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Journal of Plankton Research academic.oup.com/plankt

J. Plankton Res. (2017) 00(00): 1–20. doi:10.1093/plankt/fbx045

Growth and reproduction of the chaetognaths Eukrohnia hamata and Parasagitta elegans in the Canadian Arctic Ocean: capital breeding versus income breeding

† JORDAN J. GRIGOR1,2* , MORITZ S. SCHMID1 AND LOUIS FORTIER1   TAKUVIK JOINT INTERNATIONAL LABORATORY AND QUÉBEC-OCÉAN, UNIVERSITÉ LAVAL, QUÉBEC, QUÉBEC GV A, CANADA AND CENTER FOR SCIENCE OUTREACH, VANDERBILT UNIVERSITY, PMB ,  APPLETON PLACE, NASHVILLE, TN , USA

† PRESENT ADDRESS: CENTER FOR SCIENCE OUTREACH, VANDERBILT UNIVERSITY, NASHVILLE, TN 37212, USA

*CORRESPONDING AUTHOR: [email protected]

Received November 29, 2016; editorial decision August 10, 2017; accepted August 12, 2017

Corresponding editor: Marja Koski

In Arctic seas, primary production and the availability of food for zooplankton are strongly pulsed over the short productive summer. We tested the hypothesis that Eukrohnia hamata and Parasagitta elegans, two similar and sympatric arctic chaetognaths, partition resources through different reproductive strategies. The two species had similar natural longevities of around 2 years. Eukrohnia hamata, which occurred at epi- and meso-pelagic depths, spawned two distinct broods in autumn and spring. Offspring production coincided with drops in the frequency of E. hamata with visible lipid reserves, characteristic of capital breeders. Growth was positive from April to January and negative in February and March. Growth and maturation were similar for the two broods. Storage reserves contained in an oil vacuole may allow E. hamata to reproduce and grow outside the short production season. Parasagitta elegans produced one brood in summer–autumn during peak production in near-surface waters, characteristic of income breeders. In winter, P. elegans co-inhabited meso-pelagic waters with E. hamata, where it neither grew nor reproduced. As the Arctic warms, the development of an autumn phytoplankton bloom could favour the summer–autumn brood of P. elegans.

KEYWORDS: Eukrohnia hamata; Parasagitta elegans; chaetognaths; reproduction; growth; annual routines; Beaufort Sea; Arctic Ocean

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INTRODUCTION may depend on the seasonal partitioning of resources, which can be achieved through differences in vertical Arrow worms or chaetognaths form a highly successful distribution, diet and reproductive strategies. For instance, phylum of semi-gelatinous marine zooplankton repre- the reproductive strategies of the two dominant arctic sented by ~200 species worldwide, with biomass esti- herbivorous copepods differ markedly in ice-covered – et al. mated at 10 30% that of copepods (Bone , 1991). waters. The large capital-breeder Calanus hyperboreus They can represent a significant fraction of the diet of reproduces in winter, fuelling egg production with et al. many animals such as amphipods (Gibbons , 1992), lipids accumulated in summer (Conover, 1967; Hirche other chaetognaths (Pearre, 1982), seabirds (Mehlum and Niehoff, 1996; Pasternak et al., 2001), whereas its and Gabrielsen, 1993), and are the preferred prey of the fi fi congener, Calanus nmarchicus, does not reserve lipids to larvae of some tropical sh and commercially important fuel its reproduction (income breeding, Sainmont et al., et al. et al. decapods (Sampey , 2007; Saunders , 2012). 2014). Low amounts of wax esters (Connelly et al., Chaetognaths are hermaphrodites. Spermatogonia 2012; Connelly et al., 2016), and peak reproduction in bud off from testes parallel to the tail walls to produce – fi spring summer in the epipelagic P. elegans (Kramp, spermatocytes, which are transmitted to a conspeci cto 1939; Sameoto, 1971; Grigor et al., 2014), suggest income fertilize its oocytes (Alvarino, 1992; Bergey et al., 1994). breeding with the summer maximum in prey abundance Each chaetognath possesses one pair of seminal vesicles fuelling reproduction. By contrast, the accumulation of on the tail segment and one pair of seminal receptacles wax esters in an oil vacuole (Pond, 2012), and year-round at the posterior ends of the oviducts. Two individuals fi breeding in Gerlache Strait, Antarctica (Øresland, 1995), rst come into contact with each other, before sperm is suggest capital breeding fuelled by lipid reserves in passed from the seminal vesicles of one individual to the E. hamata. seminal receptacles of the other (Goto and Yoshida, We describe the life histories of E. hamata and P. ele- 1985). Hatching strategies vary amongst species. For gans over an annual cycle based on weekly sampling of Parasagitta elegans instance, releases buoyant eggs directly zooplankton in the Amundsen Gulf (Beaufort Sea) from into the water (Kotori, 1975; Hagen, 1999), whereas the August 2007 to July 2008, complemented by collections young of Eukrohnia hamata are retained for some time in fi from other areas of the Canadian Arctic in autumn of the folded lateral ns of the adults (Alvarino, 1968 and the 2 years. In particular, growth of size cohorts, repro- references therein). duction and oil reserves are tracked to explore the In contrast to the high diversity of chaetognaths in hypothesis that E. hamata is a capital breeder that et al. other seas (De Souza , 2014), only three species are spawns during most of the year, while P. elegans is an frequently reported in Arctic plankton surveys. income breeder, reproducing during periods of high Parasagitta elegans is a neritic species, often peaking in prey availability. abundance in epipelagic waters; E. hamata is abundant in meso-pelagic and deep waters; and Pseudosagitta maxima, growing much larger (up to 90 mm) than the other species (40–45 mm), is typically bathy-pelagic but may METHOD also occur near the surface in the Arctic (Bieri, 1959; Alvarino, 1964; Terazaki and Miller, 1986; Sameoto, Study area 1987). A fourth species, Heterokrohnia involucrum has also Sampling was conducted on-board the CCGS Amundsen, been recorded at bathy-pelagic depths, so far only in the primarily from October 2007 to August 2008 in the Arctic Ocean (Dawson, 1968). While their contribution Beaufort Sea (Fig. 1). To complete the annual cycle of to higher trophic levels is poorly documented, arctic observations, additional collections from the Labrador chaetognaths may consume an important fraction of Sea, the Canadian Archipelago and Baffin Bay were copepod biomass. Although admittedly little better than included in the analyses (Fig. 1). In addition to the 27 a guess, Welch et al. (1992) estimated that chaetognaths stations sampled at weekly or higher resolution in the in Lancaster Sound ingest 51% of the copepod biomass Amundsen Gulf region (69–72°N, 121–131°W) from − − annually (164 of 319 kJ m 2 yr 1). November 2007 to August 2008, two stations were At high arctic latitudes, resource availability is sampled in Nachvak Fjord in August 2007, two stations strongly pulsed seasonally, with maximum phytoplank- in Parry Channel in October 2007 and two stations in ton and zooplankton biomass occurring during the short northern Baffin Bay in September 2008 (Fig. 1 and ice-free season in late summer and autumn (Falk- Supplementary Table 1). Amundsen Gulf, our main Petersen et al., 2007; Falk-Petersen et al., 2009;;Søreide sampling region, is a 400 km long, 170 km wide channel et al., 2010). Here, the co-existence of similar species with a maximum bottom depth of ~630 m that connects

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Downloaded from https://academic.oup.com/plankt/article-abstract/doi/10.1093/plankt/fbx045/4344873/Growth-and-reproduction-of-the-chaetognaths by guest on 05 October 2017 J. J. GRIGOR ET AL. j ANNUAL LIFE CYCLES OF TWO ARCTIC ARROW WORMS

Fig. 1. Bathymetric maps of the Canadian Arctic Ocean indicating the regions and stations (black circles) where chaetognaths were sampled from August 2007 to September 2008. Station IDs provided.

the south-eastern part of the Beaufort Sea to the water column at single stations in Nachvak Fjord, Parry Canadian Archipelago. Amundsen Gulf is typically cov- Channel and Baffin Bay were obtained using a ered with sea ice from October to early June (Barber conductivity-temperature-depth (CTD) system. We also and Hanesiak, 2004). Three water masses are detected collected seawater samples from 9–10 depths in the in the Amundsen Gulf (Geoffroy et al., 2011 and refer- upper 100 m, using the CTD rosette equipped with 24 ences therein); the Pacific Mixed layer (PML; 0–60 m), 12 1 Niskin-type bottles (OceanTest Equipment). the Pacific Halocline (PH; 60–200 m) and the Atlantic Immediately after sampling, subsamples (500 ml) for the layer (AL; >200 m). Nachvak Fjord is a pristine 45-km determination of total chl a were filtered onto 25 mm long sill-fjord in Nunatsiavut, Northern Labrador, with Whatman GF/F filters (nominal porosity of 0.7 μm). a maximum depth of 210 m (Bell and Josenhans, 1997; Chl a was measured using a Turner Designs 10-AU Simo-Matchim et al., 2016). The deep semi-enclosed fluorometer, after 24 h extraction in 90% acetone at basin of Baffin Bay lies further north, and is connected 4°C in the dark without grinding (acidification method via Parry Channel to the Beaufort Sea in the west of Parsons et al., 1984). (Fig. 1). Two similar samplers were used to collect zooplankton: a square-conical net with a 1 m2 opening area, 200 μm mesh and a rigid cod-end, and a Hydrobios® Sampling Multinet with nine individual opening and closing nets In the Amundsen Gulf, estimates of weekly profiles of with 0.5 m2 openings, 200 μm mesh and rigid cod ends. temperature and salinity between November 2007 and At 12 stations, the 1 m2 net was deployed cod-end first July 2008 are from Geoffroy et al. (2011), and those of (non-filtering) to 10 m above the seabed and hauled − chlorophyll a (chl a) biomass are from Darnis and back to the surface at a speed of 0.5 m s 1. At 22 sta- Fortier (2014). Salinity and temperature profiles of the tions, the Multinet was deployed to 10 m above the

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− seabed and retrieved at 0.5 m s 1, sampling sequentially et al., 1996; Choe and Deibel, 2000; Grigor et al., 2014), over pre-set depth intervals, the overall thickness of we assumed that monthly growth of a cohort could not − which varied from 100 to 520 m. Typically, 3 × 20-m exceed 7 mm mo 1. Second, the possibility that a cohort depth strata were sampled from 10 m above the seafloor was absent from the population in one month if clearly upward, and 3 × 20-m depth strata were sampled from present during the preceding or following month in the 60 m depth to the surface. The remaining interval (from time series was excluded. Solutions aimed to avoid 70 m above the bottom to 60 m below the surface) was cohort length overlaps. Goodness-of-fit was tested using then divided into three equal sampling layers the Chi-square statistic. Parasagitta elegans data for August (Supplementary Table 1). Of the 34 hauls, 24 were are from Nachvak Fjord in 2007 due to the scarcity of made during the day-time (06:00–17:59) and 10 were this species in the Amundsen Gulf collections in that made during the evening/night-time (18:00–05:59, month in 2008. Supplementary Table 1). Samples were fixed in 4% formaldehyde-seawater solution buffered with sodium borate. Estimation of maturity and oil vacuole area Eukrohnia hamata and P. elegans were stained with a Borax Carmine solution to highlight gonads (Pierce, 1941; Chaetognath body size and sampler fi Grigor et al., 2014). Oocytes (Fig. 2) in single ovaries ef ciency were counted and diameters measured under the stereo- Chaetognaths were sorted from the samples, identified microscope. Ovary length, diameter of the externally to species and when possible, measured (nearest mm) protruding part of the seminal receptacles, and width of from the top of the head to the tip of the tail, excluding the seminal vesicles (Fig. 2), were measured to the near- the caudal fin. Heavily damaged or broken individuals est 0.01 mm. The distribution of spermatogonia/sper- were excluded, but those missing heads only (~1 mm) matocytes in tails was characterized as absent, were included in the analyses, as positive identification spermatogonia present near walls only, or spermatocytes remained possible (Fig. 2) and length could be esti- dispersed throughout the tail. The width of seminal vesi- mated. Out of 8179 chaetognaths sorted, 7245 chaetog- cles was measured to the nearest 0.01 mm. The pres- naths (5918 E. hamata and 1298 P. elegans) were ence or absence of an oil vacuole (Fig. 2) was noted in included. Twenty-nine (29) Pseudosagitta maxima present 2089 individuals of E. hamata. The width and height of in the samples were not analysed further. The relative the vacuole were measured to the nearest 0.01 mm efficiency of the Multinet and square-conical net at cap- under the stereomicroscope. Area was calculated as π × turing chaetognaths was assessed by comparing the size– 0.5 width × 0.5 height. The presence of oil in the vacu- frequency distribution of E. hamata or P. elegans in the ole and/or oil droplets in the digestive tract was noted. two nets. Vertical distributions Hatching and cohort development About 19 Multinet collections (typically nine samples The occurrence of newborns (2–4 mm) in Multinet col- per haul), 1–2 per month from August 2007 to lections was used as an index of recent hatching. The September 2008, were analysed to estimate abundances subsequent growth of the different cohorts was inferred of E. hamata and P. elegans populations and age classes in − from successive monthly length–frequency distributions discrete layers of the water column (ind. m 3). Contour in collections from both samplers. Lengths from the plots were produced in the R computing environment Multinet collections were included twice in the histo- (R Development Core Team, 2008), using Akima grams to give equal weight to this sampler (0.5 m2 aper- bilinear interpolation performed vertically for every ture) and the square-conical net (1 m2 aperture). Each metre of the water column. Assuming a lognormal dis- cohort was detected by visual means, and the MIXdist tribution, species abundances A were log-transformed as library in R™ (Du, 2002) was used to estimate its mean log10(A + 1) prior to interpolation, also serving to pre- length (arithmetic mean), standard deviation and length serve abundance A = 0(Legendre and Legendre, 2012). range in each month. Monthly growth rates of each Vertical distributions of populations were also character- cohort were calculated from changes in mean length. In ized by their weighted mean depths in the water column most cases, a cohort was clearly defined in the month [Zm, m, Eq. (1a)] with standard deviations [Zs, m, length–frequency distributions. In some cases, the inter- Eq. (1b)] as described by Darnis and Fortier (2014), pretation of cohorts was aided by two assumptions. based on the earlier equations of Dupont and Aksnes First, based on published estimates of growth (Welch (2012). Zm was normalized between 0 and 1 to identify

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Fig. 2. Illustrations and photographs of E. hamata and P. elegans;(a) Diagrams of the two species indicating maturity features and the centrally positioned oil vacuole in E. hamata (illustrations by Lu Zheng, modiﬁed after Alvarino, 1992). (b) Photographs of live E. hamata (top) and P. elegans (bottom) taken in situ by a zooplankton imager (Schmid et al., 2016) in the Canadian Arctic. Specimens ~20 mm. (c) Oocytes in a P. elegans individual. (d) Ovaries in a live E. hamata individual (imaged in situ). (e) Tail sperm, seminal vesicles and seminal receptacles in a P. elegans individual.

the positions of animals relative to a station’s bottom temperatures in the AL were ~0°C. Salinities were depth: 30–32 psu in the PML, 32–34.6 psu in the PH, and >34.6 psu in the AL (Geoffroy et al., 2011). Ice algae n n was ﬁrst detected in late March in the PML and peaked Z=() wdz dz 1a − m ∑∑iii i in late April and early May (~10 mg m 3), when it was i==11i succeeded by a surface phytoplankton bloom. In July, a subsurface chl a maximum (SCM) occurred at ~40 m ⎛ n n ⎞ −3 ⎜ 2 ⎟ 2 (16 mg m ), and the phytoplankton penetrated the PH Z=−()⎜∑∑ wdz1 /1b dz11⎟ Z s ⎝ 1 ⎠ m (Darnis and Fortier, 2014). i==1 i 1

where n is the number of depth intervals that were Physical environment and primary sampled in the water column, wi is the abundance of production in autumn (other sampling animals in depth interval i, di is the thickness of depth locations) interval i and zi is its mid-point. In August 2007, a steep thermocline was observed in Nachvak Fjord between the surface and 60 m, with temperature decreasing from 3.4°Cto−1.6°C (Supplementary Fig. 1). Chl a concentrations peaked at RESULTS − 20 m (2.8 mg m 3). In October 2007, temperatures at Physical environment and primary our Parry Channel station rose from <−1°C at the sur- production in the Amundsen Gulf face to 0.4°C at ~45 m, fell to <1°C at 60 m, and then From November 2007 onwards, the PML in the rose again from −1.5°C at 200 m to 0.7°C at 500 m. − Amundsen Gulf had temperatures of −1.6 to −0.6°C, Chl a concentrations remained below 0.5 mg m 3 at but warmed to >9°C at some stations in June and July sampled depths. In September 2008, temperatures at 2008 on top of a strong thermocline. Throughout the our Bafﬁn Bay station rose from <−1°C at the surface study, temperatures in the PH were −1.6 to 0°C, and to >0.3°C at ~85 m, fell to <1.1°C at 100 m, with

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Fig. 3. (a) Chaetognath community composition (%) at Amundsen Gulf stations, in relation to bottom depth. Multinet and square-conical net collections included. (b) Weighted mean depths of E. hamata and P. elegans normalized relative to bottom depth at Amundsen Gulf stations (±1 SD, see “Method”). Multinet collections. The dotted line indicates the top of the Paciﬁc Halocline (60–200 m) and the dashed line indicates the top of the Atlantic Layer >200 m (Geoffroy et al., 2011).

smaller fluctuations in temperature in deeper waters. most pronounced in P. elegans, which, based on weighed − Chl a concentrations peaked at 45 m (1.1 mg m 3). mean depth, resided primarily in the PH from December Strong haloclines were observed in the upper 100 m at to March, rose into the PML (0–60 m) in March/April all three stations (Supplementary Fig. 1). during the development of ice algae, and returned to the PH in late June (Fig. 3b). Parasagitta elegans was 39 times more abundant than E. hamata in Nachvak Fjord in − August (462 ind. m 2). At Nachvak Fjord, Parry Channel Abundances and vertical distributions of fi chaetognath species and Baf nBay,theP. elegans population remained <200 m (Fig. 3b). Eukrohnia hamata was present at all stations in the − Amundsen Gulf with abundances ranging from 56 ind. m 2 −2 in late July to 894 ind. m in mid-April. Parasagitta elegans Length distributions and sampler efficiency waslessabundantthanE. hamata at all stations in − − Amundsen Gulf (16 ind. m 2 in November to 244 ind. m 2 Eukrohnia hamata in the Amundsen Gulf ranged in length − ≤ in December), and in Parry Channel (320 ind. m 2)and from 2 to 40 mm ( 34 mm in other sampling regions) fi −2 and P. elegans from 2 to 42 mm (up to 45 mm in other Baf nBay(64ind.m ) in October and September, – respectively. Pseudosagitta maxima occurred in only four sampling regions). The length frequency distributions of each species were not significantly different Multinet collections from the Amundsen Gulf, typically – > in the Atlantic Layer, with maximum abundances of (Kolmogorov Smirnov test, P 0.1) between the two − ≥ 4 ind. m 2.RelativetoP. elegans, the abundance of samplers (Fig. 4). The few E. hamata and P. elegans E. hamata increased with station depth (Fig. 3a). Eukrohnia 40 mm were caught solely by the larger-aperture hamata occurred primarily in the deep AL of the Amundsen square-conical net. Gulf (>200 m, Fig. 3b), based on weighted mean depth, except on two dates in late May and late July when the E. hamata population was centred in the PH (60–200 m). Timing of reproduction In Parry Channel (October) and Baffin Bay (September), The hatching seasons of the two chaetognath species the E. hamata population remained >200 m. In the were approximately complementary over the annual Amundsen Gulf, seasonal vertical migration (SVM) was cycle (Fig. 5). Apart from the occurrence of newborns in

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Fig. 4. Length–frequency (mean % + 1 SD) distributions of E. hamata and P. elegans in the square-conical (S-C) net (1 m2 aperture, 200 μm mesh) and Multinet (0.5 m2 aperture, 200 μm mesh) in the Amundsen Gulf. Note the different scales for the two species. k is the number of collections.

October, E. hamata hatched from December to July with the production of newborns increasing from low values in December–January to a maximum in April, and ceas- ing after July (Fig. 5). Except for their absence in our collections in November and January, P. elegans newborns were observed continuously from July to February, with hatching peaking in December (Fig. 5).

Eukrohnia hamata length cohorts and life cycle Four cohorts were distinguished in all months except August and September 2008, when there were three (Fig. 6). The cohort of largest/oldest chaetognaths was labelled E1 (Eukrohnia 1), the intermediate-sized cohorts E2 and E3, and the cohort of autumn (October) newborns E4. The E1 cohort of large chaetognaths increased little in length from October to March and disappeared from the collections in April. The length– frequency distributions of intermediate cohorts E2 and E3 shifted to larger length quasi-monotonically through- − out the annual cycle from October to September. Fig. 5. Abundances (mean numbers m 2 + 1 SD) of newborn E. Cohort E2 disappeared from the collections in August. hamata and P. elegans (body lengths of 2–4 mm) in monthly Multinet – deployments from October to September. August 2007 was inserted Initially, the length frequency distribution of cohort E4 between July and September 2008 to provide a complete composite of progressed slowly to longer lengths or even regressed as the annual cycle. Number of collections shown above bars. The solid some limited numbers of newborns were added to the horizontal bar above month labels indicates sampling in the cohort starting in December. A new cohort E5 hatched Amundsen Gulf. in April (Fig. 6). Cohort E5 hardly increased in average length from April to July, as newly hatched chaetog- (Fig. 7a). Apart from this initial latency in younger ani- naths were constantly added to it, but the width of the mals, cohorts E2–E4 increased more or less regularly in adjusted Gaussian distribution increased (declining mean length from March to June. The mean length of kurtosis). all cohorts declined from January to February and this A similar pattern of annual growth was observed for decline persisted until March in cohorts E3 and E4 cohorts E1–E5 of E. hamata (Fig. 7). After a period of (Fig. 7a). latency of 3–4 months, the mean length of cohorts E4 The average lengths of cohort E4 and E5 in and E5 of newly hatched E. hamata started to increase September corresponded to the average lengths of

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Fig. 6. Monthly length–frequency distributions of E. hamata. Frequencies of newborns highlighted in orange (gray in print). Visually identified length cohorts shown as normal distributions in red (lower lines in print) with red dots indicating the mean length (gray dots in print). Each of the five cohorts is labelled with a capital E and a number from oldest (1) to youngest (5). Blue line is the total distribution obtained by summing the modelled cohort distributions (upper line in print). Chi-square values for the goodness-of-fit of the total distribution to the data are given. Sampling regions are abbreviated in each panel: PC, Parry Channel; AG, Amundsen Gulf; BB, Baffin Bay. k is the number of collections and n is the number of length measurements included (see “Method”).

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Fig. 7. (a) Monthly mean lengths (±1 SD) of the ﬁve cohorts of E. hamata in each month of the time series; (b) Monthly mean lengths (±1 SD) combined to create a possible growth trajectory for individuals that emerged in October and April, assuming a 2-year lifespan; (c) Growth-age curves of the autumn and spring broods. Circles show mean values of each characteristic (±1 SD shown as ribbons).

cohort E2 and E3 in October, respectively (Fig. 7a), For the autumn brood, growth was significantly faster in strongly suggesting the co-existence of an autumn brood the second year of life than in the first (ANCOVA, (October) and a spring brood (April) of E. hamata. P < 0.01). In the spring brood, growth rates were not Connecting the corresponding cohorts created a com- significantly different between Years 1 and 2 (ANCOVA, posite of the growth trajectory of the assumed autumn P > 0.05). Summer Eukrohnia hamata residents of epipela- and spring broods (Fig. 7b). In all months, the standard gic depths (Amundsen Gulf) were mostly second-year deviations around average lengths of the presumed members of the autumn brood and first-year members of autumn and spring broods were distinct. The E1 cohort the spring brood (Fig. 8). of large chaetognaths likely represented the final months The autumn and spring broods of E. hamata matured of life of the spring brood (Fig. 7b). If the above inter- in different seasons (Table I) but at similar body lengths pretations are correct, the growth trajectory of the (Fig. 9). In the autumn brood, all variables peaked in autumn brood terminated after 22 months with the dis- the second year of life (16 to 23 months of age) from the appearance of cohort E2 from the collections, while that winter (January–March) to July (Table I). Maturity was of the spring brood indicated a slightly longer life cycle somewhat less protracted in the spring brood, with of 2 years (24 months). Mean length at a given age did ovary length, width of seminal vesicles and diameter of not differ significantly (t-test, t = 43 df = −0.36, P = the protruding seminal receptacles first peaking in 0.72) between the autumn and spring broods (Fig. 7c). August of the second year of life at 17 months of age

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− Fig. 8. Abundances (ind. m 3)ofE. hamata age classes in discrete depth layers of the Amundsen Gulf, characterized by their mid-points (black squares). Top panels: autumn brood individuals. Bottom panels: spring brood individuals. Seabed shown in brown, unsampled sections of the water column in grey. See “Method” for further details.

Table I: Timing of peak development of maturity features in the autumn and spring broods of E. hamata and summer brood of P. elegans, and of the oil vacuole in E. hamata. Ages in months at peak development are given in parentheses. Monthly collections consisted of up to 397 and 434 E. hamata individuals from its autumn and spring broods, respectively, and 177 P. elegans

Month(s) of peak maturity (age in months) Characteristic E. hamata autumn brood E. hamata spring brood P. elegans summer brood

Number of oocytes Jan–Jul (16–23) Mar (24) Feb (20) Length of ovaries Mar–Jul (18–23) Aug (17), Jan (22) Jan–Aug (19–26) Area of oil vacuole Mar–Jul (18–23) Dec–Jan (21–22) Fraction of inds. with dispersed sperm Mar–Jul (18–23) Nov (20) Feb–Mar (20–21), Aug (26) Width of seminal vesicles Feb–Jul (17–23) Aug (17), Feb (23) Aug (14), Aug (26) Diameter of protruding seminal receptacles Mar–Jul (18–23) Aug (17), Feb (23) Jan (19)

(Table I). Maturity indices and oil vacuole area peaked systematically around the 21th month of life (Fig. 9d). at different times from November (age 20 months) to Seminal vesicle width, and sperm receptacle diameter March (age 24 months). In both broods, oocyte number, began to develop by the 21th month of life as well ovary length and oil vacuole area started to increase by (Fig. 9e and f). the end of the ﬁrst year of life (Fig. 9a–c). Some chae- A vacuole was observed in 99% of E. hamata (n = tognaths had dispersed sperm in the tail during their 2089), the exception being in newborns 2–3 mm long ﬁrst year, but sperm frequency started to increase from the spring brood. Overall, oil reserves were

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Fig. 9. Development of sexual features (a, oocyte number; b, ovary length; d, sperm load; e, seminal vesicle width; f, seminal receptacle diameter) and oil vacuole area (c) with length for the autumn and spring broods of E. hamata. Circles show mean values of each characteristic (±1SD shown as ribbons). Vertical line indicates average length (15.4 mm) at 1 year of age. Maturity results were obtained from the analyses of up to 283 individuals from each 1 mm length class in each brood.

observed in the vacuole and/or the digestive tract of Parasagitta elegans length cohorts and life 72% of the E. hamata examined. The fraction of the cycle population with oil reserves in the vacuole or the body Two cohorts were distinguished in all months except cavity peaked in February (85%), declined slowly from August 2007 and July 2008, when there were three February to April, then faster to a minimum in June (Fig. 11). The cohort of largest/oldest chaetognaths (54%) before peaking again in September (Fig. 10). Low was labelled P1 (Parasagitta 1), the intermediate-sized percentages were observed in October (72%) and cohort P2, and the cohort of summer (July) newborns December (51%).

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nearly 100% of individuals >35 mm (Fig. 14c). Seminal vesicles and receptacles started to develop around 17 mm in length (Fig. 14dande).

DISCUSSION Chaetognath brood interpretation and lifespans Fig. 10. Monthly fraction of the E. hamata population (mean % ± 1 SD) presenting oil reserves in the vacuole and/or the digestive tract Terazaki and Miller (1986) reported three separate by months. Number of water column collections shown inside each broods of E. hamata (spring, summer and autumn) in the bar (33–446 individuals per haul). North Pacific with lifespans of 8–10 months. Two-year lifespans were suggested based on the existence of two distinct size cohorts in summer in northern Norway P3. Cohort P1 (monthly mean lengths >32 mm) disap- (Sands, 1980), and Baffin Bay (Sameoto, 1987). In the peared from the collections by September. The length present study, E. hamata autumn and spring broods distribution of P2 (monthly mean lengths = 21–33 mm) (staggered by 6 months) also had lifespans of 2 years. shifted to larger sizes from July to September and then In the Japanese South Pacific, P. elegans had lifespans of remained constant until April. That of P3 (monthly 10–12 months (Terazaki, 1993). Lifespans in Arctic waters mean lengths = 5–19 mm) increased from July to ranged from 1 year in a land-locked fjord (McLaren, 1961) November, remained constant or shifted to smaller to 3 years in the Barents Sea (Falkenhaug, 1993)and sizes from December to April, and then increased Svalbard (Grigor et al., 2014). Two-year lifespans were sug- again starting in May (Fig. 11). Growth trajectories of gested in Disko Bay (Dunbar, 1940) and Lancaster Sound the inferred cohorts of P. elegans indicated relatively fast (Welch et al.,1996). In this study, a single annual summer– growth from April to September/October followed by autumn brood of P. elegans had2-yearlifecyclesinthe stagnation over the winter months and even a slight Amundsen Gulf, Parry Channel and Baffin Bay. The cap- regression in length from January to April (Fig. 12a). ture of several individuals up to 45 mm long in the pro- A decrease in the length of cohort P3 in December ductive shallow waters of Nachvak Fjord during 2007 may not be realistic, because P. elegans reproduced in could indicate a slightly longer lifespan there, and pos- December (Fig. 5). However, any winter cohort pro- sibly complicates using these data to fill in gaps in the duced was not detected in the size–frequency distribu- main Amundsen Gulf time series. Longer lifespans in tions from subsequent months (Fig. 11). In June, the fjords could be due to lower growth rates, genetic dif- body lengths of P1 and P2 were similar to those of P2 ferences or differences in feeding strategies (Pearre, andP3,respectively,inJuly(Fig.12a), which suggests 1991; Øresland, 1995). that the three cohorts represent three separate age classes of a summer–autumn brood. If this is the case, the growth trajectory of the summer–autumn brood terminated after 25 months with the disappearance of Resource partitioning in the sympatric cohort P1 from the collections (Fig. 12b). First- and E. hamata and P. elegans second-year P. elegans displayed similar seasonal vertical In arctic seas where many planktonic species depend on a distribution patterns in the Amundsen Gulf (Fig. 13). single brief annual bout of primary production in sum- In P. elegans, oocyte number, ovary length, the occur- mer, morphologically similar species can co-occur thanks rence of dispersed sperm, and seminal receptacle diam- to subtle differences in the ecological niches occupied. For eter first peaked in January or February at ages 19 or instance, in the Beaufort Sea the morphologically identical 20 months (Table I). Occurrence of sperm peaked larvae and juveniles of polar cod (Boreogadus saida)andice again in August (26 months). The width of seminal cod (Arctogadus glacialis) share the same spatio-temporal dis- vesicles reached a maximum in August early in the tribution, hatching season and growth rate, but a slightly second year of life (14 months) and again in August at larger size at hatch results in A. glacialis being longer and 26 months of age (Table I). As P. elegans increased in feeding on different prey at a given date than B. saida length, the presence of oocytes and perceptible ovaries (Bouchard et al.,2016). Additionally, the herbivorous cala- were the first sign of maturation, both indices starting noid copepod Calanus glacialis is morphologically almost to increase at 7 mm (Fig. 14a and b). Dispersed sperm identical to its sympatric congener C. hyperboreus except for was first detected around 8 mm and was present in a smaller size starting at the copepodite IV developmental

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Fig. 11. Monthly length–frequency distributions of P. elegans. Frequencies of newborns highlighted in orange (gray in print). Visually identified length cohorts shown as normal distributions in red (lower lines in print) with red dots indicating the mean length (gray dots in print). Each of the three cohorts is labelled with a capital P and a number from oldest (1) to youngest (3). Blue line is the total distribution obtained by summing the modelled cohort distributions (upper line in print). Chi-square values for the goodness-of-fit of the total distribution to the data are given. Sampling regions are abbreviated in each panel: NF, Nachvak Fjord; PC, Parry Channel; AG, Amundsen Gulf; BB, Baffin Bay. k is the number of collections and n is the number of length measurements included (see “Method”).

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Fig. 12. Monthly mean lengths (±1 SD) of the three cohorts of P. elegans (a) in each month of the time series; and (b) combined to create a possible growth trajectory for individuals that hatched in July, assuming a 25-month lifespan.

− Fig. 13. Abundances (ind. m 3)ofP. elegans age classes in discrete depth layers of the Amundsen Gulf, characterized by their mid-points (black squares). Seabed shown in brown, unsampled sections of the water column in grey. See “Method” for further details.

stage. Within their sympatric distribution, C. glacialis is elegans also partition resources in arctic seas. The popula- preferentially distributed over the shelf while C. hyperboreus tion of E. hamata generally showed a more pelagic distribu- concentrates over the slope and deeper basin (Darnis tion relative to the typically neritic P. elegans (Fig. 3), as et al.,2008and references therein). The two species also reported in previous studies (Hopcroft et al., 2005; differ in their vertical distribution and ontogenetic migra- Kosobokova and Hopcroft, 2009). Darnis et al. (2008) iden- tion (Darnis and Fortier, 2014). tiﬁed three zooplankton assemblages in the southeastern Our results support the notion that the morphologic- Beaufort Sea: the Shelf (43–182 m depth range), Polynya ally similar and sympatric chaetognaths E. hamata and P. (250–537 m) and Slope (435–1080 m) assemblages. For

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Fig. 14. Development of sexual features (a, oocyte number; b, ovary length; c, sperm load; d, seminal vesicle width; e, seminal receptacle diameter) with length in P. elegans. Circles show mean values of each characteristic (±1 SD shown as ribbons). Vertical line indicates average length (20.7 mm) at 1 year of age. Maturity results were obtained from the analyses of up to 63 individuals from each 1 mm length class.

most of the year, E. hamata associated with the Polynya when both chaetognath species associated with the assemblage, which is dominated by C. hyperboreus and the Polynya assemblage. The above observations strongly sug- Slope assemblage where omnivores and carnivores are gest SVM in both species. Furthermore, they suggest that abundant (Darnis et al., 2008). It is important to note that inter-speciﬁc competition for food can be reduced for the deepest Amundsen Gulf stations (>400 m) were not much of the year via differences in vertical distribution. sampled in January and February. Since E. hamata lives Sampling chaetognaths mostly during the day (71% of deeper in the water column, this species may have been hauls, Supplementary Table 1) reduced the possibility of under-represented in our winter samples, reducing sample diel vertical migration (DVM) distorting the reported size. In summer, however, the E. hamata population was SVM patterns. somewhat associated with the Shelf assemblage which is The two chaetognath species tended to produce off- strongly dominated by the neritic copepods Pseudocalanus spring in opposite seasons; E. hamata mainly from spp. (Darnis et al.,2008). Parasagitta elegans preferentially February to July with a second brood in the autumn associated with the Shelf assemblage, except in winter, (October, December); and P. elegans from July to

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February (Fig. 5). Consistent with our observations, E. the protandric nature of the species (Terazaki and hamata reproduced mostly in spring and summer in the Miller, 1982). All other maturation traits and the oil waters off west Greenland and northern Norway, with vacuole developed in the second year of life. In the reports of continuous low reproduction rates during North Pacific, only 3 days separated egg release from autumn and winter in west Greenland and Gerlache the appearance of juveniles (Kotori, 1975). Accordingly, Strait, Antarctica (Kramp, 1939; Sands, 1980; the successive maturation episodes in autumn and spring Øresland, 1995). In the Amundsen Gulf, E. hamata off- (Table I) coincided with the occurrence of juvenile E. spring typically emerged from brood sacs in the PH and hamata in net collections (Fig. 7b). These two maturation AL (Fig. 8), where temperatures were relatively constant cycles at 6-month intervals could be interpreted as a (≤0°C). Emergence at meso-pelagic levels suggests that sign of iteroparity but actually reflect the asynchronous E. hamata may feed on sinking particles, protozoans and maturation of the two broods, which supports the sug- copepod nauplii present at depth (Makabe et al., 2016). gestion that E. hamata is semelparous and dies after a In a study running parallel to this one in the Amundsen single reproduction effort in the second year of life Gulf, gut content observations (unpublished results) sug- (Kuhl, 1938). gested that marine snow was consumed by juveniles and Maturity depends on factors such as temperature, adults of E. hamata during all seasons, but especially dur- and quantity and size of prey (Dickey-Collas et al., ing the spring–summer algae blooms. 1996). Dunbar (1940) and Grigor et al. (2014) suggested Summer-fall reproduction in P. elegans agrees with an age-at-maturity of 1 year for P. elegans in the previous observations in Arctic waters (Kramp, 1939; Canadian and European Arctic. Consistent with this, Dunbar, 1940; McLaren, 1961; Sameoto, 1971; Grigor first-year P. elegans (3–20 mm) could not reproduce as et al., 2014). Offspring typically hatched in the PML of they lacked seminal receptacles and vesicles. However, the Amundsen Gulf (Fig. 13) where temperatures oocyte numbers and the occurrence of dispersed reached >9°C and primary production occurred. sperm started to increase at 9–12 mm corresponding Newborns hatching at greater depths in December did to an age of ca. 6 months (Table I and Fig. 14). not appear to persist within the population (Figs 5 and Contrary to E. hamata, sexual maturation in P. elegans 13). Admittedly, cohort interpretation for this species occurred from January to August, several months could also have been hampered by relatively low sample prior to the emergence of its annual brood from July sizes. A breeding season from July to February in the to early winter. Canadian sub-Arctic led Dunbar (1962) to propose that the breeding season in P. elegans is determined by temperature rather than food availability. However, the hatching of eggs in the surface layer of the Amundsen The potential role of lipid reserves: Gulf from July to January matches the emergence of the contrasting growth and reproduction nauplii and CI of the copepods Pseudocalanus spp. and in the two species Oithona similis (Darnis and Fortier, 2014) for the entirety Sullivan (1980) suggested that E. hamata requires less of the hatching period. These suitably sized prey (Saito prey than P. elegans in the Pacific Ocean, and Antarctic and Kiørboe, 2001) are major food sources for first- studies showed the same trend when E. hamata was com- feeding P. elegans (McLaren, 1969). Another report from pared with other sagittid chaetognaths (Froneman and the same location (Darnis and Fortier, 2014), suggested Pakhomov, 1998; Giesecke and Gonzalez, 2012). In E. that Pseudocalanus spp. resided deeper than P. elegans in hamata, a large fraction (72%) of total lipids are in the December 2007, which may have contributed to the form of long-term energy storage; steryl and wax esters mortality of winter offspring. Marine snow did not (Connelly et al., 2012). Despite the relatively small size appear to be a major food source for P. elegans indivi- of its oil vacuole, lipid enclosed within could have roles duals in the Canadian Arctic (unpublished results). in growth, reproduction and/or buoyancy (Kruse et al., We suggest that the generally asynchronous depth 2010; Pond, 2012; Grigor et al., 2015). By comparison, distributions, maturation and reproduction (and possibly lipids in P. elegans contain low amounts of wax and steryl food) of E. hamata and P. elegans may reduce potential esters (<1–8% of total lipids), and low to moderate competition during the early life of arctic chaetognaths. amounts of shorter-term lipid stores, such as triacylgly- cerols (Falk-Petersen et al., 1987; Lee et al., 2006; Connelly et al., 2012, 2016). Lipids in P. elegans, gained Maturation by feeding on copepods during spring–summer feeding, Dispersed sperm in the tail, early in the first year of life, may be rapidly utilized for reproduction (Choe et al., was the first sign of maturation in E. hamata, confirming 2003).

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Some studies have reported reduced growth in winter documented in several arctic zooplankton taxa (e.g. in arctic and subarctic chaetognaths (Dunbar, 1962; Kattner et al., 2007 for a review). Arctic cod (B. saida), a Grigor et al., 2014), and others have not (Welch et al., pivotal forage fish in the arctic pelagic food web, also 1996). Slow winter growth has been attributed to poor spawn in winter with the buoyant eggs hatching in the feeding as indicated by gut content analyses (Øresland, surface layer before the onset of the spring–summer pri- 1990; Falkenhaug, 1991; Grigor et al., 2015). With the mary production (Bouchard and Fortier, 2011). In the return of seasonally migrating copepods to epipelagic present study, E. hamata relied on wax ester reserves to waters as early as February (Darnis and Fortier, 2014), fuel reproduction. But contrary to other arctic capital an important food source for meso-pelagic chaetognaths breeders such as C. hyperboreus and B. saida that produce can become depleted and results in length losses. In the a single spring brood, E. hamata produced distinct present study, the annual growth pattern differed broods in the autumn and the spring. The comparison between the two species. In E. hamata growth was vari- of growth trajectories and maturity at length shows a able but positive over 10 months from March to similar developmental rate in the two broods, which − January (1.6 mm mo 1 on average for both the autumn suggests that E. hamata is not affected by differences in and spring broods), followed by a 1 to 2-month period temperature regime or food availability between the two of negative growth in late winter (January to February/ seasons. The distribution of E. hamata in the meso- March, Fig. 7b). In P. elegans, fast growth from April to pelagic layer where temperature is constant and where − September/November (2.4 mm mo 1 in Year 1 and 3.2 copepod prey resides for most of the year (Darnis and − mm mo 1 in Year 2 of life), was followed by a long peri- Fortier, 2014) may explain the parallel existence of two od of winter stagnation from September/November to sub-populations that hatch, develop and reproduce April (Fig. 12b). separated by a 6-month time-lag. Growth and morphology of E. hamata suggest that The alternative strategy to capital breeding is income long-term energy stores play a role in enabling this spe- breeding in which reproduction is fuelled by immediate cies to limit periods of starvation. Contradicting this, food availability in spring–summer. In contrast to E. however, the frequency of E. hamata with oil reserves hamata, P. elegans produced a single brood in summer, peaked from January to March during the months of typical of an income breeder. This strategy, which length decreases, and started to decline in April–May increases in the frequency of its occurrence towards low- (Fig. 10) coinciding with peak reproduction in April er latitudes (Kattner et al., 2007), is also used for instance (Fig. 5). The rebuilding oil reserve frequency from June by the Pacific sand lance (Ammodytes hexapterus) a recent to September was followed by drops in frequency in subarctic invader of the Beaufort Sea (Falardeau et al., October and then December (Fig. 10), which both coin- 2014). The end result of the remarkably different repro- cided with short bouts of reproduction (Fig. 5). The duction strategies of the two species is the staggering of observed negative correlation between oil reserve fre- three distinct broods of morphologically and ecologically quency in the population and offspring production is similar chaetognaths: the E. hamata spring cohort in consistent with the suggestion by Båmstedt (1978) that April, the P. elegans summer cohort in July, and the E. part of the lipid content of large specimens of E. hamata hamata autumn cohort in October. The early accumula- is drawn upon during reproduction, thus lowering the tion of lipids in the oil vacuole may also assist young E. average individual lipid proportion in the population. hamata at meso-pelagic depths in overcoming potential We therefore conclude that E. hamata invests its lipid food shortages in autumn and spring, while the only sur- reserves primarily into reproduction rather than growth, vival window for the lipid-poor P. elegans would be dur- which may contribute to a loss of length in February ing peak availability of prey in the surface layer in and March when prey is likely scarce in deep waters. summer. For P. elegans, migrating to depths where copepods over- winter did not appear to improve its growth rates, suggesting a resting strategy, rather than a feeding one, for CONCLUSIONS this chaetognath in mid-winter. Based on our observations from August 2007 to September 2008 in the Canadian Arctic, it appears that Capital breeding versus income breeding the processes of growth and reproduction are more sea- Capital breeding based on wax esters accumulated in sonally restricted in P. elegans compared to E. hamata. summer to fuel reproduction in winter so as to match Length and maturity data for the two species from other the emergence of offspring with the spring–summer years would help to confirm if this is a general trend. As maximum in biological production has been the Arctic warms and the ice-free season lengthens,

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