Hydrobiologia 2921293: 289-294, 1994 .F D. Ferrari & B . P Bradley (eds), Ecology and Morphology of Copepods .©1994. Kluwer Academic Publishers. Printed in Belgium

Life cycle of Calanus chilensis Brodsky in Bay of San Jorge, Antofagasta,Chile

Ruben Escribano & Luis RodriguezInstituto de Investigaciones Oceanologicas, Universidad de Antofagasta, Chile, P.O. Box 170, Antofagasta, Chile

Key words: Calanus, `El Nino', life-cycle, temperature, body-size

Abstract

The copepod Calanus chilensis is an endemic component of the zooplankton community in northern Chile . Sizedistributions of adult females, relative frequency of copepodid stages and relative numbers of adult males andnauplii, suggest the presence of at least 6 generations during the year, although the species seems to continuouslyreproduce through all seasons . Temperature profiles from 0 to 175 m indicated the presence of the `El Nino' currentduring March and April . Surface temperature ranged between 21 .1 and 13.1 °C. Warm waters during the `El Nino'event seemed to affect the body size of adult females and the normal course of cohort development, althoughthe population tended to recover rapidly through the subsequent months . We discuss the role of oceanographicconditions in controlling the life cycle of this species, as well as its continuous growth through the year comparedto other Calanus species .

Introduction

The Humboldt current coastal-upwelling system is rec-ognized as one of the most productive areas of theworld ocean, sustaining a high production of pelag-ic fishes . Fluctuations of fish populations in this area,due either to large scale phenomena or to overexploita-tion, are also well known to have strong impact on theeconomy of Peru and Chile .

Despite the importance of pelagic resources, therehas not been much effort to carry out basic researchfocused on populations that may sustain a high fishproduction . Calanus chilensis, because of its relativelylarge size and abundance in zooplankton samples of thearea (Heinrich, 1973 ; Boyd & Smith, 1980), seems tobe an important contributor to secondary productionand thus a crucial link between primary productionand fish production .

Since this species was described from the area(Brodsky, 1959), there has been no information onits annual life cycle and very little is known about itsdistribution and population changes on a seasonal timescale . This is certainly basic knowledge in evaluatingthe importance of this species for production of thewhole system. Indeed, Calanus species are recognized

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as key species worldwide in terms of secondary pro-duction and this has motivated considerable researchon their life cycles and secondary productivity . Forexample C. finmarchicus has received much attention(e .g . Marshall & Orr, 1955 ; Marshall et al. 1934 ;McLaren & Corkett, 1986), although basic knowledgeon ecophysiological aspects has also been acquired forother species, such as C. pacificus (e .g . Vidal, 1980),C. glacialis (e .g . Grainger, 1961 ; Hirche & Bohrer,1987), C. helgolandicus (e.g . Paffenhofer, 1976) .

C. chilensis is widely distributed on the Peru andnorthern Chile coasts (Brodsky, 1959 ; Heinrich, 1973)and seems to be a typical herbivorous copepod (Boyd& Smith 1980) . An additional aspect is the correlationof this species with the ENSO (El Nino Southern Oscil-lation) phenomenon . This, until recently unpredictableevent, greatly modify ecosystem function in the Chile-Peru current, but we do not know the consequencesfor some organisms with relatively short life cycles asmarine copepods . They are likely to respond by rapidchanges in demographic characters, and thus mightact as indicators of natural perturbations affecting thewhole system . Calanus chilensis appears to provide aunique opportunity to test hypotheses on the responseof pelagic populations to natural catastrophic events .

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Fig. 1 . Map showing the location of Bay of San Jorge on the Chileancoast and the fixed station used for obtaining zooplankton samples .

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This work constitutes a first attempt to outline thelife cycle of C. chilensis to examine possible respons-es to the recent 1991-92 `El Nito', and to provideinsights into the relative contribution of this species tosecondary production in the Humboldt current ecosys-tem .

I

Methods

Zooplankton samples from a fixed station (23° 39' 05S and 70° 33' 30 W), ca. 10 miles from the coast-line, at a depth of 200 m, close to the center of theBay of San Jorge (Fig. 1), were obtained, at roughlymonthly intervals, from January to December 1992 .Two plankton nets were used, one with 450 pm andanother 70 ttm mesh size, and with ca. 0.7 m and0.5 m mouth diameter respectively . Nets were towedvertically from 50 m depth to surface and, althoughsamples were not intended to be quantitative, theywere always towed ca . 0.5 m x s- t as nearly ver-tically as possible . The 450 pm net was assumed tohave undersampled small nauplii and early copepodidstages, and that late copepodids avoided the 70 ttm net,so that corrections were made through comparisons ofstages counts from both nets . Once obtained, sampleswere preserved in neutralized formalin (10%) for lateridentification, sorting and counting at the laboratory .Subsamples were obtained with a Folsom splitter and,for all stages available except nauplii, measurementsof prosome length (nearest 0.01 mm) were obtainedusing a calibrated ocular micrometer on a dissectingmicroscope . In addition to plankton samples, temper-ature profiles were obtained at the same station fromnear the bottom to surface, using a bathythermographpreviously calibrated with temperature measurementsat 5 depths using inversion thermometers attached toNansen bottles .

To understand the annual cycle of the copepod, dif-ferent generations may be distinguished according tothe following criteria . 1) Adult males of Calanus areknown to be short-lived, so that a marked peak in theirabundance may indicate the presence of a new repro-ductive cohort . 2) Presence of high concentration ofnauplii also reflects recent reproduction . 3) Relativefrequency of copepodids from CI to adult, and 4) pro-some length distributions of adult females, both revealreplacements of one generation by another .

Results

There is clear seasonality reflected in monthly temper-ature at the surface and at 50 m depth (Fig . 2) . DuringApril an unusually warm water mass was evident atboth depths . This may be attributed to the 1991-92 `ElNino' phenomenon reported at that time . Mean size ofadult females showed little seasonal pattern, althoughthere was much variation within months (Table 1) .

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The few females remaining after `El nino' in late Aprilexhibited a sharp decrease in body length .

Adult males and stages nauplii were presentthroughout the year, suggesting that reproduction maytake place at any time, but marked peaks in relativenumbers of these stages can be found (Fig . 3). Suchpeaks are evidence for multiple, nearly discrete gen-erations. At this point we need a starting point forseries of generations . Since `El Nino' seemed to havea major effect on the normal development of cohorts,causing virtual disappearence of females during April(Fig. 4, also Fig. 5), we started the cycle of C . chilensisonce conditions have supposedly returned to normal,i .e. during late April or beginning of May . We namedthis generation as G0 . Indeed both males and naupliibecame abundant shortly after that time (Fig . 3), sup-porting this designation of Go .

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Fig. 3. The relative abundance of adult males (upper panel) and nauplii (lower panel) in Bay of San Jorge 1992 . Relative numbers wereobtained after standarized counts from two nets .

From the presence of earlier copepodid stages (Fig .4) it appears that, only some Go had reached adult-hood by June. In July early stages dissapeared, suchthat all Go may be assumed to have matured at thattime. In mid August a new generation (G7) seemed toarise, although nauplii were not very abundant (Fig. 3) .Early stages dissappeared rapidly in September (Fig .4), so that G1 may be assumed as fully mature by theend of September. In October the marked peak in rela-tive numbers of adult males and nauplii suggested thepresence of G2 . This reproductive event was evidentin abundant copepodids in early November, suggest-ing that the end of G2 came in late November, alongwith the initiation of a new generation (G3) . The highnumber of adult males and nauplii during the periodNovember-December suggests that at least two differ-ent generations may have arisen at that time (G3 and

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G4). The overlapping G3 and G4 may have matured bymiddle January and have produced a generation com-parable to that in February and March of the previousyear (G5) .

Another criterion for distinguishing discretecohorts is the size of adult females, which is affected byseasonal variation in growing conditions (e .g. Deveey,1964). Changes in size distributions of females (Fig .5) match the events described above, beginning withthe highly reduced size class following the `El Nino'event in April, which was assumed as part of G5 grow-ing under high temperature . During December the sizedistribution of females appeared bimodal supportingthe suggestion that these were two (G3 and G4) distinctgenerations at that time .

Discussion

Laboratory and field observations indicate that bothtemperature and food cause seasonal changes in bodysize (e .g. Deevey, 1964 ; Klein Breteler & Gonzalez,

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Fig . 4. Relative frequency (%) of developmental stages copepodites CI to adult (males + females) of Calanus chilensis in Bay of San Jorge1992 .

1988; Escribano & McLaren, 1992). Our data showthat, except for a marked decrease in size during the `ElNino' event, the seasonal pattern of female length wasnot clearly associated with either surface temperature,or temperature at 50 m . However there is a significantnegative correlation (F1,8 = 9.32, P < 0.05) betweenfemale length and the mean integrated temperature ofthe water column (50 to 0 m) . Although we do not haveinformation on food availability, there is evidence foran increase in primary productivity in the area duringSeptember to November (Rodriguez et al ., 1991) . Highprimary productivity rates in this period may sustain amore intensive reproduction, as shown by the presenceof two overlapping generations (G3 and G4) . Size offemales, however, did not significantly increase in thatperiod. Therefore it appears that temperature may bea more important factor in controlling adult length ofthis species.

There are several sources of error in our results.For instance, early stages, such as CI and CII might beundersampled by the coarse net (450 µm) and our cor-rections may only partially compensate this error . In

nature advection and vertical migration might differ-entially affect distribution of stages in the whole watercolumn beyond 50 m depth. It is unlikely, however,that such shortcomings affect our general conclusionson existence of discrete generations, which were con-sistently revealed by the criteria chosen to distinguishcohorts .

Although discrete generations are evident from ourresults, it seems that C. chilensis is able to develop con-tinuously throughout the year. Continuous productionof this copepod might be a result of adequate grow-ing conditions through the entire year . An apparentlack of association between seasonal food availabilityand adult size sugggest that food is not limiting forthis species, and that development and growth maybe temperature-dependent, as suggested for some oth-er marine copepods (e .g . McLaren, 1978; McLarenet al., 1989). Seasonal patterns in body weight mightgive further insights on such a possibility, although itis obvious that much work needs to be done on thisvery interesting copepod .

Acknowledgements

We thank the crew of the ship Rano-Kau . Ian McLarenand two anonymous reviewers greatly improved anearlier version of this work. This study is part of aMonitoring Program of the Institute for Oceanologi-cal Research (110), University of Antofagasta . Sup-port has been received by the National OceanographicCommittee (CONA-Chile) .

References

Boyd, C . M. & S . L . Smith, 1980. Grazing patterns of copepods inthe upwelling system off Peru. Limnol. Oceanogr. 25 : 583-596 .

Brodsky, K . A., 1959. On the phylogenetic relationship of certainspecies of Calanus (Copepoda) from the northern and southernhemispheres . Zool . J ., Acad . of Sci. URSS., 10: 1537-1553 .(Translation from Russian)

Conover, R . J ., 1965 Notes on the moulting cycle, development ofsexual characters and sex ratio in Calanus hyperboreus . Crus-taceana 8 : 308-320 .

Deevey, G. B ., 1964 . Annual variations in length of copepods in theSargasso Sea off Bermuda. J. Mar. Biol . Ass . U.K. 44: 589-600.

Escribano, R . & I . A . McLaren, 1992. Influence of food and tem-perature on lengths and weights of two marine copepods . J . Exp .Mar. Biol. Ecol . 159: 77-88

SEP23

OCT7

NOV6

NOV 20

DEC 15Fig. 5. Size-frequency distributions of adult females Calanus chilensis in Bay of San Jorge 1992 .

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Grainger, E . H ., 1961 The copepods Calanus glacialis Jaschnov andCalanus finmarchicus (Gunnerus) in Canadian Arctic-SubarcticWaters . J. Fish. Res . Can. 18 : 663-678

Heinrich, A. K., 1973 . Horizontal distribution of copepods in thePeru current region . Oceanology 13 : 97-103 .

Hirche, H . J. & R. N. Bohrer, 1987 . Reproduction of the arcticcopepod Calanus glacialis in the Fram Strait. Mar. Biol . 94 : 11-17 .

Klein Breteler, W. C. M. & S . R . Gonzalez, 1988 . Influence oftemperature and food concentration on body size, weight andlipid content of two calanoid copepod species . Hydrobiologia167/168 : 201-210 .

Marshall, S . M . & A. P. Off, 1955 . The Biology of a Marine CopepodCalanus finmarchicus (Gunnerus) . Oliver & Boyd, Edinburgh .

Marshall, S . M., A . G . Nicholls & A . P. Off, 1934. On the biology ofCalanus finmarchicus . V : seasonal distribution, size, weight andchemical composition in Loch Striven in 1933 and their relationto the phytoplankton. J . Mar. Biol. Ass . U .K. 19: 793-828.

McLaren, I . A ., 1978 . Generation lengths of some temperate marinecopepods : estimation, predictions and implications . J . Fish . Res .Can. 35 : 1330-1342.

McLaren, I . A . & C . J. Corkett, 1986 . Life cycles and productionof two copepods on the Scotian Shelf, eastern Canada . SyllogeusNo.58 362-368 .

McLaren, 1. A ., J .- M . Sevigny & C. J . Corkett, 1989 . Temperature-dependent development in Pseudocalanus species . Can. J. Zool .67:559-564.

Paffenhdfer, G . A ., 1976 . Feeding, growth, and food conversion ofthe marine planktonic copepod Calanus helgolandicus . Limnol .Oceanogr. 21 : 39-50 .

Rodriguez, L ., V. Marin, M . Farias & E . Oyarce, 1991 . Identificationof an upwelling zone by remote sensing and in situ measurements .Mejillones del Sur Bay (Antofagasta-Chile) . Sci . Mar. 55 : 467-473

Vidal, J ., 1980 . Physioecology of zooplankton . I . Effects of phyto-plankton concentration, temperature, and body size on the growthrate of Calanus pacificus and Pseudocalanus sp . Mar. Biol . 56:111-134 .