Temperature-dependent development and growth of Calanus chilensis Brodsky from Northern Chile

LJournal of Experimental Marine Biology and Ecology,229 (1998) 19–34

Temperature-dependent development and growth of Calanuschilensis Brodsky from Northern Chile

*Ruben Escribano , Luis Rodriguez, Claudia IrribarrenInstituto de Investigaciones Oceanologicas, Universidad de Antofagasta, P.O. Box 170, Antofagasta, Chile

Received 2 May 1997; received in revised form 13 December 1997; accepted 9 February 1998

Abstract

Development and growth of Calanus chilensis Brodsky were studied under laboratoryconditions to establish the temperature-dependent rate function of embryonic development, toanalyze potential maternal effects on development rates, and to study development and growthfrom egg to adult. As in previous studies, embryonic duration estimated at 9, 12, 15, 18 and 208C,

ˇ ´was described by the Belehradek model of development and the fitted equation was D 5 947.722.05(T 1 11.0) , where D is embryonic duration (days) and T is temperature (8C). The parameter

values, a 5 947.7 and t 5 11.0, were comparable to those published for C. marshallae. At a0

constant temperature of 158C the embryonic duration depended on females, indicating a significantmaternal effect and increasing variance within temperatures. When reared with excess of food at158C, individual copepodites grew exponentially, with a generation time of 38 days. The

21weight-specific growth rate was 0.114 day , and changes in body length were linear throughtime. Our results show that temperature-dependent predictions of generation time, number ofgenerations per year, and female body size are not consistent with field data, suggesting that foodshortage during the annual cycle may retard development and affect adult body size. An untestedalternative hypothesis involves the potential vertical migration and permanency of individuals indeep waters. Development under low temperatures would give rise to larger animals and to fewergenerations a year, consistent with the temperature-dependent prediction. 1998 ElsevierScience B.V. All rights reserved.

Keywords: Calanus; Development; Growth; Body-size; Temperature

1. Introduction

In coastal areas planktonic copepods appear to exhibit exponential growth, suggestingthat their growth and production can be determined primarily by temperature (seeHuntley and Lopez, 1992 for review).

*Corresponding author. Fax: 156 55 247542; e-mail: [email protected]

0022-0981/98/$ – see front matter 1998 Elsevier Science B.V. All rights reserved.PI I : S0022-0981( 98 )00038-0

20 R. Escribano et al. / J. Exp. Mar. Biol. Ecol. 229 (1998) 19 –34

Temperature-dependent development and growth rates have been reported for Calanusspecies (e.g. McLaren, 1978; Uye, 1988). Such rates, however, are difficult to obtain forlate stages of Calanus species under laboratory conditions because of rearing difficulties(e.g. Marcus and Alatalo, 1989). To partially cope with such difficulties, embryonicduration has been used (e.g. McLaren et al., 1969; Guerrero et al., 1994) to estimateparameters of a temperature function for interspecific comparisons and for extrapolationsto older stages, using some general rules of copepod development (Landry, 1983;Corkett et al., 1986). For example, by applying the ‘equiproportional rule of develop-ment’ (Corkett et al., 1986), the durations of later stages can be derived from embryonicdevelopment times estimated in the laboratory (McLaren and Leonard, 1995). Suchsimplification, however, has not been entirely verified and may be critical in understand-ing the life cycles and annual production of Calanus species, which are majorcomponents of the pelagic ecosystems (e.g. Davis, 1987).

Among Calanus species, C. chilensis Brodsky may be a key link between primaryproducers and pelagic fishes in the Peruvian upwelling ecosystem (e.g. Boyd et al.,1980). The responses to food and temperature of this abundant (Heinrich, 1973) andapparently productive species (Escribano and Rodriguez, 1994) need more attention.Estimates of development rates of embryos and later stages are needed to understand itsannual life cycle (Escribano and Rodriguez, 1994) and the influence of environmentalfactors on development and growth (Escribano and Rodriguez, 1995). Although thisspecies may grow continuously throughout the year at the upwelling area off An-tofagasta (Escribano and Rodriguez, 1994, 1995), recent work (Escribano et al., 1997)indicates that its development and growth rates are highly sensitive to lack of food,suggesting that food might impact the number of generations per year and populationgrowth. This would preclude predictions of development and growth rates of this speciesby temperature alone, as suggested for other copepod species (e.g. Huntley and Lopez,1992). Here we analyze development and growth of C. chilensis under controlledconditions of food satiation, assuming that temperature alone controlled their develop-ment and growth. Then, using field observations on the annual cycle of temperature andphytoplankton biomass (Escribano et al., 1997), the species life cycle (Escribano andRodriguez, 1994), and seasonal size variation (Escribano and Rodriguez, 1995), we testthe consistency of rates of growth and development with those conditions of foodsatiation in the laboratory. Three experiments were carried out and had the followingobjectives: (a) establish the temperature-dependent development rate of eggs (Exp. I);(b) study development and growth rate of copepodid stages (Exp. II); and (c) analyzevariation in embryonic durations at a single temperature (Exp. III). Exp. III was carriedout as an attempt to understand the large variation in embryonic duration withintemperature observed in Exp. I. The possibility of genetic, or maternal effects, or bothon egg development rate was thus explored.

2. Methods

2.1. Field sampling

´Live Calanus for experiments were captured at a central area of Bahıa de Mejillones

R. Escribano et al. / J. Exp. Mar. Biol. Ecol. 229 (1998) 19 –34 21

´Fig. 1. Bahıa de Mejillones showing the sampling area from which C. chilensis copepods were captured tocarry out experiments. Mean depth at the central area is about 60 m.

(238 S), northern Chile (Fig. 1) using a Nansen-type net with 450 mm mesh verticallytowed from 50 to 0 m depth. Samples were immediately diluted with surface waters in68-l coolers and transported to the laboratory within 1 h. Live Calanus were obtainedduring three sampling periods: September–October 1994, December 1994 and April–May 1995. During such periods, phytoplankton was also obtained by towing a fine64-mm net within the upper 20 m layer and used to feed individuals in the experiments.

2.2. Laboratory experiments

Exp. I was performed during September–October 1994. At the time of zooplankton´collection the surface temperature in Bahıa de Mejillones was nearly 168C. Identification

and sorting of animals were performed at a controlled temperature of 98C and low light.From recently captured zooplankton, 60 females were sorted and each was placed inindividual vials (30 ml) containing fresh phytoplankton from the same sampling site,

4 5 21enriched with F/2 medium. Algal concentrations were estimated as 10 –10 cells mland consisted of diatoms and flagellates. Twelve females were maintained at each of fivetemperatures (9, 12, 15, 18 and 208C). Temperatures were maintained using circulatingthermostatic heaters placed in 15-l glass containers in which the vials were partiallyimmersed. Vials were observed every hour until more than five eggs could be counted atthe bottom. After egg laying, the females were removed from the vials, measured forprosome length to the nearest 0.01 mm and individually weighed. Individual dry weightwas obtained after a quick rinse in distilled water, drying to constant weight at 708C for


| 12 h and weighing with repeated (3–4 times) readings using a Denver microbalance tothe nearest 10 mg. After removal of the females, eggs were counted and the medium wasremoved by pipette and replaced with filtered seawater (0.45 mm) aerated overnight. Toestimate embryonic durations, eggs were observed and counted every hour under adissecting microscope at 98C. After each observation vials were gently shaken tooxygenate the eggs and some of the medium replaced by seawater of the sametemperature. Eggs were counted until all had hatched, or until remaining eggs showedsigns of deterioration or death. Temperature was checked 3–4 times daily for eachcontainer.

Exp. II was initiated with samples obtained in late December 1994. When zooplankton´was collected, the temperature in the water column of Bahıa de Mejillones varied

between 128C and 188C from bottom ( | 90 m) to surface, respectively. Sorting wascarried out in a coldroom at 128C, with | 20 females placed in groups of 10 in 500-mlglass jars and fed with fresh phytoplankton obtained in a vertically towed net with64-mm mesh from the same sampling site. The phytoplankton had been previouslysieved with a 153-mm mesh to remove zooplankton and then cultured in F/2 medium ina culture chamber with 12:12 dark:light period. Within 48 h eggs observed on the bottomof the jars were removed by pipette and placed in 150-ml BOD bottles ( | 150 eggs perbottle) with previously aerated and filtered seawater. Approximately 10 ml of phyto-plankton culture was added to each bottle before closing. After 3–4 days, nauplii were

4 21transferred to 1-l glass jars containing fresh medium of 10 cells ml . Quality of thephytoplankton culture was monitored daily under an inverted microscope by identifyingthe taxa present and their concentration. The phytoplankton consisted largely of thediatoms, Asterionella sp., Skeletonema costatum, Cylindroteca closterium andChaetoceros spp., with a smaller proportion of at least three species of flagellates, ofwhich only Dyctiocha fibula has been identified. Species composition did not change

5 6substantially throughout the experiments and the cultures were kept at a level of 10 –1021cells ml by removing and replenishing with enriched F/2 medium. The final

3 4 21concentration in the jars varied between 10 –10 cells ml .A total of eight jars containing between 50 and 100 nauplii were then incubated at

´158C. This temperature was similar to that observed at about 10 m in Bahıa deMejillones during the zooplankton sampling. Temperature in the coldroom was checkedtwice a day using thermometers placed around the jars and vials. As soon as naupliistage N6 and copepodids stage CI were observed, they were transferred to individualvials (30 ml) to obtain estimates of stage durations. The remaining animals were kept inthe 1-l jars, from which between 5–10 individuals were removed daily to obtain dryweights. Vials were observed three times a day under a dissecting microscope to recordthe times when the animals had molted. One l jar was sampled daily and the removedanimals were preserved in 4% formalin for later analysis. Prosome lengths weremeasured to the nearest 0.01 mm under a dissecting microscope with an ocularmicrometer. Dry weight was obtained for groups of animals (depending on the stage):5–10 individuals for CI, 5–10 for CII, 4–6 for CIII, 2–4 for CIV, 2–3 for CV, andindividually for adults. Animals were rinsed with distilled water under a concave slide,placed in pre-weighed aluminum pans, dried to constant weight at 708C, and weighed tothe nearest 10 mg using a Denver microbalance.


Stage durations were chosen as the median time when individuals had molted and thetime of previous observation. Median durations for naupliar stages and for CI, CII, CIII,CIV and CV were used to analyze the course of growth in body length and dry weight.Stage copepodite CI was estimated to occur when 50% of the animals achieved suchstage in each jar. Twelve estimates were made from individual jars. Durations of stagesfrom CI to adult were estimated from animals kept in individual vials.

´Experiment III was performed in April–May 1995. Temperature at that time in Bahıade Mejillones varied between 128C and 178C from bottom to surface. The procedure wassimilar to that of Exp. I, except that we estimated embryonic durations for eitherindividual eggs, or small groups of eggs from same females, at a constant temperature of12.58C. This rather low temperature was chosen to slow down development, such thatmore precise estimates of development rates could be obtained to analyze differencesamong females. Individual females, which laid eggs, were observed every 2 h. By usingthe information derived from Exp. I, 1 h prior to the earliest predicted time of hatchingthe eggs were counted every 20 min and subsequently every 10 min after hatching. Thisallowed estimates of embryonic durations and, by counting the remaining unhatchedeggs, within female variation. Eggs which showed no sign of hatching were not includedin the estimates.

As in previous studies (e.g. McLaren et al., 1988), embryonic duration as a function ofˇ ´temperature was studied using the Belehradek model,

2bD 5 a(T 1 t ) (1)0

where D is embryonic duration (days), T is temperature (8C) and a, t and b are0

constants. The parameter b was fixed with the value 2.05 as in other studies (e.g.McLaren, 1995) and the equation was fitted by non-linear regression, using theQuasi-Newton algorithm (Wilkinson, 1990).

The growth rate of copepodites was analyzed by using the exponential model ofgrowth,

W 5 W exp(Gt) (2)i

where W is dry weight (g), W is initial weight, t is time (days) and G the weight-specifici21growth rate (day ). We used the log linearized version as,

log W 5 log W 1 Gt (3)e e i

Eq. (3) was fitted by non-linear regression and weights of adults were included sincethey were captured as soon as they molted from stage CV, such that somatic growth maystill be taking place.

Finally, potential maternal, or genetic variation in embryonic duration was studiedusing non-parametric statistics for comparing egg developmental times estimated at aconstant temperature (12.58C) from different females. Correlation of egg developmenttimes on female size was not tested, given the small number of females.


3. Results

3.1. Embryonic developmental rate

From Exp. I the observed temperatures in the vials were (mean6S.D.) 9.1360.153,12.3760.121, 15.0860.224, 17.8560.121 and 20.1460.1428C. Although 12 femaleswere incubated at each temperature not all laid eggs and not all eggs hatched. Table 1summarizes the data for female size and number of laid eggs. To account for variation inembryonic duration among eggs within females, we considered using the mean timebetween two consecutive observations when the number of eggs had diminished.However, hatching took place in small groups of eggs hatching simultaneously. To avoidusing abnormally delayed hatching times, we chose hatching time taken by such modalgroups as better estimates of embryonic duration for each temperature. A total number of70 such data points were obtained for the modal groups of hatching time for the fivetemperatures. Embryonic times among temperatures were significantly different (F 54,65

ˇ ´17.4, P,0.001). Belehradek Eq. (1) adequately describes embryonic duration as afunction of temperature (Fig. 2). The estimated parameters and their associated statisticsare shown in Table 2.

3.2. Copepodid growth and development

During Exp. II the temperature in the coldroom did not significantly vary (mean valueof 15.360.0588C) and may be assumed to be constant during development. Table 3summarizes the estimates of stage durations for copepodites CI to CV. The cumulativetime from egg to adult yields an estimated generational time of |38 days. No adultmales were obtained, thus such estimate is only valid for females. The proportion of thistime occupied by each stage egg to adult female are shown in Table 3.

Marine copepods tend to show a linear growth in body length when plotted againstmedian time to reach various stages (e.g. Escribano, 1990), with the proportionate lengthincrements remaining constant through the stages. Such proportionality, when estimatedas |1.253, is known as ‘Brook’s law’ (Miller et al., 1977; Longhurst, 1986). Meanstage durations for copepodites CI to adult plotted against mean body lengths show that

Table 1Summary of results from experiment on embryonic duration of Calanus chilensis at five temperatures

Temp. (8C) N Length (mm) Weight (mg) Eggs number Hatched eggs

9.13 2 2.5360.050 24569.9 46 4112.37 5 2.4660.078 257635.2 82 7915.08 9 2.4760.078 193660.4 321 27317.85 4 2.5260.087 273668.3 226 21920.14 7 2.5060.075 217656.5 219 179

N is the number of females that laid eggs.Length is prosome length (mean6S.D.).Weight is individual dry weight (mean6S.D.).Egg number is the total number of laid eggs.


ˇ ´Fig. 2. Belehradek model describing embryonic development rate of C. chilensis as a function of temperature.Estimates of embryonic durations were obtained at five temperatures and the equation was fitted with a fixedvalue of b as 22.05 using a non-linear regression.

‘Brook’s law’ does not apply to the relationship in C. chilensis (Fig. 3a). Furthermore,although a linear regression can describe this relationship (F 54619, P,0.001), the1,228

mean increments through the stages do not remain constant, but rather suggest distinctphases of length increments during development of copepodids. The greatest incrementsoccur between CI and CII, then become nearly constant at about 30% between stagesfrom CII to CV, followed by a much smaller increment between CV and adulthood(Table 4). Analysis of growth in weight has been treated in a different way from that ofbody length. We assume that growth in body mass occurs continuously between

Table 2ˇ ´Statistical summary after fitting Belehradek equation with parameter b fixed as 2.05 on hatching time of

Calanus chilensis as a function of temperature2Parameter Estimate A.S.E. 95% C.L. r MSR

a 947.7 137.14 674.09–1221.400.73 0.037

t 211.0 1.71 7.51–14.420

The function was fitted with least-square non-linear regression.A.S.E. are asymptotic standard error of the estimates.C.L. are 95% confidence limits.MSR is the mean square residual.


Table 3Stage durations (days) of Calanus chilensis reared in laboratory condition under excess of food and at aconstant temperature of 158C

Stage or phase of development n Mean duration (days) S.D. Time proportion

Naupliar 12 7.4 1.33 0.19CI 12 3.5 0.81 0.09CII 12 4.1 0.98 0.11CIII 12 5.9 1.92 0.15CIV 12 6.5 1.90 0.17CV 6 10.7 3.94 0.28Total time538.1

moulting times, independently of stage of development. After 27 days no moreindividuals were available for estimating dry weight, although a few of them had alreadymatured. These very fast-developing animals did not reach weights greater than 180 mg.Statistical results from curve fitting of Eq. (3) are shown in Table 5, while the finalgrowth model is illustrated in Fig. 3b.

3.3. Variation in development rates

In Exp. III conducted at a constant temperature of 12.58C, out of eggs produced byseven females a total number of 98 estimates of embryonic durations were obtained.Each value representing either a single egg or a small group (2–5) of eggs simul-taneously hatching (Table 6). At this temperature, using pooled data from all females,the embryonic time was 1.4160.110 days (mean6S.D.). This value is close to 1.46 days,

ˇ ´the expected embryonic time predicted by the Belehradek equation derived in Exp. I.Variance of both embryonic time and development rate (1 / time) was not homogeneous

2among females (Bartlett test, x .70, **P.0.05) and there were significant differences6

among females (Kruskall-Wallis test578.19, P,0.01). Such differences result fromfemale no. 4 and female no. 7, whose eggs developed much faster than the eggs from therest of the females (Table 6). Although these females were slightly smaller in body sizethan others (Table 6), it was not possible to establish a relationship between female sizeand egg development rate, because of the small number of females.

3.4. Field observations

We have reorganized the data on phytoplankton and temperature in Escribano et al.(1997) to better understand conditions experienced by individuals in the field throughoutthe annual cycle. The pattern of temperature and stratification was characterized by acold period from June to November and a warm-period from December until May (Fig.4a). Sea surface temperatures were in the range of 15.0 to 20.78C, with a minimal valueduring the winter (July) and maximal values during summer (January to March). Suchlarge temporal variation was generally limited to the upper 20 m layer, due to a high


Fig. 3. Growth in body length (a) and body dry weight (b) of copepodites C. chilensis reared under laboratoryconditions in excess of food and at a constant temperature of 158C. Changes in body length are plotted againstmedian times to reach a copepodite stage (Stage CI to adult), while changes in dry weight are plotted on adaily basis.

level of stratification throughout the year (Fig. 4a). Below 30 m, temperatures were morestable (range of 12.7–14.08C).

The phytoplankton biomass cycle did not seem to be coupled with that of temperatureduring the year (Fig. 4b). There were two periods of high chlorophyll concentration,spring (September to November) and fall (March to May), and two periods of lowphytoplankton, in mid-Winter (June–July) and early Summer (December–January).During the low period, chlorophyll-a concentration reached minimal values around 3 mg

21 21l , while during the high period maximal values were up to 18 mg l .


Table 4Body length and length increments for stages copepodites CI to adult in Calanus chilensis reared in laboratoryconditions under excess of food and at 158C

Stage Mean length (mm) n S.D. Length increment (proportion)

CI 0.61 33 0.044 0.44CII 0.88 38 0.062 0.34CIII 1.18 37 0.077 0.28CIV 1.51 52 0.106 0.30CV 1.96 63 0.116 0.19Adult females 2.33 7 0.214

Table 5Summary statistics for curve fitting of individual growth in body dry weight (DW) in Calanus chilensis fromstages CI to adult, reared in laboratory conditions under excess of food and at 158C

Parameter Estimate S.E. 95% C.L.

Lower Upper

log W 1.153 0.194 0.766 1.541e i

G 0.114 0.010 0.094 0.133

The fitted model was log DW5log W 1G (time), where W is the initial weight at Stage CI, G is thee e i i21instantaneous growth rate (day ).

Table 6Embryonic duration of C. chilensis estimated in the laboratory at a constant temperature of 15.38C

Female N Length (mm) Embryonic duration (days) S.D.

1 19 2.499 1.49 0.1262 9 2.548 1.54 0.0423 14 2.401 1.47 0.0354 23 2.400 1.29** 0.0385 11 2.601 1.40 0.0086 12 2.560 1.42 0.0167 10 2.352 1.27** 0.019

N represents the number of either single eggs, or small groups of eggs (2–5) simultaneously hatching.**Significant differences (P,0.05).

4. Discussion

Among copepod species, egg size has been shown to be related positively to hatchingtime (McLaren et al., 1969; Kiørbe and Sabbatini, 1995). Such a relationship is expectedgiven the more general allometric relationship between size and physiological rates (e.g.Peters, 1983). This size effect on development can be examined through the parameter a

´of the Belehradek Eq. (1), which has been found to be positively related to egg size andadult size (McLaren et al., 1988). Reported values of a for Calanus species are given inMcLaren et al. (1988). C. pacificus and C. marshallae, which are similar in size with C.chilensis, have a values of 608 and 831, respectively. Our estimate for C. chilensis is948, which is closer to that of C. marshallae. Female adult size of C. chilensis obtained


´Fig. 4. Temperature cycle (a) and chlorophyll-a cycle (b) at Bahıa de Mejillones during June 1994/95. Graphswere constructed from data published in Escribano et al., 1997.

from the field for our experiments ranged between 2.4 and 2.6 mm, while reportedprosome lengths of C. marshallae are nearly 2.7 (Woodhouse, 1971). Although a similara may be a consequence of similar body size ranges, it is also important to note that thetemperature adaptation parameter (t ) of C. chilensis (11.0 in Table 2) agrees with the0

11.01 value for C. marshallae (McLaren et al., 1988). These features might reflect moregeneral ecological similarities between the two species. C. marshallae seems to beadapted to cold environments (Frost, 1974), while C. chilensis may be widely distributed

´in the cold Humboldt Current system (Marın et al., 1994).ˇAssuming that individuals in the field grow at temperature-dependent rates, Beleh-

´radek’s equation can predict development rates in natural conditions. For instance, fromthe estimated time from egg to adult females in Exp. II (38.1 days, Table 3) the

ˇ ´parameter a of the Belehradek equation for the entire period can be estimated as,

22.05a 5 38.1 /(15 1 11.0) 5 30312 (4)


In a similar manner for the developmental period between CI and adult, a is 24 425.ˇ ´The Belehradek equation to describe temperature- dependent developmental rate from

egg to adult becomes,

22.05D 5 30312(T 1 11.0) , (5)

and for development between CI and adult,22.05D 5 24225(T 1 11.0) (6)

If the development time (D) in Eq. (5) indeed represents the generation time (GT) asa function of ambient temperatures, it predicts the potential number of generations a

´year. During the annual cycle, temperature at Bahıa de Mejillones ranged between 128Cand 218C within the whole water column (Fig. 4a). Fig. 5a illustrates the relationshipsbetween temperature, generation time and the expected number of generations. Asmentioned in Section 3, the temperature pattern can be divided into two major periods.During the cold period (June to November) the mean temperature was |158C at theeuphotic layer (upper 20 m), giving rise to |4.8 generations for the 6-month period,whereas during the warm period (December to May) temperature averaged |17.58Cresulting in |5.8 generations. Therefore, 10–11 generations per year are expected. Thisestimate should be reduced somewhat due to lag between maturity and reproduction.This prediction does not agree with field observations of Escribano and Rodriguez(1994), who suggested that this species may continuously reproduce in this area andestimated about 6–7 generations in a year.

Another approach to understanding the role of temperature in controlling physiologi-cal rates is by analysing its effects on growth rates. The fitted exponential model ofgrowth of body dry weight was,

log W 5 1.153 1 0.114t (7)e

where t is the time (days) from Stage CI to adult. The value of t as a function oftemperature can be estimated from Eq. (6), such that the expected dry weights of adultsas a function of temperature are estimated as,

22.05log W 5 1.153 1 0.114[24225(T 1 11.0) ] (8)e

Changes in body length, on the other hand, are well described as a linear function oftime (Fig. 3a):

2BL 5 0.204 1 0.063t (r 5 0.949) (9)

where BL is body length (mm) and t as above. Thus the expected temperature-dependentbody lengths of adults are estimated as,

22.05BL 5 0.204 1 0.063[24225(T 1 11.0) ] (10)

It is important to stress that these predicted weights and lengths (Fig. 5b) are for adultfemales only, since no males were obtained after rearing eggs to adult.

Taking into account the seasonal divisions in cold (158C) and warm (17.58C) periods,


Fig. 5. The expected generational time (GT) and number of generations (NG) a year (a) and expected bodysizes of adult females at temperature-dependent development rates of individuals (b). The temperature rangeused is that observed in the field in a year cycle. BL, body length; DW, individual dry weight.

the expected adult female dry weights and body lengths are 105 mg and 2.14 mm, and56 mg and 1.87 mm, respectively. Lipid-discounted dry weight in field collections showsseasonal low values of about 90 mg during June and higher values of |210 mg duringOctober (Escribano and Rodriguez, 1995). Body length in the field also shows a patternof small females in June, |1.9 mm, and large ones in October, |2.6 mm (Escribano andRodriguez, 1995). Therefore, observed data in the field do not agree with temperature-dependent predictions shown in Fig. 5.

We suggest two explanations for the discrepancies between the observed number ofgenerations per year and predictions from a temperature-dependent model. Firstly, eventhough temperature may act as a good predictor of development rates of eggs,development rates of later stages are susceptible to conditions of food. This givessupport to the Escribano et al. (1997) suggestion that C. chilensis is subject to food


´shortage in Bahıa de Mejillones. Both food quantity and quality are often recalled asmajor factors affecting growth (Peterson and Hutchings, 1995), development (Vidal,1980) and egg production (e.g. Checkley, 1980; Berggreen et al., 1988) of marinecopepods.

A second explanation deals with C. chilensis behavior in the water column. Although´the upper layer (,20 m) at Bahıa de Mejillones is subject to large seasonal variability of

temperature, below 30 m temperatures are ,138C throughout the year. Although thevertical distribution of C. chilensis is not known, a greatly reduced number ofindividuals under the presence of a surface warm water mass (Escribano and Rodriguez,1994) suggests a seasonal migration to deeper waters. Development and growth in deepand cold waters may give rise to larger adults (see Fig. 5). For example, if developmentand growth takes place at temperatures of 138C, the expected weight and length are 196mg and 2.48 mm, respectively. These predictions are close to mean values of 140 mg(lipid-discounted) and 2.46 mm observed from field collections (Escribano andRodriguez, 1995). Development under low temperatures (,138C) would also yieldfewer generations a year, |7, a number more consistent with field observations.

Chlorophyll-a is mostly concentrated in the upper 20 m of the water column, but21values of $4 mg l are found most of the year ,40 m (Fig. 4b). Therefore individuals

would not necessarily be food limited and might be able to complete development inwaters ,30 m, with the accompanying lower temperature controlling physiological ratesresulting in larger size at maturity. The capacity to avoid high temperatures by migrating

˜to deeper waters might have evolved to cope with occasional ‘El Nino’ events, which areassociated with abnormally warm surface water.

At this point, neither the first or second hypothesis can be rejected. Studies of verticaldistribution during warm or cold periods might suggest the actual conditions oftemperature and food under which individuals develop and grow. Nevertheless, ifindividual growth in the field is exponential as modeled in Fig. 3b, temperature might besufficient to account for most of the variability in development and growth rates, as wellas for adult size variation. On the other hand, Escribano et al. (1997) concluded that thisspecies is highly sensitive to food quantity and that development rates might be greatly

´retarded during periods of low food in Bahıa de Mejillones. They further suggested thatthe expected number of generations in the field would be lower than those predictedfrom temperature-dependent development rates, due to retardation of development underperiods of food shortage. However, they predicted the number of generations based onthe assumption that the time between egg and adult female would be similar to that of C.pacificus (|23 days), which is the generational time estimated for this species at 158C inlaboratory rearing (Mullin and Brooks, 1970). Our results suggest that this generationtime is too short for C. chilensis at this temperature.

Acknowledgements

This work was supported by FONDECYT-Chile through Grant 94/0953 to R.Escribano. We thank C. Biaggini for assisting with the field work as well as G. Grone,


who helped look after phytoplankton cultures. Comments and corrections from twoanonymous reviewers greatly improved an earlier version.

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Temperature-dependent development and growth of Calanus chilensis Brodsky from Northern Chile

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