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Seasonal Changes in Vertical Distribution and Population Structure of the Dominant Hydrozoan Aglantha digitale in the Western Subarctic Pacific

Seasonal Changes in Vertical Distribution and Population Structure of the Dominant Hydrozoan... Article Seasonal Changes in Vertical Distribution and Population Structure of the Dominant Hydrozoan Aglantha digitale in the Western Subarctic Pacific 1 1 1 , 2 , Mari Aizawa , Tian Gao and Atsushi Yamaguchi * Graduate School of Fisheries Sciences, Hokkaido University, 3–1–1 Minato-cho, Hakodate 041-8611, Hokkaido, Japan; [email protected] (M.A.); [email protected] (T.G.) Arctic Research Center, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo 001-0021, Hokkaido, Japan * Correspondence: a-yama@fish.hokudai.ac.jp Abstract: Hydrozoans are numerically dominant taxa in gelatinous zooplankton communities of the worldwide oceans and play an energy transfer role connecting primary producers and higher trophic level organisms. In the western subarctic Pacific, St. K2 has been established as a long-term time- series monitoring station. Various studies on zooplankton have been conducted, while hydrozoans have not been treated. This study presents the abundance, vertical distribution, and population structure of the dominant hydrozoan species (Aglantha digitale) at St. K2. Samples collected by vertical stratification samplings from eight layers of 0–1000 m both day and night during four seasons in one year. Hydrozoans occur throughout the year. The annual mean abundance of A. digitale was 198.4 ind. m and composed of 91.9% of hydrozoans. The vertical distribution of A. digitale was concentrated for the epipelagic layer (0–200 m), both day and night of the most season. The bell height (BH) of A. digitale ranged between 2.4–18.9 mm. Most of the mature individuals, with gonad length larger than 10% of BH, occurred only in July. The BH of mature individuals ranged from 4.7 to 17.6 mm, with the BH of most mature individuals were larger than >10 mm. Through observation on BH at each sampling layer, small individuals with BH < 6 mm were distributed below 300 m depths throughout the seasons, expanding their vertical distribution to the deeper layers. Inter-region comparison of Citation: Gao, T.; Aizawa, M.; abundance, maturation body size, and generation length of A. digitale revealed that these parameters Yamaguchi, A. Seasonal Changes in are varied with the region and depend on the marine ecosystem structures. Vertical Distribution and Population Structure of the Dominant Keywords: hydrozoa; Aglantha digitale; abundance; population structure; life cycle Hydrozoan Aglantha digitale in the Western Subarctic Pacific. Oceans 2023, 4, 242–252. https:// doi.org/10.3390/oceans4030017 1. Introduction Academic Editors: Antonio Bode and From worldwide oceans, hydrozoans are numerically dominant taxa in gelatinous Sam Dupont zooplankton communities, feed on small zooplankton and serve as food for fishes, and Received: 26 April 2023 act as mediators transporting energy between primary producers and higher trophic level Revised: 7 June 2023 organisms [1]. Recent climate changes (North Atlantic Oscillation, North Pacific Decadal Accepted: 20 July 2023 Oscillation, El Nino, etc.) have had a significant impact on standing stocks of jellyfish Published: 31 July 2023 in worldwide oceans, and may increase the duration of occurrence of hydrozoans in the temperate to subarctic regions [2]. This increase in hydrozoans is predicted to alter the bal- ance of prey-predator relationships in marine ecosystems, with significant effects on lower and higher trophic-level organisms [3,4]. On the other hand, the chemical compositions of Copyright: © 2023 by the authors. hydrozoans are characterized by low carbon but high nitrogen and phosphorus contents, Licensee MDPI, Basel, Switzerland. and their outbreak affects the nutrient balance (C:N:P ratio) of the marine ecosystem, and This article is an open access article the decomposition of their carcasses by bacteria has a significant impact on the marine distributed under the terms and mineral cycles [5,6]. conditions of the Creative Commons In the Northern Hemisphere, Aglantha digitale is the most abundant hydrozoan in Attribution (CC BY) license (https:// both abundance and biomass at high latitudes [1]. A. digitale has been reported as the creativecommons.org/licenses/by/ most dominant hydrozoan species in the western subarctic Pacific [7,8], eastern subarctic 4.0/). Oceans 2023, 4, 242–252. https://doi.org/10.3390/oceans4030017 https://www.mdpi.com/journal/oceans Oceans 2023, 4, FOR PEER REVIEW 2 dominant hydrozoan species in the western subarctic Pacific [7,8], eastern subarctic Pacific [9], northern North Pacific [10], western Arctic Ocean [11], Toyama Bay in the southern Japan Sea [12], Norwegian fj ords and Svalbard Islands [13–15], eastern North Atlantic Oceans 2023, 4 243 [16,17], Irish Sea [18], and White Sea [19,20]. As the ecology of A. digitale, feeding mecha- nisms [21,22], feeding impact [13,20,23], and swimming behavior [24] have been reported. Pacific [9], northern North Pacific [10], western Arctic Ocean [11], Toyama Bay in the For life histories, there have been reports from various oceans, including the Oyashio re- southern Japan Sea [12], Norwegian fjords and Svalbard Islands [13–15], eastern North gion [7,8], the eastern subarctic Pacific [9], Toyama Bay [12], the western North Atlantic Atlantic [16,17], Irish Sea [18], and White Sea [19,20]. As the ecology of A. digitale, feeding [16], the Norwegian fj ords [14], and the White Sea [19]. mechanisms [21,22], feeding impact [13,20,23], and swimming behavior [24] have been In the western subarctic Pacific, St. K2 has been set as a long-term time-series station reported. For life histories, there have been reports from various oceans, including the Oyashio to monitor v region a [7 rious bio ,8], the eastern geocsubar hemical p ctic Pacific arameters [9], Toyama [25]. Bay As t [12 h ],e the info western rmation on North hydrozoans at Atlantic [16], the Norwegian fjords [14], and the White Sea [19]. St. K2 bimodal vertical distribution with peaks at 0–50 m and 200–300 m, with a minimum In the western subarctic Pacific, St. K2 has been set as a long-term time-series station at 150–200 m, and no day/night differences in abundance have been reported [26]. At St. to monitor various biogeochemical parameters [25]. As the information on hydrozoans at K2, there are several studies on zooplankton [27–31], but no specific studies on hydrozo- St. K2 bimodal vertical distribution with peaks at 0–50 m and 200–300 m, with a minimum ans are available. Despite their importance on the lower and higher trophic level organ- at 150–200 m, and no day/night differences in abundance have been reported [26]. At St. K2, there are several studies on zooplankton [27–31], but no specific studies on hydrozoans isms and material transport, information on hydrozoans in this area are currently scarce. are available. Despite their importance on the lower and higher trophic level organisms This study conducted abundance, vertical distribution, and population structure of and material transport, information on hydrozoans in this area are currently scarce. the dominant hydrozoans (A. digitale) at St. K2 in the western subarctic Pacific using for- This study conducted abundance, vertical distribution, and population structure of the malin-preserved samples collected from day and night vertically stratified samplings be- dominant hydrozoans (A. digitale) at St. K2 in the western subarctic Pacific using formalin- pr tw eserved een 0–1 samples 000 m collected covering f from our sea day and sons night of one vertically yearstratified . As new sampling scientifi sc between information, seasonal 0–1000 m covering four seasons of one year. As new scientific information, seasonal and and day-night changes in bell height (BH, Figure 1) and gonad maturation at each sam- day-night changes in bell height (BH, Figure 1) and gonad maturation at each sampling pling depth down to 1000 m have been evaluated. The results were compared with the depth down to 1000 m have been evaluated. The results were compared with the same same species in the various regions of high-latitude waters of the Northern Hemisphere. species in the various regions of high-latitude waters of the Northern Hemisphere. Figure Figure 1. 1. Pictur Pictu e on re on specimen specimens of Aglantha s of Aglantha digitale digitale (left) and their (left meas ) and ur their measu ed body parts:rbell ed body parts height : bell height (BH) and gonad length (GL) (right). (BH) and gonad length (GL) (right). 2. Materials and Methods 2. Materials and Methods 2.1. Field Sampling Day and night vertically stratified zooplankton samplings were made by oblique 2.1. Field Sampling tow of Intelligent Operative Net Sampling System (IONESS, SEA Co., Ltd., Bristol, UK) Day and night vertically stratified zooplankton samplings were made by oblique tow equipped 335 m mesh and 1.5 m mouth area, from eight layers (0–50, 50–100, 100–150, of Intelligent Operative Net Sampling System (IONESS, SEA Co., Ltd., Bristol, UK) 150–200, 200–300, 300–500, 500–750, 750–1000 m) at St. K2 (47 N, 160 E, 5230 m depth, equipped 335 µm mesh and 1.5 m mouth area, from eight layers (0–50, 50–100, 100–150, Figure 2), located in the western subarctic Pacific on 29 October 2010, 26 February, 22–23 April, and 3–4 July 2011 (Table 1). After collection, zooplankton samples were 150–200, 200–300, 300–500, 500–750, 750–1000 m) at St. K2 (47° N, 160° E, 5230 m depth, immediately preserved with 4% buffered formalin seawater. At each sampling occasion, Figure 2), located in the western subarctic Pacific on 29 October 2010, 26 February, 22–23 April, and 3–4 July 2011 (Table 1). After collection, zooplankton samples were immedi- ately preserved with 4% buffered formalin seawater. At each sampling occasion, environ- mental data such as water temperature, salinity, dissolved oxygen (DO), and chlorophyll a (Chl. a) fluorescence were measured by fluorometer and DO-sensor mounted CTD (SBE Oceans 2023, 4 244 Oceans 2023, 4, FOR PEER REVIEW 3 environmental data such as water temperature, salinity, dissolved oxygen (DO), and chloro- phyll a (Chl. a) fluorescence were measured by fluorometer and DO-sensor mounted 911 plus; Sea-Bird Electronics Inc., Bellevue, WA, USA). The details of the environmental CTD (SBE 911 plus; Sea-Bird Electronics Inc., Bellevue, WA, USA). The details of the data and zooplankton biomass have been published elsewhere [27]. environmental data and zooplankton biomass have been published elsewhere [27]. Figure 2. Location of sampling station K2 (47 N, 160 E) in the western subarctic Pacific. The Figure 2. Location of sampling station K2 (47° N, 160° E) in the western subarctic Pacific. The ap- approximate positions of the currents are superimposed [32]. proximate positions of the currents are superimposed [32]. Table 1. Zooplankton samplings (eight vertical stratification samplings between 0–1000 m) at St. K2 Table 1. Zooplankton samplings (eight vertical stratification samplings between 0–1000 m) at St. K2 in the western subarctic Pacific gyre. D: day, N: night. in the western subarctic Pacific gyre. D: day, N: night. Season Sampling Date Local Time (Day/Night) Season Sampling Date Local Time (Day/Night) 29 October 2010 12:09–13:52 (D) Autumn 29 October 2010 12:09–13:52 (D) 29 October 2010 22:09–23:38 (N) Autumn 26 February 2011 12:35–14:41 (D) 29 October 2010 22:09–23:38 (N) Winter 26 February 2011 22:01–23:56 (N) 26 February 2011 12:35–14:41 (D) 22 April 2011 21:59–23:56 (N) Winter Spring 23 April 26 Februa 2011 ry 2011 12:45–14:37 22 (D) :01–23:56 (N) 3 July 2011 12:05–13:55 (D) 22 April 2011 21:59–23:56 (N) Summer 3–4 July 2011 22:51–0:55 (N) Spring 23 April 2011 12:45–14:37 (D) 3 July 2011 12:05–13:55 (D) 2.2. Sample Analysis Summer 3–4 July 2011 22:51–0:55 (N) In the land laboratory, hydrozoans were sorted from the sub-samples divided at 1/2–1/64 according to the amount of samples. Bell height (BH) and gonad length (GL) of A. digitale, the numerically and biomass-dominated hydrozoans, were measured at a 2.2. Sample Analysis precision of 0.05 mm by using an eyepiece micrometer under a stereomicroscope (Figure 1). In the land laboratory, hydrozoans were sorted from the sub-samples divided at 1/2– Individuals with more than 10% GL in BH were treated as mature individuals [7,12,16]. 1/64 according to the amount of samples. Bell height (BH) and gonad length (GL) of A. As an index of the vertical distribution, the depth of the population center (D ) was 50% digitale, the numerically and biomass-dominated hydrozoans, were measured at a preci- calculated using the following formula [30,33]. sion of 0.05 mm by using an eyepiece micrometer under a stereomicroscope (Figure 1). 50 p Individuals with more than D 10%= Gd L in + BH w d  ere treated as mature individuals [7,12,16]. 50% 1 As an index of the vertical distribution, the depth of the population center (D50%) was calculated using the following formula [30,33]. 50𝑝 𝐷 𝑑 𝑑 where d1 is the depth (m) of the upper depth of the 50% individual occurrence layer, d2 is the sampling depth interval (m) of the 50% individual occurrence layer, p1 is the cumula- tive individual percentage (%) that occurred at depths shallower than the 50% individual occurrence layer, and p2 is the individual percentage (%) at the 50% individual occurrence Oceans 2023, 4 245 Oceans 2023, 4, FOR PEER REVIEW 4 where d is the depth (m) of the upper depth of the 50% individual occurrence layer, d is 1 2 the sampling depth interval (m) of the 50% individual occurrence layer, p is the cumulative layer. Day-night differences in vertical distributions on each collection date were tested individual percentage (%) that occurred at depths shallower than the 50% individual by the Kolmogorov-Smirnov test. occurrence layer, and p is the individual percentage (%) at the 50% individual occurrence BH of A. digitale was expressed by histograms based on the integrated abundance layer. Day-night differences in vertical distributions on each collection date were tested by −2 the Kolmogorov-Smirnov test. (ind. m ) at 0–1000 m water column for the day and night of each sampling date. The BH of A. digitale was expressed by histograms based on the integrated abundance depth composition of each BH interval (1 mm) was also calculated. (ind. m ) at 0–1000 m water column for the day and night of each sampling date. The depth composition of each BH interval (1 mm) was also calculated. 3. Results 3.1. Hydrography 3. Results 3.1. Hydr Vertography ical distributions of temperature, salinity, dissolved oxygen, and fluorescence at each sampling date are shown in Figure 3. Throughout the season, the temperature was Vertical distributions of temperature, salinity, dissolved oxygen, and fluorescence −1 at 0.7–8.5 °C, salinity for 32.5–34.5, DO ranged between 0.6 and 10.4 mg L , and fluores- at each sampling date are shown in Figure 3. Throughout the season, the temperature was cence w at 0.7–8.5 as 0.02– C, 2.3 salinity 2. Seaso for nal 32.5–34.5, thermoclDO ine dev ranged elopbetween ed around 0.6 5 and 0 m10.4 in Ju mg ly and L , Oct andober, fluor and tempera escence was tures w 0.02–2.32. ere almost consta Seasonal thermocline nt for 100 m developed in February a around nd April 50 m. For in July all sea and sons, October, and temperatures were almost constant for 100 m in February and April. For temperature showed a minimum of 1–2 °C approximately at 100 m, then had a maximum all seasons, temperature showed a minimum of 1–2 C approximately at 100 m, then had of about 3.5 °C around 200 m, and finally decreased with increasing depth. Salinity in- a maximum of about 3.5 C around 200 m, and finally decreased with increasing depth. creased with depth for all seasons. Salinity was similar for depths below 100 m in February Salinity increased with depth for all seasons. Salinity was similar for depths below 100 m and April, while was below 33 at <50 m, forming surface halocline in July and October. in February and April, while was below 33 at <50 m, forming surface halocline in July and −1 DO decreased with increasing depth and was extremely low, less than 2 mg L below 200 October. DO decreased with increasing depth and was extremely low, less than 2 mg L m depth. Fluorescence was high at the surface layer above the thermocline (<50 m) in July below 200 m depth. Fluorescence was high at the surface layer above the thermocline and October and at 0–100 m in February and April. (<50 m) in July and October and at 0–100 m in February and April. Fluorescence 024 68 10 12 0 2468 10 12 02 468 10 12 024 68 10 12 -1 DO(mg L ) 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 Temperature (℃) 024 68 0 2468 0 246 8 0 2468 Salinity 32.5 33.0 33.5 34.0 34.5 32.5 33.0 33.5 34.0 34.5 32.5 33.0 33.5 34.0 32.5 33.0 33.5 34.0 34.5 34.5 29 Oct. 2010 26 Feb. 2011 22 Apr. 2011 3 July 2011 Figure 3. Vertical distribution of temperature, salinity, dissolved oxygen, and fluorescence at St. K2 Figure 3. Vertical distribution of temperature, salinity, dissolved oxygen, and fluorescence at St. K2 in the subarctic Pacific gyre on four occasions from October 2010 to July 2011. Note that the vertical in the subarctic Pacific gyre on four occasions from October 2010 to July 2011. Note that the vertical scale (depth) is in the logscale. scale (depth) is in the logscale. 3.2. Aglantha digitale 3.2. Aglantha digitale Hydrozoans occurred in the western subarctic Pacific throughout the year. A. digitale Hydrozoans occurred in the western subarctic Pacific throughout the year. A. digitale was the most abundant species, with an annual mean abundance of 198.4 ind. m at −2 was the most abundant species, with an annual mean abundance of 198.4 ind. m at 0– 0–1000 m water column, composed of 91.9% of hydrozoan abundance (Table 2). 1000 m water column, composed of 91.9% of hydrozoan abundance (Table 2). The day-night vertical distribution and D50% of A. digitale at each sampling date are shown in Figure 4. The vertical distribution of A. digitale was concentrated at 0–200 m both day and night for most seasons. While in October, the certain population density was seen to extend below 300 m both day and night. The highest population density of A. digitale −3 was 1.36 ind. m at 100–150 m depth during a night in February. D50% of A. digitale was at Depth (m) Oceans 2023, 4, FOR PEER REVIEW 5 26–129 m depth through day and night of all seasons. Diel change in vertical distribution was observed in July, with significantly shallower depths at night (p < 0.05). Histograms on BH of A. digitale and their vertical distribution composition both day and night at each sampling date are shown in Figure 5. The BH of A. digitale ranged be- tween 2.4 and 18.9 mm. In October and February, the most numerous individuals were seen for the BH at 8–16 mm both day and night. On the other hand, two modes of BH at 3–5 mm and 8–17 mm were observed for both day and night in April. In July, the majority of individuals was at the BH in 8–17 mm both day and night. Most of the mature speci- mens, GL composed >10% of the BH, occurred only in July. The BH of the mature individ- uals ranged from 4.7 to 17.6 mm, with most of them was at >10 mm. Concerning the vertical distribution composition of each BH of A. digitale, the distri- Oceans 2023, 4 246 bution below 300 m was seen in October for all BH sizes, indicating that the extension of vertical distribution down to the deeper layer was a typical feature of all BH ranges (Fig- ure 5). In February, the modal BH individuals at 8–16 mm BH were distributed near the Table 2. Annual mean standing stocks of cnidarian species for 0–1000 m water column at St. K2 in surface both day and night, while other smaller and larger individuals were distributed the western subarctic Pacific from October 2010 to July 2011. Values are mean  SD. at deeper layers. In April, small individuals with BH < 6 mm were distributed below 300 Standing Stock m, while most the individuals with a BH > 12 mm were distributed below 100 m. In July, Family Species (ind. m ) (%) individuals with BH smaller than 6 mm were distributed at >200 m, but at night, the main individuals with BH betwAglantha een 8 an digitale d 16 mm were concentrated for the surface layer at 0– Rhopalonematidae 198.4  107.8 91.9 Muller, 1776 50 m. Other Cnidaria (including fragments difficult 17.4  10.1 8.1 to make species identification) Table 2. Annual mean standing stocks of cnidarian species for 0–1000 m water column at St. K2 in the western subarctic Pacific from October 2010 to July 2011. Values are mean ± SD. The day-night vertical distribution and D of A. digitale at each sampling date are 50% Standing Stock shown in Figure 4. The vertical distribution of A. digitale was concentrated at 0–200 m both Family Species −2 (ind. m ) (%) day and night for most seasons. While in October, the certain population density was seen to extend below 300 mAgl both antday ha di and gitanight. le Muller The , highest population density of A. digitale Rhopalonematidae 198.4 ± 107.8 91.9 was 1.36 ind. m at 100–150 m depth during a night in February. D of A. digitale was at 1776 50% 26–129 m depth through day and night of all seasons. Diel change in vertical distribution Other Cnidaria (including fragments difficult to make species identification) 17.4 ± 10.1 8.1 was observed in July, with significantly shallower depths at night (p < 0.05). Figure 4. Day (open) and night (solid) vertical distribution of Aglatha digitale at St. K2 in the western Figure 4. Day (open) and night (solid) vertical distribution of Aglatha digitale at St. K2 in the subarctic Pacific gyre during four sampling occasions (October 2010, February, April, and July 2011). western subarctic Pacific gyre during four sampling occasions (October 2010, February, April, and Distribution cores (D50%) are shown by the triangles. Diel changes were tested by the Kolmogorov- July 2011). Distribution cores (D ) are shown by the triangles. Diel changes were tested by the 50% Smirnov test (*: p < 0.05). Kolmogorov-Smirnov test (*: p < 0.05). Histograms on BH of A. digitale and their vertical distribution composition both day and night at each sampling date are shown in Figure 5. The BH of A. digitale ranged between 2.4 and 18.9 mm. In October and February, the most numerous individuals were seen for the BH at 8–16 mm both day and night. On the other hand, two modes of BH at 3–5 mm and 8–17 mm were observed for both day and night in April. In July, the majority of individuals was at the BH in 8–17 mm both day and night. Most of the mature specimens, GL composed >10% of the BH, occurred only in July. The BH of the mature individuals ranged from 4.7 to 17.6 mm, with most of them was at >10 mm. Oceans 2023, 4, FOR PEER REVIEW 6 Oceans 2023, 4 247 Figure 5. Histograms on bell heights of Aglantha digitale integrated over 0–1000 m water column Figure 5. Histograms on bell heights of Aglantha digitale integrated over 0–1000 m water column at at St. K2 in the western subarctic Pacific gyre during the day (upper) and night (lower) of the four St. K2 in the western subarctic Pacific gyre during the day (upper) and night (lower) of the four sampling occa sampling occasions sions (O (October ctober 22010, 010, February, February, April, April, and June 2011). Depth and June 2011). Depth distribution distribution compositions compositions within the eight depth strata of 0–1000 m water column is also shown for each panel. within the eight depth strata of 0–1000 m water column is also shown for each panel. Concerning the vertical distribution composition of each BH of A. digitale, the distri- 4. Discussion bution below 300 m was seen in October for all BH sizes, indicating that the extension 4.1. Abundance of A. digitale of vertical distribution down to the deeper layer was a typical feature of all BH ranges At St. K2, A. digitale was the predominant hydrozoan, accounting for more than 90% (Figure 5). In February, the modal BH individuals at 8–16 mm BH were distributed near of the hydro the surfacez both oan day abun and dan night, ce (Tab while le 2). other A. dismaller gitale is and a co lsmopolitan arger individuals species wer w e idistributed dely distrib- uted at deeper at high layers. latitude In are Apr ail, s in t small he Nort individuals hern Hem with isp BH here [ < 6 2 mm ,4,13] wer . In eform distributed ation obelow n abun- 300 m, while most the individuals with a BH > 12 mm were distributed below 100 m. In dance, BH, BH of mature specimens, and generation time of A. digitale reported from var- July, individuals with BH smaller than 6 mm were distributed at >200 m, but at night, the ious locations are summarized in Table 3. In the present study, the abundance of A. digitale main individuals with BH between 8 and −2 16 mm were concentrated for the surface layer at ranged between 58.5 and 391.1 ind. m for the 0–1000 m water column. This value well 0–50 m. −2 corresponds with the values reported in the subarctic Pacific (368 ind. m ) [10] and the −2 northeastern North Pacific (38–221 ind. m ) [11]. As for the marginal areas of the western 4. Discussion −2 subarctic Pacific, values in the Oyashio region during spring (16–316 ind. m ) [8] and val- 4.1. Abundance of A. digitale −2 ues based on the annual sampling in the Oyashio region (55–896 ind. m ) [7] are also At St. K2, A. digitale was the predominant hydrozoan, accounting for more than 90% of comparable. For the areas with similar values of A. digitale abundance in this study (<100 the hydrozoan abundance (Table 2). A. digitale is a cosmopolitan species widely distributed −2 ind. m ), the Norwegian fj ords (Korsfj ord and Fanafj ord) [14] and the Arctic Ocean [15] at high latitude areas in the Northern Hemisphere [2,4,13]. Information on abundance, BH, −2 are available. On the other hand, high abundances of A. digitale over 1000 ind. m have BH of mature specimens, and generation time of A. digitale reported from various locations −2 been reported for Toyama Bay in the southern Japan Sea (maximum: 4427 ind. m ) [12], are summarized in Table 3. In the present study, the abundance of A. digitale ranged between −2 −2 the Irish coast in the North Atlantic (5350 ind. m ) [18] and the White Sea (5000 ind. m ) 58.5 and 391.1 ind. m for the 0–1000 m water column. This value well corresponds with [19] (Table 3). A characteristic of these regions is the semi-enclosed embayment having a the values reported in the subarctic Pacific (368 ind. m ) [10] and the northeastern North Pacific (38–221 ind. m ) [11]. As for the marginal areas of the western subarctic Pacific, limiting water exchange with the outer region. These facts suggest that the semi-enclosed values in the Oyashio region during spring (16–316 ind. m ) [8] and values based on the area may have maintained a higher population of A. digitale without transportation by annual sampling in the Oyashio region (55–896 ind. m ) [7] are also comparable. For flushing discharge caused by the ocean currents. In summary, the abundance of A. digitale the areas with similar values −2 of A. digitale abundance in this study (<100 ind. m ), the is less than 1000 ind. m for the oceanic open area where the current transport would Norwegian fjords (Korsfjord and Fanafjord) [14] and the Arctic Ocean [15] are available. prevent to accumulation of high density/abundance. While in the semi-enclosed embay- On the other hand, high abundances of A. digitale over 1000 ind. m have been reported −2 ment condition, A. digitale can maintain high density/abundance (>5000 ind. m ) under for Toyama Bay in the southern Japan Sea (maximum: 4427 ind. m ) [12], the Irish coast low flushing and transport to the other region. 2 2 in the North Atlantic (5350 ind. m ) [18] and the White Sea (5000 ind. m ) [19] (Table 3). A characteristic of these regions is the semi-enclosed embayment having a limiting water exchange with the outer region. These facts suggest that the semi-enclosed area may have Oceans 2023, 4 248 maintained a higher population of A. digitale without transportation by flushing discharge caused by the ocean currents. In summary, the abundance of A. digitale is less than 1000 ind. m for the oceanic open area where the current transport would prevent to accumulation of high density/abundance. While in the semi-enclosed embayment condition, A. digitale can maintain high density/abundance (>5000 ind. m ) under low flushing and transport to the other region. Table 3. Regional comparison on abundance, bell height, and generation length of Aglantha digitale from worldwide ocean. Sampling Bell Height (mm) Generation Abundance Region Reference 2 1 Length (year ) (ind. m ) Season Depth (m) Range Mature Toyama Bay, Annual 0–500 73–4427 1–17 6–17 2 [12] southern Japan Sea Eastern/Western Summer 0–150 0–368 – 8.5–15.2 – [10] subarctic Pacific Oyashio region Annual 0–2000 55–896 1–23 11–23 1 [7] Oyashio region Spring <200 16–316 4–18 – 1 [8] northeastern North Summer 0–150 38–221 0.6–17 1.1–16 – [11] Pacific Northern Pacific Summer <200 – 5–20 15< 1 [9] Southern Irish Summer 0–25 <5350 – – – [18] coastal water Northeast Atlantic Autumn/winter 0–100 – 1–18 – – [17] Ocean Korsfjord and Annual 0–640 156–358 – – 2 [14] Fanafjord White Sea Annual 0–100 5–5000 – 8–12 1 [19] High-Arctic coastal Annual 0–180 <720 – – – [15] Western Subarctic Annual 0–1000 58.5–391.1 2.4–18.9 4.7–17.6 1 This study Pacific (K2) 4.2. Vertical Distribution of A. digitale Vertical distribution of A. digitale was concentrated at <200 m for most seasons. Season- ally, diel changes in vertical distribution were seen in July when the thermocline developed, and deeper distribution (>300 m) was observed in October (Figure 5). In July, it should be noted that the day-night differences in abundance were substantially low at night and no size fraction less than 8 mm at night-histogram. It can be concluded that there is a spatial horizontal heterogeneity in the distribution of medusae. While diel changes in vertical distribution were denied in this study, nocturnal ascent diel vertical migration of A. digitale has also been reported from the Saanich Inlet off Vancouver [9]. The deepening vertical distribution of A. digitale has also been reported in the fjords of Svalbard from August to October [15]. These findings correspond with the results of this study. As a new finding of this study, the depth distribution at each BH was determined with season and day/night. Small individuals (<6 mm BH) were distributed for the deep layers or extremely shallower depths in all seasons (Figure 5). These facts suggest that small individuals with less swimming ability could be easily transported vertically from the vertical mixing and diffusion of water masses. Swimming behaviors of six hydrozoan species, including A. digitale, are highly varied with species, and A. digitale is considered to be a jet-swimming species [24,34]. Within the three hydrozoan species applying jet-swimming, A. digitale is the smallest body size and has the longest jet interval in time [24]. These facts indicate that A. digitale is most affected by vertical and horizontal water diffusion, especially for their small-sized specimen, which has less swimming ability. These low swimming abilities of the small individuals of A. digitale would be difficult to stay in a stable layer because of the vulnerability of the diffusion of the water masses. It induces an extremely shallower or deeper distribution of them. Oceans 2023, 4 249 The main prey item of A. digitale is reported to be small copepods such as Pseudo- calanus [20,22,24]. For Pseudocalanus in the western subarctic Pacific, two species: P. minutus and P. newmani are present [35]. Within them, P. minutus accumulates lipids in their body and is known to have a resting (diapausing) stage at the deep layer during its life history, and their descent to deep-sea achieved summer to autumn [35,36]. Since the diapausing P. minutus at the deep layer contains much lipids, their nutrition values would be high, and the swimming behavior of dormant copepods is reduced to maintain a low metabolic rate [37,38]. These characteristics of the deep-sea dormant P. minutus (small body size, high nutritional value, and low swimming behavior) suggest that they are a sufficient prey item for A. digitale. Thus, the extension of the vertical distribution of A. digitale to the deep layer during October can be explained from viewpoint of their food availability (e.g., to capture nutrient-rich P. minutus distributing deep layer during these seasons). 4.3. Population Structure and Body Size of A. digitale The BH range of A. digitale observed in this study (2.4–18.9 mm) well corresponds to those reported in Toyama Bay in the southern Japan Sea [12], in the spring Oyashio region [8], in the northeastern North Pacific [11], and in the northeastern North Atlantic [17] (Table 3). It should be noted that most of the listed studies applied similar mesh sizes to this study (200–335 m); thus, differences in the applied mesh size would be negligible. Concerning BH, large BH (up to 20 mm) have been reported from the Saanich Inlet off Vancouver and annual observations in the Oyashio region [7,9]. For such a subarctic coastal area, the abundance of small copepods, the primary prey of A. digitale, has been reported to be high [39]. These facts suggest that favorable food conditions would be an important factor in achieving large body sizes of A. digitale. The minimum maturation size of A. digitale: 6 mm BH has been reported in Toyama Bay, southern Japan Sea [12]. Such a small mature specimen of A. digitale (8–12 mm BH) has also been reported in the White Sea [19]. Common characteristics of these areas with small maturation sizes of A. digitale are that these areas are semi-enclosed seas having high abundances of them (>1000 ind. m ) (Table 3). The feeding mode of A. digitale is basically carnivorous [13,20,23,24]. The energy transfer for such a higher trophic level organism is considered to be higher in the areas where the marine ecosystems are composed of simply limited species [40,41]. The regions where high abundance and small maturation body size of A. digitale Toyama Bay and the White Sea are characterized by semi-enclosed seas, having such high energy transfer efficiency food web and marine ecosystem structures composed by the limited species [12,19]. Thus, in the areas where the marine ecosystem is composed of the simple species structure and high energy transfer efficiency to the higher trophic level organisms, abundance of A. digitale would be high, and they may mature at smaller body-sizes. In this study, the observed minimum maturation size of A. digitale was small as 4.7 mm, while most of the mature specimens were at BH over 10 mm (Figure 5). These facts suggest that the few small body-sized mature individuals are considered to be transported to the oceanic St. K2 from the marginal areas, such as the Aleutian Islands or the Okhotsk Sea. In this study, one or two cohorts were identified for BH of A. digitale on each sampling date (Figure 5). while because of the scarce sampling occasions (four times per year), it was difficult to trace the growth of each cohort. For the developmental stages, mature specimens only occurred in July (Figure 5). These facts suggest that the life history of A. digitale is a one-year generation length having reproduction in summer for the western subarctic Pacific. Concerning the life span of A. digitale, one or two generations per year have been reported in the Oyashio region [7,8], Toyama Bay in the southern Japan Sea [12], Saanich Inlet off Vancouver [9], Norwegian fjords [14], and the White Sea [19] (Table 3). Thus, the generation time in this study, one year, is an ordinary generation length for A. digitale in the open oceanic region. On the other hand, two generations per year of A. digitale have been reported for Toyama Bay in the southern Japan Sea and Norwegian fjords (Table 3). These regions are Oceans 2023, 4 250 semi-enclosed seas where the energy transfer efficiency to the higher trophic level organisms is expected to be high. Thus, the abundance, maturation body size, and generation length of A. digitale would be related and determined by the component organisms in the marine ecosystem in each region. In semi-enclosed seas composed of the simple species group, because of the high energy transfer to hydrozoans A. digitale, they may have high abundance and small maturation sizes, which implies a shorter generation time. Thus, two generations per year of A. digitale have seen such areas [12,24]. The major reproductive period summer observed in this study is also consistent with the life history of this species in the adjacent Oyashio region [7]. In these regions, summer is the season when copepods, the main prey of A. digitale, reaches annual peak abundance at the surface layer [35,39]. It is interpreted that A. digitale may mature and have reproduction under sufficient food conditions during the summer season. Author Contributions: Conceptualization, M.A. and A.Y.; methodology, M.A. and A.Y.; software, M.A.; validation, M.A. and A.Y.; formal analysis, M.A.; investigation, M.A.; resources, M.A.; data curation, A.Y.; writing—original draft preparation, T.G.; writing—review and editing, A.Y.; visualiza- tion, T.G.; supervision, A.Y.; project administration, A.Y.; funding acquisition, A.Y. All authors have read and agreed to the published version of the manuscript. Funding: Part of this study was supported by Grant-in-Aid for Challenging Research (Pioneering) 20K20573, Scientific Research 22H00374 (A), 20H03054 (B), 19H03037 (B), and 17H01483 (A) from the Japan Society for the Promotion of Science (JSPS). This study was partially supported by the Arctic Challenge for Sustainability II (ArCS II; JPMXD1420318865) and the Environmental Research and Technology Development Fund (JPMEERF20214002) of the Environmental Restoration and Conservation Agency of Japan. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Data will be available from request to the corresponding author. Acknowledgments: We thank the captains, officers, crews, and researchers onboard the R/V Mirai, JAMSTEC, for their great efforts during the field sampling. Conflicts of Interest: The authors declare no conflict of interest. References 1. Arai, M.N. Pelagic coelenterates and eutrophication: A review. Hydrobiologia 2001, 451, 69–87. [CrossRef] 2. Purcell, J.E. Climate effects on formation of jellyfish and ctenophore blooms: A review. J. Mar. Biol. Assoc. U. K. 2005, 85, 461–476. [CrossRef] 3. Purcell, J.E. 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Seasonal Changes in Vertical Distribution and Population Structure of the Dominant Hydrozoan Aglantha digitale in the Western Subarctic Pacific

Aizawa, Mari; Gao, Tian; Yamaguchi, Atsushi
Oceans , Volume 4 (3) – Jul 31, 2023
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Article Seasonal Changes in Vertical Distribution and Population Structure of the Dominant Hydrozoan Aglantha digitale in the Western Subarctic Pacific 1 1 1 , 2 , Mari Aizawa , Tian Gao and Atsushi Yamaguchi * Graduate School of Fisheries Sciences, Hokkaido University, 3–1–1 Minato-cho, Hakodate 041-8611, Hokkaido, Japan; [email protected] (M.A.); [email protected] (T.G.) Arctic Research Center, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo 001-0021, Hokkaido, Japan * Correspondence: a-yama@fish.hokudai.ac.jp Abstract: Hydrozoans are numerically dominant taxa in gelatinous zooplankton communities of the worldwide oceans and play an energy transfer role connecting primary producers and higher trophic level organisms. In the western subarctic Pacific, St. K2 has been established as a long-term time- series monitoring station. Various studies on zooplankton have been conducted, while hydrozoans have not been treated. This study presents the abundance, vertical distribution, and population structure of the dominant hydrozoan species (Aglantha digitale) at St. K2. Samples collected by vertical stratification samplings from eight layers of 0–1000 m both day and night during four seasons in one year. Hydrozoans occur throughout the year. The annual mean abundance of A. digitale was 198.4 ind. m and composed of 91.9% of hydrozoans. The vertical distribution of A. digitale was concentrated for the epipelagic layer (0–200 m), both day and night of the most season. The bell height (BH) of A. digitale ranged between 2.4–18.9 mm. Most of the mature individuals, with gonad length larger than 10% of BH, occurred only in July. The BH of mature individuals ranged from 4.7 to 17.6 mm, with the BH of most mature individuals were larger than >10 mm. Through observation on BH at each sampling layer, small individuals with BH < 6 mm were distributed below 300 m depths throughout the seasons, expanding their vertical distribution to the deeper layers. Inter-region comparison of Citation: Gao, T.; Aizawa, M.; abundance, maturation body size, and generation length of A. digitale revealed that these parameters Yamaguchi, A. Seasonal Changes in are varied with the region and depend on the marine ecosystem structures. Vertical Distribution and Population Structure of the Dominant Keywords: hydrozoa; Aglantha digitale; abundance; population structure; life cycle Hydrozoan Aglantha digitale in the Western Subarctic Pacific. Oceans 2023, 4, 242–252. https:// doi.org/10.3390/oceans4030017 1. Introduction Academic Editors: Antonio Bode and From worldwide oceans, hydrozoans are numerically dominant taxa in gelatinous Sam Dupont zooplankton communities, feed on small zooplankton and serve as food for fishes, and Received: 26 April 2023 act as mediators transporting energy between primary producers and higher trophic level Revised: 7 June 2023 organisms [1]. Recent climate changes (North Atlantic Oscillation, North Pacific Decadal Accepted: 20 July 2023 Oscillation, El Nino, etc.) have had a significant impact on standing stocks of jellyfish Published: 31 July 2023 in worldwide oceans, and may increase the duration of occurrence of hydrozoans in the temperate to subarctic regions [2]. This increase in hydrozoans is predicted to alter the bal- ance of prey-predator relationships in marine ecosystems, with significant effects on lower and higher trophic-level organisms [3,4]. On the other hand, the chemical compositions of Copyright: © 2023 by the authors. hydrozoans are characterized by low carbon but high nitrogen and phosphorus contents, Licensee MDPI, Basel, Switzerland. and their outbreak affects the nutrient balance (C:N:P ratio) of the marine ecosystem, and This article is an open access article the decomposition of their carcasses by bacteria has a significant impact on the marine distributed under the terms and mineral cycles [5,6]. conditions of the Creative Commons In the Northern Hemisphere, Aglantha digitale is the most abundant hydrozoan in Attribution (CC BY) license (https:// both abundance and biomass at high latitudes [1]. A. digitale has been reported as the creativecommons.org/licenses/by/ most dominant hydrozoan species in the western subarctic Pacific [7,8], eastern subarctic 4.0/). Oceans 2023, 4, 242–252. https://doi.org/10.3390/oceans4030017 https://www.mdpi.com/journal/oceans Oceans 2023, 4, FOR PEER REVIEW 2 dominant hydrozoan species in the western subarctic Pacific [7,8], eastern subarctic Pacific [9], northern North Pacific [10], western Arctic Ocean [11], Toyama Bay in the southern Japan Sea [12], Norwegian fj ords and Svalbard Islands [13–15], eastern North Atlantic Oceans 2023, 4 243 [16,17], Irish Sea [18], and White Sea [19,20]. As the ecology of A. digitale, feeding mecha- nisms [21,22], feeding impact [13,20,23], and swimming behavior [24] have been reported. Pacific [9], northern North Pacific [10], western Arctic Ocean [11], Toyama Bay in the For life histories, there have been reports from various oceans, including the Oyashio re- southern Japan Sea [12], Norwegian fjords and Svalbard Islands [13–15], eastern North gion [7,8], the eastern subarctic Pacific [9], Toyama Bay [12], the western North Atlantic Atlantic [16,17], Irish Sea [18], and White Sea [19,20]. As the ecology of A. digitale, feeding [16], the Norwegian fj ords [14], and the White Sea [19]. mechanisms [21,22], feeding impact [13,20,23], and swimming behavior [24] have been In the western subarctic Pacific, St. K2 has been set as a long-term time-series station reported. For life histories, there have been reports from various oceans, including the Oyashio to monitor v region a [7 rious bio ,8], the eastern geocsubar hemical p ctic Pacific arameters [9], Toyama [25]. Bay As t [12 h ],e the info western rmation on North hydrozoans at Atlantic [16], the Norwegian fjords [14], and the White Sea [19]. St. K2 bimodal vertical distribution with peaks at 0–50 m and 200–300 m, with a minimum In the western subarctic Pacific, St. K2 has been set as a long-term time-series station at 150–200 m, and no day/night differences in abundance have been reported [26]. At St. to monitor various biogeochemical parameters [25]. As the information on hydrozoans at K2, there are several studies on zooplankton [27–31], but no specific studies on hydrozo- St. K2 bimodal vertical distribution with peaks at 0–50 m and 200–300 m, with a minimum ans are available. Despite their importance on the lower and higher trophic level organ- at 150–200 m, and no day/night differences in abundance have been reported [26]. At St. K2, there are several studies on zooplankton [27–31], but no specific studies on hydrozoans isms and material transport, information on hydrozoans in this area are currently scarce. are available. Despite their importance on the lower and higher trophic level organisms This study conducted abundance, vertical distribution, and population structure of and material transport, information on hydrozoans in this area are currently scarce. the dominant hydrozoans (A. digitale) at St. K2 in the western subarctic Pacific using for- This study conducted abundance, vertical distribution, and population structure of the malin-preserved samples collected from day and night vertically stratified samplings be- dominant hydrozoans (A. digitale) at St. K2 in the western subarctic Pacific using formalin- pr tw eserved een 0–1 samples 000 m collected covering f from our sea day and sons night of one vertically yearstratified . As new sampling scientifi sc between information, seasonal 0–1000 m covering four seasons of one year. As new scientific information, seasonal and and day-night changes in bell height (BH, Figure 1) and gonad maturation at each sam- day-night changes in bell height (BH, Figure 1) and gonad maturation at each sampling pling depth down to 1000 m have been evaluated. The results were compared with the depth down to 1000 m have been evaluated. The results were compared with the same same species in the various regions of high-latitude waters of the Northern Hemisphere. species in the various regions of high-latitude waters of the Northern Hemisphere. Figure Figure 1. 1. Pictur Pictu e on re on specimen specimens of Aglantha s of Aglantha digitale digitale (left) and their (left meas ) and ur their measu ed body parts:rbell ed body parts height : bell height (BH) and gonad length (GL) (right). (BH) and gonad length (GL) (right). 2. Materials and Methods 2. Materials and Methods 2.1. Field Sampling Day and night vertically stratified zooplankton samplings were made by oblique 2.1. Field Sampling tow of Intelligent Operative Net Sampling System (IONESS, SEA Co., Ltd., Bristol, UK) Day and night vertically stratified zooplankton samplings were made by oblique tow equipped 335 m mesh and 1.5 m mouth area, from eight layers (0–50, 50–100, 100–150, of Intelligent Operative Net Sampling System (IONESS, SEA Co., Ltd., Bristol, UK) 150–200, 200–300, 300–500, 500–750, 750–1000 m) at St. K2 (47 N, 160 E, 5230 m depth, equipped 335 µm mesh and 1.5 m mouth area, from eight layers (0–50, 50–100, 100–150, Figure 2), located in the western subarctic Pacific on 29 October 2010, 26 February, 22–23 April, and 3–4 July 2011 (Table 1). After collection, zooplankton samples were 150–200, 200–300, 300–500, 500–750, 750–1000 m) at St. K2 (47° N, 160° E, 5230 m depth, immediately preserved with 4% buffered formalin seawater. At each sampling occasion, Figure 2), located in the western subarctic Pacific on 29 October 2010, 26 February, 22–23 April, and 3–4 July 2011 (Table 1). After collection, zooplankton samples were immedi- ately preserved with 4% buffered formalin seawater. At each sampling occasion, environ- mental data such as water temperature, salinity, dissolved oxygen (DO), and chlorophyll a (Chl. a) fluorescence were measured by fluorometer and DO-sensor mounted CTD (SBE Oceans 2023, 4 244 Oceans 2023, 4, FOR PEER REVIEW 3 environmental data such as water temperature, salinity, dissolved oxygen (DO), and chloro- phyll a (Chl. a) fluorescence were measured by fluorometer and DO-sensor mounted 911 plus; Sea-Bird Electronics Inc., Bellevue, WA, USA). The details of the environmental CTD (SBE 911 plus; Sea-Bird Electronics Inc., Bellevue, WA, USA). The details of the data and zooplankton biomass have been published elsewhere [27]. environmental data and zooplankton biomass have been published elsewhere [27]. Figure 2. Location of sampling station K2 (47 N, 160 E) in the western subarctic Pacific. The Figure 2. Location of sampling station K2 (47° N, 160° E) in the western subarctic Pacific. The ap- approximate positions of the currents are superimposed [32]. proximate positions of the currents are superimposed [32]. Table 1. Zooplankton samplings (eight vertical stratification samplings between 0–1000 m) at St. K2 Table 1. Zooplankton samplings (eight vertical stratification samplings between 0–1000 m) at St. K2 in the western subarctic Pacific gyre. D: day, N: night. in the western subarctic Pacific gyre. D: day, N: night. Season Sampling Date Local Time (Day/Night) Season Sampling Date Local Time (Day/Night) 29 October 2010 12:09–13:52 (D) Autumn 29 October 2010 12:09–13:52 (D) 29 October 2010 22:09–23:38 (N) Autumn 26 February 2011 12:35–14:41 (D) 29 October 2010 22:09–23:38 (N) Winter 26 February 2011 22:01–23:56 (N) 26 February 2011 12:35–14:41 (D) 22 April 2011 21:59–23:56 (N) Winter Spring 23 April 26 Februa 2011 ry 2011 12:45–14:37 22 (D) :01–23:56 (N) 3 July 2011 12:05–13:55 (D) 22 April 2011 21:59–23:56 (N) Summer 3–4 July 2011 22:51–0:55 (N) Spring 23 April 2011 12:45–14:37 (D) 3 July 2011 12:05–13:55 (D) 2.2. Sample Analysis Summer 3–4 July 2011 22:51–0:55 (N) In the land laboratory, hydrozoans were sorted from the sub-samples divided at 1/2–1/64 according to the amount of samples. Bell height (BH) and gonad length (GL) of A. digitale, the numerically and biomass-dominated hydrozoans, were measured at a 2.2. Sample Analysis precision of 0.05 mm by using an eyepiece micrometer under a stereomicroscope (Figure 1). In the land laboratory, hydrozoans were sorted from the sub-samples divided at 1/2– Individuals with more than 10% GL in BH were treated as mature individuals [7,12,16]. 1/64 according to the amount of samples. Bell height (BH) and gonad length (GL) of A. As an index of the vertical distribution, the depth of the population center (D ) was 50% digitale, the numerically and biomass-dominated hydrozoans, were measured at a preci- calculated using the following formula [30,33]. sion of 0.05 mm by using an eyepiece micrometer under a stereomicroscope (Figure 1). 50 p Individuals with more than D 10%= Gd L in + BH w d  ere treated as mature individuals [7,12,16]. 50% 1 As an index of the vertical distribution, the depth of the population center (D50%) was calculated using the following formula [30,33]. 50𝑝 𝐷 𝑑 𝑑 where d1 is the depth (m) of the upper depth of the 50% individual occurrence layer, d2 is the sampling depth interval (m) of the 50% individual occurrence layer, p1 is the cumula- tive individual percentage (%) that occurred at depths shallower than the 50% individual occurrence layer, and p2 is the individual percentage (%) at the 50% individual occurrence Oceans 2023, 4 245 Oceans 2023, 4, FOR PEER REVIEW 4 where d is the depth (m) of the upper depth of the 50% individual occurrence layer, d is 1 2 the sampling depth interval (m) of the 50% individual occurrence layer, p is the cumulative layer. Day-night differences in vertical distributions on each collection date were tested individual percentage (%) that occurred at depths shallower than the 50% individual by the Kolmogorov-Smirnov test. occurrence layer, and p is the individual percentage (%) at the 50% individual occurrence BH of A. digitale was expressed by histograms based on the integrated abundance layer. Day-night differences in vertical distributions on each collection date were tested by −2 the Kolmogorov-Smirnov test. (ind. m ) at 0–1000 m water column for the day and night of each sampling date. The BH of A. digitale was expressed by histograms based on the integrated abundance depth composition of each BH interval (1 mm) was also calculated. (ind. m ) at 0–1000 m water column for the day and night of each sampling date. The depth composition of each BH interval (1 mm) was also calculated. 3. Results 3.1. Hydrography 3. Results 3.1. Hydr Vertography ical distributions of temperature, salinity, dissolved oxygen, and fluorescence at each sampling date are shown in Figure 3. Throughout the season, the temperature was Vertical distributions of temperature, salinity, dissolved oxygen, and fluorescence −1 at 0.7–8.5 °C, salinity for 32.5–34.5, DO ranged between 0.6 and 10.4 mg L , and fluores- at each sampling date are shown in Figure 3. Throughout the season, the temperature was cence w at 0.7–8.5 as 0.02– C, 2.3 salinity 2. Seaso for nal 32.5–34.5, thermoclDO ine dev ranged elopbetween ed around 0.6 5 and 0 m10.4 in Ju mg ly and L , Oct andober, fluor and tempera escence was tures w 0.02–2.32. ere almost consta Seasonal thermocline nt for 100 m developed in February a around nd April 50 m. For in July all sea and sons, October, and temperatures were almost constant for 100 m in February and April. For temperature showed a minimum of 1–2 °C approximately at 100 m, then had a maximum all seasons, temperature showed a minimum of 1–2 C approximately at 100 m, then had of about 3.5 °C around 200 m, and finally decreased with increasing depth. Salinity in- a maximum of about 3.5 C around 200 m, and finally decreased with increasing depth. creased with depth for all seasons. Salinity was similar for depths below 100 m in February Salinity increased with depth for all seasons. Salinity was similar for depths below 100 m and April, while was below 33 at <50 m, forming surface halocline in July and October. in February and April, while was below 33 at <50 m, forming surface halocline in July and −1 DO decreased with increasing depth and was extremely low, less than 2 mg L below 200 October. DO decreased with increasing depth and was extremely low, less than 2 mg L m depth. Fluorescence was high at the surface layer above the thermocline (<50 m) in July below 200 m depth. Fluorescence was high at the surface layer above the thermocline and October and at 0–100 m in February and April. (<50 m) in July and October and at 0–100 m in February and April. Fluorescence 024 68 10 12 0 2468 10 12 02 468 10 12 024 68 10 12 -1 DO(mg L ) 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 0.0 0.5 1.0 1.5 2.0 2.5 Temperature (℃) 024 68 0 2468 0 246 8 0 2468 Salinity 32.5 33.0 33.5 34.0 34.5 32.5 33.0 33.5 34.0 34.5 32.5 33.0 33.5 34.0 32.5 33.0 33.5 34.0 34.5 34.5 29 Oct. 2010 26 Feb. 2011 22 Apr. 2011 3 July 2011 Figure 3. Vertical distribution of temperature, salinity, dissolved oxygen, and fluorescence at St. K2 Figure 3. Vertical distribution of temperature, salinity, dissolved oxygen, and fluorescence at St. K2 in the subarctic Pacific gyre on four occasions from October 2010 to July 2011. Note that the vertical in the subarctic Pacific gyre on four occasions from October 2010 to July 2011. Note that the vertical scale (depth) is in the logscale. scale (depth) is in the logscale. 3.2. Aglantha digitale 3.2. Aglantha digitale Hydrozoans occurred in the western subarctic Pacific throughout the year. A. digitale Hydrozoans occurred in the western subarctic Pacific throughout the year. A. digitale was the most abundant species, with an annual mean abundance of 198.4 ind. m at −2 was the most abundant species, with an annual mean abundance of 198.4 ind. m at 0– 0–1000 m water column, composed of 91.9% of hydrozoan abundance (Table 2). 1000 m water column, composed of 91.9% of hydrozoan abundance (Table 2). The day-night vertical distribution and D50% of A. digitale at each sampling date are shown in Figure 4. The vertical distribution of A. digitale was concentrated at 0–200 m both day and night for most seasons. While in October, the certain population density was seen to extend below 300 m both day and night. The highest population density of A. digitale −3 was 1.36 ind. m at 100–150 m depth during a night in February. D50% of A. digitale was at Depth (m) Oceans 2023, 4, FOR PEER REVIEW 5 26–129 m depth through day and night of all seasons. Diel change in vertical distribution was observed in July, with significantly shallower depths at night (p < 0.05). Histograms on BH of A. digitale and their vertical distribution composition both day and night at each sampling date are shown in Figure 5. The BH of A. digitale ranged be- tween 2.4 and 18.9 mm. In October and February, the most numerous individuals were seen for the BH at 8–16 mm both day and night. On the other hand, two modes of BH at 3–5 mm and 8–17 mm were observed for both day and night in April. In July, the majority of individuals was at the BH in 8–17 mm both day and night. Most of the mature speci- mens, GL composed >10% of the BH, occurred only in July. The BH of the mature individ- uals ranged from 4.7 to 17.6 mm, with most of them was at >10 mm. Concerning the vertical distribution composition of each BH of A. digitale, the distri- Oceans 2023, 4 246 bution below 300 m was seen in October for all BH sizes, indicating that the extension of vertical distribution down to the deeper layer was a typical feature of all BH ranges (Fig- ure 5). In February, the modal BH individuals at 8–16 mm BH were distributed near the Table 2. Annual mean standing stocks of cnidarian species for 0–1000 m water column at St. K2 in surface both day and night, while other smaller and larger individuals were distributed the western subarctic Pacific from October 2010 to July 2011. Values are mean  SD. at deeper layers. In April, small individuals with BH < 6 mm were distributed below 300 Standing Stock m, while most the individuals with a BH > 12 mm were distributed below 100 m. In July, Family Species (ind. m ) (%) individuals with BH smaller than 6 mm were distributed at >200 m, but at night, the main individuals with BH betwAglantha een 8 an digitale d 16 mm were concentrated for the surface layer at 0– Rhopalonematidae 198.4  107.8 91.9 Muller, 1776 50 m. Other Cnidaria (including fragments difficult 17.4  10.1 8.1 to make species identification) Table 2. Annual mean standing stocks of cnidarian species for 0–1000 m water column at St. K2 in the western subarctic Pacific from October 2010 to July 2011. Values are mean ± SD. The day-night vertical distribution and D of A. digitale at each sampling date are 50% Standing Stock shown in Figure 4. The vertical distribution of A. digitale was concentrated at 0–200 m both Family Species −2 (ind. m ) (%) day and night for most seasons. While in October, the certain population density was seen to extend below 300 mAgl both antday ha di and gitanight. le Muller The , highest population density of A. digitale Rhopalonematidae 198.4 ± 107.8 91.9 was 1.36 ind. m at 100–150 m depth during a night in February. D of A. digitale was at 1776 50% 26–129 m depth through day and night of all seasons. Diel change in vertical distribution Other Cnidaria (including fragments difficult to make species identification) 17.4 ± 10.1 8.1 was observed in July, with significantly shallower depths at night (p < 0.05). Figure 4. Day (open) and night (solid) vertical distribution of Aglatha digitale at St. K2 in the western Figure 4. Day (open) and night (solid) vertical distribution of Aglatha digitale at St. K2 in the subarctic Pacific gyre during four sampling occasions (October 2010, February, April, and July 2011). western subarctic Pacific gyre during four sampling occasions (October 2010, February, April, and Distribution cores (D50%) are shown by the triangles. Diel changes were tested by the Kolmogorov- July 2011). Distribution cores (D ) are shown by the triangles. Diel changes were tested by the 50% Smirnov test (*: p < 0.05). Kolmogorov-Smirnov test (*: p < 0.05). Histograms on BH of A. digitale and their vertical distribution composition both day and night at each sampling date are shown in Figure 5. The BH of A. digitale ranged between 2.4 and 18.9 mm. In October and February, the most numerous individuals were seen for the BH at 8–16 mm both day and night. On the other hand, two modes of BH at 3–5 mm and 8–17 mm were observed for both day and night in April. In July, the majority of individuals was at the BH in 8–17 mm both day and night. Most of the mature specimens, GL composed >10% of the BH, occurred only in July. The BH of the mature individuals ranged from 4.7 to 17.6 mm, with most of them was at >10 mm. Oceans 2023, 4, FOR PEER REVIEW 6 Oceans 2023, 4 247 Figure 5. Histograms on bell heights of Aglantha digitale integrated over 0–1000 m water column Figure 5. Histograms on bell heights of Aglantha digitale integrated over 0–1000 m water column at at St. K2 in the western subarctic Pacific gyre during the day (upper) and night (lower) of the four St. K2 in the western subarctic Pacific gyre during the day (upper) and night (lower) of the four sampling occa sampling occasions sions (O (October ctober 22010, 010, February, February, April, April, and June 2011). Depth and June 2011). Depth distribution distribution compositions compositions within the eight depth strata of 0–1000 m water column is also shown for each panel. within the eight depth strata of 0–1000 m water column is also shown for each panel. Concerning the vertical distribution composition of each BH of A. digitale, the distri- 4. Discussion bution below 300 m was seen in October for all BH sizes, indicating that the extension 4.1. Abundance of A. digitale of vertical distribution down to the deeper layer was a typical feature of all BH ranges At St. K2, A. digitale was the predominant hydrozoan, accounting for more than 90% (Figure 5). In February, the modal BH individuals at 8–16 mm BH were distributed near of the hydro the surfacez both oan day abun and dan night, ce (Tab while le 2). other A. dismaller gitale is and a co lsmopolitan arger individuals species wer w e idistributed dely distrib- uted at deeper at high layers. latitude In are Apr ail, s in t small he Nort individuals hern Hem with isp BH here [ < 6 2 mm ,4,13] wer . In eform distributed ation obelow n abun- 300 m, while most the individuals with a BH > 12 mm were distributed below 100 m. In dance, BH, BH of mature specimens, and generation time of A. digitale reported from var- July, individuals with BH smaller than 6 mm were distributed at >200 m, but at night, the ious locations are summarized in Table 3. In the present study, the abundance of A. digitale main individuals with BH between 8 and −2 16 mm were concentrated for the surface layer at ranged between 58.5 and 391.1 ind. m for the 0–1000 m water column. This value well 0–50 m. −2 corresponds with the values reported in the subarctic Pacific (368 ind. m ) [10] and the −2 northeastern North Pacific (38–221 ind. m ) [11]. As for the marginal areas of the western 4. Discussion −2 subarctic Pacific, values in the Oyashio region during spring (16–316 ind. m ) [8] and val- 4.1. Abundance of A. digitale −2 ues based on the annual sampling in the Oyashio region (55–896 ind. m ) [7] are also At St. K2, A. digitale was the predominant hydrozoan, accounting for more than 90% of comparable. For the areas with similar values of A. digitale abundance in this study (<100 the hydrozoan abundance (Table 2). A. digitale is a cosmopolitan species widely distributed −2 ind. m ), the Norwegian fj ords (Korsfj ord and Fanafj ord) [14] and the Arctic Ocean [15] at high latitude areas in the Northern Hemisphere [2,4,13]. Information on abundance, BH, −2 are available. On the other hand, high abundances of A. digitale over 1000 ind. m have BH of mature specimens, and generation time of A. digitale reported from various locations −2 been reported for Toyama Bay in the southern Japan Sea (maximum: 4427 ind. m ) [12], are summarized in Table 3. In the present study, the abundance of A. digitale ranged between −2 −2 the Irish coast in the North Atlantic (5350 ind. m ) [18] and the White Sea (5000 ind. m ) 58.5 and 391.1 ind. m for the 0–1000 m water column. This value well corresponds with [19] (Table 3). A characteristic of these regions is the semi-enclosed embayment having a the values reported in the subarctic Pacific (368 ind. m ) [10] and the northeastern North Pacific (38–221 ind. m ) [11]. As for the marginal areas of the western subarctic Pacific, limiting water exchange with the outer region. These facts suggest that the semi-enclosed values in the Oyashio region during spring (16–316 ind. m ) [8] and values based on the area may have maintained a higher population of A. digitale without transportation by annual sampling in the Oyashio region (55–896 ind. m ) [7] are also comparable. For flushing discharge caused by the ocean currents. In summary, the abundance of A. digitale the areas with similar values −2 of A. digitale abundance in this study (<100 ind. m ), the is less than 1000 ind. m for the oceanic open area where the current transport would Norwegian fjords (Korsfjord and Fanafjord) [14] and the Arctic Ocean [15] are available. prevent to accumulation of high density/abundance. While in the semi-enclosed embay- On the other hand, high abundances of A. digitale over 1000 ind. m have been reported −2 ment condition, A. digitale can maintain high density/abundance (>5000 ind. m ) under for Toyama Bay in the southern Japan Sea (maximum: 4427 ind. m ) [12], the Irish coast low flushing and transport to the other region. 2 2 in the North Atlantic (5350 ind. m ) [18] and the White Sea (5000 ind. m ) [19] (Table 3). A characteristic of these regions is the semi-enclosed embayment having a limiting water exchange with the outer region. These facts suggest that the semi-enclosed area may have Oceans 2023, 4 248 maintained a higher population of A. digitale without transportation by flushing discharge caused by the ocean currents. In summary, the abundance of A. digitale is less than 1000 ind. m for the oceanic open area where the current transport would prevent to accumulation of high density/abundance. While in the semi-enclosed embayment condition, A. digitale can maintain high density/abundance (>5000 ind. m ) under low flushing and transport to the other region. Table 3. Regional comparison on abundance, bell height, and generation length of Aglantha digitale from worldwide ocean. Sampling Bell Height (mm) Generation Abundance Region Reference 2 1 Length (year ) (ind. m ) Season Depth (m) Range Mature Toyama Bay, Annual 0–500 73–4427 1–17 6–17 2 [12] southern Japan Sea Eastern/Western Summer 0–150 0–368 – 8.5–15.2 – [10] subarctic Pacific Oyashio region Annual 0–2000 55–896 1–23 11–23 1 [7] Oyashio region Spring <200 16–316 4–18 – 1 [8] northeastern North Summer 0–150 38–221 0.6–17 1.1–16 – [11] Pacific Northern Pacific Summer <200 – 5–20 15< 1 [9] Southern Irish Summer 0–25 <5350 – – – [18] coastal water Northeast Atlantic Autumn/winter 0–100 – 1–18 – – [17] Ocean Korsfjord and Annual 0–640 156–358 – – 2 [14] Fanafjord White Sea Annual 0–100 5–5000 – 8–12 1 [19] High-Arctic coastal Annual 0–180 <720 – – – [15] Western Subarctic Annual 0–1000 58.5–391.1 2.4–18.9 4.7–17.6 1 This study Pacific (K2) 4.2. Vertical Distribution of A. digitale Vertical distribution of A. digitale was concentrated at <200 m for most seasons. Season- ally, diel changes in vertical distribution were seen in July when the thermocline developed, and deeper distribution (>300 m) was observed in October (Figure 5). In July, it should be noted that the day-night differences in abundance were substantially low at night and no size fraction less than 8 mm at night-histogram. It can be concluded that there is a spatial horizontal heterogeneity in the distribution of medusae. While diel changes in vertical distribution were denied in this study, nocturnal ascent diel vertical migration of A. digitale has also been reported from the Saanich Inlet off Vancouver [9]. The deepening vertical distribution of A. digitale has also been reported in the fjords of Svalbard from August to October [15]. These findings correspond with the results of this study. As a new finding of this study, the depth distribution at each BH was determined with season and day/night. Small individuals (<6 mm BH) were distributed for the deep layers or extremely shallower depths in all seasons (Figure 5). These facts suggest that small individuals with less swimming ability could be easily transported vertically from the vertical mixing and diffusion of water masses. Swimming behaviors of six hydrozoan species, including A. digitale, are highly varied with species, and A. digitale is considered to be a jet-swimming species [24,34]. Within the three hydrozoan species applying jet-swimming, A. digitale is the smallest body size and has the longest jet interval in time [24]. These facts indicate that A. digitale is most affected by vertical and horizontal water diffusion, especially for their small-sized specimen, which has less swimming ability. These low swimming abilities of the small individuals of A. digitale would be difficult to stay in a stable layer because of the vulnerability of the diffusion of the water masses. It induces an extremely shallower or deeper distribution of them. Oceans 2023, 4 249 The main prey item of A. digitale is reported to be small copepods such as Pseudo- calanus [20,22,24]. For Pseudocalanus in the western subarctic Pacific, two species: P. minutus and P. newmani are present [35]. Within them, P. minutus accumulates lipids in their body and is known to have a resting (diapausing) stage at the deep layer during its life history, and their descent to deep-sea achieved summer to autumn [35,36]. Since the diapausing P. minutus at the deep layer contains much lipids, their nutrition values would be high, and the swimming behavior of dormant copepods is reduced to maintain a low metabolic rate [37,38]. These characteristics of the deep-sea dormant P. minutus (small body size, high nutritional value, and low swimming behavior) suggest that they are a sufficient prey item for A. digitale. Thus, the extension of the vertical distribution of A. digitale to the deep layer during October can be explained from viewpoint of their food availability (e.g., to capture nutrient-rich P. minutus distributing deep layer during these seasons). 4.3. Population Structure and Body Size of A. digitale The BH range of A. digitale observed in this study (2.4–18.9 mm) well corresponds to those reported in Toyama Bay in the southern Japan Sea [12], in the spring Oyashio region [8], in the northeastern North Pacific [11], and in the northeastern North Atlantic [17] (Table 3). It should be noted that most of the listed studies applied similar mesh sizes to this study (200–335 m); thus, differences in the applied mesh size would be negligible. Concerning BH, large BH (up to 20 mm) have been reported from the Saanich Inlet off Vancouver and annual observations in the Oyashio region [7,9]. For such a subarctic coastal area, the abundance of small copepods, the primary prey of A. digitale, has been reported to be high [39]. These facts suggest that favorable food conditions would be an important factor in achieving large body sizes of A. digitale. The minimum maturation size of A. digitale: 6 mm BH has been reported in Toyama Bay, southern Japan Sea [12]. Such a small mature specimen of A. digitale (8–12 mm BH) has also been reported in the White Sea [19]. Common characteristics of these areas with small maturation sizes of A. digitale are that these areas are semi-enclosed seas having high abundances of them (>1000 ind. m ) (Table 3). The feeding mode of A. digitale is basically carnivorous [13,20,23,24]. The energy transfer for such a higher trophic level organism is considered to be higher in the areas where the marine ecosystems are composed of simply limited species [40,41]. The regions where high abundance and small maturation body size of A. digitale Toyama Bay and the White Sea are characterized by semi-enclosed seas, having such high energy transfer efficiency food web and marine ecosystem structures composed by the limited species [12,19]. Thus, in the areas where the marine ecosystem is composed of the simple species structure and high energy transfer efficiency to the higher trophic level organisms, abundance of A. digitale would be high, and they may mature at smaller body-sizes. In this study, the observed minimum maturation size of A. digitale was small as 4.7 mm, while most of the mature specimens were at BH over 10 mm (Figure 5). These facts suggest that the few small body-sized mature individuals are considered to be transported to the oceanic St. K2 from the marginal areas, such as the Aleutian Islands or the Okhotsk Sea. In this study, one or two cohorts were identified for BH of A. digitale on each sampling date (Figure 5). while because of the scarce sampling occasions (four times per year), it was difficult to trace the growth of each cohort. For the developmental stages, mature specimens only occurred in July (Figure 5). These facts suggest that the life history of A. digitale is a one-year generation length having reproduction in summer for the western subarctic Pacific. Concerning the life span of A. digitale, one or two generations per year have been reported in the Oyashio region [7,8], Toyama Bay in the southern Japan Sea [12], Saanich Inlet off Vancouver [9], Norwegian fjords [14], and the White Sea [19] (Table 3). Thus, the generation time in this study, one year, is an ordinary generation length for A. digitale in the open oceanic region. On the other hand, two generations per year of A. digitale have been reported for Toyama Bay in the southern Japan Sea and Norwegian fjords (Table 3). These regions are Oceans 2023, 4 250 semi-enclosed seas where the energy transfer efficiency to the higher trophic level organisms is expected to be high. Thus, the abundance, maturation body size, and generation length of A. digitale would be related and determined by the component organisms in the marine ecosystem in each region. In semi-enclosed seas composed of the simple species group, because of the high energy transfer to hydrozoans A. digitale, they may have high abundance and small maturation sizes, which implies a shorter generation time. Thus, two generations per year of A. digitale have seen such areas [12,24]. The major reproductive period summer observed in this study is also consistent with the life history of this species in the adjacent Oyashio region [7]. In these regions, summer is the season when copepods, the main prey of A. digitale, reaches annual peak abundance at the surface layer [35,39]. It is interpreted that A. digitale may mature and have reproduction under sufficient food conditions during the summer season. Author Contributions: Conceptualization, M.A. and A.Y.; methodology, M.A. and A.Y.; software, M.A.; validation, M.A. and A.Y.; formal analysis, M.A.; investigation, M.A.; resources, M.A.; data curation, A.Y.; writing—original draft preparation, T.G.; writing—review and editing, A.Y.; visualiza- tion, T.G.; supervision, A.Y.; project administration, A.Y.; funding acquisition, A.Y. All authors have read and agreed to the published version of the manuscript. Funding: Part of this study was supported by Grant-in-Aid for Challenging Research (Pioneering) 20K20573, Scientific Research 22H00374 (A), 20H03054 (B), 19H03037 (B), and 17H01483 (A) from the Japan Society for the Promotion of Science (JSPS). This study was partially supported by the Arctic Challenge for Sustainability II (ArCS II; JPMXD1420318865) and the Environmental Research and Technology Development Fund (JPMEERF20214002) of the Environmental Restoration and Conservation Agency of Japan. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Data will be available from request to the corresponding author. Acknowledgments: We thank the captains, officers, crews, and researchers onboard the R/V Mirai, JAMSTEC, for their great efforts during the field sampling. Conflicts of Interest: The authors declare no conflict of interest. References 1. Arai, M.N. Pelagic coelenterates and eutrophication: A review. Hydrobiologia 2001, 451, 69–87. [CrossRef] 2. Purcell, J.E. Climate effects on formation of jellyfish and ctenophore blooms: A review. J. Mar. Biol. Assoc. U. K. 2005, 85, 461–476. [CrossRef] 3. Purcell, J.E. 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Journal

Oceans – Multidisciplinary Digital Publishing Institute

Published: Jul 31, 2023

Keywords: hydrozoa; Aglantha digitale; abundance; population structure; life cycle

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