Timing of reproductive events in the marine copepod

ARTICLE

Timing of reproductive events in the marine copepod Calanus glacialis:a pan-Arctic perspectiveMalin Daase, Stig Falk-Petersen, Øystein Varpe, Gerald Darnis, Janne E. Søreide, Anette Wold, Eva Leu, Jørgen Berge, Benoit Philippe,and Louis Fortier

Abstract: The timing of reproductive events of Calanus glacialis is closely coupled to the two major marine primaryproduction events in the Arctic: the ice algal and phytoplankton blooms. Reproductive strategies vary between differentphysical and biological environments of the European and Canadian Arctic. In the Canadian Beaufort Sea and the highArctic Rijpfjorden on Svalbard, C. glacialis utilized the ice algae bloom to fuel spawning in spring, while growth anddevelopment of the new generation was primarily supported by the phytoplankton bloom. In the predominantly ice-freeArctic Kongsfjorden (Svalbard), C. glacialis was mainly a capital breeder spawning early in the season in the absence of food.This enabled the offspring to synchronize their growth and development with the phytoplankton bloom and, thus,reproduce successfully despite the lack of an early ice algal bloom. The variability in life history traits observed in theCanadian and European Arctic is compared with data from other Arctic regions to present a pan-Arctic perspective on lifecycle strategies of C. glacialis.

Résumé : La chronologie des évènements de reproduction de Calanus glacialis est étroitement liée a deux évènements majeurstouchant a la production primaire marine dans l’Arctique, soit les proliférations d’algues de glace et de phytoplancton. Lesstratégies de reproduction varient selon les milieux physiques et biologiques dans l’Arctique européen et canadien. Dans la merde Beaufort canadienne et dans la région de Rijpfjorden de Svalbard, dans l’Extrême Arctique européen, C. glacialis tire l’énergienécessaire a son frai printanier de la prolifération d’algues de glace, alors que la croissance et le développement de la nouvellegénération s’appuient principalement sur la prolifération de phytoplancton. Dans la région arctique de Kongsfjorden (Svalbard),exempte de glace en bonne partie, C. glacialis est principalement un reproducteur sur capital qui fraye au début de la saison enl’absence de nourriture. Cela permet a sa progéniture de synchroniser sa croissance et son développement avec la proliférationde phytoplancton, ce qui en assure le succès de reproduction malgré l’absence d’une prolifération hâtive d’algues de glace. Lavariabilité des caractéristiques du cycle biologique observée dans l’Arctique canadien et européen est comparée a des donnéespour d’autres régions arctiques afin de brosser un portrait pan-arctique des stratégies associées au cycle de vie de C. glacialis.[Traduit par la Rédaction]

IntroductionCopepods of the genus Calanus are key species in the pelagic

ecosystems of the Arctic seas (Jaschnov 1970; Conover 1988; Falk-Petersen et al. 2002). They convert low-energy carbohydrates andproteins from their algae diet into high-energy wax ester lipids(Lee et al. 2006; Falk-Petersen et al. 2009a), which makes themextremely lipid-rich (50%–70% lipids of dry mass) and thus impor-tant food items for higher trophic levels such as fish, birds, andmammals (Falk-Petersen et al. 1990). Their populations displayvarious life history strategies that reflect adaptations to differentenvironmental conditions (Conover 1988; Falk-Petersen et al.2009b). These varying traits include life cycle length, size and ageat maturation (Falk-Petersen et al. 2009b), and the degree of lipid-based gonad maturation and egg production (i.e., whether theyprimarily use stored energy (capital breeders) or are dependent onfood (income breeders) for reproduction; Varpe et al. 2009). Witha circumpolar distribution, Calanus glacialis populations experi-

ence a large range of environmental conditions, and high variabil-ity in life history traits are indeed observed along spatial andtemporal gradients (Falk-Petersen et al. 2007; Pertsova andKosobokova 2010; Leu et al. 2011). Much of the distribution area ofC. glacialis is seasonally ice-covered and harbors two main algalproduction events: the ice algal bloom, when ice is present, andthe later phytoplankton bloom, after the ice break-up (Horneret al. 1992; Legendre et al. 1992; Gosselin et al. 1997; Ji et al. 2013).The relative abundance and timing (including the time lag be-tween the two blooms) of the two production regimes is subject tothe prevailing sea conditions (Arrigo and van Dijken 2004; Ji et al.2013).

Calanus glacialis is not strictly herbivorous (Ohman and Runge1994; Levinsen et al. 2000b; Campbell et al. 2009), but it feedsmainly on microalgae during the spring bloom (Runge & Ingram1988; Tourangeau and Runge 1991; Juul-Pedersen et al. 2006) and isalso able to exploit ice algae at the ice–water interface (Runge &

Received 17 September 2012. Accepted 6 April 2013.

M. Daase and A. Wold. Norwegian Polar Institute, Fram Centre, N-9296 Tromsø, Norway.S. Falk-Petersen. Norwegian Polar Institute, Fram Centre, N-9296 Tromsø, Norway; Akvaplan-niva, Fram Centre, N-9296 Tromsø, Norway; Department of Arctic and Marine Biology, Facultyof Biosciences, Fisheries and Economics, University of Tromsø, N-9037 Tromsø, Norway.Ø. Varpe. Akvaplan-niva, Fram Centre, N-9296 Tromsø, Norway; Norwegian Polar Institute, Fram Centre, N-9296 Tromsø, Norway; The University Centre in Svalbard, P.O. Box 156, N-9171Longyearbyen, Norway.G. Darnis and L. Fortier. Québec Océan, Département de Biologie, Université Laval, Québec, Quebec, Canada.J.E. Søreide. The University Centre in Svalbard, P.O. Box 156, N-9171 Longyearbyen, Norway.E. Leu. Norwegian Polar Institute, Fram Centre, N-9296 Tromsø, Norway; Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany.J. Berge. Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, University of Tromsø, N-9037 Tromsø, Norway; The University Centre in Svalbard,P.O. Box 156, N-9171 Longyearbyen, Norway.B. Philippe. Institut des Sciences de la Mer, Université de Québec a Rimouski, Rimouski, Quebec, Canada.

Corresponding author: Malin Daase (e-mail: [email protected]).

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Can. J. Fish. Aquat. Sci. 70: 871–884 (2013) dx.doi.org/10.1139/cjfas-2012-0401 Published at www.nrcresearchpress.com/cjfas on 10 April 2013.

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http://dx.doi.org/10.1139/cjfas-2012-0401

Ingram 1988; Tourangeau and Runge 1991; Plourde et al. 2005).Calanus glacialis fuels gonadmaturation and egg production eithersolely with internal energy storage before the onset of the springbloomor by utilizing the ice algal or pelagic blooms to fuel spawn-ing (i.e., dependent on concurrent food intake; Smith 1990; Hircheand Kattner 1993; Kosobokova and Pertsova 2005; Plourde et al.2005). The two strategies are referred to as capital and incomebreeding, respectively (Jönsson 1997; Varpe et al. 2009). The phy-toplankton bloom is then utilized to fuel growth and develop-ment of nauplii and copepodites. This mixed reproductivestrategy enables C. glacialis to extend the reproductive season be-yond the brief periods of high primary production and optimizeits growth and development. There are marked fitness conse-quences related to the ability to schedule annual events such asmigrations, growth, and reproduction in relation to the seasonal-ity in food availability and predation (Varpe et al. 2007; Varpe2012). Specifically, the capacity to time reproduction in a way tomatch the peak of highest food quality and quantity with theoccurrence of those stages that can utilize this food sourcemay bea crucial adaptation that determines if growth and developmentare successful or not (cf. Cushing 1990).

Herewe investigate how variability in the availability of the twoprime food sources, the ice algae and the phytoplankton, influ-ences the timing of reproductive events of C. glacialis. Because oflogistical constraints in the high Arctic, data covering an entireyear or even just the entire reproduction period of C. glacialis arescarce (Madsen et al. 2001; Søreide et al. 2010) as are data coveringmore than 1 year at the same location (Pertsova and Kosobokova2010). We therefore chose to compare key life history traits ofC. glacialis from Arctic regions displaying different environmentalconditions to elucidate what drives the phenology of reproductiveevents in C. glacialis populations and how this species may beaffected by environmental changes. The two main regions in-cluded in this study, the Canadian Arctic (Amundsen Gulf) andEuropean Arctic (Svalbard) (Fig. 1), differ with regard to ice condi-tions, hydrography, light, and thus primary production regimesand the relative importance of ice algae versus phytoplankton.We assumed that the C. glacialis populations are mixed through-out the Arctic (e.g., Nelson et al. 2009) and that the responses ofC. glacialis reflect primarily phenotypic plasticity, although wecannot exclude that evolution may have led to specialized localadaptations in resident populations. While we acknowledge thatlife history traits may also be top-down controlled (e.g., Kaartvedt2008; Varpe and Fiksen 2010; Berge et al. 2012), we restrict ouranalysis to bottom-up processes mediated through variability infood availability and the particular role of the two blooms of icealgae and phytoplankton. We focus on plasticity shown in lifehistory traits closely interrelated to food availability such as tim-ing of reproduction (spawning, occurrence of young life stages),timing of seasonal vertical migration, and main overwinteringdevelopmental stage. Finally, we compared the variability in tim-ing of reproductive events observed in our data with previouslypublished data on population dynamics of C. glacialis from otherArctic regions to present a more extensive picture of the life his-tory of C. glacialis in seasonal ice-covered waters. The environmen-tal conditions encountered at one location in a given yearmay notbe representative for that region, since interannual variabilityand local variation in ice formation and hydrography are largethroughout the Arctic. The environmental conditions encoun-tered in the different study areas will, however, illustrate thevariety of conditions that C. glacialismay inhabit on a local as wellas pan-Arctic scale.

Study areaData on ice algal and phytoplankton production as well as on

C. glacialis population dynamics were compiled for Rijpfjordenand Kongsfjorden in Svalbard (79°N–80°N) and the AmundsenGulf and Franklin Bay (69°N–71°N) in the Canadian Arctic (Table 1).

These areas are located north of the Arctic Circle (Fig. 1) and expe-rience pronounced seasonality in incident solar radiation(Table 1). The hydrographic conditions encountered in these areasduring the study period are summarized in Table 1.

SvalbardThe archipelago of Svalbard is located in a border area between

Atlantic and Arctic climatic (Stroemberg 1989) and biogeographiczones (Narayanaswamy et al. 2010). The main pathway of Atlanticwater into the Arctic Ocean (the West Spitsbergen Current, WSC)runs along the western coast of Svalbard, and high interannualvariability in the strength of the WSC and the inflow of Atlanticwater to the Arctic (Saloranta and Haugan 2001; Walczowski andPiechura 2006) are observed in Svalbard waters, which are oftenmodified by local oceanographic processes (e.g., freshwater run-off, wind-driven circulation, and cooling; Cottier et al. 2005).

Rijpfjorden is a north-facing fjord with a wide opening towardsthe broad shallow shelf (100–200 m deep), which extends to theshelf-break of the Polar Basin at �81°N. Rijpfjorden is dominatedby cold Arctic water masses, and the inflow of Atlantic water ismuch less pronounced compared with Kongsfjorden, which is aglacial fjord located on the west coast of Svalbard (79°N). TheKongsfjorden marine ecosystem functions under the balance ofinflux of Atlantic waters from theWSC and Arctic waters from thecoastal current (Hop et al. 2002, 2006; Svendsen et al. 2002), andinterannual variations in the inflowof Atlantic water are common(Svendsen et al. 2002; Cottier et al. 2005). In Rijpfjorden, ice for-mation usually starts in the inner part of the fjord in late autumn(November–December), the fjord is ice covered by January–February, and ice breakup starts in June (Søreide et al. 2010).Kongsfjorden used to be ice-covered in winter as recently as 2005.However, in the period 2006 to 2010 Kongsfjorden did not developa fast ice cover during winter because of an extensive flooding ofwarm Atlantic water from the WSC during the winter 2005–2006(Cottier et al. 2007).

Amundsen Gulf and Franklin BayThe Amundsen Gulf is located at 71°N, with Franklin Bay being

a shallow bay south of the Amundsen Gulf. The Amundsen Gulfbridges the Beaufort Sea to the Canadian Arctic Archipelago. Off-shore annual and multiyear sea ice is found beyond the BeaufortSea shelf-break outside the Amundsen Gulf. The waters of theregion typically comprise the Polar Mixed Layer (salinity < 31.6;0–50 m), the Pacific Halocline (salinity of 32.4–33.1; 50–200 m),and the Atlantic watermass layer (salinity > 34; >200m) (Carmackand MacDonald 2002). Along the inner shelf region, seasonal seaice begins to form in October, and ice consolidates over the entireregion in December (Galley et al. 2008). Ice breakup occurs be-tween May and August. At the entrance of Amundsen Gulf thecircum-arctic flaw lead polynya enlarges to form the CapeBathurst polynya, which on average opens up in the second weekof June (Darnis et al. 2008), but large interannual variability in theextent and persistence of open water regions are observed (Arrigoand van Dijken 2004). During the study period 2007–2008, land-fast ice did not consolidate in the Amundsen Gulf because ofatmospheric forcing (ice formation starting 6 weeks later thanusual), and the ice cover remainedmobile throughout the winter,promoting a more rapid ice breakup in spring approximately1 month earlier than normal (Barber et al. 2010; Forest et al. 2011b;Tremblay et al. 2011).

Materials and methodsData from Rijpfjorden, Svalbard, were gathered during the Nor-

wegian International Polar Year (IPY) projects “Climate effects onplanktonic food quality and trophic transfer in ArcticMarginal IceZones” (CLEOPATRA) and Ice-edge. Field campaigns were carriedout on a monthly basis in Rijpfjorden from February to October2007. These data have been published previously, and zooplank-

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ton sampling procedures, ice algal and phytoplankton sampling,and hydrographic conditions are described in detail in Søreideet al. (2010), Leu et al. (2010), and Leu et al. (2011) (see also Table 1).

In Kongsfjorden, zooplankton has been sampled regularly forthe past 15 years along standard stations (Norwegian Polar Institute,unpublished data; Kwasniewski et al. 2003), but data on the entireannual cycle of C. glacialis are fragmented. Here, we compiled datafrom 2006 and 2007, when zooplanktonwere sampled several timesover the season (April, May, July, August in 2006 and May, July,

August, October in 2007). Calanus glacialis abundance was com-piled from three stations in the central part of Kongsfjorden(KB1, KB2, KB3, bottom depth �300 m). Zooplankton sampleswere analyzed following procedures described by Kwasniewskiet al. (2003) (Table 1). Chlorophyll a (Chl a) concentration mea-sured in 2006 is based on fluorometrical analysis of filtered sea-water samples and is published previously by Seuthe et al. (2011).In 2007, Chl a concentrations in the water column were based onweekly fluorescence measurements taken between May and

Fig. 1. Study area: Amundsen Gulf, Franklin Bay, Kongsfjorden, and Rijpfjorden. Also marked are North Water Polynya, Disko Bay,Lurefjorden, and the White Sea (see Discussion).

Daase et al. 873


September (Narcy et al. 2009; Table 1). Hydrographic conditions in2006 and 2007 are described in Cottier et al. (2007) andWillis et al.(2008).

In Svalbard themorphologically similar Atlantic species Calanusfinmarchicus co-occurs with C. glacialis. Most ecological investiga-tions in this region adopt a morphological-based method fordiscriminating between the two species, and we used size classesderived from length–frequency analyses of prosome length byKwasniewski et al. (2003) todistinguishbetweencopepodite stagesofC. glacialis and C. finmarchicus. Prosome length of C. glacialismay, how-ever, vary interannually at the same location (Kwasniewski et al.2003), and recently a molecular investigation has revealed amuchhigher overlap in terms of prosome length than previously as-sumed (Gabrielsen et al. 2012), documenting a high, but regionallyvariable, potential for misidentification when based on prosomelength alone. However, these misidentifications seem for themost part to be unidirectional, in that errors occur as an under-estimation of C. glacialis and a comparative overestimation ofC. finmarchicus. Also, the importance of these misidentificationsappears to vary both geographically and among developmentalstages (Gabrielsen et al. 2012). For our data fromKongsfjorden andRijpfjorden, this means that C. glacialis may have frequently beenmisidentified for C. finmarchicus, and we may therefore have un-derestimated the abundance of C. glacialis by �20%. We cannotexclude that our dataset includes C. finmarchicus. However, sincehardly any individuals of C. finmarchicuswere found to bemisiden-tified as C. glacialis based on prosome length (i.e., C. finmarchicus isnot larger than suggested by previously established size classes;Gabrielsen et al. 2012), we believe that our dataset consist mainlyof C. glacialis. Furthermore, since we are mainly interested in theabundance of different stages relative to each other and not theexact numbers, the underestimation of C. glacialis abundance by�20% should not affect the overall interpretation of our data.

Data from the Canadian Arctic were collected within the frame-work of two large interdisciplinary research projects using theresearch icebreaker CCGS Amundsen: the Canadian Arctic ShelfExchange Study (CASES) and the International Polar Year –Circumpolar Flaw Lead Study (IPY-CFL). As part of CASES, the ship

overwintered in Franklin Bay in 2003–2004 to study the ecosystemthroughout the winter. Hydrographic conditions during the studyperiod are described in Forest et al. (2008). Zooplankton samplingwas carried out on a weekly basis from November 2003 to June2004, using vertically resolved net hauls from 220 m depth to thesurface (Benoit et al. 2010). Sampling procedures are described indetail in Benoit et al. (2010). Chl a concentration of ice algae wasmeasured from the bottom 4 cm of ice cores taken between27 February and 20 June 2004 as described in Rózanska et al. (2009)and Riedel et al. (2008). Chl a fluorescence at 30 m depth wasrecorded from October 2003 to mid-July 2004 by a fluorometer at-tached on a mooring nearby the overwintering station (Tremblayet al. 2008).

During CFL 2007–2008, the CCGS Amundsen was drifting in theAmundsen Gulf (70°N–71°N; Barber et al. 2010). Thus, sample lo-cation varied, and we restricted the data to the central AmundsenGulf as defined as the area between 120°W and 127°W with abottom depth >250 m (Forest et al. 2011a; Wold et al. 2011). Hydro-graphic conditions during the sampling period are described indetail by Barber et al. (2010). Zooplankton was sampled with ver-tical resolved net hauls on a weekly to monthly basis from Octo-ber 2007 to July 2008 (Table 1). Zooplankton sampling proceduresare described in detail in Wold et al. (2011), where these data havepartly been published. Chl a concentration of ice algae was mea-sured from ice cores taken between 16 March and 5 May 2008, asdescribed by Wold et al. (2011). Only Chl a data retrieved from thebottom 3 cm of the ice core are presented here. In situ fluores-cence was measured with a Rosette-mounted fluorometer fromOctober to early August (Darnis and Fortier 2012). Water columnChl a concentration determined from regular water samples col-lected close to the mooring were used to calibrate the fluores-cence signal (Forest et al. 2011a).

In Amundsen Gulf and Franklin Bay, the Pacific subarctic spe-cies Calanus marshallae may co-occur with C. glacialis, and becauseof uncertainties in distinguishing these two species, they are of-ten pooled in a single taxon (Plourde et al. 2005; Hopcroft et al.2010). We cannot exclude that our dataset from the AmundsenGulf may include individuals of C. marshallae. However, while

Table 1. Overview of available data, sampling procedures, and main physical parameters in the study areas.

Franklin Bay Amundsen Gulf Rijpfjorden Kongsfjorden

Program CASES CFL CLEOPATRA AEM–MOSJLatitude (°N) 70 71 80 79

Sampling period Nov. 2003–Sept. 2004 Oct. 2007–July 2008 Mar.–Sept. 2007 Apr.–Sept. 2006 May–Oct. 2007Max. sample depth (m) 220 600 140 300Sampling interval �Weekly �Weekly �Monthly 4 times annuallyNo. of stations 1 50 1 3

Fluorescence from mooring × — × — —Fluorescence CTD casts — × (*) — ×Chl a ice algae (ice core length) × (4 cm) × (3 cm) × (5–8 cm) — —Chl a phytoplankton — × × × —

ZooplanktonNet MPS MPS WP2–MPS MPSMesh size (�m) 200 200 200 200Mouth opening (m2) 0.5 0.5 0.25 0.25Egg production rates × × × — —Nauplii abundance — × × × ×

Polar night 25 Nov.–17 Jan. 20 Nov.–22 Jan. 19 Oct.–23 Feb. 24 Oct.–19 Feb.Midnight sun 21 May–24 July 16 May–29 July 16 Apr.–28 Aug. 19 Apr.–25 Aug.Avg. winter water temperature (°C) −1.8 to −1.2 −1.6 −1.8 −1 to +1Max. summer water temperature (°C) 0 7–8 (<0 under 50 m) 2–4 3–6

Note: An asterisk (*) indicates data available but not presented in this study; an × symbol indicates a positive test; a long dash (—) indicates a negative test. Ice corelength for ice algae chlorophyll a (Chl a) refers to the section of the ice core (measured from bottom of sea ice) that was analyzed for ice algae Chl a concentration.Abbreviations are as follows: CASES, Canadian Arctic Shelf Exchange Study; CFL, Circumpolar Flaw Lead Study; CLEOPATRA, Climate effects on planktonic foodquality and trophic transfer in Arctic Marginal Ice Zones; AEM–MOSJ, Arctic Ecosystem monitoring–Miljøovervakning for Svalbard og Jan Mayen (Environmentalmonitoring for Svalbard and Jan Mayen); MPS, multiple plankton sampler (Hydrobios, Kiel).



C. marshallae prevails south of the Bering Strait, its abundancesdiminish towards the Chucki Sea and Amundsen Gulf (Frost 1974;Matsuno et al. 2011; Nelson et al. 2009), and the contribution ofC. marshallae to the Calanus glacialis–marshallae population in theAmundsen Gulf region should not bias our interpretation (Nelsonet al. 2009).

Calanus nauplii were not identified to species, and naupliiabundance was most likely underestimated at all locationssince Calanus nauplii are not caught quantitatively with a meshsize of 200 �m. Nauplii abundance estimates should therefore betreated with caution, but the timing of nauplii occurrence is nev-ertheless shown as an additional indication of when reproductionmay have started.

Calanus glacialis biomass was calculated from stage-specific drymasses as described in Daase et al. (2007). Nauplii were not in-cluded into biomass calculations.

Results

Rijpfjorden 2007In 2007 a consolidated ice cover had formed in Rijpfjorden by

the beginning of February and lasted until the end of June (Fig. 2a).The fjord was ice-free by 12 July. Water temperature remainedclose to –1.8 °C as long as the fjord was ice-covered. During sum-mer, the surface water warmed up to 2–4 °C (Table 1). Highest icealgae Chl a concentrations were observed in late April 2007 (10–48 mg·m−2). By the beginning of June the ice algae Chl a concen-tration had decreased to 8–22 mg·m−2 (Fig. 2a). The Chl a concen-tration below the sea ice began to increase in June (mainly washedoff ice algae). During the period of ice breakup, a brief peak pro-duction period of phytoplankton had already occurred in the be-ginning of July. Thus there was a 1- to 2-month gap between peakice algae and peak phytoplankton production in Rijpfjorden.Abundance of C. glacialis was low from March to June (�900–3800 individuals·m−2), and the population consisted mainly of theoverwintering stages CIV and adults. Abundance increased sharplyduring summer and autumn (27 000–69 500 individuals·m−2;Fig. 2a). Spawning started at the end of April during the ice algaebloom, and maximum egg production rates were observed inearly June (Table 2). Nauplii and young stages (CI and CII) appearedat high abundance first in July when the phytoplankton produc-tion peaked (Fig. 2a) and were present until September, at whichtime CIV and CV were the most common copepodite stages, form-ing the overwintering population (Fig. 2a). Most of the C. glacialispopulationwas concentrated below 50m inMarch (Fig. 3) and hadsurfaced to the upper 50 m by June. In July, the upper 20 m wereavoided, and the population (now mainly young stages) was con-centrated in the 20–50 m layer where maximum Chl a concentra-tions were recorded (Fig. 3). In August, part of the population hadstarted to descend, and by September the population was concen-trated below 100 m (Fig. 3). Biomass in Rijpfjorden increased from500–2000 mg dry mass (DM)·m−2 during spring and early summerto 5000–10 000 mg DM·m−2 in summer and peaked in September,reaching 21 000 mg DM·m−2 (Fig. 4).

Kongsfjorden 2006–2007Sea ice did not form in Kongsfjorden in 2006 and 2007 (Fig. 2b).

Water temperatures varied from0–1 °C inwinter to up to 3–6 °C inJuly to September (Table 1). Timing of onset and magnitude of thespring bloom varied between the 2 years in Kongsfjorden. In 2006,the bloom peaked as early as April (10 �g·L−1; Fig. 2b), while Chl aconcentrations were low in May (0.2 �g·L−1), indicating a post-bloom situation. In 2007, a bloomwas observed in the first half ofMay but Chl a concentrations were much lower than in 2006(Fig. 2b).

In 2006, the total C. glacialis copepodite abundance peaked inlate May (�233 100 individuals·m−2, 31 May) but had decreasedsharply by July and August (�18 000 individuals·m−2; Fig. 2b).

The population consisted mainly of females at the end of April2006, and a peak of nauplii and CI occurred in May (Fig. 2b). In2007, the total abundance varied little from May to October(20 000–30 000 individuals·m−2), and highest nauplii abundancewas observed in May during the phytoplankton bloom (Fig. 2b). Inboth years, CI and CII dominated in middle to end of May (Fig. 2b).The overwintering population in 2006–2007 probably consistedmainly of CV, since it was the dominant stage in August 2006.There was still a high proportion of CIV in October 2007, and thus,the 2007–2008 overwintering population was most likely com-posed of CIV and CV (Fig. 2b). The C. glacialis population was con-centrated in the upper 100m in May (Fig. 3) and in a greater depthin August. In 2007 a deeper distribution signaled that the down-ward migration to overwintering depth had already started byJuly. High biomass was observed in Kongsfjorden in April 2006(7000 mg DM·m−2), and it increased slightly over the summer to11 000 mg DM·m−2. In 2007, biomass was very low in May (700 mgDM·m−2), but a sharp increase was observed over the sample pe-riod, and by July and October biomass was as high as in summer2006 (12 000 mg DM·m−2) (Fig. 4).

Franklin Bay 2003–2004Franklin Bay was covered by first-year land-fast ice fromDecem-

ber 2003 to June 2004 (Fig. 2c). Ice breakup started at the end ofMay (Fig. 2c). Water temperatures remained below 0 °C through-out the study period (Table 1). Ice algal Chl a concentration startedto increase in April, forming an ice algal bloom in the third weekof May (�30 mg Chl a·m−2), and biomass declined rapidly in June(0.72 mg Chl a·m−2). At the same time, water column Chl a con-centrations (as estimated by fluorescence measurements), whichhad been low throughout spring, increased sharply as the icebroke up in June and remained relatively high until the beginningof July (Fig. 2c). Thus there was a 2- to 3-week time gap betweenpeaks in the ice algal and phytoplankton blooms.

Calanus glacialis abundance in Franklin Bay was variable fromNovember to January (700–8000 individuals·m−2). From January toJune, a general decrease in C. glacialis abundance was observed(minimum 1000 individuals·m−2 in June), followed by an increaseduring summer–autumn (6800 individuals·m−2 in September;Fig. 2c). Copepodites CV increased in relative abundance in June.Spawning was first observed in May (Table 2), but a few youngcopepodites were already observed in April and May, indicatingthat some spawning occurred earlier in the season. However, highrelative abundance of young copepodite stages occurred first inJuly in Franklin Bay (Fig. 2c), and a large part of the populationwasstill composed of CI and CII in September (Fig. 2c).

The C. glacialis population was concentrated below 50 to 100 mfrom December to May, and CIV was the dominant overwinteringstage (Fig. 3). Abundance in the upper 50 m increased in late May(Fig. 3). Nauplii abundance was not recorded in Franklin Bay in2003–2004, and biomass of C. glacialis varied throughout the studyperiod from 80 to 2000 mg DM·m−2 (Fig. 4).

Amundsen Gulf 2007–2008Ice started to form in Amundsen Gulf in October 2007, ice

breakup started in the first week of May 2008, and ice concentra-tionwas <5% bymid June (Fig. 2d; see also Barber et al. 2010; Forestet al. 2011b; Tremblay et al. 2011). Water temperatures at the sur-face remained below 0 °C until early June and increased up to 7–8°C during summer at the surface (Table 1). No visible ice algaewereobserved during the first 2 weeks of March in the Amundsen Gulf.Ice algal Chl a concentration increased from 0.2–3mg·m−2 inmid-March to 10–20 mg·m−2 by the end of April (Fig. 2d) and hadsharply declined by the beginning of May. Phytoplankton Chl aconcentration peaked inmid-May (3.8mg·m−3 at 5m depth) about2 weeks after the peak ice algae biomass. Chl a estimates derivedfrom the fluorometer attached to the conductivity–temperature–depth rosette indicated a second peak in mid-July (Fig. 2d).

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Calanus glacialis abundance varied throughout autumn andwinter (6000–43 000 individuals·m−2). Minimum abundance ofC. glacialis (850 individuals·m−2) was observed in May (Fig. 2d). Thepopulation increased over the summer (maximum of 13 000

individuals·m−2 in June; Fig. 2d). Until May, CIII and CIV were thedominant stages in all layers. During spring (March–May), therelative abundance of CIV increased, while CV made up a largerpart of the population in June–August (Fig. 2d). Spawning started

Fig. 2. (a) Seasonal development of phytoplankton chlorophyll a (Chl a) concentration (based on Chl a measurements at 5 m and fluorescencemeasurements at 17 m) and ice algae Chl a concentration (mean values, error bars are standard deviations, SD) (upper panel), total abundance ofCalanus glacialis (copepodites and adults), abundance of C. glacialis CI and Calanus nauplii (middle panel), and stage composition of C. glacialis (lowerpanel) in Rijpfjorden, Svalbard, in 2007; (b) Seasonal development of phytoplankton Chl a concentration (based on Chl ameasurements averagedover upper 50 m in 2006 and average fluorescence in upper 50 m in 2007) (upper panel), total abundance of C. glacialis (copepodites and adults),abundance of C. glacialis CI and Calanus nauplii (middle panel), and stage composition of C. glacialis (lower panel) in Kongsfjorden, Svalbard, 2006 and2007; (c) Seasonal development of phytoplankton Chl a concentration (estimated frommean fluorescence at 30 m at mooring site CA20, redrawnfrom Tremblay et al. (2008), arbitrary units) and ice algae Chl a concentration (redrawn after Rózanska et al. (2009)) (upper panel), total abundance ofC. glacialis (copepodites and adults) and abundance of C. glacialis CI (middle panel), and stage composition of C. glacialis in Franklin Bay, 2003–2004(lower panel); (d) Seasonal development of phytoplankton Chl a concentration (based on Chl a concentration measured at 5 m and fluorescencemeasurements at 20 m) and ice algae Chl a concentration (mean values, error bars are SD) (upper panel), total abundance of C. glacialis (copepoditesand adults), abundance of C. glacialis CI and Calanus nauplii (middle panel), and stage composition of C. glacialis in Amundsen Gulf, 2007–2008 (lowerpanel). Timing of ice formation and ice breakup is indicated on top of each subplot. AF, adult females.



in the second week of April 2008, and maximum egg productionrate was observed in early May (Table 2). Young copepodites (CI)appeared inmid-June (Fig. 2d), and their abundance peaked in lateJuly shortly after the second peak in phytoplankton bloom. FromNovember to April, the C. glacialis population was distributedmainly below 50 m, whereas abundance in the upper 50 m washigh from April to May, indicating that the spring ascent tookplace in this period (Fig. 3). In mid-July, the upper 20 m weredevoid of all stages, and young stages (CII–CIII) were abundantbetween 20 and 50 m depth (Fig. 3). Calanus nauplii appeared inJanuary, and a first peak was observed in March. However, thesewere most likely nauplii of Calanus hyperboreus, whose reproduc-tive period lasted until early April (Darnis et al. 2012). Naupliiremained abundant throughout the spring and summer, withpeaks observed in May and at the end of June. These peaks in latespring and early summer were most likely nauplii of C. glacialis.Biomass of C. glacialis varied throughout the study period from400to 5000 mg DM·m−2 (Fig. 4).

Discussion

Timing of reproductive events in different environmentalsettings

Our findings suggest that ice conditions (and incident sunlight)determine the timing of ice algal and phytoplankton blooms andsubsequently the timing of life history events of C. glacialis (such asegg production and recruitment to first copepodite stage) in dif-ferent arctic regions (Fig. 5; Table 2). The environmental condi-tions that C. glacialis encounters on a pan-Arctic scale can bedistinguished into three main categories: (I) regions with a long-lasting ice cover, primarily Arctic water and two major bloomevents that occur with some time lag in between them; (II) openshelf systems with high variability in timing of ice formation andbreakup, inflow of warmer water (Pacific or Atlantic), and twobloom events that may overlap; (III) regions with no or limited icecover, inflow of warmer water (Pacific or Atlantic), and only onemajor pelagic spring bloom event.

Rijpfjorden is representative of the first type of environment (I,Fig. 5). There, C. glacialis adopted the strategy of income breedingby using ice algal bloom in April–May to fuel maturation, eggproduction, and spawning. The new generation (nauplii and CI)was prominent at the peak in the phytoplankton bloom, ensuringgood conditions for growth and development of early stages. Theadvantage of this strategy in an environment with bimodal foodsupply is that food-independent developmental phases such asthe development from egg to the first feeding nauplii stage III(NIII; Peterson 2001) can occur between the blooms. Thus, bothfood sources of the rather brief primary production season can beexploited if there is a match in timing between reproduction andice algae bloom as well as between development to first feedingstage and phytoplankton bloom (Søreide et al. 2010; Varpe 2012).

Although at a lower latitude, Franklin Bay shares similaritieswith Rijpfjorden, such as a long-lasting ice cover and two majorbloom events (Forest et al. 2008). Reproduction and occurrenceof young stages of C. glacialis followed the same pattern as inRijpfjorden, indicating that this species used the same strategy toexploit the sequence of bloom events in these two locations. How-ever, the proportion of young stages (CI and CII) was highest laterin the season (September) in Franklin Bay. Since developmentfrom egg to CI at water temperatures encountered during sum-mer (<0 °C) takes �46 days (Corkett et al. 1986), considerablereproduction must have taken place at the end of July.

A persistent ice cover and a tight coupling between ice algalbloom and timing of C. glacialis reproduction have also been ob-served in other locations, such as Barrow Strait, the CanadianArctic archipelago, and subarctic Hudson Bay (Runge et al. 1991;Tourangeau and Runge 1991; Ringuette et al. 2002).T

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Daase et al. 877


Amundsen Gulf represents an open shelf system where the on-set, distribution, and duration of the seasonal ice cover may behighly variable (II, Fig. 5; Galley et al. 2008). Both an ice algal anda phytoplankton bloom occur, but their peaks may appear closerin time and be more variable in occurrence and distribution be-cause of more dynamic ice conditions (Arrigo and van Dijken2004). In 2008, spawning, growth, and development in AmundsenGulf were also closely coupled with the two blooms. However, fewC. glacialis females were present during the ice algal bloom in earlyApril. At that time the population consisted mainly of CIII andCIV, indicating that the ice algae was more important for thedevelopment of CIII–CIV than for reproduction. Wold et al. (2011)and Tremblay et al. (2011) suggested that record low ice cover(NSIDC 2011) and favourable winds for nutrient replenishmentprovided favourable conditions for a second spawning event latein the productive season of 2007. These additional recruits wouldmost likely not have had time to develop beyond CIII before the

onset of the overwintering period, explaining the high proportionof CIII in the 2007–2008 overwintering population and the surpris-ingly low numbers of CVs and females in spring 2008. A secondreproduction event may also have occurred during summer 2008in Amundsen Gulf, as the proportion of young stages (CI and CII)was highest relatively late in the season (end of July), suggestingthat considerable reproduction must have taken place during thephytoplankton bloom in June. A similar scenario may explain thehighnumbersofCI andCII later in the season (August–September) asobserved in 2004 in Franklin Bay. Wold et al. (2011) propose thatC. glacialis is able to rapidly develop from CIII and CIV to femalesduring spring and summer under favourable conditions. Thesefemales may then be able to spawn late in the season if food isavailable. Late spawning may be more successful in a system suchas the Amundsen Gulf region than in Svalbard; a longer period ofincoming solar radiation as well as wind-induced mixing and up-welling events can provide favourable conditions for growth and

Fig. 3. Vertical distribution and abundance (individuals·m−3) of copepodite stages of C. glacialis in Amundsen Gulf, Franklin Bay, Rijpfjorden,and Kongsfjorden from January to December. Note differences in scaling of x axis. AF, adult females.



development over a more extensive productive season (althoughnutrient replenishment of the surface layer is not systematic;Tremblay et al. 2008).

Calanus glacialis may encounter conditions similar to those inAmundsen Gulf in other polynyas, such as the North Waterpolynya (Ringuette et al. 2002) and the North East Water polynya(Hirche and Kwasniewski 1997), as well as on the European andSiberian shelves (Kosobokova and Hirche 2001) and in Disko Bayon the west coast of Greenland (Madsen et al. 2001) (II, Fig. 5).Differences in timing of recruitment across the North Waterpolynya could be related to lags in ice melt and onset of phyto-plankton between the eastern and western sectors of the polynya(Ringuette et al. 2002). After experiencing early ice melt, the east-ern polynya displayed an earlier phytoplankton bloom and re-cruitment of C. glacialis.Disko Bay can be ice-covered from Januaryto April–May, with an ice algal bloom peaking just as the icebreaks up (Madsen et al. 2001), although a consolidated ice covermay also be absent in some years (Swalethorp et al. 2011). Ice algaland phytoplankton blooms occur closely in time (usually in April–May), functioning as one major bloom event. Thus, spawning isprobably fueled more by the phytoplankton bloom (Swalethorpet al. 2011), and income breeding is the common strategy (Madsenet al. 2001). Also in Disko Bay, smaller blooms are observedthroughout summer (Madsen et al. 2001), supporting growth anddevelopment until late in the season. Similar to the AmundsenGulf in 2008, CIII and CIV can dominate the population prior tothe bloom (Madsen et al. 2001; Swalethorp et al. 2011), indicatingthat part of the population overwinters as CIII and CIV and maydevelop to CIV and CV next spring.

Another combination of light regime, ice cover, and water tem-perature can be found in the White Sea, where an isolated relictpopulation of C. glacialis exists (Kosobokova 1999). Similar to otherArctic regions, the White Sea is ice-covered during winter andspring. Water temperatures are below zero, and an ice algalbloom occurs here in addition to the phytoplankton bloom,which starts as soon as the ice breaks up. However, being on theArctic Circle, the productive season starts much earlier here thanfurther north. Kosobokova (1999) concluded that reproduction ofC. glacialis was food-dependent in the White Sea, with eggs andnauplii peaking during the phytoplankton bloom. Growth anddevelopment of C. glacialis are also found to depend on watertemperature during the growth season (Pertsova and Kosobokova2010). Cold years defined by late ice breakup and low water tem-peratures can delay the appearance of the new generation by 3–4 weeks. Contrary to other Arctic regimes, water temperaturesduring summer often reach up to 15–25 °C in theWhite Sea, forcingC. glacialis to terminate reproduction andmigrate to deeperwaters

(Kosobokova 1999). In both cold and warm years, the growth sea-son in the White Sea ended in July with the occurrence of CIV.

Despite being one of the northernmost locations included inthis study, Kongsfjorden exhibits the least “Arctic-like” condi-tions. Sea ice does not consolidate every year or is completelylacking, relatively warm Atlantic water intrudes, and only onemajor bloom occurs in spring (III, Fig. 5). Our data show that asuccessful development and high recruitment of C. glacialis is pos-sible in a high Arctic environment lacking an ice algal bloom.Unfortunately, no data on the onset of spawning and egg produc-tion rates are available for Kongsfjorden. However, young cope-podites (CI) were present from late April to late May. Assuming

Fig. 4. Seasonal variation in total Calanus glacialis biomass(mg DM·m−2) observed in all four study areas. Calanus glacialisbiomass was calculated from stage-specific dry masses as describedin Daase et al. (2007).

Fig. 5. Conceptual figure showing phenology of Calanus glacialis lifehistory events at different locations and latitudes (based on datacollected in Table 2). Roman numbers refer to three main types ofenvironmental conditions (see Discussion).

Daase et al. 879


that development from egg to CI takes about 46 days at 0 °C(Corkett et al. 1986), spawning would have started in mid-Marchand peaked in April. Since the spring bloom in both years did notoccur beforemid-April, at least part of the C. glacialis population inKongsfjorden had opted for reproduction without additional foodsupply (i.e., following the strategy of a capital breeder). This is inagreement with observations made in Kongsfjorden in spring2003 and 2004 (Kwasniewski et al. 2013). Females were abundantin April 2006, while peak abundance of CI coincided with that ofnauplii (Fig. 2b), indicating that the main reproductive periodprobably stretched over a timewindowof approximately 1month,coinciding at least partly with the spring bloom.

Interestingly, this high number of recruits in spring 2006 couldnot be sustained until the end of summer, when abundance andbiomass of C. glacialis in 2006 equaled those observed in 2007(Fig. 4). Watermass exchange between Kongsfjorden and the shelfis common, however, during summer, and variability in Calanusabundancemay be affected by advection (Cottier et al. 2005;Williset al. 2006).

An ice-free regime such as Kongsfjorden seems to favour a cap-ital breeding strategy. Similar observations have been made inLurefjorden, an enclosed fjord on the west coast of Norway lo-cated at 60°N. Here a relict population of C. glacialis dominates theCalanus assemblage (Eiane et al. 1999; Niehoff and Hirche 2005).The fjord is not ice-covered during winter, and gonad maturationand egg production were found to be decoupled from the phyto-plankton bloom (Niehoff and Hirche 2005). Conditions in Kongs-fjorden and Lurefjorden may be indicative of the kind ofenvironment C. glacialis could encounter in the future in areaswhere ice conditions will become severely reduced and watertemperatures increase.

Since warmer water and lack of ice prolong the productiveseason in ice-free areas, a possible explanation for the capitalbreeding observed in Kongsfjorden and Lurefjorden is thatC. glacialis takes advantage of long feeding seasons by storing re-sources that are used for breeding next spring. In such systems,one should expect interannual variability in the degree of capitalbreeding depending on the duration of the feeding season theyear before. Feeding late in the season would be particularly ad-vantageous if the predation risk is low at this time of the year(Varpe et al. 2009). However, capital breeding cannot be seen as anadaptation to a longer productive season. For one reason, thisstudy showed that the population in Amundsen Gulf, where theproductive season can last long into the autumn, uses an incomebreeder rather than capital breeder strategy. Furthermore, thearctic C. hyperboreus, which occurs in the central Arctic Oceanwhere primary production is low, is almost exclusively a capitalbreeder (Conover and Siferd 1993; Hirche and Niehoff 1996).However, the Atlantic C. finmarchicus, which occurs in area with along primary productive season, is mainly an income breeder(Richardson et al. 1999).

For C. glacialis, the main difference between populations in ice-free and ice-covered areas is the lack of an ice algae bloom andthus the lack of a bimodal food distribution. Most likely, differentannual routines may maximize fitness in these two cases (cf.Varpe 2012). The capital breeding strategy allows eggs to be pro-duced independently of concurrent food intake and thereforepotentially prior to the spring bloom. For situations with apelagic bloom only, the offspring can develop through the food-independent development stages before the spring bloom startsand then utilize the bloom production. Model predictions suggestthis to be the optimal strategy when the feeding season is early(Varpe et al. 2009). A head start on reproduction and developmentin spring also allows the overwintering stage to be reached early.Descent to diapausemay therefore also take place early. In an areawith ice algae blooms, the females may, through income breed-ing, produce offspring while feeding on ice algae, whereas theoffspring utilize the pelagic bloom (Søreide et al. 2010). Indeed,

the pelagic bloom as well as the population development ofC. glacialis in Kongsfjorden occurred 1–2 months ahead of that inRijpfjorden. By the time young stages appeared in Rijpfjorden inJuly, the development in Kongsfjorden had already reached itsfinal stage, and the descent to overwintering depths had started.In Rijpfjorden, the bulk of the population had descended todeeper layers first in September. Early descent to overwinteringdepths, prior to the end of the phytoplankton bloom, may increasefitness because it might reduce the predation risk (Kaartvedt 2000;Varpe et al. 2007) or exposure to unfavourable abiotic conditions(i.e., high temperature in Lurefjorden; Niehoff and Hirche 2005).Despite the differences in annual routines in Kongsfjorden andRijpfjorden, both populationsmanaged to build up a high amountof biomass by the end of the productive season (Fig. 4), indicatingthat the respective strategies are both successful.

Life span and seasonal migrationWhile C. glacialis is capable of developing from eggs to wax

ester-rich copepodite stages III and IV within a single year (Scottet al. 2000), the increase in body mass and lipid reserves duringdevelopment from CIV to CV is only achieved in a single yearunder favourable conditions, and often a second year is necessary.Most studies therefore concluded that C. glacialis has a 1- to 2-yearlife cycle (Tande et al. 1985; Conover 1988; Kosobokova 1999;Fig. 5). Despite the differences in environmental settings and re-productive strategies in Rijpfjorden and Kongsfjorden, we did notfind any evidence of differences in life span between these fjords.In both fjords, CIV and CV were found to be the main overwinter-ing stages, supporting the assumption that C. glacialis is able tofulfil its life cycle in 1–2 years.

The high amount of CIII and CIV in the overwintering popula-tion of the Amundsen Gulf would indicate a 2-year life cycle.However, as discussed above, we suggest that overwintering CIIIand CIV may develop into females during spring and summerunder favourable conditions. By reproducing later in the season,these females would shorten the life cycle to 1 year. Nevertheless,late offspring bear the risk of running out of time to develop to astage suitable for diapause (Varpe et al. 2007). In such cases, it maybe beneficial for members of the parent generation to rather fol-low a 2-year life cycle, with the possibility of early and even capitalbreeding in their second year (Varpe et al. 2009).

Owing to lack of data from late summer and early autumn, it isdifficult to estimate the time of descent in Amundsen Gulf andFranklin Bay. At both locations, young copepodites were abun-dant quite late in the summer. These copepodites would mostlikely need time to graze in surface waters to accumulate enoughenergy for overwintering. Data from October to December indi-cate that the bulk of the population reached greater depth as lateas December (Fig. 3). Over the course of the production season, avariable vertical distribution of C. glacialismay be explained by thegradual deepening of the subsurface chlorophyll maximum inAmundsen Gulf (16 m in late April to 56 m in early August; Forestet al. 2011a) and Franklin Bay (Tremblay et al. 2008). This featuremay have led to the deepening of the distribution of C. glacialis andnot only the migration to depth of a fraction of the populationready to overwinter. Martin et al. (2010) found that diatoms con-tributed 10 timesmore in the subsurface chlorophyllmaximum inthe lower euphotic zone, and cells were larger (cells >20 �m) thanin the upper mixed layer of Canadian Arctic waters in late sum-mer. Thus, food seems to be still available to C. glacialis in latesummer, but distributed deeper in the water column.

Favourable conditions early in the season do not guarantee ashorter life cycle if conditions become detrimental later in theseason. In the White Sea, high water temperatures in the upperlayers force C. glacialis to migrate to greater depth early in thesummer (Kosobokova 1999; Pertsova and Kosobokova 2010), sodespite favourable spring conditions such as an early onset of ice



algal and spring bloom and a long productive season, C. glacialishas a 2-year life cycle in the White Sea.

Our data provided little insight into the interaction between lifespan and reproductive strategies. One unknown factor is theamount of energy actually needed for overwintering. How muchlipids need to be stored before the descent, and how do energyreserves during diapause vary between populations and loca-tions? If small lipid reserves are sufficient, and ice algae fuel re-production, a late descent and thus a shorter life cycle may bebeneficial. If large lipid reserves are needed, it may be worthpostponing breeding to breed early in the second year, especiallywhen capital breeding is beneficial (Varpe et al. 2009). These as-pects of the life history may be state-dependent, with those indi-viduals that have accumulated enough lipids benefitting from anearly ascent, while those that still profit from continued feeding(late recruits) may remain in the surface layers until late in theseason (Jónasdóttir 1999; Miller et al. 2000; Pond and Tarling 2011).This suggests that these strategies need to be investigated on anindividual basis (i.e., Vogedes et al. 2010).

The phenology of C. glacialis in a changing ArcticSøreide et al. (2010) suggested that variability in ice cover might

lead tomismatch between the timing of ice algal and phytoplank-ton blooms and timing of reproduction and development, sincethe development from egg to the first feeding nauplius stage (NIII)of C. glacialis takes about 2 weeks (Daase et al. 2011). The offspringcan therefore exploit the second bloom more efficiently if it doesnot follow the first one too closely. An early ice breakup mayabbreviate the ice algal bloom period, and also the gap betweenice algal and phytoplankton blooms, and hence lead to poorergrowth condition for the C. glacialis population.

Ringuette et al. (2002) found a close relationship between thetiming of the phytoplankton bloom and recruitment of C. glacialisCI. We expanded the dataset used by Ringuette et al. (2002) withdata from the present study and from Disko Bay (Fig. 6; Table 3)and analyzed the relationship between the week of peak phyto-plankton and ice algae bloom and week of first occurrence of CIand week of maximum CI abundance (Fig. 6). We used “time offirst occurrence of CI” as a proxy for the start of reproduction. Thevariable “time of maximum CI abundance” provides an estimatefor the time of peak reproduction activity. In both cases we as-sume mortality of young to be independent of time of the season.There was a positive relationship between the week of peak phy-

toplankton bloom and week of both first occurrence of CI andmaximum CI abundance (linear regression R2 = 0.36, p < 0.1 andR2 = 0.67, p < 0.01, respectively; Fig. 6a). The relationship was alsopositive for week of first occurrence of CI after removing datapoints from locations without ice cover (R2 = 0.56, p < 0.05). Therewas also a positive relationship betweenweeks of highest ice algalproduction and maximum CI abundance (Fig. 6b). These relation-ships imply that an earlier onset of the spring bloom (e.g., due toreduced ice cover) may lead to an earlier start of reproduction inC. glacialis, confirming the observations made by Ringuette et al.(2002). However, these results should be treated with caution asthey are based on only a few data points, in particular the rela-tionship with the timing of the ice algae bloom. The results illus-trate the gap in data that needs to be addressed to make formalanalyses of the relationships between timing of food availabilityand reproduction. Studies with high temporal resolution withinseasons are needed to increase the precision of the estimates in-cluded in this kind of analyses.

Amundsen Gulf in 2008 represents a scenario where icebreakup and ice algal bloom occurred earlier than normal. Still,the tight coupling between the occurrence of eggs, nauplii, andearly copepodite stages with ice algal and phytoplankton bloomsindicates that reproduction did not fail for the population. How-ever, the biomass in autumn was much lower in Amundsen Gulfthan in Rijpfjorden (Fig. 4), where the estimated biomass is amongthe highest observed on a pan-Arctic scale (Table 2). Søreide et al.(2010) argue that in 2007 in Rijpfjorden the occurrences of ice algaland phytoplankton blooms and C. glacialis reproduction wereperfectly timed. So one could argue that the recruitment in an“early-ice-break-up“ scenario may not be as successful as in a“well-timed” scenario, which is in agreement with multiyear ob-servations from Rijpfjorden (Leu et al. 2011). Kongsfjorden wouldbe representative of an ice-free scenario, and as discussed above,C. glacialis can thrive under these conditions. The absence of an icealgal bloom seems to be compensated by applying a capital breed-ing strategy and thus timing the growth and development of re-cruits to the phytoplankton bloom.

In summary, C. glacialis populations subjected to various envi-ronmental conditions across the Arctic showed variability in thetiming of reproductive events. Our study suggests that the season-ality of the environment and hence the timing of primary produc-tion are key drivers of this variability. The degree of capital versus

Fig. 6. (a) Relationship between week of highest chlorophyll a (Chl a) concentration in the water column and week of first appearance of CIof Calanus glacialis and week of maximum CI abundance. Dotted line shows regression line of week of Chl a maximum versus week ofmaximum CI abundance (R2 = 0.36, p < 0.1). Solid line shows regression line of week of Chl a versus week of first occurrence of CI (R2 = 0.6,p < 0.01). Grey points depict data from areas without ice cover. Regression excluding these points: R2 = –0.19, p > 0.5 (Chl a maximum versusmaximum CI) and R2 = 0.56, p < 0.05 (Chl a maximum versus first occurring CI). (b) Relationship between week of highest ice algae Chl aconcentration and week of first appearance of CI of C. glacialis and week of maximum CI abundance (see Table 3 for details).

Daase et al. 881


income breeding was found to vary with the feeding environ-ment. Populations that have access to an ice algae bloom prior tothe phytoplankton bloom seem to favour an income breedingstrategy, perhaps with some capital breeding in parallel with theice algae feeding, while those living in an openwater system, withonly onemajor bloom event, start reproduction prior to the onsetof this bloom. The variability observed suggests that C. glacialis hasa flexible reproductive strategy that may explain its wide distri-bution in Arctic continental shelf seas.

How much energy is actually needed for overwintering andreproduction, what triggers ascent and descent, and how does themale part of the population develop throughout the season aresome of the questions that need to be addressed in future studiesto better understand life history adaptations of C. glacialis to dif-ferent environmental conditions and the eventual impact of cli-mate change on this key species.

AcknowledgementsWe are grateful to Fanny Narcy for providing chlorophyll data

fromKongsfjorden.We thank the numerous researchers that pro-vided data for this study through their work within CASES, CFL,and CLEOPATRA. This study was supported by the IPY Canada,Natural Sciences and Engineering Research Council (NSERC) ofCanada, and the Canadian Museum of Nature, the NorwegianResearch Council (Project No. 178766/S30, CLEOPATRA) as part ofthe Norwegian contribution to the IPY (IPY 2007–2009) and byStatoil (Ice-edge program) as part of Statoil–ARCTOS Arctic Re-search Programme (SAARP). Further support was provided by theNorwegian Research Council through the projects CLEOPATRA IIand CircA (Project Nos. 216537 and 214271).

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Table 3. Overview of timing of ice algae and phytoplankton bloom and timing of CI recruitment in different Arctic regions.

Location YearLatitude(°N) Ice-covered

Week of max.ice algae Chl aconcentration

Week ofmax. Chl aconcentrationin water column

Week of firstoccurrenceof CI

Week of peakCI abundance Reference

Northern Iceland 1993 67 No 16 21 Gislason andAstthorsson 1998

Disko Bay 1996 69 Yes 18 22 21 29 Madsen et al. 2001Disko Bay 1997 69 Yes 15 19 20 Madsen et al. 2001Franklin Bay 2004 71 Yes 20 28 (*) 37 This studyAmundsen Gulf 2008 71 Yes 17 20 16 27 This studyBarrow Strait 1994 74 Yes 26 28 Ringuette et al. 2002Barrow Strait 1995 74 Yes 28 >32 Ringuette et al. 2002Barents Sea 1987 75 Yes 22 21 Melle and Skjodal 1998Eastern North Water 1998 77 Yes (Polynya) 19 20 Ringuette et al. 2002Western North Water 1998 77 Yes (Polynya) 22 24 Ringuette et al. 2002Kongsfjorden 2006 79 No 17 15 20 This studyKongsfjorden 2007 79 No 19 24 This studyRijpfjorden 2007 81 Yes 18 28 24 29 This study

Note: Relationship between timing of bloom and CI recruitment is shown in Fig. 6. The asterisk (*) indicates that time of first occurrence of CI in Franklin Bay is notincluded because CI were present throughout the winter.



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http://nsidc.org/arcticseaicenews/

http://dx.doi.org/10.4319/lo.1994.39.1.0021

http://dx.doi.org/10.1134/S0001437010040090

http://dx.doi.org/10.1134/S0001437010040090

http://dx.doi.org/10.1023/A%3A1013111832700


http://dx.doi.org/10.4319/lo.2011.56.4.1310

http://dx.doi.org/10.1046/j.1365-2419.1999.00007.x


http://dx.doi.org/10.1016/S0967-0645(02)00179-0


http://dx.doi.org/10.4319/lo.1988.33.2.0280


http://dx.doi.org/10.1029/2000JC000478

http://dx.doi.org/10.1007/s003000000114

http://dx.doi.org/10.1007/s003000000114

http://dx.doi.org/10.1007/s00300-010-0930-9

http://dx.doi.org/10.1007/BF02114675

http://dx.doi.org/10.111/j.1365-2486.2010.02175.x

http://dx.doi.org/10.111/j.1365-2486.2010.02175.x



http://dx.doi.org/10.1007/BF01344337

http://dx.doi.org/10.1029/2007JC004547

http://dx.doi.org/10.1029/2011.GL048825



http://dx.doi.org/10.1890/08-1817.1

http://dx.doi.org/10.1890/08-1817.1

http://www.ncbi.nlm.nih.gov/pubmed/20391994

http://dx.doi.org/10.1111/j.0030-1299.2007.15893.x

http://dx.doi.org/10.1111/j.1600-0706.2008.17036.x

http://dx.doi.org/10.1093/plankt/fbq068

http://dx.doi.org/10.1029/2006GL025872

http://dx.doi.org/10.1029/2006GL025872



http://dx.doi.org/10.1007/s00300-007-0373-0

http://dx.doi.org/10.1007/s00300-011-1062-6

http://dx.doi.org/10.1007/s00300-011-1062-6

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