Hydrobiologia 453/454: 143–151, 2001.R.M. Lopes, J.W. Reid & C.E.F. Rocha (eds), Copepoda: Developments in Ecology, Biology and Systematics.© 2001 Kluwer Academic Publishers. Printed in the Netherlands.

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The influence of coastal upwelling on the distribution of Calanus chilensisin the Mejillones Peninsula (northern Chile): implications for itspopulation dynamics

Ruben Escribano1, Victor H. Marin2 & Pamela Hidalgo1

1Instituto de Investigaciones Oceanologicas, Universidad de Antofagasta, P.O. Box 170, Antofagasta,Chile. E-mail: rescribano@uantof.cl2Departamento de Ciencias Ecologicas, Universidad de Chile, Santiago, Chile

Key words: Calanus, upwelling, production, advection, temperature effects

Abstract

A field experiment was carried out in October 1998 during active upwelling in a coastal area off the MejillonesPeninsula (23◦ S). Zooplankton was sampled at day and night, during two subsequent days at 4 stations inside andoutside of the upwelling plume. Three depth strata were sampled: 0–20 m, 20–80 m and 80–200 m. Oceanographicdata were obtained in a grid of 23 stations using a CTDO, a fluorometer and a Doppler current meter. Calanuschilensis was mostly represented by late stages, i.e. copepodid C5 and adult males and females. There were noday/night effects on vertical distribution, and abundance was significantly higher inside the upwelling plume in theupper 20-m layer at nearly 14 ind. m−3, compared to ca. 5 ind. m−3 outside the upwelling plume. Temperatureat 10 m depth and biomass, estimated from stage numbers and their mean dry weights, were used to estimategrowth and daily production of Calanus at temperature-dependent rates. The potential loss of biomass from theupwelling center because of advection in the upwelling plume was estimated from current data in the Ekmanlayer and biomass density. The mean cross-shelf component of the current was estimated at 10.4 km d−1 withinthe upwelling plume. This yielded a loss of biomass of 9.7 mg dry weight m−2 . Production, estimated by atemperature-dependent approach, ranged between 44 and 35 mg dry weight m−2 d−1, at mean temperatures of14.6 ◦C and 15.8 ◦C inside and outside of the upwelling plume respectively. Within the plume, as much as 22%of daily production may be advected offshore. However, a higher concentration of biomass in the upwelling plumeallowed a greater production compared to surrounding areas. A mass balance approach suggests that advectivelosses may not have a major impact on the C. chilensis population, because of very high daily production attemperature-dependent rates.

Introduction

In coastal upwelling systems, epipelagic copepodsmust cope with offshore transport because of advec-tion driven by the cross-shelf component in the Ek-man layer (Bowden, 1983; Hutchings et al., 1995;Graham & Largier, 1997; Peterson, 1998). Frac-tions of populations may be advected away fromupwelling centers and hence become separated fromhigh nearshore concentrations of phytoplankton, themain food source of most planktonic copepods. Somecopepods may exhibit adaptations to avoid such off-shore advection. Among these adaptations, diel ver-

tical migration (DVM) has been proposed as partof a dispersal/retention mechanism (Peterson et al.,1979). In upwelling systems, such as the northernBenguela, copepods species do exhibit vertical move-ments, at least within the upper 100 m (Verheye etal., 1992, 1994). Thus, DVM may play an importantrole for retention in that system. The occurrence ofcoastal eddies and alongshore components of currentsmight also help to prevent offshore transport (Wrob-lewski, 1980; Hutchings et al., 1995). Retention zonescan also develop as a result of upwelling fronts innearshore areas that cause an ‘upwelling shadow’ nearthe coast (Graham & Largier, 1997). All these mech-

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anisms may operate in upwelling zones, but still someproportion of cohorts may undergo offshore transportduring active upwelling. The impact that these pro-cesses may have on quantitative aspects of populationshas not been fully studied.

In northern Chile, there is a wind-driven upwellingcenter off the Mejillones Peninsula (Rodriguez et al.,1991), which is very active year-round (Escribano,1998). In this coastal ecosystem, Calanus chilensisdominates the herbivore zooplankton (Heinrich, 1973;Gonzalez & Marin, 1998). Little is known about themechanisms that allow retention of this calanoid spe-cies in nearshore areas. Upwelling in coastal watersoff the Mejillones Peninsula is very intense and wellrestricted to a narrow band nearshore, where phyto-plankton is mostly concentrated (Escribano, 1998).Offshore transport may affect the available time forfeeding within phytoplankton patches.

Calanus chilensis reproduce continuously year-round at northern Chile (Escribano & Rodriguez,1994, 1995), suggesting that food is not limiting pop-ulation growth (Escribano & McLaren, 1999). Lackof evidence of food shortage was the basic assump-tion to develop a temperature-dependent model toestimate annual production of C. chilensis in the up-welling zone off the Mejillones Peninsula (Escribano& McLaren, 1999). In this paper, we used such amodel to evaluate the role that potential, temperature-dependent, daily production may have in compensat-ing potential population losses due to offshore advec-tion in the upper layer. We estimated potential trans-port by direct measurements of currents during activeupwelling. In addition, we analyzed day/night verticaldistribution, in an attempt to determine whether DVMis an important factor in retaining coastal populationswithin nearshore areas.

Materials and methods

During the austral spring season (early October 1998),a field experiment was carried out onboard the re-search vessel B/C PuriHaalar in the coastal zone offthe Mejillones Peninsula, northern Chile. Sea surfacetemperature (SST) data from two NOAA satellites(NOAA-D and NOAA-J), were used to identify the up-welling plume. Images were downloaded in real time,about four images per day, during September–October1998. These images were used for the planning of asampling grid, consisting of 23 oceanographic stationsand 4 additional stations for zooplankton sampling

(Fig. 1). At each of the oceanographic stations, cur-rents were measured at fixed depths (0, 5, 10, 20, 30,40, 50, 75, 100, 125, 150 and 200 m) using an AnderaaRCM9 profiling current meter. The 23 oceanographicstations were all sampled in about 26 h on October2, 1998. Current data were corrected for the speed ofsound, calculated from temperature and salinity valuesrecorded with a Seabird CTDO. Further analysis ofthe current data was done by removing the vertical-averaged value for each component of velocity. Thevalues for each station were averaged to produce pointestimates for different layers of the water column.These point estimates were in turn used in the gen-eration of surfaces for each component at each layer,using kriging as the interpolation method (Jongmannet al., 1995).

The four zooplankton stations were visited on thetwo subsequent days, October 3–4, 1998. These sta-tions were located inside and outside the upwellingplume, according to SST data, two for each zone.The number of zooplankton stations and the distanceamong them were small, because they had to besampled within a single daytime/nighttime period (∼8 h for the nighttime period). The small number ofstations was partially compensated by replicating thedaytime/nighttime periods. The same hydrographicaldata described above were obtained in the zooplanktonstations. Zooplankton was collected using a Hensennet of 0.5 m in diameter, with a 200 µm mesh,equipped with a Digital General Oceanics flowmeterand a double opening/closing mechanism. Three depthstrata were sampled through vertical tows of the net:0–20 m, 20–80 m and 80–200 m, assuming the upperlayer as representative of the offshore-advective Ek-man layer, the 20–80 m layer as a transition zone, andthe deeper layer as a compensating flow. Zooplanktonsamples were preserved in 10% buffered formalin. Inthe laboratory, all stages of Calanus were sorted, andprosome length measured to the nearest 10 µm. Cope-pod biomass was estimated from numerical abundanceof each stage and its mean dry weight. Copepoditeweights were calculated from the length-weight re-lationships established for this species (Escribano &Rodriguez, 1995; Escribano & McLaren, 1999). Dryweights were corrected for losses from preservation byincreasing them in 30% as in Escribano & McLaren(1999) and carbon content was assumed as 40% of dryweight (Omori & Ikeda, 1984; Båmstedt, 1986).

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Figure 1. Location of the Mejillones Peninsula, near Antofagasta, northern Chile, illustrating the sampling stations of the oceanographic grid,and 4 zooplankton stations. The grid was carried out on October 2, 1998, and zooplankton sampling in the next two subsequent days.

Daily production rates were estimated according toEscribano & McLaren (1999) as follows:

PR =n∑

i=1

Bi(egi − 1), (1)

where PR is production rate (mg dry weight m−2 d−1),Bi is biomass (mg dry weight m−2) of copepoditestages 1–5 (C1–C5), and gi the weight-specific growthrate (d−1) of these stages, estimated as:

gi = ln(Wi+1/Wi)/Di , (2)

where Wi+1 and Wi are the weights of two subsequentstages and Di the development time between thesestages. Temperature-dependent stage durations wereestimated from the equation given by Escribano &McLaren (1999) as:

Di = pi[5887(T + 11.0)−2.05], (3)

where pi is the proportion of time occupied by eachcopepodite stage, relative to the time from hatching toC1, assuming the ‘equiproportional rule’ of Corkett etal. (1986), and T is the temperature measured in thefield at 10 m depth.

Daily copepodite production rates inside and out-side the upwelling plume were calculated by summa-tion of the stage-specific production from C1 to C5.We assumed that females did not experience somaticgrowth once matured. The contribution of egg produc-tion to the total production was not taken into accountin our estimates. The daily copepodid production wasthen compared to advected biomass, which was es-timated as the product between integrated biomass ofCalanus chilensis in the upper 20 m and the mean flowof current inside and outside the upwelling plume.Total integrated biomass of C. chilensis included allcopepodite stages from C1 to adults. We defined dailyloss of biomass as the total (20-m integrated) biomassthat is transported in a day for more than 37 km, whichwas approximately the extent of the upwelling plume.

Results

Oceanographic conditions

Daily satellite images indicated that upwelling wasactive, and that the cold plume persisted in a north-west orientation up to 37 km from the shoreline

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Figure 2. Distribution of sea surface temperature during active upwelling off the Mejillones Peninsula, near Antofagasta, northern Chile:Satellite image is for October 1, 1998, the day before sampling. Dotted lines show in situ measurements of temperature on a 26-h samplinggrid.

Figure 3. Vertical profiles of chlorophyll-a concentration at two distinct areas at the upwelling site off the Mejillones Peninsula, northern Chile:(a) inside the upwelling plume, (b) outside the plume.

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for at least three days during our study (Fig. 2a).Our in situ measurements of sea surface temperat-ure were also consistent with satellite data (Fig. 2b).Chlorophyll-a levels showed a subsurface maximumof 2.2 mg m−3 at about 10 m depth in the stationsinside the plume (Fig. 3a), whereas values were lower(∼1.3 mg m−3) and vertically homogeneous outsidethe plume (Fig. 3b).

The current field (averaged in the upper 20 m)revealed that a branch of the plume was movingeastward into the Mejillones Bay (Fig. 4). This well-marked inflow of recently upwelled water may be animportant mechanism for nutrient input into the bay,and might thus explain its very high primary produc-tion rates (Marin et al., 1993). The magnitudes of thecurrent vectors were in the range of 0.08 and 0.14 ms−1 (Fig. 5). In a vertical section of currents acrossthe upwelling plume (Fig. 6), the current speed de-creased to zero at about 20 m depth over the plumelocation. Therefore, the Ekman layer was probablylocated above the upper 20-m depth.

The average magnitude of the westward flow of theEkman layer within the upwelling plume was about0.12 m s−1 (Fig. 5), which is equivalent to 10.4 kmd−1. Thus, a particle would take about 3.5 d to moveover 37 km. Following the same reasoning, in sur-rounding areas, with an average flow of 0.8 m s−1

(Fig. 5), this time would lengthen to 5.4 d. These es-timates can then be used to estimate mean transport ofbiomass in the upper 20 m layer.

Distribution, production and advection of Calanus

Because the three sampled strata had different depths,copepod density (number m−3) was converted to in-tegrated abundance (number m−2) for each stratum, toallow comparisons between layers and stations. Latecopepodid stages (mainly C5s, adult females, andmales) were predominant in all the samples. Higherabundances were obtained in the 20–80 m layer, andthe population was apparently aggregated within theupwelling plume (Table 1). Analysis of variance (AN-OVA) on log-transformed data showed non-significantdifferences (F1,43 = 0.42, P > 0.05) in total abund-ance (all stages) between the two subsequent daysof sampling. Therefore, data from the two samplingdays were thereafter pooled, resulting in two replic-ate samples for upwelling (UL) and non-upwellinglocations (NUL). We found significant differencesbetween depth strata for all stages, as well as differ-ences between locations (UL and NUL) for adults, but

Table 1. Abundance (number m−2) and vertical distribu-tion of Calanus chilensis during active upwelling off theMejillones Peninsula, northern Chile. Upwelling (UL) andnon-upwelling locations (NUL) are represented by stationsinside and outside of the upwelling plume, respectively. Thepercentage (%) is relative to total abundance in the watercolumn. ADF and ADM: adult females and males

Strata Stage Upwelling Non upwelling

Day Night Day Night

ADF 59.4 122.0 13.4 25.6

ADM 3.8 60.0 4.8 7.8

0–20 m C5 17.4 53.4 34.8 39.6

C4 7.0 32.0 7.8 5.2

C3 0.0 9.0 2.4 2.2

Total 87.6 276.4 63.2 80.4

% 20.7 47.7 19.9 27.0

ADF 100.2 91.2 50.4 21.0

ADM 39.0 48.6 24.0 7.8

20–80 m C5 61.2 61.8 92.4 71.4

C4 72.0 12.6 19.8 69.0

C3 0.6 0.0 2.4 0.0

Total 273.0 214.2 189.0 169.2

% 64.4 37.0 59.4 56.9

ADF 39.6 20.4 22.8 12.0

ADM 4.8 24.0 10.8 6.0

80–200 m C5 18.0 32.4 24.0 28.8

C4 1.2 12.0 8.4 1.2

C3 0.0 0.0 0.0 0.0

Total 63.6 88.8 66.0 48.0

% 15.0 15.3 20.7 16.1

Table 2. Analysis of variance to test differences in distribu-tion of Calanus chilensis sampled day and night, from threedifferent depth strata and from two stations inside (UL) andtwo stations outside (NUL) the upwelling plume. Day/nightsampling was repeated for two subsequent days. ADF andADM: adult females and males, respectively

Source of Stages

variation ADF ADM C5 C4

Strata F-ratio 3.1 5.6 4.9 4.1

P 0.05 <0.01 <0.05 <0.05

Day/Night F-ratio 0.2 1.1 0.1 0.8

P 0.64 0.31 0.80 0.39

UL/NUL F-ratio 10.2 6.4 0.1 0.1

P <0.01 <0.05 0.79 0.85

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Figure 4. Current field off the Mejillones Peninsula, northern Chile, during active upwelling. Vectors represent average intensities of currentsthrough a 26-h sampling period at 23 stations.

Figure 5. Distribution of magnitudes of average speed of currents(m s−1) at the upwelling site off the Mejillones Peninsula, northernChile.

not for copepodids C4 and C5. Day/night effects onabundance were not significant (Table 2).

Table 3. Temperature-dependent production and estimated offshoreadvection of biomass (mg dry weight m−2) of Calanus chilensis inthe upper 20 m layer, at the upwelling site off the Mejillones Pen-insula, northern Chile. Estimates were made on a daily basis forlocations inside the upwelling plume (UL) and outside the plume(NUL), and the balance represents the net gain in daily biomass.Mean temperatures at 10 m depth at both locations were used toestimate biomass production. g is the weight-specific growth ratesestimated by a temperature-dependent model

UL NUL

Temperature (◦C) 14.6 15.8

Mean biomass (mg dry weight m−2) 28.0 10.0

g (d−1) 0.78–1.57 0.86–1.72

Mean daily production 43.5 34.7

(mg dry weight m−2 d−1)

Offshore transport (mg m−2 d−1) 9.7 2.1

Daily loss (%) 22.2 6.0

Daily balance (mg dry weight m−2) 33.8 32.6

Temperatures (means from two stations) at 10 mdepth were 14.6 ◦C and 15.8 ◦C for the upwelling loc-

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ations (UL) and the non-upwelling locations (NUL),respectively. The weight-specific growth rate (g) waslower for late stages (C5) and greater in stage C1. Bio-mass of Calanus chilensis was larger in UL as com-pared to NUL (Table 3). This resulted in higher dailyproduction in the UL, despite a lower temperature. Inthat location, offshore transport was higher, at estim-ated flows of about 10.4 km d−1. This yielded higherbiomass losses in the UL, although compensated byhigher daily production rates (Table 3). If no additionalgains are considered, such as advective inputs to thestudy site, the balance between daily gains (produc-tion) and losses (advection) of biomass under theseconditions indicated that about 22% of daily produc-tion may be advected offshore by remaining in theupper 20 m inside the upwelling plume (Table 3).However, as we noted in Table 3, at both locations thebalances were positive.

Discussion

In coastal upwelling ecosystems, copepods are ex-posed to potential transport offshore. This influencestheir population dynamics, because advected indi-viduals are lost from coastal upwelling areas wherefeeding conditions are favourable for their growth.Although late stages might encounter sufficient foodoffshore to sustain their basic needs, egg productionmay be food-limited (Checkley, 1980), thus affectingthe production of new cohorts.

The maintenance of coastal zooplankton withinupwelling areas may be associated with active mi-gration between layers moving in opposite directions(Peterson et al., 1979; Verheye & Field, 1992). How-ever, the information available on the subject is stillscarce and inconclusive in respect of copepods (Ver-heye et al., 1992). The population of Calanus chilensisin our study area is apparently restricted to the upper50 m of the water column (Escribano, 1998). Dielvertical migration (DVM) is probably limited by lowoxygen waters (<0.5 ml O2 l−1), which may occur inthe upper 100 m nearshore (Morales et al., 1996; Es-cribano, 1998). The present results suggested a patternof DVM by C. chilensis only between the 0–20 m and20–80 m layers in the UL, but this was not evidentin the NUL (Table 1). Such apparent DVM was notdetected by ANOVA, because no significant day/nightdifferences were found (Table 2). In other words, mostof the C. chilensis population remained above 80-

m depth, and offshore advection was likely a majorprocess affecting the dynamics of this species.

Our temperature-dependent method to estimate theproduction of Calanus chilensis assumes that indi-viduals encounter sufficient food to sustain maximalgrowth rates (Escribano & McLaren, 1999). Althoughdevelopment and growth of Calanus chilensis seemto be highly sensitive to food-shortage under labor-atory conditions (Escribano et al., 1997), low foodconcentration is unusual in the study area, at least dur-ing the spring. Escribano & McLaren (1999) foundno evidence of food limitation for production of thisspecies throughout the annual cycle in the same area.However, they also observed substantial horizontalvariability in biomass and cohort development aroundthe coastal zone during the upwelling season. Al-though they explained this variability as derived fromadvection and mixing, the question remained whetherfood-satiating conditions depended on spatial location,as a result of the highly aggregated phytoplankton.The present data showed that food was quite low inareas outside the upwelling plume (Fig. 3), suggestingthat part of the C. chilensis population was exposed tolow food. However, on an annual basis, C. chilensisseems to grow at temperature-dependent rates in mostof the study area (Escribano & Hidalgo, 2000b). Year-round reproduction (Escribano & Rodriguez, 1994),seasonal increase in abundance with temperature (Es-cribano & Hidalgo, 2000b), high abundance of eggsand early stages in all seasons, and lack of correlationof specific production with phytoplankton (Escribano& McLaren, 1999) give further support to this view.

Our mass balance exercise did not consider po-tential sources of biomass accumulation, such as eggproduction, apart from daily in situ production of im-mature copepodids. However, absence of early cope-podids C1 and C2, and very low numbers of C3(Table 1), suggest that contribution from cohort de-velopment was very low at the time of sampling. Anadditional biomass input may occur from advectionand mixing processes, but it is difficult to exam-ine such possibility with the available data. In anycase, our estimates indicate that daily production wasprobably sufficient to compensate for losses from theupwelling center.

Temperature-dependent growth of calanoid cope-pods may not occur in other upwelling systems, suchas the southern Benguela, where a lack of depend-ence of growth on temperature, apparently caused bylow phytoplankton concentration, has been suggested(Pitcher et al., 1996; Richardson & Verheye, 1999).

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Figure 6. Transversal section of current speed (m s−1) across theupwelling plume, showing the Ekman layer located above the upper20 m. Measurements were made over a 26-h sampling period andwere corrected for the tidal cycle by removing the mean vector ofthe water column.

Large copepods are more likely to be food-limitedthan small ones in that area (Richardson & Verheye,1999). Hirst & Lampitt (1998) used a large data set oncopepod growth for modeling the potential interactionbetween temperature and body size on the weight-specific growth rate of copepods. They suggest the useof a general equation:

Log10g = 0.0208[T] − 0.3221[log10BW]−1.1408, (4)

where BW is body weight (µg C), and g and T aspreviously defined. Using our data on mean bodyweights for each copepodid stage, from C1 to C5,and mean temperature at UL and NUL, we estimatedg applying Equation 4. The estimates yielded valuesbetween 0.041 and 0.099 d−1 at UL, and between0.043 and 0.105 d−1 at NUL. These values were con-siderably lower than the estimates of g obtained byour temperature-dependent approach (Table 3), and

yielded much lower (∼ one order of magnitude) dailyproduction rates. Assuming that C. chilensis grows ex-ponentially (Escribano et al., 1997), the developmenttime between stages can be estimated from Equa-tion 2. The mean dry weight of C5 was 132.2 µg,and that of C1 was 8.3 µg. Since g from C1 to C5was 0.07 d−1 on average (as estimated from Equa-tion 4), the development time between C1 and C5would be Di = ln (132.2/8.3)/0.07, i.e. ∼40 d. Be-cause the development time from egg to C1 is about7.5 d at 15 ◦C (Escribano et al., 1998), estimatesbased on Equation 4 imply that the generation timeof C. chilensis is about 50 d. However, identificationof more than 11 generations per year, and consider-able overlapping of cohorts, resulting from continuousproduction at estimated generation times between 15and 22 d (Escribano & McLaren, 1999), strongly sug-gest that Equation 4 underestimates g for C. chilensis,and that our estimates are much more consistent withfield observations of seasonal cohort development inthis zone (Escribano & Rodriguez, 1994; Escribano &McLaren, 1999).

The balance between production and advectionsuggested that about 22% of C. chilensis biomass maybe lost to offshore waters during upwelling. This is animportant fraction of the population that had alreadybeen recruited, although there is a net gain of biomasseach day (Table 3). Advected individuals could re-turn to nearshore waters by sinking at the frontal zoneto reach a reversing flow (Verheye & Field, 1992).However, it is unlikely in the study area, because C.chilensis is restricted to the upper layers (Escribano,1998; Escribano & Hidalgo, 2000a). Large eddies mayalso prevent or decrease offshore transport, but timingis probably a constraint, given the short life-span ofthe local population of C. chilensis.

Acknowledgements

This work received financial support from the ChileanFunding for Science and Technology, FONDECYTgrant 198/0366. Satellite data were provided by theCenter for Spatial Studies of the Universidad de Chile.G. Olivares helped in analyzing current data. HansG. Dam and an anonymous reviewer helped to clarifyideas and provided important corrections to an earlierversion. This work is a contribution to GLOBEC-Chile National Program through Fondap-HumboldtProgram.

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