upwelling filament just reached 11 km

offshore with a total length of 35 km. Currents at all

depths were moving southward with an average

speed of 0.34 m s�1. The near-surface current field

showed a southward flow that followed the coastline

(Figure 5).

November 1999 was the only period sampled

during a spin-up phase. Currents were measured

after the wind was spinning-up for two days (Figure

4). Alongshore wind speed was 0.5 m s�1 slower

than the previous spring period (October 1998) and

Table I. Parameters used to characterize the advective environment off Mejillones Peninsula for each sampling period. Wind parameters

are: phase of upwelling (Up-phase), days after a large upwelling event (LUE) and one-week accumulated Ekman transport (the week prior

to sampling). Satellite parameters are maximum offshore extension of the main upwelling filament (MOE) and length of the upwelling

filament (LOF).

Wind parameters

Period Up-phase LUE (days) Ekman Transport (m3 km�1�107)

October 1998 Spin-down 6 4.72

January 1999 Max-w 10 8.08

November 1999 Spin-up 3 11.65

January 2000 Spin-down 3 13.45

Satellite-image parameters

Period MOE (km) LOF (km)

October 1998 50 91

January 1999 11 35

November 1999 8 39

January 2000 Not available Not available

0.0

2.0

4.0

6.0

8.0

0.0

2.0

4.0

6.0

8.0

0.0

2.0

4.0

6.0

8.0

0.0

2.0

4.0

6.0

8.0

19-Sep 24-Sep 29-Sep 4-Oct 9-Oct 14-Oct 31-Dec 5-Jan 10-Jan 15-Jan 20-Jan 25-Jan 30-Jan

27-Oct 1-Nov v6-Nov 11-Nov 16-Nov 21-Nov 26-Nov 30-Dic 4-Jan 9-Jan 14-Jan 19-Jan 24-Jan

Oct.1998

Nov. 1999

Jan.1999

0002.naJ

Alo

ngsh

ore

win

d (m

s-1 )

Alo

ngsh

ore

win

d (m

s-1 )

Alo

ngsh

ore

win

d (m

s-1 )

Alo

ngsh

ore

win

d (m

s-1 )

Figure 4. Daily records of the alongshore component of wind. The black dots indicate the days when the oceanographic surveys took place

in each period.

250 A. Giraldo et al.

Downloaded By: [Giraldo, Alan] At: 17:38 13 May 2009

the last upwelling event had occurred only three days

before (Figure 4). The upwelling filament was much

smaller (total length�39 km) reaching only 8 km

offshore. Equatorward flows were found only at a

depth of 5 m (Table I), both with an onshore

component, inside Mejillones Bay (average�0.38 m s�1, 308), and an offshore component

(average�0.3 m s�1, 3408) off Punta Angamos

(Figure 5). This flow reversed poleward-onshore at

10 m (average�0.27 m s�1, 1358). Below 10 m the

flow was poleward as in the other sampling periods

(average�0.2 m s�1, 1608)The January 2000 sampling period corre-

sponded, as October 1998, to a spin-down phase

although with a faster alongshore wind speed

(Table I, Figure 4). Changes in alongshore wind

speed occurred at a somewhat higher frequency, i.e.

shorter upwelling events, than in the other sam-

pling periods. The dominant flow was clearly pole-

ward (average�0.33 m s�1, 2088).Integrated Ekman transport for seven days pre-

vious to sampling was considerably different among

sampling periods with the lowest value in October

1998, reaching a maximum by January 2000

(Table I).

Copepodid abundance and growth

Since abundance and growth of Calanus chilensis may

vary in according to location, i.e. within or outside

the upwelling plume (Giraldo et al. 2002), we

divided and treated separately our data for both

zones. Table II summarizes the abundance of all

stages for each cruise inside and outside the upwel-

ling plumes in the upper 80 m. There were remark-

able and significant differences in copepodid

abundances between periods (F3,74�14.6, p�

0.01). Abundance was also higher inside the upwel-

ling plume than outside, except for the summer

1999 (Table II). There was also variation in stage

23.30°S

23.10°S

22.90°S

22.70°S

Oct 1998 0.7m s-1 Jan 1999 0.7m s-1

Jan 2000 0.7ms-1Nov 1999 0.7m s-1

70.80° W 70.40° W 70.80° W 70.40° W

23.30°S

23.10°S

22.90°S

22.70°S

Figure 5. Vector diagrams for the current velocity at 5 m during each sampling period. The current fields were obtained from direct

measurements.

Table II. Abundance (mean9SD) of copepodid stages of Calanus

chilensis during upwelling off Mejillones Peninsula for four

sampling periods. All copepodid stages from C1 to adult were

added.

Integrated abundance (number m�2)

Sampling period Inside plume Outside plume

October 1998 384.29301.98 229.29138.95

January 1999 101.8996.59 118.8983.50

November 1999 2557.391640.82 729.69297.55

January 2000 14,753.8914,452.91 5166.692370.42

Calanus chilensis and coastal upwelling circulation 251

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frequency distribution, both between periods and

location (inside/outside the plume) with increased

abundance of young copepodids (C1 to C3) during

November 1999 and January 2000, although all

copepodid stages were present during the four

sampling periods (Figure 6), suggesting that produc-

tion of cohorts was occurring in all cases.

In order to examine if copepodids were actually

exposed to potential transport in the upper more

advective Ekman layer, which corresponds to the

upper 20 m in the study area (Marın et al. 2001), we

compared the vertical distribution of copepodid

stages between two sampled strata (0�20 m and

20�80 m) during November 1999, when all stages

were well represented (Figure 6). Since samples were

obtained in daytime and nighttime hours, a vertical

distribution index (VDI) was calculated as VDI�ln

(n1)/ln(n2), where n1 and n2 are the abundances

(number m�2) in two adjacent vertical strata. The

VDI as a function of sampling time is shown in

Figure 7. Early C1�C3 appeared aggregated in the

upper 20 m layer, independently of time of the day,

with no evidence for diel vertical migration (DVM).

Stage C4 seem more uniformly distributed in both

0�20 and 20�80 m layers and they do not seem to

perform DVM either. Stage C5 and adult females

became more abundant in the deeper 20�80 m layer

in the daytime and they might have been performing

DVM, whereas adult males showed a similar pattern

as C4 (Figure 7).

Size of adult females might reflect growing condi-

tions during copepodid development. Dry weight of

females was highly variable both within and between

sampling periods, but there were no significant

differences between periods (F3,146�2.4, p�0.05).

The instantaneous weight-specific growth rate (g)

also showed much variation within periods, i.e.

between upwelling vs. non-upwelling zones (Table III).

0 10 20 30 40 50 60

Sta

ges

C1

C2

C3

C4

C5

adM

AdF

Upwelling

Non-upwelling

0 5 10 15 20 25 30 35

C1

C2

C3

C4

C5

adM

AdF

0 5 10 15 20 25 30

C1

C2

C3

C4

C5

adM

AdF

Frequency (%)0 5 10 15 20 25 30

C1

C2

C3

C4

C5

adM

AdF

October 1998

January 1999

November 1999January 2000

Figure 6. Stage distribution (%) of copepodids of Calanus chilensis sampled during four periods inside (upwelling) and outside (non-

upwelling) of the upwelling plume off Mejillones Peninsula. AdF and AdM are adult females and males, respectively.

252 A. Giraldo et al.

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This variation is mostly explained by differences in

temperature between zones. This because lower

temperatures inside the upwelling plume yield longer

durations of stages, since they are estimated by a

temperature-dependent equation (Equation 2), thus

reducing the growth rate. Among sampling periods

however the variation of g did not show a clear

tendency and judging by overlapping standard devia-

tions in all cases they do not significantly differ to each

other. To avoid any seasonal effect we compared g

between both springs and summers. Between spring

1998 and spring 1999 the value of t-test was 0.3

(p�0.05) and between summer 1999 and summer

2000 the t-test was 0.10 (p�0.05), confirming

the absence of significant difference in copepodid

growth.

Discussion

The four sampling periods covered distinct phases of

an upwelling event. November 1999 corresponded

to spin-up, January 1999 to maximum wind and

October 1998 and January 2000 to spin-down.

Upwelling intensity was also substantially different

judging by estimated amounts of Ekman transport.

The near-surface (5 m) current field responded to

these different wind phases as expected from a

system where Ekman dynamics occurs on top of a

poleward flow (Marın et al. 2001). That is, during

spin-up, cold water filaments with a 0.3 m s�1

equatorward speed are generated at Punta Angamos.

If spin-up conditions are maintained for at least 4

days, then offshore filaments are generated otherwise

only onshore filaments are found (i.e. Marin et al.

2001). The shift or reversal in surface currents

during the spin-up/spin-down transition seems to

be rather fast (B1 day), as exemplified by a

comparison of velocities during both October 1998

and January 2000. The spin-down condition is

characterized by a 0.2 m s�1 poleward flow. Our

data and those of Shaffer et al. (1997) suggest that

this flow has a seasonal component, being faster

during summer.

From the standpoint of zooplankton expatriation,

the offshore component (u) may be critical. This

component, based on our current meter and satellite

image data, fluctuated between�0.14 and

0.07 m s�1. Thus, taking into account that the

VD

I [I

n(n 1

/n2)

]

-3

-2

-1

0

1

2

3

0 4 8 12 16 20 24

0 4 8 12 16 20 24

-3

-2

-1

0

1

2

3

C1-C3

C4

Sampling time(h)

-3

-2

-1

0

1

2

3C5

-3

-2

-1

0

1

2

3

-3

-2

-1

0

1

2

3Adult females

Adult males

0 4 8 12 16 20 24

0 4 8 12 16 20 24

0 4 8 12 16 20 24

Figure 7. The vertical distribution index (VDI) as a function of

sampling time of copepodid stages of Calanus chilensis during

upwelling in November 1999 sampled in two depth strata: 0�20 m

and 20�80 m off Mejillones Peninsula. The shaded areas indicate

nighttime hours.

Table III. Female weights (W), the weight-specific growth rate (g)

and daily production rate (PR) of the copepodids of Calanus

chilensis off Mejillones Peninsula during four periods. Estimated

values were divided into two different sampling zones: upwelling

(inside the upwelling plume) and non-upwelling (outside the

upwelling plume). W was estimated from individuals (n��30)

for each period and g is the mean from all copepodids from C1

through adult females.

Sampling period Zone W (mg) g (day�1)

October 1998 Upwelling 217958.3 0.2690.072

Non-upwelling 178941.7 0.2790.093

January 1999 Upwelling 164952.4 0.2690.094

Non-upwelling 155937.9 0.3190.114

November 1999 Upwelling 155952.2 0.2090.089

Non-upwelling 153925.3 0.2790.131

January 2000 Upwelling 116935.8 0.2190.107

Non-upwelling 107931.8 0.2590.138

Calanus chilensis and coastal upwelling circulation 253

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spin-up phase may last 4 days, organisms may be

advected up to 50 km offshore, a condition that

could have occurred during October 1998 and

January 1999. If we considered the average value

for u (Bu���0.06 m s�1), then a 4-day spin-up

phase would transport organisms only 20 km off-

shore. This last condition would apply to the flows

during November 1999 and January 2000.

Considering the data presented in this paper, the

data from Shaffer et al. (1997) and Marın et al.

(2001), the coastal ocean in the northern Humboldt

Current System (up to at least 50 km offshore) is

dominated by a poleward flow covering the upper

300 m of the water column. Upwelling events,

generated by increases in the always-dominant south

winds, may reverse the surface (B10 m) currents.

These equatorward flows influenced by the coastal

geometry and bottom topography generate cold water

filaments that may advect organisms as far as 50 km

offshore. However, the most ‘typical’ condition seems

to be that offshore advection will only reach 10 km

offshore.

Calanus chilensis belongs to the C. helgolandicus

species group (Bradford 1988). One of the charac-

teristics of the species in this group is that copepodite

stage C5 overwinter in deep water, a strategy

associated to the advantage of ‘return flows’ which

would mantain species in ‘optimum environments’

(Bradford 1988). Calanus chilensis is then an ‘unu-

sual’ species given its absence of deep water over-

wintering (Gonzalez & Marın 1998) and lack, or

limited, DVM as shown in Figure 7 and as previously

reported by Escribano (1998). Vertical distribution

limited to the upper layer might a consequence of the

shallow oxygen minimum layer in the coastal zone off

northern Chile (Morales et al. 1999), which may

impose constraints for vertical migration of zoo-

plankton (Ulloa et al. 2001; Rojas et al. 2002).

Variability in copepodid abundance between sam-

pling periods may result from the influence of

changing environmental conditions. Increased pri-

mary production and hence better food conditions

may have resulted in greater population growth in

the last two cruises, when Chla was higher and

upwelling more intense. However all cruises were

carried out during spring�summer conditions, i.e.

during the reproductive period for the species

(Escribano & Rodriguez 1994) and even although

Chla was greater in November 1999 and January

2000, adult sizes and growth rates were not sig-

nificantly greater. This species seems to continu-

ously reproduce in the area throughout the year

(Escribano & McLaren 1999) and the possibility of

food-limitation for its population growth seems

unlikely, especially in the spring/summer period.

Moreover, Chla may be considered only as an index

Weak/moderate upwelling Strong upwelling

High advection

High retention

Poleward current Poleward current

Calanus lowabundance

Calanus highabundance

Figure 8. A conceptual model to illustrate the effect of changing upwelling intensity on the interplay between water advection and retention

of the surface layer off Mejillones Peninsula (northern Chile). The outcome from the interaction between the cold upwelling plume and a

poleward current can be modulated by intensity of upwelling resulting in variable advective conditions, which may affect the abundance of

copepodids of Calanus chilensis.

254 A. Giraldo et al.

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of food availability, because other food sources, such

as components of the microzooplancton are very

abundant in this upwellling area (Gonzalez et al.

2000), and may serve as alternate food resources for

C. chilensis, as reported for other Calanus species

(Ohman & Runge 1994).

Temperature is another factor affecting individual

growth in copepods (Huntley & Lopez 1992) and

thus potentially influencing population abundance.

Indeed, we should recall that our estimates of growth

come from a temperature-dependent model, i.e.

increased temperatures should yield greater growth

rates. However, under increased temperature during

the summer 2000, growth was not incremented;

suggesting that temperature effect on the growth rate

may not suffice to explain differences in biomass and

population abundance. In fact, Escribano & Hidalgo

(2000) found no correlation between temperature

and C. chilensis abundance after 7 years of data from

1991 to 1998. Therefore, variation in copepodid

abundances among cruises in the present study

cannot be explained by our temperature-dependent

growth rates. Losses from the population might be

another line of explanation for variability in popula-

tion size.

Our data showed that upon changing upwelling

intensity the advective environment may shift from a

situation where either retention or offshore advec-

tion can dominate the upper layer (Figure 5).

During October 1998 and January 1999, individuals

were more exposed to offshore transport, coinciding

with low copepodid abundance, as compared to

conditions in November 1999 and January 2000,

when upwelling was more intense, but retention

nearshore was more likely because onshore flows

prevailed (Figure 5). Therefore, offshore advection

may deserve special attention in Mejillones upwel-

ling systems in order to explicate the dynamics of

C. chilensis population size.

The presence of a permanent poleward current

(Shaffer et al. 1997; Marın et al. 2001) in the area,

interacting with the upwelling plume, results in

increased water retention in the nearshore under

conditions of strong upwelling. We have illustrated

the interplay between upwelling intensity and ad-

vective conditions as shown in Figure 8. In this

conceptual model we suggest that weak/moderate

upwelling gives rise to a poleward dominant flow and

the cold plume is advected southwest (see Figure 5).

By contrast, upon strong upwelling the poleward

flow is weakened and a northward and onshore flow

prevails. The later condition will favour Calanus

retention in the upwelling zone, increasing their

abundance and giving rise to higher production

rates, because of greater copepodid biomass.

Further studies should examine the role of chan-

ging predation pressure on the Calanus population.

The possibility that egg production may change

upon varying food availability should also be con-

sidered. Both density-dependent mortality and egg

production rate may strongly influence variability in

population size. In coastal upwelling systems, how-

ever, varying advective conditions appear as a key

role regulating population size and production of

epipelagic copepods.

Acknowledgements

The field study was supported by FONDECYT-

Chile, Grant 198-0366. Data analysis and manu-

script preparation was supported by the Center for

Oceanographic Research in the South-Eastern

Pacific (COPAS) funded by FONDAP-CONICYT

Program of Chile.

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