Vertical Distribution and Seasonal Variation of Pelagic Chaetognaths in Sagami Bay, Central Japan

Plankton Benthos Res 7(2): 41–54, 2012 Plankton & Benthos Research © The Plankton Society of Japan

Vertical distribution and seasonal variation of pelagic chaetognaths in Sagami Bay, central Japan

1,2, 2 2 1 HIROOMI MIYAMOTO *, SHUHEI NISHIDA , KAZUNORI KURODA & YUJI TANAKA

1 Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, 4–5–7 Konan, Minato-ku, Tokyo 108–8477, Japan 2 Atmosphere and Ocean Research Institute, University of Tokyo, 5–1–5 Kashiwanoha, Kashiwa, Chiba 277–8564, Japan Received 22 November 2011; Accepted 24 February 2012

Abstract: The vertical distribution and seasonal variation of pelagic chaetognaths was investigated in Sagami Bay, based on stratified zooplankton samples from the upper 1,400 m. The chaetognaths were most abundant in the 100– 150 m layer in January and May 2005, whereas they were concentrated in the upper 50 m in the other months. Among the 28 species identified, Zonosagitta nagae had the highest mean standing stock, followed by Flaccisagitta enflata and Eukrohnia hamata. Cluster analysis based on species composition and density separated chaetognath communities into four groups (Groups A–D). While the distribution of Group C was unclear due to their rare occurrence, the other groups were more closely associated with depth than with season. The epipelagic group (Group A) was further divided into four sub-groups, which were related to seasonal hydrographic variation. The mesopelagic group (Group B) was mainly composed of samples from the 150–400 m layer, although Group A, in which the epipelagic species Z. nagae dominated, was distributed in this layer from May to July. Below 400 m, all samples were included in the bathypelagic group (Group D). In this group, Eukrohnia hamata was dominant with larger standing stocks than in other tropical-temperate waters, suggesting that intrusions of subarctic water drive the large standing stock of this species. Combined, these observations suggest that the seasonal and vertical patterns of the chaetognath community in Sagami Bay are influenced by hydrographic changes in the epipelagic layer and the submerged subarctic water in the mesopelagic layer.

Key words: arrow worm, bathypelagic layer, cluster analysis, diversity, zooplankton

several researchers (e.g. Furuhashi 1961, Tokioka 1959). Introduction Nagasawa & Marumo (1975, 1982), Terazaki & Marumo Chaetognatha is a phylum of small marine carnivorous (1979), Terazaki (1992), and Kotori (1987) investigated the invertebrates, commonly called arrow worms. The phylum vertical distributions of epipelagic chaetognaths. Although encompasses approximately 130 species, of which about 90 studies on meso- and bathypelagic layers (>400 m) are species are holoplankton (Thuesen 2012). Planktonic chae- much fewer, chaetognath abundances and distribution have tognaths are distributed throughout pelagic ecosystems, been reported by Kitou (1966a, b, 1967a), Marumo & Na- often dominating mesozooplankton next to copepods gasawa (1973), Johnson & Terazaki (2003), and Ozawa et (Bone et al. 1991, Ball & Miller 2006), and are important al. (2007). While a large body of knowledge has accumu- secondary consumers (Reeve 1970). In addition, chaeto- lated on the distribution of chaetognaths, little is known of gnaths have species-specific ranges in the ocean environ- the seasonal variation in vertical distribution throughout ment and are regarded as important indicators of water the water column from epipelagic to bathypelagic depths. masses (Bieri et al. 1959, Nagai et al. 2006). Because of Sagami Bay faces the western North Pacific and is lo- their importance in the pelagic food web, the distribution cated in the central part of Honshu, Japan. Toward the cen- of pelagic chaetognaths around Japan has been reported by tre of the bay, there is an approximately 1,500 m deep sub- marine canyon called the Sagami Trough. The bay opens * Corresponding author: H. Miyamoto; E-mail, [email protected]. widely to the Pacific Ocean and bay water is influenced by ac.jp the Kuroshio (Iwata 1979, Kawabe & Yoneno 1987), which 42 H. Miyamoto et al.

ventory of species, (2) examine the depth and seasonal variation of total chaetognath standing stock and species composition, and (3) examine the relationships between the observed patterns and oceanographic conditions and water masses. The distributional patterns of each species in relation to their size will be addressed in a companion paper.

Materials and Methods

Sampling and sample processing Zooplankton samples were collected in the daytime (ca. three hours during 9:07–16:52) in January, May, July, Sep- tember, and November 2005 as well as in January and May 2006 at a fixed station (Stn S3; 35° 00′N, 139° 30′E) in central Sagami Bay using an Intelligent Operative Net Sam- pling System (IONESS: mesh aperture, 0.33 mm; effective mouth area, 1 m2), which is a modified open/closing net system based on the MOCNESS (Wiebe et al. 1985), during cruises of the T/S Seiyo-Maru (Fig. 1). The IONESS was towed obliquely in discrete layers. In January 2005, samples were collected only from eight layers in the upper 200 m (200–150, 150–100, 100–75, 75–50, 50–25, 25–10, Fig. 1. Map of the study site and location of the sampling sta- 10–5, 5–0 m) bay a single tow, while in May 2005, 15 lay- tion S3. Arrows indicate the Kuroshio (KU) and Oyashio (OY) ers in the upper 1,100 m (deep tow: 1,100–1,000, 1,000– currents. 800, 800–600, 600–500, 500–400, 400–300, 300–200; shallow tow: 200–150, 150–100, 100–75, 75–50, 50–25, 25–10, 10–5, 5–0 m) were sampled by two tows. The flows along the southern coast of Honshu (Fig. 1). The bay 0–1,400 m layer was covered in all the other months. In is also influenced by river inflow as well as outflowing September 2005, sampling for shallow (0–200 m) and deep water from Tokyo Bay (Kinoshita & Hiromi 2005). The (200 m–1,400 m) layers was conducted four days apart for North Pacific Intermediate Water (NPIW), which origi- logistical purposes, while the collections in July, Novem- nates from the subarctic region, enters the bay within the ber 2005, and May 2006 were made by consecutive shal- meso- and bathypelagic zones. The salinity of the mesope- low and deep tows (deep tow: 1,400–1,200, 1,200–1,000, lagic water fluctuates according to the strength of the in- 1,000–800, 800–600, 600–400, 400–300, 300–200; shal- trusions (Senjyu et al. 1998, Yasuda 2003). These charac- low tow: 200–150, 150–100, 100–75, 75–50, 50–25, 25–10, teristics, along with its easy access for repeated sampling, 10–5, 5–0 m). In January 2006, the IONESS sampled eight make Sagami Bay an ideal site for examining the seasonal discrete layers from 1,400 m to the surface (1,400–1,000, variation of zooplankton and its relationships with oceano- 1,000–600, 600–400, 400–200, 200–150, 150–100, 100– graphic conditions throughout the water column, including 50, 50–0 m) by a single tow. The volume of water filtered meso- and bathypelagic zones. was estimated with a flow meter (Tsurumi-seiki Co. Ltd.) Extensive research has been conducted on the spatio- attached in the mouth of the net. The volume of water fil- temporal variation of zooplankton in Sagami Bay, includ- tered by each net ranged from 130–940 m3 (mean: 434 m3). ing studies of euphausiids (Hirota et al. 1982), copepods The samples were immediately fixed and preserved in ~5% (Shimode et al. 2006, Kuriyama & Nishida 2006), amphi- formaldehyde/seawater solution buffered with sodium tet- pods (Nomura et al. 2003), and chaetognaths (Marumo & raborate. Nagasawa 1973, Nagasawa & Marumo 1977, 1982), with Chaetognaths were separated from the zooplankton recent observations on the gelatinous fauna being con- samples or aliquots were taken with a box-type or a cylin- ducted using underwater vehicles and video cameras (Hunt der-type splitter (Motoda 1959). More than 600 individuals & Lindsay 1999, Lindsay & Hunt 2005). However, previ- per sample were counted and identified under a stereo- or ous studies often suffered from limitations of sampling compound microscope following Kitou (1967b) and apply- coverage, with respect to season, depth, and/or equipment. ing Bieri’s (1991) system for generic names. As for the tax- To address such limitations, we used an opening-closing onomic status of Eukrohnia bathypelagica Alvariño, 1962, net appropriate for chaetognath sampling, covering almost we followed Aurich (1970) and Tokioka (1974) who as- the entire depth range (0–1,400 m) and during all seasons. signed it as a junior synonym of E. hamata (Möbius, 1875). Specifically, this study aimed to (1) revise the existing in- The classification of these two species was also not sup- Chaetognaths in Sagami Bay 43 ported by a genetic marker (Miyamoto 2010). Vertical profiles of temperature and salinity were ob- tained using a conductivity, temperature, depth (CTD) sen- sor (Falmouth Scientific, Inc.) attached in the mouth of the IONESS during each sampling cruise. A monthly CTD (Falmouth Scientific, Inc.) cast from 1,000 m to the surface was also carried out during other cruises of the Seiyo- Maru at Stn S3. The average values of temperature and salinity in the stratum were calculated from this CTD data. Data analysis The species composition comparisons between samples were compared by applying the Bray-Curtis similarity index (Bray & Curtis 1957). The density (ind. m－3) was square-root transformed prior to the analysis to reduce bias caused by extremely abundant species. An inverse analysis was performed to examine species associations (Field et al. 1982). To avoid spurious associations among rare species, i.e. Sagitta bipunctata Quoy and Gaimard, 1827, Zonosa- gitta bedoti (Beraneck, 1895), and Z. pulchra (Doncaster, 1902), were excluded from the analysis since they were collected in only one series of tows. The unweighted pair- group method using arithmetic averages was applied to classify samples and species based on the similarity ma- trix. The core of the vertical distribution of each species was estimated applying the weighted mean depth (WMD; Pe- Fig. 2. Seasonal and vertical distribution of temperature and arre 1973). The weighted mean temperature (WMT) and salinity at Stn. S3. Arrows show the days of zooplankton sam- salinity (WMS) of dominant species were also calculated pling with IONESS and CTD observations. Triangles indicate to show the core of distribution in relationship to tempera- days of CTD observation only. Below 200 m, depth ranges are ture and salinity (Matsuzaki 1975). 200 m intervals.

Results Standing stock Hydrography The standing stock of chaetognaths in the upper 200 m The surface water was well mixed in the upper 200 m ranged from 252 (January 2006) to 4,960 ind. m－2 (May during December 2004–April 2005, with a temperature of 2006), with an average of 1,920±1,970 (SD) ind. m－2 (Fig. 14–15°C in the upper 80 m in April (Fig. 2). The thermo- 3). In the 200–1,000 m layer, the average was 524±358 cline started to form in May and continued to develop in ind. m－2 with peaks in May 2006 and November 2005. The the upper 40 m in August and September. Also, the iso- average stocks within the 0–1,000 m and 0–1,400 m layers pleth of 13°C and 34.5 salinity were shallower in August from July 2005 to May 2006 were 2,970±2,360 and and September than in the other seasons. In October, the 3,020±2,330 ind. m－2, respectively, and those in January depth of the thermocline increased to 150 m accompanied 2005 and 2006 were lower than in the other months in the by vertical mixing, followed by weakened stratiﬁcation upper 200 m. due to enhanced mixing by cooling of the surface water The density was mostly highest in the 0–50 m range (av- from November. The mixed layer reached approximately erage 31±40 ind. m－3), with the exception of January and 120 m in February 2006 and existed until April when the May 2005, and decreased roughly with depth (Fig. 3) to the surface temperature started to increase. While the salinity minimum of 0.02 ind. m－3 in the 1,200–1,400 m layer. in the upper 200 m was mostly higher than 34.4, low-salin- Species diversity ity water (<34.2) occurred in the upper 30 m from June to September 2005. Whereas the water temperature below A total of 28 species belonging to 16 genera were identi- 200 m showed little seasonal variation, there were marked ﬁed, of which 16 species were collected on every of the depressions in salinity (<34.25) in the 300–700 m layer sampling occasion (Table 1). Heterokrohnia specimens during August 2005–April 2006. were counted as a single species; a detailed examination of the Heterokrohnia specimens is still in progress, but it in- 44 H. Miyamoto et al.

Fig. 3. Vertical distribution of density, the number of species, and diversity index (H′). SS represents standing stock (ind. m－2) of the entire water column. The diversity indices at the same depth range (Upper 200 m, 50 m intervals; Lower 200 m, 200 m intervals) are shown except for on three sampling occasions. dicates that they contain two or more undescribed species. regularis (Aida, 1897), Eukrohnia hamata, Flaccisagitta The number of species from each vertical series ranged enflata (Grassi, 1881), and Serratosagitta pacifica (To- from 16 (May 2006) to 26 (November 2005) and tended to kioka, 1940). Eukrohnia hamata accounted for more than be smaller in May and July. This seasonal pattern in the 4.8% of the total chaetognath standing stock within the en- water column was consistent with that in the upper 200 m tire water column between May 2005 and 2006, except in (Fig. 3). The species number and diversity index were the September 2005. In September, Fl. enflata and Mesosa- highest in the upper 400 m and decreased with depth. gitta minima (Grassi, 1981) comprised more than 20% and Below 400 m, the species number was generally less than were more abundant than Z. nagae. In November 2005 and six species in each layer. Within the upper 200 m, the January 2006, because the standing stocks of epipelagic peaks in both the species number and the diversity index in chaetognaths were low, E. hamata accounted for more than each layer tended to shift to shallower depths from May to 30%. January. The cluster analysis based on the Bray-Curtis similarity indices between samples identified four major groups Species composition (A–D) among the 91 samples at an 85% dissimilarity level Zonosagitta nagae (Alvariño 1967) comprised an aver- (Fig. 4A). Group A mainly included samples from the age of 48% of standing stock of total chaetognaths in the upper 150 m (Fig. 4B) and was further classified into four whole integrated water column between May 2005 and sub-groups that appear to correspond with the seasonal

May 2006 (Table 1), with particularly high values in July pattern of hydrographic conditions. Group A1 was com- 2005 (53%) and May 2006 (84%), while it constituted less posed of samples from 75–150 m in November 2005 and than 5% in November 2005 and January 2006. The other from 0–150 m in January 2005 and 2006, in which Se. pa- species that occupied more than 3% were Aidanosagitta ciﬁca and Fl. enﬂata comprised approximately 50% of the Chaetognaths in Sagami Bay 45 - l a c D 3 2 6 s 1 1 1 a 5 5 0 3 M 4 3 1 1 6 5 2 2 0 6 6 0 6 2 0 2 5 8 0 3 8 7 7 2 7 3 1 , , 9 , 0 8 7 7 7 w 2 4 1 7 6 9 3 6 8 2 1 1 1 3 8 1 4 2 1 1 4 6 1 8 7 1 2 W 9 D e g M a 3 3 7 0 r W 2 3 3 6 2 4 2 0 0 9 6 0 5 3 6 4 1 3 9 1 6 1 e 5 . 9 . . . 4 . 5 . . . 2 8 5 3 3 2 8 9 1 2 7 9 e 1 v S . . 7 5 0 6 0 . 5 . . . . . 3 . , 9 . 5 0 . 8 . 8 . . g 2 9 6 0 3 7 2 2 2 2 0 3 – 5 – 1 0 1 1 1 A 9 1 4 5 1 1 S 3 4 1 a r e v D A . 6 9 6 7 8 M 6 7 1 6 0 0 0 0 2 9 3 0 0 7 3 0 5 8 8 4 0 6 4 2 – 1 8 1 1 – – – – – – – 2 – 2 2 – 3 5 – 6 7 1 W 1 – 0 2 3 y * a 0 y 6 4 7 8 0 4 8 6 2 1 9 9 8 4 7 . . . 6 ...... a M . 3 5 0 1 7 S . 9 4 6 . 6 5 . 9 . , 3 2 1 1 1 o 8 3 9 – 2 3 6 2 2 – – – – – – 5 – 2 – – M 1 2 – 4 2 1 S 5 – t 5 0 0 D 0 0 2 0 2 4 3 9 M 3 5 1 9 4 2 0 y 6 0 2 0 5 8 9 9 5 8 5 0 9 6 9 2 , 5 , 8 1 1 a 4 5 1 – 4 7 4 7 9 2 1 2 7 – 1 5 – 1 – – 3 7 – 5 2 W 2 1 4 3 M * y r m a 8 o 4 6 u r 6 5 9 5 2 8 4 3 5 3 0 1 4 1 3 4 7 4 6 4 7 7 0 . . f ...... 5 . . n 4 5 2 4 9 2 0 1 1 0 S . 6 0 3 7 . . . 8 . . . 5 . 0 . 0 1 7 1 1 7 . a a 5 3 7 – 2 1 2 1 1 1 0 1 – 0 2 – 1 – 1 2 J – 7 1 4 – S 1 0 8 . 0 t a d e h t m D 0 0 5 o r 0 0 7 6 0 5 M 7 3 9 9 7 5 f 3 3 3 0 0 0 8 0 2 0 3 5 9 2 0 2 7 0 6 7 , , , 8 1 1 * d 3 r 4 2 2 4 2 7 1 7 7 2 1 – 2 6 – 2 1 1 6 7 5 1 7 W 8 7 5 2 e e t b a l m u e 1 c 2 2 l 4 2 7 0 3 7 2 v 2 7 5 7 6 5 8 7 9 9 1 8 8 6 ...... 1 5 ...... 0 . a 8 9 4 o 0 1 0 7 7 S 0 6 3 0 6 4 . 5 . . 5 . . . 9 . 3 0 1 0 1 . 0 0 6 1 c 2 2 1 2 0 8 2 1 1 1 4 2 5 2 – 6 – 2 3 N 3 1 1 3 1 S 2 4 1 1 e r . e y l w D e 3 v S 1 0 0 0 8 2 i M 8 5 3 t 1 S 0 2 3 6 6 9 0 7 3 5 9 5 3 , 1 * 1 c r f 1 1 5 – 1 – 9 1 9 2 – 7 1 8 3 – 5 – 2 6 2 6 – 1 W 6 6 3 1 e e o p b s s e m e e u 0 0 l t 6 4 8 3 0 9 6 8 7 4 6 7 3 3 0 9 a 7 p . 4 . . . 0 . 6 . 3 . . 1 . 6 4 2 0 9 3 3 v e S 7 . . 4 0 2 0 . . 3 5 6 6 . . , 3 0 5 4 8 . 7 0 m r 1 9 3 – 1 – 6 5 1 1 – 8 1 0 2 – 2 – 2 4 S 1 3 – 5 S 1 5 6 2 e 0 g 4 a , r 1 e D – 0 0 v 0 0 7 M 7 8 8 3 7 5 4 A 3 3 d 0 0 2 5 7 3 5 8 2 2 3 3 , 7 , 5 1 6 0 6 . n 8 ) 3 8 1 – 1 7 6 3 1 2 – 1 – – – – – 2 7 – 4 9 1 7 W 1 – 1 D , a 0 M 3 0 * 0 1 W 5 , 8 6 6 7 9 8 2 7 8 3 9 8 y 2 2 0 2 . . . . 6 ( 2 . . . . l . . 1 3 8 3 9 6 1 S 0 0 5 . . . . . 2 2 , 0 0 0 4 0 1 4 7 u – h 6 4 1 3 – 0 4 2 1 1 1 – 4 – – – – 1 – 1 – J 4 1 0 S 1 – 2 1 t p , 0 e 0 d 0 D 0 2 n 5 – a 0 3 7 8 4 M 4 0 0 5 1 9 9 2 6 1 0 e 0 2 4 0 9 2 3 2 , 5 5 3 5 1 1 4 1 1 1 1 7 1 2 1 – 1 3 1 6 1 3 5 9 – – – 6 – 2 – 9 5 – W 6 – – 7 f 0 m d e o e 2 g t * h n 3 5 y 2 3 0 9 0 a 0 3 3 7 3 0 0 g 2 4 2 1 7 . . 7 . . . 2 . . i . a 3 9 0 3 4 9 6 6 5 S 4 2 8 ...... 7 7 . e 6 1 0 4 6 . g r 3 4 8 . 5 1 – 0 2 7 3 6 1 0 0 – – – 1 – 6 M – 6 S 4 – 2 – – 1 w n i l d p n a D m ) 7 a 2 6 0 M 8 0

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Fig. 4. Dendrogram of cluster analysis based on species composition and density (A), and vertical distribution of each group (B). The pattern of each cell in (B) corresponds to that in (A).

total number of chaetognaths (Fig. 5). Group A1 was dis- Groups A3 and A4, the next dominant species differed be- tributed in high-salinity water (>34.5) (Fig. 2). Group A2 tween the groups (Group A3, M. minima; A4, M. decipiens consisted of samples from the upper 75 m, which was char- (Fowler, 1905)). The species diversity index was higher in acterized by low-salinity and high-temperature waters in Group A4 than A3. Group A3 was distributed across a wider September and November. The top three species, Fl. en- range of salinities than Group A4. Group B contained sam- ﬂata, Se. paciﬁca, and A. regularis in Group A2 comprised ples collected from 100–400 m depth during all sampling 76.5% of the total number of chaetognaths. Group A3 occasions except in May 2005. This group mainly oc- mainly included samples from July 2005 and May 2006, curred in the transitional layer between high-salinity water and Group A4 occurred in May, July, and September 2005. at approximately 150 m and the salinity-minimum layer Although the most dominant species was Z. nagae in both around 600 m. The typical species in this group were M. Chaetognaths in Sagami Bay 47

belonging to Groups 1–4 were distributed below 500 m (Table 1). Group 1 was composed of Caecosagitta macrocephala and Eukrohnia fowleri. Caecosagitta macrocephala was the second most dominant species in Groups 1–4. These species mainly occurred below the NPIW (Fig. 7). The boreal species Parasagitta elegans (Verrill, 1873) and Pseudosagitta scrippsae (Alvariño, 1962) made up Group 2. Parasagitta elegans was distributed at 400–1,400 m and Ps. scrippsae was mainly distributed from 600–1,000 m (Fig. 8), although it was found at 200–400 m in January 2006. Parasagitta elegans and/or Ps. scrippsae were found in May and November 2005 and January 2006. The standing stocks of Pa. elegans and Ps. scrippsae were much larger in November and January 2006, respectively. Bathyspadella oxydentata Miyamoto & Nishida, 2011 and Heterokrohnia sp., which were collected by the net tows nearest to the bottom, formed Group 3. Group 4 had a single species, E. hamata. The average weighted mean depth (WMD) of E. hamata was 665 m from May 2005 to May 2006. The standing stock of this species in the whole water column was greatest in November, with the peak density (1.15 ind. m－3) at 600–800 m. Parasagitta elegans, Ps. scrippsae, and E. hamata were mainly found in the NPIW. Group 5 had seven species, Flaccisagitta hexaptera (d’Orbigny, 1836), Krohnitta subtilis (Grassi, 1881), Meso- sagitta decipiens, M. neodecipiens, Ps. lyra, Serratosagitta pseudoserratodentata (Tokioka, 1939), and Solidosagitta zetesios (Fowler, 1905), which were distributed from 90– 500 m. The WMDs of these species, with the exception of So. zetesios, were deepest in May 2005. Of the Group 5 species, the WMDs of Se. pseudoserratodentata, K. subu- tilis, M. decipiens, and So. zetesios were shallowest in Sep- Fig. 5. Density, species diversity, and species composition of tember 2005 (Table 1). Although the species were mainly the groups shown in Fig. 4. Vertical bars in density and diversity found in the transitional layer between the NPIW and the indices indicate standard deviations. epipelagic water, Fl. hexaptera, Se. pseudoserratodentata, Ps. lyra, and K. subtilis also occurred in the Kuroshio decipiens, M. neodecipiens (Tokioka, 1959), and Pseudosa- water. Group 6 was dominated by Zonosagitta nagae, Fl. gitta lyra (Krohn, 1853). Group C included three samples, enflata, M. minima, and Se. pacifica, and all species, ex- two of which were from the upper 10 m in May 2005 and cept Aidanosagitta regularis, were present on all sampling the other from 100–150 m in May 2006. Zonosagitta nagae occasions. The WMDs of the Group 6 species were shal- was dominant in this group, and the densities were fewer lowest in September and deepest in May 2005. Flaccisa- than in Groups A and B. Group D contained 29 samples, gitta enflata and A. regularis were distributed across a all of which were collected below 400 m except for one wide range of salinities, but were mainly distributed in sample from 300–400 m in May 2005. This group was fur- high-temperature water (>20°C). These species were found ther clustered into two sub-groups (Group D1 and D2). in higher temperature and lower salinity water compared Group D1 was mostly distributed in deeper layers than to other species. Zonosagitta nagae was also distributed Group D2. The dominant species in both groups was E. ha- across a wide range of salinities. However, their tempera- mata, but it was much less abundant in Group D2, resulting ture range was also wider than that of Fl. enflata. Con- in higher percentages of Caecosagitta macrocephala versely, the standing stock of this species in Kuroshio (Fowler, 1904) and E. fowleri Ritter-Záhony, 1909 in this water was remarkably lower than that in the coastal area. group. Group D1 was mainly distributed in the layer that Serratosagitta pacifica, Pterosagitta draco (Krohn, 1853), was influenced by the NPIW. and Z. nagae were distributed across a wide temperature range (10–24°C), whereas the salinity range for these spe- Assemblages of species cies was mostly high with the exception of one sample. The inverse cluster analysis resulted in seven groups of Group 7 species [A. crassa (Tokioka, 1938), A. neglecta species at a similarity level of 20% (Fig. 6). The species (Aida, 1897), Ferosagitta ferox (Doncaster, 1902), Fe. ro- 48 H. Miyamoto et al.

Fig. 6. Dendrogram of species association (inverse) analysis. busta (Doncaster, 1902), and K. pacifica Aida, 1897] with the present study. The extremely high local diversity mostly occurred in the upper 30 m, and A. crassa was the in Sagami Bay is attributable to the influence of a variety only species that occurred on all sampling occasions of water masses that may be responsible for the observed (Table 1). All of the species in Group 7, except A. crassa, changes in species composition of chaetognaths, both in were found at high temperatures (24°C) from September to space and time, as discussed in the following paragraphs. January. The Heterokrohnia specimens occurred in the deepest samples, coinciding with several previous reports of their occurrence in near-bottom layers (Casanova & Chidgey Discussion 1987, 1990, Casanova 1992, 1994). Heterokrohnia bathybia We recorded the occurrence of 28 species of pelagic Marumo & Kitou, 1966 was reported in the western north chaetognaths in Sagami Bay, including the first record of Pacific (Marumo & Kitou 1966). The Heterokrohnia speci- Heterokrohnia specimens. The 27 species have already mens collected herein differ from H. bathybia in body been reported by Tokioka (1939), Marumo & Nagasawa length and the proportion of tail segment to body and ap- (1973), Nagasawa & Marumo (1977), and Miyamoto & pear to represent several undescribed species. Nishida (2011). This number represents approximately 30% In the present study, high species diversity was found of the global species richness of pelagic chaetognaths and during summer and autumn, and was attributed to the oc- is higher than that reported from other well-investigated currence of species regarded as tropical species (Marumo regions such as the Sargasso Sea (17 species: Pierrot-Bults & Nagasawa 1973), and which are included in Group 7. & Nair 2010), east Atlantic Ocean (20 species: Pierrot- This pattern is similar to the previous results of Nagasawa Bults & Nair 2010), Arctic Ocean (seven species: Sameoto and Marumo (1977), and is consistent with the seasonal 1987), Sulu and Celebes seas (22 species: Johnson & Ter- change of copepod diversity in the epipelagic layer of Sag- azaki 2006), South China sea and Gulf of Thailand (27 ami Bay (Shimode et al. 2006). In the meso- and bathype- species: Alvariño 1967, Rottman 1978), Indian Ocean (23 lagic layer (>400 m layer), the seasonal change in the di- species: Nair et al. 2002), Antarctic Ocean (six species: versity index was unclear in comparison with that in the Johnson et al. 2004), and off Chile (22 species: Fagetti epipelagic layer. The number of species and the diversity 1972). These studies covered depth ranges of approxi- index decreased with depth, which is consistent with previ- mately 1,000 m to the surface, and thus are comparable ous studies such as those from off Valparaíso, Chile (Ulloa Chaetognaths in Sagami Bay 49

Fig. 7. Relative standing stock (ind. m－2) of chaetognaths in relation to temperature and salinity. The areas of the circles represent percentages; the maximum standing stock (ind. m－2) during the observation in the present study is defined as 100%. Gray circles represent the density in the water strongly influenced by the Kuroshio current. A star indicates the weighted mean temperature (WMT) and salinity (WMS) for each species. Temperature and salinity indicating Kuroshio water, coastal water, and North Pacific Intermediate Water (NPIW) are shown by the grey symbols; the values are referenced from Iwata (1979) and Senjyu et al. (1998). 50 H. Miyamoto et al.

such as phytoplankton and detritus. They are highly effi- cient predators as they couple beating with their well-de- veloped muscles (Feigenbaum 1991) and mechano-recep- tion by ciliary fence receptors covering the whole body surface (Feigenbaum 1991, Bone & Goto 1991) in addition to the possible use of venom (Thuesen 1991). However, their feeding structures consist of a relatively simple as- semblage of hooks, teeth, and mouth and they are devoid of complex feeding appendages such as those found in copepods and ostracods. This may prevent them from exploit- ing diverse feeding niches that are potentially available in the mesopelagic depths (see also Ozawa et al. 2007). We identified four groups of samples based on their species composition. While the distribution of Group C was unclear due to the rarity occurrence of the species in the group, the distribution of the other groups was more closely related to depths than to seasons. The boundaries between these groups that were identified, i.e. 150 m and 400 m, coincide well with the 200 m and 500 m boundaries proposed by Marumo & Nagasawa (1973). The distribution of these groups corresponds with the vertical hydrographic structure in Sagami Bay. Group A was mainly distributed in the water mass formed by the mixing of Kuro- shio and coastal waters, while Group D was mainly in the NPIW. Group B was found in the transitional layers between the mixed epipelagic water and the NPIW. The seasonal change of the dominant species in the epi- Fig. 8. Vertical distribution of Pseudosagitta scrippsae, Para- pelagic layer (0–150 m) in Sagami Bay observed in the sagitta elegans and Eukrohnia hamata. present study was also reported by Nagasawa & Marumo (1977: Zonosagitta nagae in March–August, Flaccisagitta enflata in August–November, Serratosagitta pacifica in et al. 2000), the Sulu and Celebes seas (Johnson et al. December–February). We further observed that the com- 2006), and the waters south of the Kuroshio (Ozawa et al. munity was not homogeneous but was structured vertically 2007). This pattern contrasts with that observed in many within the upper 150 m in July, September, and November other pelagic animals, such as copepods and ostracods 2005. The boundary between the different assemblages (Roe 1972, Angel 1993, Yamaguchi et al. 2002, Shimode et corresponded with the thermocline and halocline, suggest- al. 2006, Kuriyama & Nishida 2006), in which species di- ing that the species composition was influenced by temper- versity peaks in the mesopelagic layer. In Sagami Bay, the ature and salinity. copepod diversity in June 1996 tended to increase with According to Nagai et al. (2006, 2008) the occurrence depth in the upper 200 m, but reached a plateau below that and abundance of chaetognath species is highly dependent layer (Shimode et al. 2006), which is considerably different on temperature, but only partially on salinity. In the pres- to the pattern observed in the chaetognaths in the present ent study, some species (e.g., Fl. enflata and A. regularis) study (July 2005). Shimode et al. (2006) reported that the were distributed across a wide range of salinities but over a community structure of copepods changed in the 200–300 narrow range of high temperatures. Conversely, Pterosa- m layer and that the copepods inhabiting below that depth gitta draco and Se. pacifica, as well as the species of consisted mainly of species with diverse feeding modes Group 5, occurred over a wide range of temperatures but (carnivores, suspension feeders, and omnivores) and tactics in a limited salinity range, while Z. nagae occurred within such as the use of venom (Nishida & Ohtsuka 1996), am- a wide spectrum of both temperature and salinity. It should bush predation (Matsuura & Nishida 2000), detection of be noted that these apparent differential influences of tem- chemical cues (Nishida & Ohtsuka 1997), and specialized perature and salinity according to the species distribution detritivory (Nishida et al. 2002). It has been suggested that may not be due to a direct response of the species to these food-resource partitioning is one of the major factors al- factors, but could rather reflect a complex mixing of waters lowing the co-existence of many species at mesopelagic and the ecological specificity of the population growth of depths (Kuriyama & Nishida 2006, Matsuura et al. 2010). any particular species in such waters. In contrast, pelagic chaetognaths are essentially carnivo- Marumo & Nagasawa (1973) reported the dominance of rous and are unable to utilize inactive organic particles Mesosagitta decipiens, M. neodecipiens, and Pseudosa- Chaetognaths in Sagami Bay 51

Table 2. Standing stock (ind. m－2) of Eukrohnia hamata and species closely-related to E. hamata in each area.

Juvenile of E. hamata & Sampling E. bathype- E. hamata & Area E. hamata E. bathype- Reference layer (m) lagica E. macro- lagica nuera Subpolar region Oyashio region 0–5,000 1,475 360 784 – Ozawa et al. 2007 Okhotsk Sea 0–2,000 970 273 1,315 – Ozawa et al. 2007 Bering Sea 0–3,000 2,164 512 1,945 – Ozawa et al. 2007 Georges Bank, western North Atlantic 0–max 1,000 43.5 1.8 – – Cheney 1985 Buffin Bay, North Atlantic 0–max 1,043 130–626 – – – Samemoto 1987 Australian sector, Southern Ocean 0–500 534–1,089 – – – Johnson & Terazaki 2004 Tropical-temperate region Oyashio-Kuroshio mixing region 0–5,000 – 54 – – Ozawa et al. 2007 Northern Sargasso Sea (33°N) 0–1,000 4–6 – – – Pierrot-Bults & Nair 2010 Northern Sargasso Sea (29°N) 0–1,000 1–5 – – – Pierrot-Bults & Nair 2010 Northern Sargasso Sea 0–max 1,000 0.9 0.05 – – Cheney 1985 Southern Sargasso Sea (24°N) 0–1,000 0 – – – Pierrot-Bults & Nair 2010 Southern Sargasso Sea (19°N) 0–1,000 4 – – – Pierrot-Bults & Nair 2010 Southern Sargasso Sea (14°N) 0–1,000 4–20 – – – Pierrot-Bults & Nair 2010 Eastern North Atlantic (11°N) 0–1,000 – – – 2 Pierrot-Bults & Nair 2010 Eastern North Atlantic (03°N) 0–1,000 – – – 18 Pierrot-Bults & Nair 2010 Eastern South Atlantic (13°S) 0–1,000 – – – 35 Pierrot-Bults & Nair 2010 Eastern South Atlantic (25°S) 0–1,000 – – – 16 Pierrot-Bults & Nair 2010 Off Varaiso, South Pacific 0–900 6.632 – – – Ulloa et al. 2000 Sagami Bay 0–max 1,400 194±131 – – – The present study gitta lyra in the mesopelagic layer in Sagami Bay. These in deeper layers than K. subtilis, M. decipiens, and Se. species coincide with the dominant species in Group B, pseudoserratodentata were less shallow in September, which was distributed within 150–400 m in the present suggesting that the species may have been less affected by study. However, Groups A3 and A4, which were dominated the upwelling. However the WMD of So. zetesios was in by Z. nagae, occurred at 150–300 m in May 2005 and the shallower range as for the other three species in Sep- 2006. In particular, the density of Z. nagae at 150–300 m tember. Terazaki (1973) and Terazaki & Marumo (1982) re- in May was highest among all samples. According to Na- ported that young individuals of So. zetesios were distrib- gasawa & Marumo (1977), Z. nagae actively reproduces uted in shallower layers (200–300 m) than adults, and were from May to July in the bay and is abundant in the epipe- abundant in summer in Sagami Bay. In our other study, the lagic layer. The present study clearly showed that Z. nagae young individuals without ovaries were also abundant in was also abundant in the mesopelagic layer during their re- the 200–400 m layer in September (unpublished data), in- productive season. dicating that the shallow WMD of So. zetesios is due to an It has been reported that meso- and bathypelagic chaeto- increase in number of young individuals. gnaths move to epipelagic layers by upwelling (Alvariño Group D was mainly distributed below 400 m and con- 1965, Ulloa et al. 2000, 2004, Noblezada et al. 2008). Dur- tained two sub-groups with a boundary at around 1,000 m, ing our observation, the occurrence of upwelling in the which coincides with the boundary between the NPIW and central part of the bay in September 2005 was suggested the Pacific Deep Water (Iwata 1986). It has been suggested from an offshore meandering of the Kuroshio paths (infor- that Parasagitta elegans and Ps. scrippsae, which are dis- mation provided by the Japan Coast Guard; Kanagawa Pre- tributed in the epipelagic layer of subarctic areas, inhabit fectural Fisheries Station). Also, in the vertical profile of areas below 600 m in Sagami Bay (Marumo 1966, temperature and salinity in the present study, the isopleths Marumo & Nagasawa 1973). Marumo (1966) reported that of 13°C and 34.5 salinity in September were shallower than these species occur in the mesopelagic layer due to the in- in the other seasons, suggesting the occurrence of upwell- trusion of subarctic water. In the present study, these spe- ing. Of the Group 5 species, Se. pseudoserratodentata, M. cies were distributed below 400 m and occurred in May, decipiens, and K. subtilis were found in shallower layers in September, and November 2005 and January 2006 when September compared to the other months, suggesting that low-salinity water (<34.2) was present at 400–800 m. Ac- the distributional range of the three species was pushed cording to Senjyu (1998) salinities of less than 34.2 indi- shallower by the upwelling. In contrast, the WMDs of all cate a strong intrusion of subarctic water in the mesope- species except Solidosagitta zetesios that were distributed lagic layer of Sagami Bay, suggesting that the abundance 52 H. Miyamoto et al. of the two boreal species is strongly influenced by subarctic water. References In regions north of 60°N Eukrohnia hamata occurs near Alvariño A (1965) Chaetognaths. 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