Small copepods matter: population dynamics of Microsetella norvegica in a high-latitude coastal ecosystem

Small copepods matter: population dynamics of Microsetella norvegica in a high-latitude coastal... Abstract We investigated the population dynamics of a small and little-studied harpacticoid copepod, Microsetella norvegica, in a sub-Arctic Norwegian fjord (Balsfjord 69°N). We sampled with a 90 μm mesh WP-2 net and a 20 L Go-Flo bottle and found that the WP-2 under-sampled all juvenile stages. The abundance and biomass were high, peaking in June with 9349 × 103 ind. m−2 and 1678 mg C m−2. Microsetella were most abundant in the surface, but females and males demonstrated a distinct migration to below 50 m from October to March. Consistently, individual female body carbon content was highest in October (0.39 μg C ind−1) and lowest in March (0.18 μg C ind−1). Males were present throughout the year, and females with eggs were found from April to September. The average clutch size was 11 ± 2 eggs female−1, and our study supports the observation that females can release their egg sac before the eggs have hatched, possibly to produce a new one. With its high abundance and biomass, a flexible reproductive strategy and specialized feeding preferences, M. norvegica is likely a key species in high-latitude coastal ecosystems. INTRODUCTION Most harpacticoid copepods are benthic, inhabiting all types of surfaces and sediments at all depths (Azovsky et al., 2016). The majority are substrate-bound (Dahms and Qian, 2004), and common habitats are seagrass blade surfaces and on or within bottom sediments (Bell et al., 1987). However, one harpacticoid species, Microsetella norvegica, appears especially adapted to a pelagic lifestyle. It is frequently associated with aggregates and marine snow (Kiørboe, 2000; Koski et al., 2005, 2007), and it has been suggested to be important for regulating the downward flux of carbon in coastal ecosystems (Green and Dagg, 1997; Koski et al., 2005, 2007). Microsetella norvegica is reported as highly abundant in temperate (Uye et al., 2002) as well as sub-Arctic (Arendt et al., 2013) seas, and may even be the numerically dominant copepod species in the mesozooplankton community (Dugas and Koslow, 1984; Arendt et al., 2013). Although M. norvegica has received increased attention during recent decades (Diaz and Evans, 1983; Uye et al., 2002; Turner, 2004; Arendt et al., 2013; Koski et al., 2014), knowledge of its biology and ecology is still rudimentary compared to that for calanoid copepod species. One likely reason is that M. norvegica is not efficiently sampled with standard plankton nets (e.g. mesh size 180 μm) due to its tiny size (<550 μm total length) and slender bodies. On the other hand, M. norvegica is often recorded in fish stomachs (Demchuk et al., 2015; Falkenhaug and Dalpadado, 2014), pointing to their wide distribution and importance as prey for fish in coastal ecosystems. Balsfjord (69°N) is a high-latitude, cold-water fjord with Arctic characteristics regarding irradiance and seasonality in primary production (Eilertsen and Taasen, 1984). The fjord is semi-enclosed and advection is reduced due to an entrance sill at 30 m depth, making it well suited for studies of zooplankton population dynamics. Previous studies have concluded that Calanus finmarchicus is the dominant zooplankton species in Balsfjord (Tande, 1982). However, other investigations, sampling zooplankton with Niskin water bottles (Pasternak et al., 2000) or plankton nets with 64 μm mesh size (Davis, 1976), reported high-relative abundance of M. norvegica during all seasons, although quantitative abundances were not presented. There are presently few quantitative studies focusing on M. norvegica seasonal abundance in high-latitude ecosystems, and therefore its population dynamics are not well known in these areas. For instance, aspects of its reproductive strategy, such as the timing and extent of the reproductive period, clutch size and the seasonal variation in ratio of males to females have not been fully described for high latitudes. Furthermore, many small copepods are winter-active in the surface at high latitudes (Madsen et al., 2008; Møller et al., 2006), but the over-wintering strategy for M. norvegica is not well known. We investigated the population dynamics of M. norvegica in Balsfjord through monthly sampling from June 2013 to June 2014. Our main objectives were to (i) study seasonal patterns of developmental stage composition, abundance, biomass and vertical distribution and (ii) determine the timing of reproduction of M. norvegica. In addition, we evaluated sampling efficiency for the different developmental stages of M. norvegica by comparing abundances obtained with a WP-2 net (90 μm mesh) with those obtained with a 20 L Go-Flo bottle. METHOD Study site and sampling The study was conducted at station Svartnes in Balsfjord (Fig. 1), northern Norway (69°22’N, 19°06’E). The fjord is 5 km at its widest, 46 km long. A shallow sill at the mouth (30 m depth) separates the fjord from coastal water to seaward (Reigstad, 2000; Wexels Riser et al., 2010). Balsfjord has two basins. The outermost is 130 m deep, and the innermost, where station Svartnes is located, is 185 m deep. The sun passes below the horizon between 26 November and 18 January (polar night), and stays above the horizon between 28 May and 19 July (midnight sun). Stratification of the water column generally starts in May and lasts until September (Eilertsen and Taasen, 1984). Vertical profiles of salinity, temperature, density and fluorescence were obtained for each sampling date using a CTD profiler (Seabird model 25 Sealogger) from the surface to 175 m (station depth was 180 m). Station Svartnes is part of a large hydrographic monitoring program (https://dataverse.no/dataverse/nmdc), and our monthly sampling results were supplemented with additional hydrographic data from the monitoring program. Fluoresence data from June 2014 are missing due to malfunction of the fluoresence sensor. Fig. 1. View largeDownload slide Map of the Tromsø area, showing the location of sampling station Svartnes in Balsfjord, northern Norway. Fig. 1. View largeDownload slide Map of the Tromsø area, showing the location of sampling station Svartnes in Balsfjord, northern Norway. Microsetella norvegica Monthly sampling was conducted during daytime from June 2013 to June 2014 from R/V “Hyas.” We aimed at collecting all developmental stages of M. norvegica, from nauplii to adult copepodites, and therefore sampled with both a WP-2 net (Hydro-Bios, 90 μm mesh size) and a 20 L Go-Flo bottle (General Oceanics). The WP-2 net was equipped with a filtering cod end and a closing mechanism to allow discrete sampling from 175 to 50 m and 50 to 0 m depth ranges. The contents of the cod end were concentrated with a 90 μm mesh sieve. Due to the small mesh size of the WP-2 net, the towing speed was slow, 0.2–0.3 m/s. The filtration volume was calculated from wire length, and no visual indications of clogging were observed. The Go-Flo bottle collected water at 5, 20 and 50 m depth, and its contents were concentrated with a 20 μm mesh sieve. All zooplankton samples were preserved with buffered formaldehyde at 4% final concentration. Individuals of M. norvegica were counted and identified using a stereo microscope (Leica MZ16) at 40–100× magnification. Developmental stages were identified according to Hirakawa (1974) and Huys and Boxshall (1991). Due to their small size, M. norvegica nauplii were not identified to stage but counted as one group. Copepodite stages CIV and CV were not separated due to their morphological similarity and are reported as M. norvegica CIV–CV. Other stages were enumerated separately. Females carrying an egg sac and detached egg sacs in the sample were also enumerated. From each subsample, a minimum of 300 individuals were counted. Subsample volumes ranged from 7 to 100% of the entire sample. A total of 65 samples were analysed in this study. To obtain comparative estimates of the WP-2 and Go-Flo sampling efficiency in the surface layer, the Go-Flo samples were integrated from 0 to 50 m depth, assuming the sample depths represented the midpoint in each interval. Carbon and nitrogen contents of M. norvegica females were determined in October, January, March and May to cover the seasonal variations in body condition. For these analyses, additional samples were collected with the WP-2 net and live animals were transported to the laboratory where 600 females without egg sacs were sorted out. The females were rinsed in filtered seawater and duplicates of 300 animals from each sampling date were gently dropped onto combusted GF/F filters and stored frozen (−20°C) until analysis. The organic carbon and organic nitrogen contents of females were determined with a CHN Lab-Leeman 440 elemental analyser. Results for blank filters without copepods were subtracted from those for filters containing M. norvegica. To obtain a length–carbon relationship, the body lengths of 50 M. norvegica females from the same sample were measured using a stereo microscope (Zeiss Discovery V20). To achieve population biomass of M. norvegica, the carbon contents of all copepodite stages were estimated from an empirical length–carbon correlation (Uye et al., 2002),   C=2.65×10−6×BL1.95, (1)where C is the carbon content (μg) and BL the total body length (μm). Body lengths of at least 10 individuals of each developmental stage were measured for selected samples to cover the full seasonal cycle. Average body lengths of all six naupliar stages were obtained from measurements of totally 55 nauplii of different stages (from June only) and applied to equation (1). The length and width of 30 egg sacs were measured and the sac volume was calculated assuming cylindrical shape. All 30 egg sacs were dissected and the individual eggs were counted, the diameter was measured and the volume of individual eggs was calculated (as the volume of a sphere). Statistical analyses Differences in sampling efficiency between the WP-2 net and Go-Flo bottle for the different developmental stages were tested for statistical significance by applying a nonparametric Mann–Whitney U-test for independent samples (IBM SPSS statistics version 24). Due to the seasonal, and hence uneven, occurrence of the younger developmental stages, including nauplii, CI, CII and CIII (Table I), these were merged and tested as one group. Table I: Integrated (0–50 m) abundance (103 ind. m−2) of M. norvegica developmental stages obtained with Go-Flo bottle (G) and WP-2 (W)   Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093    Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093  Data are presented for each sampling date, and the mean of all samplings is provided. A statistically significant difference between abundances obtained with Go-Flo and WP-2 is indicated by a * (P < 0.05). No statistically significant difference between samplers is indicated by “ns.” Table I: Integrated (0–50 m) abundance (103 ind. m−2) of M. norvegica developmental stages obtained with Go-Flo bottle (G) and WP-2 (W)   Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093    Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093  Data are presented for each sampling date, and the mean of all samplings is provided. A statistically significant difference between abundances obtained with Go-Flo and WP-2 is indicated by a * (P < 0.05). No statistically significant difference between samplers is indicated by “ns.” RESULTS Hydrography The water column was stratified from late May to late November, with warm surface water (8–10°C) over colder water (2–4°C) below a thermocline at 40–80 m (Fig. 2A). A core of warm, saline (32.5 g kg−1) water was present in the surface from early June, and the water masses gradually cooled from September. During winter, from January to April, the water column was well mixed with temperatures from 2 to 4°C. Three periods with low salinity were observed: in June 2013, January 2014 and June 2014 (Fig. 2B). These events were most likely caused by snowmelt (June) and heavy snowfall (January). The fluorescence started to increase at the beginning of April, with maxima observed in June 2013 and in May–June 2014, indicating spring bloom conditions around 13 and 20 m depth, respectively (Fig. 2C). Between late October and early March, the fluorescence was below the detection limit. Fig. 2. View largeDownload slide (A) Temperature (°C), (B) salinity (g kg−1) and (C) fluorescence at station Svartnes from August 2013 to June 2014. The black vertical lines indicate dates of sampling, ND implies no data. Fig. 2. View largeDownload slide (A) Temperature (°C), (B) salinity (g kg−1) and (C) fluorescence at station Svartnes from August 2013 to June 2014. The black vertical lines indicate dates of sampling, ND implies no data. Comparison of sampling methods The M. norvegica population in Balsfjord was sampled using a WP-2 net (90 μm mesh) and a Go-Flo water bottle (volume 20 L). When averaging all stages and sampling integrated over 0–50 m, a 2.2-fold higher abundance of M. norvegica individuals was obtained with the Go-Flo bottle, than with the WP-2 net (Table I), and the difference is statistically significant (Mann–Whitney U-test, P = 0.024). The discrepancy between the two sampling methods was statistically significant for the group of nauplii plus young copepodites CI–CIII (P = 0.023) and for CIV–CV (P = 0.017). Females and males were sampled generally equally well with the Go-Flo and WP-2 (P > 0.5). When presenting data on M. norvegica population dynamics, we will use the data obtained with the Go-Flo bottle integrated from 50 to 0 m depth, while the data obtained by WP-2 will be used to evaluate the seasonal shifts in vertical distribution of females and males. Body lengths and female carbon and nitrogen weight The body length of all developmental stages varied seasonally and peaked in June (Fig. 3). Females had the largest body size, followed by males. The range in C and N contents for individual females throughout the sampling period was 0.18–0.39 μg C ind−1 and 0.03–0.05 μg N ind−1 (Table II). The individual carbon weight (mean ± standard deviation) was highest in October (0.39 ± 0.01 μg C ind−1) and lowest in March (0.18 ± 0.04 μg C ind−1), while the N content varied little between the sampled months (Table II). The C:N ratio of females ranged from 11.2 ± 0.5 in October to 6.0 ± 0.3 in May. Fig. 3. View largeDownload slide Microsetella norvegica seasonal body length (mean ± SD). Fig. 3. View largeDownload slide Microsetella norvegica seasonal body length (mean ± SD). Table II: Body length (μm) of M. norvegica females in October, January, March and May   October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3    October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3  Carbon content (μg C ind−1), nitrogen content (μg N ind−1) and C/N ratio (atomic) are given as the mean ± SD (N = 2 filters, each containing 300 females). Table II: Body length (μm) of M. norvegica females in October, January, March and May   October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3    October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3  Carbon content (μg C ind−1), nitrogen content (μg N ind−1) and C/N ratio (atomic) are given as the mean ± SD (N = 2 filters, each containing 300 females). Vertical distribution Females and males were present throughout the water column year-round, but with an apparent seasonal shift (Fig. 4). From May to September, the vast majority were present in the upper 50 m, and few adults were found deeper in the water column. About half of the M. norvegica adult population were found below 50 m from October to January. The entire population was dominated by males and females in this winter period, with a modest contribution of developmental stages CIV–CV (Table I). From March onwards, the adult population abundance increased in the upper 50 m while declining below (Fig. 4). Fig. 4. View largeDownload slide Vertical distribution of the sum of M. norvegica females and males from May 2013 to June 2014 as sampled with a WP-2 net (90 μm mesh) and integrated in the surface (50–0 m) and in the deep layer (175–50 m). Data are presented in terms of abundance (103 ind. m−2). For months with more than one sampling, the mean is given. Fig. 4. View largeDownload slide Vertical distribution of the sum of M. norvegica females and males from May 2013 to June 2014 as sampled with a WP-2 net (90 μm mesh) and integrated in the surface (50–0 m) and in the deep layer (175–50 m). Data are presented in terms of abundance (103 ind. m−2). For months with more than one sampling, the mean is given. Population dynamics Microsetella norvegica was found in high abundance in the upper water column (0–50 m) of Balsfjord year-around (Fig. 5). The maximum was observed in June 2014, a total abundance of 9349 × 103 ind. m−2 (2977 × 103 copepodites and 6372 × 103 nauplii), and the minimum (418 × 103 ind. m−2) occurred in late January (Table I). A clear seasonal succession of developmental stages was observed in the upper 50 m (Fig. 5). Females, males and CIV–CV had high abundances throughout the year. Ovigerous females were only present from April to August (Fig. 5). Interestingly, detached egg sacs were found over a longer time-period, from April to October (Fig. 5). Nauplii were present simultaneously with ovigerous females (Table II, Fig. 5). Copepodite stages CI–CIII were present from May to September with maximum observed abundances in June. Fig. 5. View largeDownload slide Integrated (0–50 m) abundance (ind m−2) of M. norvegica developmental stages sampled with Go-Flo from May 2013 to June 2014. Note the logarithmicy-axes. Fig. 5. View largeDownload slide Integrated (0–50 m) abundance (ind m−2) of M. norvegica developmental stages sampled with Go-Flo from May 2013 to June 2014. Note the logarithmicy-axes. The integrated population biomass of M. norvegica in the upper 50 m was below 400 mg C m−2 in winter (November to mid-March), and building up from early spring (March) to summer (Fig. 6). The highest observed biomass, 1.7 g C m−2, was found in June 2014 (Fig. 6). Males and females made up the largest contribution to biomass, except for June when smaller stages also contributed significantly. Fig. 6. View largeDownload slide Integrated (0–50 m) biomass (mg C m−2) and relative stage composition (% contribution) of M. norvegica sampled with Go-Flo from May 2013 to June 2014. ND implies no data, for months with more than one sampling, the mean is given. Fig. 6. View largeDownload slide Integrated (0–50 m) biomass (mg C m−2) and relative stage composition (% contribution) of M. norvegica sampled with Go-Flo from May 2013 to June 2014. ND implies no data, for months with more than one sampling, the mean is given. Microsetella norvegica fecundity Males and females were present during all months investigated (Table III). The sex ratios were skewed toward females from March to June, and strongly skewed toward males in November and January (no data are available for December). In the remaining months, the sex ratios were close to 1. Females with egg sacs were present from April to August, and the total number of egg sacs (sum of egg sacs attached to females and detached egg sacs in the sample) was highest in June. The fraction of detached egg sacs ranged from 36% to 100% of the total number of egg sacs recorded (Table III). The total egg sacs:females ratios were in general below 1, although as high as 1.6 in May (Table III). The egg sacs:females ratios were also slightly higher than 1 in April (Table III). No relationship was found between female body length and the number of eggs in the attached egg sacs (regression R2 = 0.000005, P = 0.99, n = 30), but there was a significant positive correlation between female body length and egg sac volume (R2 = 0.47, P < 0.0001) and between clutch size and the average volume of a single egg (R2 = 0.15, P = 0.03) (data not shown). The number of eggs in an egg sac ranged from 6 to 13, with a mean ± SD of 11 ± 2 eggs (Table IV). Nauplii were present in the period from April to August, with a peak of 6 372 000 nauplii m−2 in June 2014 (Table I). This corresponds to a mean concentration of 127 440 nauplii m−3 in the upper 50 m, or about 130 nauplii L−1. Table III: Integrated (0–50 m) seasonal abundance of (103 ind m−2) of M. norvegica females (#F), females to males (F:M), egg sacs (#ES total, i.e. the sum of detached egg sacs and egg sacs attached to females), percentage detached egg sacs (%ES detached) and the ratio of total (attached and detached) egg sacs to total females (ES:F) for each sampling date Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  All data were obtained from samples collected with the Go-Flo. Temperature (°C) is presented as average for the 0–50 depth interval. Table III: Integrated (0–50 m) seasonal abundance of (103 ind m−2) of M. norvegica females (#F), females to males (F:M), egg sacs (#ES total, i.e. the sum of detached egg sacs and egg sacs attached to females), percentage detached egg sacs (%ES detached) and the ratio of total (attached and detached) egg sacs to total females (ES:F) for each sampling date Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  All data were obtained from samples collected with the Go-Flo. Temperature (°C) is presented as average for the 0–50 depth interval. Table IV: Microsetella norvegica mean ± SD body length (N = 30), number of eggs per egg sac (N = 30), egg volume (N = 150) and egg sac volume (N = 30) in June 2014 Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  Table IV: Microsetella norvegica mean ± SD body length (N = 30), number of eggs per egg sac (N = 30), egg volume (N = 150) and egg sac volume (N = 30) in June 2014 Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  DISCUSSION For a species, Gaston (2008) argues that “it is rare to be common” and that “common species are typically both abundant and widespread.” There are only a few previous observations of M. norvegica in high-latitude Norwegian fjords, and an earlier study explicitly stated that this species is rare in Balsfjord (Hopkins, 1981). In strong contrast, we found high abundances of M. norvegica throughout the year, with a population peak exceeding 9 000 000 ind. m−2 in the upper 50 m in June 2014. This is among the highest abundances ever reported for this species, and the first quantitative estimate including all copepodite stages and nauplii of M. norvegica at similarly high latitudes (69°N). Microsetella norvegica—abundant and widespread? Due to its small body size, M. norvegica is not efficiently caught by a WP-2 net with 180 μm mesh, which is a widely used zooplankton sampler. By now, it is a well-known fact that copepods with body lengths shorter than 800 μm are significantly underestimated when sampled with 180–200 μm mesh (Gallienne and Robins, 2001), and a mesh size of 80 μm has been suggested as suitable for sampling small copepods in the marine environment (Riccardi, 2010). However, we found that all copepodite stages of M. norvegica, except females and males, were under-sampled with a 90 μm mesh compared to the Go-Flo bottle. The high abundances of M. norvegica found in Balsfjord are likely common, as high numbers have also been reported from different geographical areas (from 45°S to 69°N), where zooplankton have been sampled with mesh sizes of 100 μm or smaller (Table V). For example, M. norvegica is abundant in the White Sea, Russia (Demchuk et al., 2015), in Godthåpsfjord, Greenland (Arendt et al., 2013), in Storfjorden, Norway (Halliday et al., 2001), on the Scotian Shelf, Canada (Dugas and Koslow, 1984), in the Central North Sea (Koski et al., 2007), in the Inland Sea of Japan (Uye et al., 2002) and on the Patagonian Shelf, Argentina (Antacli et al., 2014; Temperoni et al., 2014) (Table V). There are also a number of studies highlighting the importance of M. norvegica as prey for a variety of fish species in different habitats. For example, it was found to be the preferred prey of sprat in Hardangerfjord, Norway (Falkenhaug and Dalpadado, 2014), three-spined stickleback in the White Sea (Demchuk et al., 2015), larval jack mackerel off eastern Tasmania (Young and Davis, 1992) and for anchovies and sardines in the north-western Mediterranean Sea (Morote et al., 2010). We therefore suggest that M. norvegica is one of the supposedly rare species that is actually both abundant and widespread (sensuGaston, 2008) in fjords and coastal ecosystems at high and temperate latitudes. It is, thus, a key copepod species in these ecosystems. Table V: Maximum abundances (individuals m−3) of M. norvegica reported from different regions Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Abundances of copepodites (C) and nauplii (N) are given separately when possible; otherwise the abundances represent total abundance of individuals, as reported in the respective studies. Mesh sizes (μm) of sampling devices are provided. aSampled with water bottles, mesh size at which sample was concentrated is given. Table V: Maximum abundances (individuals m−3) of M. norvegica reported from different regions Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Abundances of copepodites (C) and nauplii (N) are given separately when possible; otherwise the abundances represent total abundance of individuals, as reported in the respective studies. Mesh sizes (μm) of sampling devices are provided. aSampled with water bottles, mesh size at which sample was concentrated is given. Population dynamics and C/N composition During winter (October to March), the population consisted mostly of adults, with a predominance of males. The over-wintering females did not carry eggs. About 50% of the adult population showed a distinct seasonal migration to below 50 m from October to March, while the other half remained in the upper water column. From this observation, it is difficult to conclude whether M. norvegica are winter-active or not, but we also measured a 53% decline in body C, a 25% reduction in body N and a decline in C/N ratio in females from October to March. This probably reflects low energy intake during winter, which is comparable with seasonal patterns in carbon content and C/N ratios for both the C. finmarchicus in diapause and the winter-active Metridia longa in Balsfjord (Tande, 1982; Grønvik and Hopkins, 1984). The decreasing carbon content and C/N ratio through the winter (Table II) could reflect both a shift in body composition from more carbon-rich lipids in autumn to relatively more nitrogen-rich proteins in early spring when the copepods prepare for reproduction. However, this assumption is based on speculation, as lipid accumulation in this species has not been confirmed. When comparing the measured (CHN analyzer) with the calculated (equation (1)) carbon content of M. norvegica females, the calculated values were always higher but the degree of discrepancy was variable. For instance, in October, the C content calculated from body length was 10% higher than the measured concentration, whereas in March the calculated C content was almost twice the measured concentration. This also points to a relatively large difference in body condition (e.g. lipid content), while body length was relatively stable (464 μm in October and 457 μm March). Nevertheless, it is likely that M. norvegica reduce their feeding activities during winter, although their tolerance for starvation is not known. It should also be noted that in a sub-Arctic Greenlandic fjord, M. norvegica did not display a defined time for leaving the upper 100 m (Arendt et al., 2013). In March, the majority of the males and females had ascended from the deeper layers and were found in close to equal numbers in the upper 50 m depth (female:male ratio from 0.7 to 1.3). Females with eggs first appeared in April, when the sex ratios strongly favoured females (Table III). Nauplii occurred from April to August, and copepodite stages CI–CIII were present from June to September. Body sizes of M. norvegica varied with season and all the developmental stages were largest in the warm, high production period (May–June) (Fig. 3). The decrease in body sizes observed from June to August likely results from newly moulted copepodites from the new cohort of nauplii produced in April. Based on the clearly observed distinction between the cohorts of developmental stages, we suggest that M. norvegica has a single generation per year in Balsfjord. This is in contrast to the suggested five or six generations per year in the significantly warmer (25°C in summer) central part of the Inland Sea of Japan (Uye et al., 2002). In general, males were more abundant than females from August to March, while the sex ratio was skewed toward females in April–June (no data are available for July). An adult sex ratio skewed toward males is rarely reported for pelagic copepods (Kiørboe, 2006; Hirst et al., 2010). As the availability of males to fertilize females may be a limiting factor for population growth (Kiørboe, 2007), an even sex ratio may be regarded as an advantage for the reproductive success for M. norvegica. It has been reported that for copepods lacking seminal receptacles the adult sex ratio is closer to 1:1, as repeated mating is necessary to allow continued fertilization of eggs (Kiørboe, 2006). Mironova and Pasternak (2017) recently described the occurrence of seminal receptacles in female M. norvegica. The reason for the unusual dominance of males found in this study could instead be a result of differences in gender-specific mortality due to predation or starvation. Higher mortality rates for females could have occurred, as the total abundance of females decreased from October to early March. Predatory mortality rates in copepods are related to behavioural traits, with a higher mortality rate among copepods for feeding-current grazers and cruise feeders than for ambush-feeding species, with similarly greater relative mortality for males actively searching for females (Greve et al., 2017). As the behavioural traits of male and female M. norvegica have not yet been described, it is not straight forward to conclude whether the possibly gender-specific mortality rates result from differential predation. Copepods may also display gender-specific tolerance to starvation that can partly be explained by differences in body size (Holm et al., 2018). However, for copepods such as M. norvegica where the females are larger than the males, this should result in lower starvation tolerance and greater mortality rates for males than for females. An alternative explanation for the observed sex ratios in this study is environmental sex determination. Adult sex ratios influenced by environmental parameters, such as temperature or pheromones, have been found for many Crustaceans, including copepods (Svensen and Tande, 1999). Clearly, more information is needed on the gender-specific mortality rates and sex determination mechanisms in order to explain the unusually high abundance of M. norvegica males throughout the year. Patterns of reproduction The spring bloom in Balsfjord starts in March and reaches a maximum in late April (Eilertsen et al., 1981). We anticipated that reproduction of M. norvegica would not be restricted to this short bloom period, a strategy differing from that of C. finmarchicus, which spawns during a short period of 3–4 weeks in connection to the bloom (Diel and Tande, 1992). As M. norvegica may feed on marine snow particles (Koski et al., 2005, 2007), we expected prolonged reproduction outlasting the spring bloom. Defined according to the fraction of egg-carrying females, the reproductive onset was in April, with its main reproductive period in May/June. However, females with eggs were observed until September, and detached egg sacs were recorded until November. This is in agreement with Davis (1976) and Koski et al. (2014), who reported that reproduction of M. norvegica started in April and May in the surface. In Balsfjord, Davis (1976) first observed females with eggs in late March and did not observe any carrying eggs after mid-September. Given that concurring data, we conclude that the egg production of M. norvegica is triggered by the onset of the spring bloom, but that females can continue reproducing until September. They start spawning around the same time as the broadcast-spawning C. finmarchicus, and they possibly compensate for lower production rates by prolonged spawning and egg carrying (Kiørboe and Sabatini, 1995). Egg carrying copepods produce smaller clutches than broadcast spawners (Bunker and Hirst, 2004). Egg hatching is temperature-dependent (Bunker and Hirst, 2004), and for a sac spawner the production of a new egg sac must wait until hatching of eggs from a sac already carried (Koski et al., 2014). Sac-spawning copepods are assumed to keep the egg sac until the eggs hatch. However, an unusual reproductive strategy has been suggested for M. norvegica. In a sub-Arctic fjord, Koski et al. (2014) found as many as 4.5-fold more egg sacs than females in May. They suggested that M. norvegica sheds its egg sacs before the eggs hatch, allowing each female to produce a new sac of eggs earlier. We made similar observations in Balsfjord, with 1.6 egg sacs per female in May. This finding is also supported by studies on M. norvegica gonad morphology (Diaz and Evans, 1983; Mironova and Pasternak, 2017). Diaz and Evans (1983) also observed females possessing an egg sac while simultaneously developing new eggs internally, and they suggested that M. norvegica spawns more than once, producing more offspring faster than more typical sac-spawning copepods. This may explain the apparent paradox that a slowly growing species like M. norvegica can achieve such high abundances, as already pointed out by Koski et al. (2014). Microsetella norvegica in the food web Microsetella norvegica reproduces relatively slowly but can build up dense populations in fjords and coastal ecosystems. In Balsfjord, the total M. norvegica surface biomass during spring and summer was 600–1700 mg C m−2 and they sustain a level of 200–300 mg C m−2 during winter. They are a substantial and continuously available source of energy for fish and other predators. The maximum abundance of M. norvegica in this study was 9 × 106 ind m−2, corresponding to 156 copepodites L−1 and 127 nauplii L−1. This points to their importance not only as prey but also as grazers. They are repeatedly observed in association with aggregates (Green and Dagg, 1997; Kiørboe, 2000), and the grazing rate on discarded larvacean houses was found to be 0.14 μg C ind−1 d−1 in the North Sea (Koski et al., 2007). At the abundances of M. norvegica copepodites observed in Balsfjord, their grazing impact on marine snow could be ∼350 mg C m−2 d−1 in the upper 50 m depth. In comparison, sedimentation rates in Balsfjord in June are on the order of 100–200 mg C m−2 d−1 (Reigstad and Wassmann, 1996). Microsetella are under-sampled with standard zooplankton nets, making it plausible to suggest that it is substantially more abundant than previously reported. We suggest that M. norvegica plays an essential role in the carbon cycle of fjords and coastal ecosystems, perhaps particularly so at high latitudes. CONCLUSIONS This is the first study to report high abundances of M. norvegica all through the year in a high-latitude fjord, specifically Balsfjord. We expected M. norvegica to be active through winter, but we found that about half of the adult population migrated below 50 m from October to January. Furthermore, a decline in body C:N ratios from 11.2 in October to 6.0 in May indicates low energy intake during winter. Reproduction of M. norvegica was not limited to the spring bloom period, as females with eggs were observed from April to September. Moreover, our study suggests that M. norvegica females shed their egg sacs before the contained clutches of eggs are hatched, thus allowing more rapid production of clutches. A prolonged reproductive period, combined with production of multiple egg sacs by each female, may compensate for the small clutch size of 11 ± 2 eggs female−1. So far, few studies have specifically targeted M. norvegica and their role in the pelagic food webs of high-latitude waters. We argue that it is potentially a key species with high-ecological impact in coastal ecosystems of temperate climes like the Mediterranean Sea and extending far to the north including the Arctic. Our results demonstrate that increasing our knowledge of the structure and function of coastal, pelagic ecosystems will require including small and less well-known copepod species in our sampling schemes. ACKNOWLEDGEMENTS We wish to thank Sigrid Øygarden and the crew at R/V “Hyas” for assistance during sampling. Rahman Mankettikkara and Hans Christian Eilertsen kindly provided the supplementary hydrography data from the UiT time series program “Havmiljødata.” We are grateful that Coralie Barth-Jensen and Helena Kling-Michelsen provided copepod length measurements and that Frøydis Strand prepared some of the figures. We are indebted to three anonymous referees for their constructive comments and to Charles B. Miller for his valuable remarks and editing of the English. FUNDING This work received financial support by UiT the Arctic University of Norway, the “CarbonBridge” project, Project number 226415, funded by The Research Council of Norway and the “Microsnow” project funded by the Fram Centre flagship “Fjord and Coast.” REFERENCES Antacli, J. C., Hernandez, D. R. and Sabatini, M. E. ( 2014) First report on the contribution of small-sized species to the copepod community structure of the southern Patagonian shelf (Argentina, 47–55 degrees S). Sci. Mar. , 78, 17– 26. 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Google Scholar CrossRef Search ADS   Author notes Corresponding editor: Roger Harris © The Author(s) 2018. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Plankton Research Oxford University Press

Small copepods matter: population dynamics of Microsetella norvegica in a high-latitude coastal ecosystem

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Abstract

Abstract We investigated the population dynamics of a small and little-studied harpacticoid copepod, Microsetella norvegica, in a sub-Arctic Norwegian fjord (Balsfjord 69°N). We sampled with a 90 μm mesh WP-2 net and a 20 L Go-Flo bottle and found that the WP-2 under-sampled all juvenile stages. The abundance and biomass were high, peaking in June with 9349 × 103 ind. m−2 and 1678 mg C m−2. Microsetella were most abundant in the surface, but females and males demonstrated a distinct migration to below 50 m from October to March. Consistently, individual female body carbon content was highest in October (0.39 μg C ind−1) and lowest in March (0.18 μg C ind−1). Males were present throughout the year, and females with eggs were found from April to September. The average clutch size was 11 ± 2 eggs female−1, and our study supports the observation that females can release their egg sac before the eggs have hatched, possibly to produce a new one. With its high abundance and biomass, a flexible reproductive strategy and specialized feeding preferences, M. norvegica is likely a key species in high-latitude coastal ecosystems. INTRODUCTION Most harpacticoid copepods are benthic, inhabiting all types of surfaces and sediments at all depths (Azovsky et al., 2016). The majority are substrate-bound (Dahms and Qian, 2004), and common habitats are seagrass blade surfaces and on or within bottom sediments (Bell et al., 1987). However, one harpacticoid species, Microsetella norvegica, appears especially adapted to a pelagic lifestyle. It is frequently associated with aggregates and marine snow (Kiørboe, 2000; Koski et al., 2005, 2007), and it has been suggested to be important for regulating the downward flux of carbon in coastal ecosystems (Green and Dagg, 1997; Koski et al., 2005, 2007). Microsetella norvegica is reported as highly abundant in temperate (Uye et al., 2002) as well as sub-Arctic (Arendt et al., 2013) seas, and may even be the numerically dominant copepod species in the mesozooplankton community (Dugas and Koslow, 1984; Arendt et al., 2013). Although M. norvegica has received increased attention during recent decades (Diaz and Evans, 1983; Uye et al., 2002; Turner, 2004; Arendt et al., 2013; Koski et al., 2014), knowledge of its biology and ecology is still rudimentary compared to that for calanoid copepod species. One likely reason is that M. norvegica is not efficiently sampled with standard plankton nets (e.g. mesh size 180 μm) due to its tiny size (<550 μm total length) and slender bodies. On the other hand, M. norvegica is often recorded in fish stomachs (Demchuk et al., 2015; Falkenhaug and Dalpadado, 2014), pointing to their wide distribution and importance as prey for fish in coastal ecosystems. Balsfjord (69°N) is a high-latitude, cold-water fjord with Arctic characteristics regarding irradiance and seasonality in primary production (Eilertsen and Taasen, 1984). The fjord is semi-enclosed and advection is reduced due to an entrance sill at 30 m depth, making it well suited for studies of zooplankton population dynamics. Previous studies have concluded that Calanus finmarchicus is the dominant zooplankton species in Balsfjord (Tande, 1982). However, other investigations, sampling zooplankton with Niskin water bottles (Pasternak et al., 2000) or plankton nets with 64 μm mesh size (Davis, 1976), reported high-relative abundance of M. norvegica during all seasons, although quantitative abundances were not presented. There are presently few quantitative studies focusing on M. norvegica seasonal abundance in high-latitude ecosystems, and therefore its population dynamics are not well known in these areas. For instance, aspects of its reproductive strategy, such as the timing and extent of the reproductive period, clutch size and the seasonal variation in ratio of males to females have not been fully described for high latitudes. Furthermore, many small copepods are winter-active in the surface at high latitudes (Madsen et al., 2008; Møller et al., 2006), but the over-wintering strategy for M. norvegica is not well known. We investigated the population dynamics of M. norvegica in Balsfjord through monthly sampling from June 2013 to June 2014. Our main objectives were to (i) study seasonal patterns of developmental stage composition, abundance, biomass and vertical distribution and (ii) determine the timing of reproduction of M. norvegica. In addition, we evaluated sampling efficiency for the different developmental stages of M. norvegica by comparing abundances obtained with a WP-2 net (90 μm mesh) with those obtained with a 20 L Go-Flo bottle. METHOD Study site and sampling The study was conducted at station Svartnes in Balsfjord (Fig. 1), northern Norway (69°22’N, 19°06’E). The fjord is 5 km at its widest, 46 km long. A shallow sill at the mouth (30 m depth) separates the fjord from coastal water to seaward (Reigstad, 2000; Wexels Riser et al., 2010). Balsfjord has two basins. The outermost is 130 m deep, and the innermost, where station Svartnes is located, is 185 m deep. The sun passes below the horizon between 26 November and 18 January (polar night), and stays above the horizon between 28 May and 19 July (midnight sun). Stratification of the water column generally starts in May and lasts until September (Eilertsen and Taasen, 1984). Vertical profiles of salinity, temperature, density and fluorescence were obtained for each sampling date using a CTD profiler (Seabird model 25 Sealogger) from the surface to 175 m (station depth was 180 m). Station Svartnes is part of a large hydrographic monitoring program (https://dataverse.no/dataverse/nmdc), and our monthly sampling results were supplemented with additional hydrographic data from the monitoring program. Fluoresence data from June 2014 are missing due to malfunction of the fluoresence sensor. Fig. 1. View largeDownload slide Map of the Tromsø area, showing the location of sampling station Svartnes in Balsfjord, northern Norway. Fig. 1. View largeDownload slide Map of the Tromsø area, showing the location of sampling station Svartnes in Balsfjord, northern Norway. Microsetella norvegica Monthly sampling was conducted during daytime from June 2013 to June 2014 from R/V “Hyas.” We aimed at collecting all developmental stages of M. norvegica, from nauplii to adult copepodites, and therefore sampled with both a WP-2 net (Hydro-Bios, 90 μm mesh size) and a 20 L Go-Flo bottle (General Oceanics). The WP-2 net was equipped with a filtering cod end and a closing mechanism to allow discrete sampling from 175 to 50 m and 50 to 0 m depth ranges. The contents of the cod end were concentrated with a 90 μm mesh sieve. Due to the small mesh size of the WP-2 net, the towing speed was slow, 0.2–0.3 m/s. The filtration volume was calculated from wire length, and no visual indications of clogging were observed. The Go-Flo bottle collected water at 5, 20 and 50 m depth, and its contents were concentrated with a 20 μm mesh sieve. All zooplankton samples were preserved with buffered formaldehyde at 4% final concentration. Individuals of M. norvegica were counted and identified using a stereo microscope (Leica MZ16) at 40–100× magnification. Developmental stages were identified according to Hirakawa (1974) and Huys and Boxshall (1991). Due to their small size, M. norvegica nauplii were not identified to stage but counted as one group. Copepodite stages CIV and CV were not separated due to their morphological similarity and are reported as M. norvegica CIV–CV. Other stages were enumerated separately. Females carrying an egg sac and detached egg sacs in the sample were also enumerated. From each subsample, a minimum of 300 individuals were counted. Subsample volumes ranged from 7 to 100% of the entire sample. A total of 65 samples were analysed in this study. To obtain comparative estimates of the WP-2 and Go-Flo sampling efficiency in the surface layer, the Go-Flo samples were integrated from 0 to 50 m depth, assuming the sample depths represented the midpoint in each interval. Carbon and nitrogen contents of M. norvegica females were determined in October, January, March and May to cover the seasonal variations in body condition. For these analyses, additional samples were collected with the WP-2 net and live animals were transported to the laboratory where 600 females without egg sacs were sorted out. The females were rinsed in filtered seawater and duplicates of 300 animals from each sampling date were gently dropped onto combusted GF/F filters and stored frozen (−20°C) until analysis. The organic carbon and organic nitrogen contents of females were determined with a CHN Lab-Leeman 440 elemental analyser. Results for blank filters without copepods were subtracted from those for filters containing M. norvegica. To obtain a length–carbon relationship, the body lengths of 50 M. norvegica females from the same sample were measured using a stereo microscope (Zeiss Discovery V20). To achieve population biomass of M. norvegica, the carbon contents of all copepodite stages were estimated from an empirical length–carbon correlation (Uye et al., 2002),   C=2.65×10−6×BL1.95, (1)where C is the carbon content (μg) and BL the total body length (μm). Body lengths of at least 10 individuals of each developmental stage were measured for selected samples to cover the full seasonal cycle. Average body lengths of all six naupliar stages were obtained from measurements of totally 55 nauplii of different stages (from June only) and applied to equation (1). The length and width of 30 egg sacs were measured and the sac volume was calculated assuming cylindrical shape. All 30 egg sacs were dissected and the individual eggs were counted, the diameter was measured and the volume of individual eggs was calculated (as the volume of a sphere). Statistical analyses Differences in sampling efficiency between the WP-2 net and Go-Flo bottle for the different developmental stages were tested for statistical significance by applying a nonparametric Mann–Whitney U-test for independent samples (IBM SPSS statistics version 24). Due to the seasonal, and hence uneven, occurrence of the younger developmental stages, including nauplii, CI, CII and CIII (Table I), these were merged and tested as one group. Table I: Integrated (0–50 m) abundance (103 ind. m−2) of M. norvegica developmental stages obtained with Go-Flo bottle (G) and WP-2 (W)   Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093    Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093  Data are presented for each sampling date, and the mean of all samplings is provided. A statistically significant difference between abundances obtained with Go-Flo and WP-2 is indicated by a * (P < 0.05). No statistically significant difference between samplers is indicated by “ns.” Table I: Integrated (0–50 m) abundance (103 ind. m−2) of M. norvegica developmental stages obtained with Go-Flo bottle (G) and WP-2 (W)   Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093    Nauplii*  CI*  CII*  CIII*  CIV–CV*  Femalesns  Malesns  Total*  Date  G  W  G  W  G  W  G  W  G  W  G  W  G  W  G  W  27.05.13  1235  9  234  21  70  78 178  23  53  0  20  125  398  36  49  1723  629  28.06.13  2165  0  552  10  785  15  657  26  26  0  994  1102  276  385  5455  1538  23.08.13  121  0  46  10  221  15  237  26  253  0  828  1102  922  385  2519  1538  19.09.13  0  0  3  0  31  0  21  8  61  86  768  904  876  1004  1759  2002  15.10.13  0  0  0  0  0  0  0  0  26  10  514  248  1253  567  1792  826  19.11.13  0  0  0  0  0  0  0  0  23  10  163  205  358  383  543  599  08.01.14  0  0  0  0  0  0  0  0  39  0  167  322  588  387  794  709  30.01.14  0  0  0  0  0  0  0  0  12  2  116  108  289  143  418  254  04.03.14  0  0  0  0  0  0  0  0  9  11  190  214  278  227  477  452  25.03.14  0  0  0  0  0  0  0  0  43  8  579  395  459  476  1081  878  29.04.14  213  0  0  0  0  0  0  0  51  31  916  897  445  604  1626  1532  06.05.14  678  0  0  0  0  0  0  0  239  96  1083  1169  801  705  2801  1971  16.06.14  6372  870  517  24  229  0  97  0  24  5  1616  290  494  86  9349  1276  Mean  821  68  104  5  103  8  80  9  62  22  620  566  544  415  2334  1093  Data are presented for each sampling date, and the mean of all samplings is provided. A statistically significant difference between abundances obtained with Go-Flo and WP-2 is indicated by a * (P < 0.05). No statistically significant difference between samplers is indicated by “ns.” RESULTS Hydrography The water column was stratified from late May to late November, with warm surface water (8–10°C) over colder water (2–4°C) below a thermocline at 40–80 m (Fig. 2A). A core of warm, saline (32.5 g kg−1) water was present in the surface from early June, and the water masses gradually cooled from September. During winter, from January to April, the water column was well mixed with temperatures from 2 to 4°C. Three periods with low salinity were observed: in June 2013, January 2014 and June 2014 (Fig. 2B). These events were most likely caused by snowmelt (June) and heavy snowfall (January). The fluorescence started to increase at the beginning of April, with maxima observed in June 2013 and in May–June 2014, indicating spring bloom conditions around 13 and 20 m depth, respectively (Fig. 2C). Between late October and early March, the fluorescence was below the detection limit. Fig. 2. View largeDownload slide (A) Temperature (°C), (B) salinity (g kg−1) and (C) fluorescence at station Svartnes from August 2013 to June 2014. The black vertical lines indicate dates of sampling, ND implies no data. Fig. 2. View largeDownload slide (A) Temperature (°C), (B) salinity (g kg−1) and (C) fluorescence at station Svartnes from August 2013 to June 2014. The black vertical lines indicate dates of sampling, ND implies no data. Comparison of sampling methods The M. norvegica population in Balsfjord was sampled using a WP-2 net (90 μm mesh) and a Go-Flo water bottle (volume 20 L). When averaging all stages and sampling integrated over 0–50 m, a 2.2-fold higher abundance of M. norvegica individuals was obtained with the Go-Flo bottle, than with the WP-2 net (Table I), and the difference is statistically significant (Mann–Whitney U-test, P = 0.024). The discrepancy between the two sampling methods was statistically significant for the group of nauplii plus young copepodites CI–CIII (P = 0.023) and for CIV–CV (P = 0.017). Females and males were sampled generally equally well with the Go-Flo and WP-2 (P > 0.5). When presenting data on M. norvegica population dynamics, we will use the data obtained with the Go-Flo bottle integrated from 50 to 0 m depth, while the data obtained by WP-2 will be used to evaluate the seasonal shifts in vertical distribution of females and males. Body lengths and female carbon and nitrogen weight The body length of all developmental stages varied seasonally and peaked in June (Fig. 3). Females had the largest body size, followed by males. The range in C and N contents for individual females throughout the sampling period was 0.18–0.39 μg C ind−1 and 0.03–0.05 μg N ind−1 (Table II). The individual carbon weight (mean ± standard deviation) was highest in October (0.39 ± 0.01 μg C ind−1) and lowest in March (0.18 ± 0.04 μg C ind−1), while the N content varied little between the sampled months (Table II). The C:N ratio of females ranged from 11.2 ± 0.5 in October to 6.0 ± 0.3 in May. Fig. 3. View largeDownload slide Microsetella norvegica seasonal body length (mean ± SD). Fig. 3. View largeDownload slide Microsetella norvegica seasonal body length (mean ± SD). Table II: Body length (μm) of M. norvegica females in October, January, March and May   October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3    October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3  Carbon content (μg C ind−1), nitrogen content (μg N ind−1) and C/N ratio (atomic) are given as the mean ± SD (N = 2 filters, each containing 300 females). Table II: Body length (μm) of M. norvegica females in October, January, March and May   October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3    October  January  March  May  Body length, μm  464 ± 37  438 ± 36  457 ± 41  486 ± 45  μg C female−1  0.39 ± 0.01  0.30 ± 0.04  0.18 ± 0.04  0.26 ± 0.01  μg N female−1  0.04 ± 0.00  0.04 ± 0.01  0.03 ± 0.01  0.05 ± 0.00  C/N female−1  11.2 ± 0.5  9.8 ± 1.2  8.2 ± 1.6  6.0 ± 0.3  Carbon content (μg C ind−1), nitrogen content (μg N ind−1) and C/N ratio (atomic) are given as the mean ± SD (N = 2 filters, each containing 300 females). Vertical distribution Females and males were present throughout the water column year-round, but with an apparent seasonal shift (Fig. 4). From May to September, the vast majority were present in the upper 50 m, and few adults were found deeper in the water column. About half of the M. norvegica adult population were found below 50 m from October to January. The entire population was dominated by males and females in this winter period, with a modest contribution of developmental stages CIV–CV (Table I). From March onwards, the adult population abundance increased in the upper 50 m while declining below (Fig. 4). Fig. 4. View largeDownload slide Vertical distribution of the sum of M. norvegica females and males from May 2013 to June 2014 as sampled with a WP-2 net (90 μm mesh) and integrated in the surface (50–0 m) and in the deep layer (175–50 m). Data are presented in terms of abundance (103 ind. m−2). For months with more than one sampling, the mean is given. Fig. 4. View largeDownload slide Vertical distribution of the sum of M. norvegica females and males from May 2013 to June 2014 as sampled with a WP-2 net (90 μm mesh) and integrated in the surface (50–0 m) and in the deep layer (175–50 m). Data are presented in terms of abundance (103 ind. m−2). For months with more than one sampling, the mean is given. Population dynamics Microsetella norvegica was found in high abundance in the upper water column (0–50 m) of Balsfjord year-around (Fig. 5). The maximum was observed in June 2014, a total abundance of 9349 × 103 ind. m−2 (2977 × 103 copepodites and 6372 × 103 nauplii), and the minimum (418 × 103 ind. m−2) occurred in late January (Table I). A clear seasonal succession of developmental stages was observed in the upper 50 m (Fig. 5). Females, males and CIV–CV had high abundances throughout the year. Ovigerous females were only present from April to August (Fig. 5). Interestingly, detached egg sacs were found over a longer time-period, from April to October (Fig. 5). Nauplii were present simultaneously with ovigerous females (Table II, Fig. 5). Copepodite stages CI–CIII were present from May to September with maximum observed abundances in June. Fig. 5. View largeDownload slide Integrated (0–50 m) abundance (ind m−2) of M. norvegica developmental stages sampled with Go-Flo from May 2013 to June 2014. Note the logarithmicy-axes. Fig. 5. View largeDownload slide Integrated (0–50 m) abundance (ind m−2) of M. norvegica developmental stages sampled with Go-Flo from May 2013 to June 2014. Note the logarithmicy-axes. The integrated population biomass of M. norvegica in the upper 50 m was below 400 mg C m−2 in winter (November to mid-March), and building up from early spring (March) to summer (Fig. 6). The highest observed biomass, 1.7 g C m−2, was found in June 2014 (Fig. 6). Males and females made up the largest contribution to biomass, except for June when smaller stages also contributed significantly. Fig. 6. View largeDownload slide Integrated (0–50 m) biomass (mg C m−2) and relative stage composition (% contribution) of M. norvegica sampled with Go-Flo from May 2013 to June 2014. ND implies no data, for months with more than one sampling, the mean is given. Fig. 6. View largeDownload slide Integrated (0–50 m) biomass (mg C m−2) and relative stage composition (% contribution) of M. norvegica sampled with Go-Flo from May 2013 to June 2014. ND implies no data, for months with more than one sampling, the mean is given. Microsetella norvegica fecundity Males and females were present during all months investigated (Table III). The sex ratios were skewed toward females from March to June, and strongly skewed toward males in November and January (no data are available for December). In the remaining months, the sex ratios were close to 1. Females with egg sacs were present from April to August, and the total number of egg sacs (sum of egg sacs attached to females and detached egg sacs in the sample) was highest in June. The fraction of detached egg sacs ranged from 36% to 100% of the total number of egg sacs recorded (Table III). The total egg sacs:females ratios were in general below 1, although as high as 1.6 in May (Table III). The egg sacs:females ratios were also slightly higher than 1 in April (Table III). No relationship was found between female body length and the number of eggs in the attached egg sacs (regression R2 = 0.000005, P = 0.99, n = 30), but there was a significant positive correlation between female body length and egg sac volume (R2 = 0.47, P < 0.0001) and between clutch size and the average volume of a single egg (R2 = 0.15, P = 0.03) (data not shown). The number of eggs in an egg sac ranged from 6 to 13, with a mean ± SD of 11 ± 2 eggs (Table IV). Nauplii were present in the period from April to August, with a peak of 6 372 000 nauplii m−2 in June 2014 (Table I). This corresponds to a mean concentration of 127 440 nauplii m−3 in the upper 50 m, or about 130 nauplii L−1. Table III: Integrated (0–50 m) seasonal abundance of (103 ind m−2) of M. norvegica females (#F), females to males (F:M), egg sacs (#ES total, i.e. the sum of detached egg sacs and egg sacs attached to females), percentage detached egg sacs (%ES detached) and the ratio of total (attached and detached) egg sacs to total females (ES:F) for each sampling date Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  All data were obtained from samples collected with the Go-Flo. Temperature (°C) is presented as average for the 0–50 depth interval. Table III: Integrated (0–50 m) seasonal abundance of (103 ind m−2) of M. norvegica females (#F), females to males (F:M), egg sacs (#ES total, i.e. the sum of detached egg sacs and egg sacs attached to females), percentage detached egg sacs (%ES detached) and the ratio of total (attached and detached) egg sacs to total females (ES:F) for each sampling date Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  Month  Dates (D/M/Y)  Temp, °C (0–50 m)  # F  F:M  # ES total  % ES detached  ES:F  Jan  08/01/14  4.5  166  0.3  0  –  –  30/01/14  3.2  116  0.4  0  –  –  March  04/03/14  2.6  190  0.7  0  –  –  25/03/14  2.4  579  1.3  0  –  –  April  29/04/14  3.2  916  2.1  979  49  1.1  May  27/05/13  nd  125  3.5  124  49  1  06/05/14  3.5  1083  1.4  1225  98  1.6  June  28/06/13  5.6  994  3.6  940  73  0.9  16/06/14  6.7  1616  3.3  1367  36  0.8  Aug  23/08/13  8.0  828  0.9  82  96  0.1  Sept  19/09/13  8.6  768  0.9  20  100  <0.1  Oct  15/10/13  8.4  514  0.4  5  100  <0.1  Nov  19/11/13  6.4  163  0.5  0  –  –  All data were obtained from samples collected with the Go-Flo. Temperature (°C) is presented as average for the 0–50 depth interval. Table IV: Microsetella norvegica mean ± SD body length (N = 30), number of eggs per egg sac (N = 30), egg volume (N = 150) and egg sac volume (N = 30) in June 2014 Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  Table IV: Microsetella norvegica mean ± SD body length (N = 30), number of eggs per egg sac (N = 30), egg volume (N = 150) and egg sac volume (N = 30) in June 2014 Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  Body length (μm)  # Eggs egg sac−1  Volume egg−1 (mm3)  Volume egg sac−1 (mm3)  542 ± 38  11 ± 2  152 ± 45  8463 ± 2711  DISCUSSION For a species, Gaston (2008) argues that “it is rare to be common” and that “common species are typically both abundant and widespread.” There are only a few previous observations of M. norvegica in high-latitude Norwegian fjords, and an earlier study explicitly stated that this species is rare in Balsfjord (Hopkins, 1981). In strong contrast, we found high abundances of M. norvegica throughout the year, with a population peak exceeding 9 000 000 ind. m−2 in the upper 50 m in June 2014. This is among the highest abundances ever reported for this species, and the first quantitative estimate including all copepodite stages and nauplii of M. norvegica at similarly high latitudes (69°N). Microsetella norvegica—abundant and widespread? Due to its small body size, M. norvegica is not efficiently caught by a WP-2 net with 180 μm mesh, which is a widely used zooplankton sampler. By now, it is a well-known fact that copepods with body lengths shorter than 800 μm are significantly underestimated when sampled with 180–200 μm mesh (Gallienne and Robins, 2001), and a mesh size of 80 μm has been suggested as suitable for sampling small copepods in the marine environment (Riccardi, 2010). However, we found that all copepodite stages of M. norvegica, except females and males, were under-sampled with a 90 μm mesh compared to the Go-Flo bottle. The high abundances of M. norvegica found in Balsfjord are likely common, as high numbers have also been reported from different geographical areas (from 45°S to 69°N), where zooplankton have been sampled with mesh sizes of 100 μm or smaller (Table V). For example, M. norvegica is abundant in the White Sea, Russia (Demchuk et al., 2015), in Godthåpsfjord, Greenland (Arendt et al., 2013), in Storfjorden, Norway (Halliday et al., 2001), on the Scotian Shelf, Canada (Dugas and Koslow, 1984), in the Central North Sea (Koski et al., 2007), in the Inland Sea of Japan (Uye et al., 2002) and on the Patagonian Shelf, Argentina (Antacli et al., 2014; Temperoni et al., 2014) (Table V). There are also a number of studies highlighting the importance of M. norvegica as prey for a variety of fish species in different habitats. For example, it was found to be the preferred prey of sprat in Hardangerfjord, Norway (Falkenhaug and Dalpadado, 2014), three-spined stickleback in the White Sea (Demchuk et al., 2015), larval jack mackerel off eastern Tasmania (Young and Davis, 1992) and for anchovies and sardines in the north-western Mediterranean Sea (Morote et al., 2010). We therefore suggest that M. norvegica is one of the supposedly rare species that is actually both abundant and widespread (sensuGaston, 2008) in fjords and coastal ecosystems at high and temperate latitudes. It is, thus, a key copepod species in these ecosystems. Table V: Maximum abundances (individuals m−3) of M. norvegica reported from different regions Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Abundances of copepodites (C) and nauplii (N) are given separately when possible; otherwise the abundances represent total abundance of individuals, as reported in the respective studies. Mesh sizes (μm) of sampling devices are provided. aSampled with water bottles, mesh size at which sample was concentrated is given. Table V: Maximum abundances (individuals m−3) of M. norvegica reported from different regions Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Region  Latitude  Max abund. (Ind. m−3)  Mesh size (μm)  Reference  Balsfjord, Norway  69°N  156 800 (C)  20a  This study  127 440 (N)  White Sea, Russia  66°N  20 000  93  Demchuk et al. (2015)  Godthåpsfjord, Greenland  64°N  91 995 (C)  45  Arendt et al. (2013)  408 125 (N)  Storfjorden, Norway  62°N  20 000  53  Halliday et al. (2001)  Sandsfjorden, Norway  59°N  3990  45a  Nielsen and Andersen (2002)  Central North Sea  56°N  1100 (C)  50a  Koski et al. (2007)  500 (N)  Scotian Shelf, Canada  42–43°N  3940  80  Dugas and Koslow (1984)  Inland Sea of Japan  34°N  73 200 (C)  94  Uye et al. (2002)  25 000 (N)  40a  Patagonian Shelf, Argentina  47–66°S  917  66  Antacli et al. (2014)  Patagonian Shelf, Argentina  43–45°S  256  67  Temperoni et al. (2014)  Abundances of copepodites (C) and nauplii (N) are given separately when possible; otherwise the abundances represent total abundance of individuals, as reported in the respective studies. Mesh sizes (μm) of sampling devices are provided. aSampled with water bottles, mesh size at which sample was concentrated is given. Population dynamics and C/N composition During winter (October to March), the population consisted mostly of adults, with a predominance of males. The over-wintering females did not carry eggs. About 50% of the adult population showed a distinct seasonal migration to below 50 m from October to March, while the other half remained in the upper water column. From this observation, it is difficult to conclude whether M. norvegica are winter-active or not, but we also measured a 53% decline in body C, a 25% reduction in body N and a decline in C/N ratio in females from October to March. This probably reflects low energy intake during winter, which is comparable with seasonal patterns in carbon content and C/N ratios for both the C. finmarchicus in diapause and the winter-active Metridia longa in Balsfjord (Tande, 1982; Grønvik and Hopkins, 1984). The decreasing carbon content and C/N ratio through the winter (Table II) could reflect both a shift in body composition from more carbon-rich lipids in autumn to relatively more nitrogen-rich proteins in early spring when the copepods prepare for reproduction. However, this assumption is based on speculation, as lipid accumulation in this species has not been confirmed. When comparing the measured (CHN analyzer) with the calculated (equation (1)) carbon content of M. norvegica females, the calculated values were always higher but the degree of discrepancy was variable. For instance, in October, the C content calculated from body length was 10% higher than the measured concentration, whereas in March the calculated C content was almost twice the measured concentration. This also points to a relatively large difference in body condition (e.g. lipid content), while body length was relatively stable (464 μm in October and 457 μm March). Nevertheless, it is likely that M. norvegica reduce their feeding activities during winter, although their tolerance for starvation is not known. It should also be noted that in a sub-Arctic Greenlandic fjord, M. norvegica did not display a defined time for leaving the upper 100 m (Arendt et al., 2013). In March, the majority of the males and females had ascended from the deeper layers and were found in close to equal numbers in the upper 50 m depth (female:male ratio from 0.7 to 1.3). Females with eggs first appeared in April, when the sex ratios strongly favoured females (Table III). Nauplii occurred from April to August, and copepodite stages CI–CIII were present from June to September. Body sizes of M. norvegica varied with season and all the developmental stages were largest in the warm, high production period (May–June) (Fig. 3). The decrease in body sizes observed from June to August likely results from newly moulted copepodites from the new cohort of nauplii produced in April. Based on the clearly observed distinction between the cohorts of developmental stages, we suggest that M. norvegica has a single generation per year in Balsfjord. This is in contrast to the suggested five or six generations per year in the significantly warmer (25°C in summer) central part of the Inland Sea of Japan (Uye et al., 2002). In general, males were more abundant than females from August to March, while the sex ratio was skewed toward females in April–June (no data are available for July). An adult sex ratio skewed toward males is rarely reported for pelagic copepods (Kiørboe, 2006; Hirst et al., 2010). As the availability of males to fertilize females may be a limiting factor for population growth (Kiørboe, 2007), an even sex ratio may be regarded as an advantage for the reproductive success for M. norvegica. It has been reported that for copepods lacking seminal receptacles the adult sex ratio is closer to 1:1, as repeated mating is necessary to allow continued fertilization of eggs (Kiørboe, 2006). Mironova and Pasternak (2017) recently described the occurrence of seminal receptacles in female M. norvegica. The reason for the unusual dominance of males found in this study could instead be a result of differences in gender-specific mortality due to predation or starvation. Higher mortality rates for females could have occurred, as the total abundance of females decreased from October to early March. Predatory mortality rates in copepods are related to behavioural traits, with a higher mortality rate among copepods for feeding-current grazers and cruise feeders than for ambush-feeding species, with similarly greater relative mortality for males actively searching for females (Greve et al., 2017). As the behavioural traits of male and female M. norvegica have not yet been described, it is not straight forward to conclude whether the possibly gender-specific mortality rates result from differential predation. Copepods may also display gender-specific tolerance to starvation that can partly be explained by differences in body size (Holm et al., 2018). However, for copepods such as M. norvegica where the females are larger than the males, this should result in lower starvation tolerance and greater mortality rates for males than for females. An alternative explanation for the observed sex ratios in this study is environmental sex determination. Adult sex ratios influenced by environmental parameters, such as temperature or pheromones, have been found for many Crustaceans, including copepods (Svensen and Tande, 1999). Clearly, more information is needed on the gender-specific mortality rates and sex determination mechanisms in order to explain the unusually high abundance of M. norvegica males throughout the year. Patterns of reproduction The spring bloom in Balsfjord starts in March and reaches a maximum in late April (Eilertsen et al., 1981). We anticipated that reproduction of M. norvegica would not be restricted to this short bloom period, a strategy differing from that of C. finmarchicus, which spawns during a short period of 3–4 weeks in connection to the bloom (Diel and Tande, 1992). As M. norvegica may feed on marine snow particles (Koski et al., 2005, 2007), we expected prolonged reproduction outlasting the spring bloom. Defined according to the fraction of egg-carrying females, the reproductive onset was in April, with its main reproductive period in May/June. However, females with eggs were observed until September, and detached egg sacs were recorded until November. This is in agreement with Davis (1976) and Koski et al. (2014), who reported that reproduction of M. norvegica started in April and May in the surface. In Balsfjord, Davis (1976) first observed females with eggs in late March and did not observe any carrying eggs after mid-September. Given that concurring data, we conclude that the egg production of M. norvegica is triggered by the onset of the spring bloom, but that females can continue reproducing until September. They start spawning around the same time as the broadcast-spawning C. finmarchicus, and they possibly compensate for lower production rates by prolonged spawning and egg carrying (Kiørboe and Sabatini, 1995). Egg carrying copepods produce smaller clutches than broadcast spawners (Bunker and Hirst, 2004). Egg hatching is temperature-dependent (Bunker and Hirst, 2004), and for a sac spawner the production of a new egg sac must wait until hatching of eggs from a sac already carried (Koski et al., 2014). Sac-spawning copepods are assumed to keep the egg sac until the eggs hatch. However, an unusual reproductive strategy has been suggested for M. norvegica. In a sub-Arctic fjord, Koski et al. (2014) found as many as 4.5-fold more egg sacs than females in May. They suggested that M. norvegica sheds its egg sacs before the eggs hatch, allowing each female to produce a new sac of eggs earlier. We made similar observations in Balsfjord, with 1.6 egg sacs per female in May. This finding is also supported by studies on M. norvegica gonad morphology (Diaz and Evans, 1983; Mironova and Pasternak, 2017). Diaz and Evans (1983) also observed females possessing an egg sac while simultaneously developing new eggs internally, and they suggested that M. norvegica spawns more than once, producing more offspring faster than more typical sac-spawning copepods. This may explain the apparent paradox that a slowly growing species like M. norvegica can achieve such high abundances, as already pointed out by Koski et al. (2014). Microsetella norvegica in the food web Microsetella norvegica reproduces relatively slowly but can build up dense populations in fjords and coastal ecosystems. In Balsfjord, the total M. norvegica surface biomass during spring and summer was 600–1700 mg C m−2 and they sustain a level of 200–300 mg C m−2 during winter. They are a substantial and continuously available source of energy for fish and other predators. The maximum abundance of M. norvegica in this study was 9 × 106 ind m−2, corresponding to 156 copepodites L−1 and 127 nauplii L−1. This points to their importance not only as prey but also as grazers. They are repeatedly observed in association with aggregates (Green and Dagg, 1997; Kiørboe, 2000), and the grazing rate on discarded larvacean houses was found to be 0.14 μg C ind−1 d−1 in the North Sea (Koski et al., 2007). At the abundances of M. norvegica copepodites observed in Balsfjord, their grazing impact on marine snow could be ∼350 mg C m−2 d−1 in the upper 50 m depth. In comparison, sedimentation rates in Balsfjord in June are on the order of 100–200 mg C m−2 d−1 (Reigstad and Wassmann, 1996). Microsetella are under-sampled with standard zooplankton nets, making it plausible to suggest that it is substantially more abundant than previously reported. We suggest that M. norvegica plays an essential role in the carbon cycle of fjords and coastal ecosystems, perhaps particularly so at high latitudes. CONCLUSIONS This is the first study to report high abundances of M. norvegica all through the year in a high-latitude fjord, specifically Balsfjord. We expected M. norvegica to be active through winter, but we found that about half of the adult population migrated below 50 m from October to January. Furthermore, a decline in body C:N ratios from 11.2 in October to 6.0 in May indicates low energy intake during winter. Reproduction of M. norvegica was not limited to the spring bloom period, as females with eggs were observed from April to September. Moreover, our study suggests that M. norvegica females shed their egg sacs before the contained clutches of eggs are hatched, thus allowing more rapid production of clutches. A prolonged reproductive period, combined with production of multiple egg sacs by each female, may compensate for the small clutch size of 11 ± 2 eggs female−1. So far, few studies have specifically targeted M. norvegica and their role in the pelagic food webs of high-latitude waters. We argue that it is potentially a key species with high-ecological impact in coastal ecosystems of temperate climes like the Mediterranean Sea and extending far to the north including the Arctic. Our results demonstrate that increasing our knowledge of the structure and function of coastal, pelagic ecosystems will require including small and less well-known copepod species in our sampling schemes. ACKNOWLEDGEMENTS We wish to thank Sigrid Øygarden and the crew at R/V “Hyas” for assistance during sampling. 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Journal of Plankton ResearchOxford University Press

Published: Jun 4, 2018

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