Population dynamics of Calanus chilensis in the ChileanEastern Boundary Humboldt Current

RUBEN ESCRIBANO

Instituto de Investigaciones OceanoloÂgicas, Universidad deAntofagasta, PO Box 170, Antofagasta, Chile (e-mail:escriban@reuna.cl)

ABSTRACT

A study of the population dynamics of Calanus chilensiswas carried out in the coastal area of the MejillonesPeninsula (23°S), which is an upwelling site in theEastern Boundary Humboldt Current. Information wasderived from time-series sampling (15 day interval) atthree stations, and from two broad-scale cruises: underactive upwelling, and under 1997/1998 El NinÄo con-ditions. Calanus chilensis showed continuous repro-duction throughout the year. In the study area,upwelling takes place intermittently year-round, sug-gesting that Calanus production is not limited by food.Advection played an important role in structuring thespatial distribution of Calanus, both during upwellingand under El NinÄo conditions. Population losses fromupwelling and offshore transport may be compensatedby rapid turnover rates of cohorts, growing at tem-perature-dependent rates and hence allowing popula-tion recovery, even in abnormally warm waters duringEl NinÄo conditions.

Key words: Calanus, El NinÄo, food limitation,temperature, upwelling

INTRODUCTION

The Eastern Boundary Humbold Current (EBHC) isrecognized as one of the large and highly productivemarine ecosystems of the world oceans (Mann andLazier, 1991). This system owes its productivity to thefertilizing effect of wind-driven upwelling and is sub-ject to major interannual variation because of El NinÄoevents. In the coastal area of northern Chile, popu-

lations of Calanus chilensis Brodsky, an abundant(Heinrich, 1973) herbivorous copepod, may bestrongly in¯uenced by the variability caused by theinterplay between upwelling-dominated periods and ElNinÄo years. Upwelling may induce high primary pro-duction rates, but this seems to be restricted to anarrow continental shelf off central and northernChile. Calanus completes its life cycle in coastal watersand must cope with a high variability in temperatureand food availability, both of which may vary withupwelling and the presence of abnormally warm watersduring El NinÄo conditions.

Earlier observations suggested that C. chilensis innorthern Chilean waters might grow under non-lim-iting conditions of food availability. The evidencecame from a multigenerational life cycle and contin-uous year-round reproduction (Escribano and Rodri-guez, 1994). However, more recent experimental workhas shown that development rates of C. chilensis arestrongly dependent on food quantity and that devel-opment may be greatly retarded at food levels likely tobe found at times in the ®eld (Escribano et al., 1997).Nevertheless, the extent to which animals are indeedexposed to such low levels of food is an open question,given the high spatial and temporal variability of foodin upwelling systems.

In addition to its fertilizing effects, upwelling maypose constraints on the population dynamics of Calanus.For instance, the dependence of development andgrowth rates of copepods on ambient temperature mayexert a major effect on cohort development and pro-duction. Pulses of upwelling may drastically changewater-column strati®cation and temperature condi-tions, thus regulating copepod growth. Moreover, thevertical distribution of C. chilensis is restricted to theupper 50 m layer (Boyd et al., 1980; Sameoto, 1981),perhaps limited by a typically shallow oxygen-minimumlayer (OML, <0.5 mL O2 L±1) in the coastal area ofnorthern Chile (Morales et al., 1996). Such an OMLmay limit the vertical distribution of Calanus and pre-vent copepods from performing diel vertical migrations.Restricted vertical distribution might then cause signi-®cant population losses from the upwelling centres dueto offshore advection (Peterson et al., 1979; Wroblew-ski, 1980).

Received for publication 20 March 1998

Accepted for publication 3 July 1998

FISHERIES OCEANOGRAPHY Fish. Oceanogr. 7:3/4, 245±251, 1998

Ó 1998 Blackwell Science Ltd. 245

In the present work, the in¯uence of variability ofcoastal upwelling and the presence of the 1997/1998El NinÄo on the population dynamics of C. chilensis inthe Humboldt Current is analysed. The interactionbetween horizontal and vertical distribution is alsoexamined, under supposedly `normal' upwelling con-ditions and during an El NinÄo situation. The studyaims to answer whether or not food availability mayact as a limiting factor for growth and development ofcohorts. If the annual life cycle is not limited by food,temperature may be the crucial variable to understandand predict secondary production.

MATERIALS AND METHODS

Information for the present study is derived from twosources. The ®rst was a one year time series of sam-pling, from June 1996 to June 1997, at roughly 15 dayintervals, in the northern Bay of Mejillones (23°S).Three stations inside the bay (Fig. 1) were sampled toobtain oceanographic data and zooplankton. Thesecond source consisted of two broad-scale surveysduring December 1996 and July 1997, covering 53 and60 stations, respectively (Fig. 1).

A similar sampling procedure was applied in boththe time-series sampling and the broad-scale surveys.Oceanographic CTD pro®les and zooplankton sampleswere obtained in the upper 200 m for the surveys anddown to 80 m in the Bay of Mejillones for the timeseries. Temperature, salinity and dissolved oxygenwere obtained with a SeaBird SBE-19 CTD equippedwith a YSI Beckman oxygen sensor, while ¯uorescencewas measured with a Wetstar ¯uorometer attached toan Ocean Sensor CTD OS200. Fluorescence wasconverted to chlorophyll a concentration after anin situ calibration, in which chlorophyll a was esti-mated by ®ltering 1 L of seawater obtained at ®vedepths through GF/C Whatman ®lters, extractingpigments in 90% v/v acetone for 24 h and readingabsorbance at 665 nm, according to Strickland andParsons (1972).

For the broad-scale surveys, zooplankton was sam-pled with a 200 lm Hensen-type General Oceanicsnet, equipped with a double opening-closing systemand a digital ¯owmeter to estimate the ®ltered volumeof water. The net was hauled vertically at about 1 ms±1 in two depth strata: 200±50 m and 50±0 m. Sam-ples were preserved in 10% buffered formalin. Duringthe July survey, an additional 100 lm mesh net washauled vertically from 50 to 0 m. This sample was usedto estimate the abundance of copepod eggs. In thetime-series sampling, a 100 lm mesh zooplankton netwas hauled vertically from near the bottom to the

surface. This net was assumed to retain equally allstages of Calanus, including eggs and nauplii.

Variability of upwelling was analysed from wind dataand sea surface temperature (SST). Wind speed and di-rection was measured from November 1996 to July 1997at one near-shore station (Fig. 1). Measurements weremade at 5 min intervals, from which hourly vector av-erages were obtained. SST was measured every 4 h usingtwo temperature data loggers located at about 1 m depthin each bay (Fig. 1). Frequency and intensity of upwel-ling was estimated from the Ekman transport (Bowden,1983), using the equation given by Mann and Lazier(1991):

Mx � sy=f; �1�

where Mx represents Ekman transport (m3 s±1 km±1), fis the Coriolis parameter and sy denotes the along-shore wind stress (Pa). Mx is positive for south windsand negative for north winds, and tau (s) was esti-mated as:

sy � qcd�VyjVyj�; �2�

Figure 1. Map of the Mejillones Peninsula. Dots indicatethe stations for the broad-scale surveys. The crosses in thenorthern bay show the three stations for the time-seriessampling. The small square at I. Sta Maria indicates thestation for collection of the wind data.

246 R. Escribano

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where qa is the air density (1.2 kg m±3), Cd is anempirical constant (� 0.0013) and Vy is the velocityof the alongshore component of the wind (m s±1).

Variability of upwelling was studied by applicationof a cross-correlation function between time series ofEkman transport and daily means of SST, whileeventual in¯uences of oceanographic factors on pop-ulation parameters of C. chilensis were examined bystepwise multiple regressions, ®xing P� 0.1 to retainsigni®cant variables.

To study the vertical distribution of copepoditestages, a vertical migration parameter (VMP) was es-timated, in accordance with Huntley and Escritor(1991), as:

VMP � log�n1=n2�; �3�

where n1 and n2 are total abundances of copepodites inthe upper 50 m of the water column and in the deep(200±50 m) layer, respectively.

RESULTS

Annual cycle

The seasonal cycle of water-column temperature ischaracterized by a cold mixed period in the australwinter (June/July), then a highly strati®ed periodduring the austral spring/summer with surface warmingand a shallow thermocline. There was an intrusion of awarm water mass, at the end of April, when the 1997/98 El NinÄo ®rst appeared in the area (Fig. 2a). Phy-toplankton biomass, however, remained high(>5 mg a m±3 of chlorophyll a) in April and May1997, and only by July/August 1997 were the levelssharply reduced (Fig. 2b). Low levels of oxygen(<1 mL L±1) were observed throughout the year below50 m depth, except after the intrusion of El NinÄowater when the entire water column became oxygen-ated (Fig. 2c).

Figure 3 shows daily measurements of SST and es-timated Ekman transport. From November 1996 toJuly 1997, SST showed a signi®cant positive warming

Figure 2. Oceanographic conditions in the Bay of Mejillones over a 1 year cycle. (a) Temperature, (b) chlorophyll a and (c)dissolved oxygen. Contours were constructed from mean values at the three sampling stations, at resolutions of 5 m from thesurface to the bottom and a time interval of 15 days.

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Population dynamics of Calanus chilensis 247

trend (F1, 279 � 143, P < 0.001). After the arrival ofEl NinÄo conditions SST became more stable. How-ever, potential upwelling, as indicated by Ekmantransport, remained high and positive for the entireperiod. Also there was a strong negative cross-corre-lation between SST and Ekman transport, which wassigni®cant for time lags of up to 3 days (r > 0.30 ,P < 0.05), suggesting that upwelling was not inhibitedby the presence of El NinÄo.

The seasonal cycle of C. chilensis in the Bay ofMejillones was dominated by sharp changes in totalbiomass and numbers. In the cold winter/spring period(June±October), biomass was high and then it de-creased through the summer, but tended to increaseslightly again during winter 1997 (June±July) whenEl NinÄo conditions were present (Fig. 4a). Thenumber of individuals was high in the summer, be-cause the population was mostly represented by nau-plii and early copepodite stages (Fig. 4b). Eggabundance also declined in the summer (Fig. 4c),even though the sex ratio was more or less stable(Fig. 4d). Stepwise multiple regressions (P � 0.1 toretain variables) showed no in¯uence of either tem-perature or chlorophyll a on biomass, number, or eggabundance of C. chilensis.

Spatial variation

The SST distribution shows that upwelling was activein December 1996, resulting in various nearshore cold-water lenses. SST ranged between 16°C and 20.9°C,in the upwelling lenses and in offshore waters, re-spectively (Fig. 5a). In July 1997 (Fig. 5b), SST wasmore uniform in the range of 17.8°C to 19.8°C. Someupwelling was apparently taking place, although up-welled waters were still relatively warm at around

18°C. Surface chlorophyll a was in the range of 1.1±6.4 mg m±3 in December, while in July the range was1.2±4.5 mg m±3. Surface chlorophyll a distribution(Fig. 5c,d) was negatively associated with SST inDecember (r � ± 0.607, P < 0.001), but not in July(r � ± 0.156, P > 0.05).

Figure 3. Estimated Ekman transport (vertical bars) and sea surface temperature (SST; continuous line) at the MejillonesPeninsula, during November 1996 and July 1997. Ekman transport was estimated from hourly wind data and temperaturemeasured four times a day.

Figure 4. Annual cycle of Calanus chilensis in the Bay ofMejillones during June 1996 and July 1997. Data are plottedas means of the three sampling stations (Fig. 1). Biomass (a)was estimated from dry weights and numbers of individualstages.

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248 R. Escribano

Stepwise multiple regression revealed a strong as-sociation between total abundance of C. chilensis(Fig. 6a) and the chlorophyll a maximum at eachsampling station in December (F � 15.515,P < 0.001), although in July the total abundance(Fig. 6b) was negatively associated with SST(F � 10.336, P < 0.01), but not with either surface ormaximum chlorophyll a at each station.

The vertical migration parameter (VMP) as afunction of time of the day did not show any diel mi-gration pattern on either cruise, although it did revealthat in July, copepods were more restricted to the upper50 m, as compared with the December cruise (Fig. 7).

DISCUSSION

Development and growth of marine copepods may bedetermined primarily by ambient temperature (Landry,1975; Miller et al., 1977; Uye, 1988; Huntley and Lo-pez, 1992), although this is a matter of some contro-versy (Huntley and Boyd, 1984; Mullin, 1991; Kleppelet al., 1996). In this regard, C. chilensis has been as-

sumed to be growing without food limitationthroughout the year (Escribano and Rodriguez, 1994,1995). The evidence for this supposition is based ontheir year-round reproduction and the appearance ofsuccessive cohorts. Indeed, conditions in the EBHCseem to favour upwelling all year round (Marin et al.,1993; also the present study), even under El NinÄoconditions (Fig. 3). This upwelling might sustain highprimary production rates throughout the year,preventing the occurrence of food-limited periods forCalanus. The presence of high biomass, high numbersof copepodites and eggs, and a stable sex ratiothroughout seasons, all of which were not correlatedwith food quantity, indicate that reproduction is takingplace all year round. This gives additional support tothe view that Calanus is able to complete its annual lifecycle under non-limiting conditions of food availabilty.

During upwelling, abundance of Calanus cope-podites is associated with chlorophyll a, which is mostlyconcentrated within and around the upwelling lensesand ®laments. Aggregation of copepods in upwellinglenses may result from advection that simply

Figure 5. Sea surface temperatureand chlorophyll a distribution in thearea of the Mejillones Peninsula duringtwo surveys: December 1996 (upwel-ling situation) and July 1997 (1997/1998 El NinÄo conditions). Contourlines were constructed from stationpositions shown in Fig. 1.

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Population dynamics of Calanus chilensis 249

accumulates individuals in frontal zones derived fromthe surface waters being transported offshore. Thisphysical effect on horizontal distribution may causeaggregation of copepods in zones where high phyto-plankton biomass is expected and may thus promotegrowth under conditions without food limitation. Such

a pattern of distribution may be drastically changedduring El NinÄo conditions, when the water mass in alarge extension becomes more homogeneous and nostrong frontal zones are developed. This change mightexplain the lack of correlation between copepodabundance and temperature observed during El NinÄoconditions. Nevertheless, even during these condi-tions, chlorophyll a levels are not dramatically low,suggesting that copepods may still be growing at tem-perature-dependent rates. In fact, in our time series inthe Bay of Mejillones, copepod abundance does notseem to be affected by the ®rst appearance of El NinÄo. Ifdevelopment, growth and hence production rates aretemperature dependent, the population could recoverrapidly and the rapid succession of cohorts at hightemperatures might compensate for advective losses tooffshore waters.

ACNOWLEDGEMENTS

This work has been funded by FONDECYT±Chile,Grant 196/1265 and the Chilean National ProgrammeFONDAP. Valuable comments on the manuscriptwere provided by Ian McLaren. This article is a con-tribution to Chile±GLOBEC National Programmefrom Programa de OceanografõÂa FONDAP±Humboldt.

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Figure 6. Spatial distribution of Cal-anus chilensis copepodites in the area ofMejillones Peninsula during two sur-veys: (a) December 1996 (upwellingsituation) and (b) July 1997 (1997/1998 El NinÄo conditions). Numbers areintegrated over the depth range 200 mto the surface.

Figure 7. The vertical migration parameter (VMP) as afunction of time of the day in Calanus chilensis during twosurveys: (a) December 1996 (upwelling situation) and (b)July 1997 (1997/ 1998 El NinÄo conditions). Positive valuesindicate greater abundance in the upper 50 m layer, whilenegative values represent greater abundance in the deep(200±50 m) layer.

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