Plankton Benthos Res 9(1): 1–14, 2014 Plankton & Benthos Research © The Plankton Society of Japan

Seasonal and diel changes in the vertical distribution of oncaeid in the epipelagic zone of the Kuroshio Extension region

1, 2 3 4 HIROSHI ITOH *, KAORU NAKATA , KATSUYUKI SASAKI , TADAFUMI ICHIKAWA & 4 KIYOTAKA HIDAKA

1 Suidosha Co. Ltd., 8–11–11, Ikuta, Tama-ku, Kawasaki, 214–0038, Japan 2 Fisheries Research Agency, 15F, Queen’s Tower B, 2–3–3, Minato Mirai, Nishi-ku, Yokohama, 220–6115, Japan 3 1–15–422, Nishi 23, Minami 7, Chuou-ku, Sapporo, 064–0807, Japan 4 National Research Institute of Fisheries Science, 2–12–14, Fukuura, Kanazawa-ku, Yokohama, 236–8648, Japan Received 17 June 2013; Accepted 9 November 2013

Abstract: composition and vertical distribution of oncaeid copepods, which are potentially important prey for juvenile fish, were investigated in the Kuroshio Extension region, the NW Pacific, in April, August, November 1998 and February 2001. Samples were collected from 8 discrete layers in the epipelagic zone (0–200 m depth) using MOCNESS (0.064 mm mesh) during both day and night. Thirty-five oncaeid species were identified. ‘’ (s.l.) zernovi and Spinoncaea ivlevi were numerically the dominant species comprising 20.0–48.2% and 15.2–26.8%, re- spectively, of adult oncaeid copepods in the epipelagic zone. Cluster analysis on all samples revealed that these were separated into three groups with discrete vertical ranges; the first one appearing in the 0–50 m depth surface layer in April and August and consisting mainly of Oncaea (s. str.), the second one located in the deepest layer and composed mostly of ‘O.’ zernovi and S. ivlevi with some mesopelagic species, and the third one located above the second one and having intermediate species composition. Species-specific vertical distributions indicate that most oncaeid popula- tions shifted downward from August to November, when the thermocline remarkably descended. However, most On- caea spp. did not show a downward shift with the thermocline, and were positively correlated to appendicularian abundances, suggesting that appendicularian houses, known to be oncaeid habitats and to provide food, were a possi- ble factor affecting their vertical distribution. Niche partitioning, allowing coexistence of congeners, might be ex- plained by differences in body size and distribution layers in Oncaea and by differences in distribution layer in Trico- nia.

Key words: Copepoda, Kuroshio Extension, , seasonal change, vertical distribution

fish depends strongly on an adequate food supply, espe- Introduction cially on the supply of small copepods, spatial and tempo- The Kuroshio Extension region is in the northern part of ral changes in the fauna substantially influence the subtropical circulation of the NW Pacific, where water the recruitment of fish populations. The importance of temperatures show remarkable seasonal changes in the epi- small copepods as food supplies, has been shown by many pelagic zone due to its location in the temperate zone. This studies on the larvae and juveniles of Japanese sardine, the area is known to be important in the reproduction of com- Japanese anchovy Engraulis japonicus (Houttuyn), the mercially utilized fish species such as the Japanese sardine chub mackerel Scomber japonicus Houttuyn, the spotted Sardinops melanostictus (Temminck et Schlegel) and the mackerel Scomber australasicus Cuvier, and the Pacific Pacific saury Cololabis saira (Brevoort) (Noto & Yasuda saury in the transition area between the Kuroshio Exten- 1999, Tian et al. 2004). As the survival success of juvenile sion and the Oyashio Current (Takagi et al. 2009, Odate 1977). Especially in the case of the Pacific saury, occasion- * Corresponding author: H. Itoh; E-mail, [email protected] ally high relative abundances of oncaeid copepods (>70% 2 H. Itoh et al. of food items) in their stomach contents have been reported Materials and Methods (Odate 1977). Previous studies on in the Kuroshio Exten- Field sampling sion region revealed a higher zooplankton diversity con- sisting of warm water species but a low biomass compared Field surveys were conducted on 17 and 18 April to the Oyashio and the transition region (Odate 1962, (spring), 21 August (summer), 10 November (autumn) 1998 1980). However, since these studies used 335 μm mesh and 18 and 23 February (winter) 2001 at seven stations in nets, through which most small copepods are lost, our the Kuroshio Extension and the adjacent offshore regions, knowledge on the food environment provided by small- east of Honshu, Japan (Fig. 1) using the R.V. Soyo-Maru, sized copepods for fish larvae and juveniles is still limited. National Research Institute of Fisheries Science. The The present study used nets of 64 μm mesh to sample plankton samples were collected from eight discrete layers small oncaeid copepods in the epipelagic zone of the Kuro- (0–30 m, 30–50 m, 50–75 m, 75–100 m, 100–125 m, 125– shio Extension region; the term “oncaeid” in this study 150 m, 150–175 m, 175–200 m) by oblique hauls of a does not mean the genus Oncaea but the family Oncaei- MOCNESS (mouth area 0.25 m2, mesh opening 0.064 mm) dae. This family represents the main component in regard in the daytime (0900–1200) and nighttime (2100–2400); to numerical abundance and species richness of the small henceforth the day and night samples are referred to by the copepods in the area. Oncaeidae is a diverse family includ- letters “D” and “N”, respectively. Sampling was not con- ing more than 100 species (Böttger-Schnack et al. 2004), ducted at the same stations between daytime and nighttime and more than 40 species have been reported from the in the spring, autumn and winter investigations. The Kuro shio Current region of Japan (Nishibe et al. 2009). samples were immediately fixed and preserved in 5% Some species belonging to this family utilize appendicu- formalin-seawater solution. The volume of filtered water larian houses as their habitat and food (Ohtsuka et al. was estimated from the reading of a flow meter (Tsurumi- 1993), suggesting that the abundance of oncaeid copepods Seiki Co. Ltd., Japan) attached to the mouth of the net. may be related to appendicularian abundances. The vertical profiles of temperature and salinity were The vertical distribution of oncaeid copepods has been measured with a CTD (SBE 9 plus, Sea-Bird Electronics, investigated previously in the Atlantic Ocean (Boxshall Inc., USA) incorporated on a rosette sampler at each sta- 1977), the Mediterranean Sea (Böttger-Schnack 1994, tion. The CTD data in August were measured only in the 1997), the Adriatic Sea (Krŝinić 1998), the Red Sea (Bött- daytime since sampling was done at the same station in the ger 1987, Böttger-Schnack 1988, 1990a, b, 1992, 1995, daytime and nighttime. Water samples for chlorophyll-a Böttger-Schnack et al. 2001, 2004, 2008), the Arabian Sea (Chl a) concentration determination were collected by a ro- (Böttger-Schnack 1994, 1996), the Indian Ocean (Tsalkina sette sampler equipped with Niskin bottles at 0, 10, 30, 50, 1972), the South Pacific Ocean (Heron & Bradford-Grieve 75, 100, 125, 150 and 200 m depths. From each depth, a 1995), and the North Pacific Ocean (Furuhashi 1966, 200 mL water sample was filtered on a Whatman GF/F fil- Zalkina 1970, 1977, Nishibe & Ikeda 2004, Nishibe et al. ter, then transferred to a plastic vial containing 6 mL of di- 2009). Most of these studies have dealt with large scale methylformamide (Suzuki & Ishimaru 1990) and stored at vertical distributions from the surface to the bathypelagic －80°C until Chl a concentration was measured in the lab- zone. In contrast, the present study investigated seasonal oratory with a fluorometer (Turner 10-AU, Turner Designs, and diel changes in the fine scale vertical distributions of oncaeid copepods in the epipelagic zone of the Kuroshio Extension region, where there has as yet been no studies on the vertical distribution of oncaeid copepods. After the intensive taxonomic revision of oncaeid copepods of the last two decades (e.g. Heron & Bradford-Grieve 1995, Böttger-Schnack 1999, 2001, 2002, 2003, 2005), this is the second report (after Nishibe et al. 2009) of the species- specific vertical distribution and the first report of their vertical diel migration in the subtropical Pacific Ocean following the up-to-date of oncaeid copepods. The results are discussed with respect to abiotic and biotic environmental factors, mechanisms of coexistence of congeneric species, and their potential significance as food resources for fish larvae and juveniles.

Fig. 1. Location of sampling stations, off south–eastern Japan. Vertical distribution of oncaeid copepods 3

Inc., USA). ners by a dorsal projection on the first pedigerous somite. Three forms (large, medium and small forms) of Oncaea Enumeration and species identification venusta Philippi, 1843 occurred, and they were distin- In the laboratory, large organisms such as medusae and guishable from each other by differences in body length, chaetognaths were removed from the whole sample before shape of the second thoracic segment and morphology of subsampling. A 5% formalin-seawater solution was added the genital double-somite (see Böttger-Schnack & Huys to the whole sample to adjust its volume to 50, 100 or 2004). According to a recent molecular analysis (Elvers et 200 mL. Subsampling from the adjusted sample with a al. 2006), the large and small forms of O. venusta represent 1 mL Stempel pipette and enumeration under a stereomi- different genetic lineages, whereas the medium form in- croscope were repeated until the total number of enumer- cludes two genetic lineages. ated copepods exceeded 200 for enumeration of total cope- To investigate the size-dependent niche partitioning of pods and appendicularians, and until the total number of coexisting species in the same depth layer, body length adults exceeded 300 for oncaeid copepods. (from the anterior end of head to the posterior end of the Species identification followed Shmeleva (1969), furca) was measured for 20 females of the target species Gordeyeva (1972), Heron (1977), Krŝinić & Malt (1985), belonging to Oncaea and Triconia collected in August Boxshall & Böttger (1987), Böttger-Schnack & Boxshall 1998. (1990), Heron & Bradford-Grieve (1995), Böttger-Schnack Data analysis (1999, 2001, 2002, 2003, 2005), Huys & Böttger-Schnack (2007) and Wi et al. (2011). Taxonomic classification of the The data analyses of vertical distribution were per- genera followed Boxshall & Halsey (2004), Böttger- formed for the 23 species for which the lowest count in a Schnack (2001) and Böttger-Schnack & Schnack (2013). subsample exceeded 10 individuals. The family Oncaeidae currently consists of seven genera, For the cluster analysis of oncaeid communities, the of which three, i.e. Triconia, Monothula and Spinoncaea, Bray-Curtis dissimilarity index was calculated using popu- have species moved from Oncaea. Although Böttger- lation density values transformed by log (x＋1), and ordina- Schnack (2001) redefined the diagnostic characters of On- tion on a two dimensional map by non-metric multidimen- caea, some species that do not belong to Oncaea sensu sional scaling (NMDS) was also conducted. Construction Böttger-Schnack (2001) are still classified into the genus of the dendrogram and NMDS were performed using the Oncaea. As a result, the name Oncaea presently has two add-in software packages “Cluster analysis Ver. 3.3” (Haya- meanings, i.e. Oncaea sensu Philippi (1843) and Oncaea kari 2001) and Systat 11 (HULINKS Inc.), respectively. sensu Böttger-Schnack (2001); in some papers they are re- Relationships between the communities and environ- ferred to as Oncaea sensu lato (s. l.) and Oncaea sensu mental factors were shown on the NMDS ordination map stricto (s. str.), respectively. To simplify the genus and spe- with arrows indicating gradients of the factors according cies names in the following text and to follow the latest to Kruskal & Wish (1978). To test the relationship between taxonomy of Oncaeidae, we use the name Oncaea only for population density of each species and environmental fac- Oncaea s. str. and ‘Oncaea’ for Oncaea s. l. instead of add- tors, Spearman’s rank correlation coefficient was calcu- ing these Latin phrases to every species name between its lated. generic and specific names. Males of Triconia, except for For the description of vertical distributions, the depths

T. conifera (Giesbrecht, 1891) and T. furcula, were com- of 25th, 50th, 75th percentiles of a population (D25%, D50%, piled into two groups [T. elongata Böttger-Schnack, 1999 + D75%) were calculated for each species. Interspecific com- allied species and T. minuta Giesbrecht, 1892 + allied spe- parison of D50% was done by the Wilcoxon signed-rank cies] because they were easily distinguished at the group test. level but were difficult to identify to species level with the An analysis of variance (ANOVA) was carried out with limited magnification (×40 or 100) of the stereomicro- the mean population density among communities and body scope. Specimens identified as Spinoncaea ivlevi (Shmel- length among species. Tukey’s procedure was used as a eva, 1966) and ‘Oncaea’ zernovi Shmeleva, 1966 may have post hoc test when the ANOVA was significant. included their sibling species S. humesi Böttger-Schnack, 2003 and ‘O.’ bispinosa Böttger-Schnack, 2002, respec- Results tively, because of the difficulty in identification under low magnification. These sibling species have recently been Hydrographic conditions reported from Tosa Bay (Nishibe et al. 2009), which is located upstream of the Kuroshio Extension. Individuals Water temperature at the sea surface showed a remark- referred to as ‘O.’ vodjanitskii Shmeleva & Delalo, 1965 able seasonal change between 18.8 and 29.2°C, whereas it included ‘O.’ vodjanitskii and a species similar to ‘O.’ ranged only from 16.0–18.8°C at 200 m depth (Fig. 2). atlantica Shmeleva, 1967. ‘Oncaea’ sp. 1, an undescribed Mean temperature in the surface mixed layer (defined as small species of 0.25 mm body length, is allied to ‘O.’ the layer from the sea surface to just above the seasonal vodjanitskii, but could be clearly separated from its conge- thermocline) was 19.1–19.6°C in April, 29.1°C in August, 4 H. Itoh et al.

Fig. 2. Vertical profiles of temperature (Temp), salinity (Sal) and chlorophyll-a (Chl a) concentration.

24.0–24.4°C in November and 18.7°C in February. A weak time and nighttime in April. In August, their abundance thermocline（defined as Δt >0.1°C m－1）was found at was higher at night than in the daytime, and high abun- around 50–60 m depth in April, whereas a strong thermo- dances were observed above 125 m (D) or 150 m depth cline was found at 25–95 m depth in August and at 90– (N), which was much deeper than the thermocline at 160 m depth in November. In February, a weak thermo- 25–95 m depth. In November, although the abundance was cline was found at 120–153 m depth in the daytime, low, they were concentrated in the 0–100 m (D) or whereas the water column was well mixed showing only 0–125 m (N) layer just above the thermocline. In February, slight traces of a thermocline at around 190 m depth in the the depth limits of high abundance (>5×102 ind. m－3) were nighttime. 125 m (D) and 100 m depth (N). Salinity ranged from 34.09–34.74 in the surface layer, Vertical distribution of copepods and from 34.61–34.82 at 200 m depth (Fig. 2). A remark- able halocline was found in the upper part of the thermo- Abundance of copepods was generally high cline in August and November due to low salinity (<34.5) (>3×103 ind. m－3) in the surface layer above 50–125 m above the halocline. In April and February, salinity was depth and was low (<2×103 ind. m－3) in the layers deeper high (>34.6) and uniform throughout the 0–200 m water than 150 m during all seasons (Fig. 3). The highest abun- column. dance of 16×103 ind. m－3 was found in the 0–30 m layer at night in February. The seasonal pattern of the vertical dis- Vertical distribution of chlorophyll-a concentration tribution of copepods was similar to that of appendiculari- Chl a concentrations were high in the shallower layers. ans. That is, high abundances of >3×103 ind. m－3 were ob- Layers where the value exceeded 0.2 mg m－3 were shal- served in the layers above 50 m in April, 125 m in August, lower than 100 m in April and in August, shallower than 125 m (D) and 100 m (N) in November, and 150 m (D) and 75 m in November, and shallower than 100 m (D) and 125 m (N) in February. In these upper layers, Calanoida 125 m (N) in February (Fig. 2). In August, Chl a concen- and Cyclopoida generally accounted for the major portion trations peaked (0.41 mg m－3) at 100 m depth just below of the copepod community, whereas oncaeid copepods the thermocline, and low concentrations (<0.2 mg m－3) were >50% in the deeper depths. The seasonal patterns of were found from the sea surface to 50 m depth. It was abundance of oncaeid copepods were largely similar to <0.1 mg m－3 in the layers below 150 m depth during all those of total copepods, but oncaeid copepods were gener- seasons except at 200 m depth in February (D). ally more evenly distributed in the 0–200 m water column than total copepods. The abundance of oncaeid copepods Vertical distribution of appendicularians was highest (3.6×103 ind. m－3) in the 75–100 m depth layer Abundance and vertical distribution of appendicularians at night in August, while the abundance in the 0–30 m sur- showed an apparent seasonal variation (Fig. 3). Their abun- face layer was higher, especially at night, in April and Feb- dance was higher in August and February than in April ruary than in August and November. and November, with the maximum abundance of 1.1×103 ind. m－3 in the surface layer at night in August. They were concentrated in the 0–50 m layer in both day- Vertical distribution of oncaeid copepods 5

Fig. 3. Vertical distribution of abundance of appendicularians (top) and copepods (lower). Solid lines in the bottom panels indicate proportion (%) of oncaeids with respect to total copepods.

Seasonal fluctuation in the number of species and abun- 20.0–48.2% and 15.2–26.8%, respectively. The most abun- dance of adult oncaeid copepods dant species after these two species were Oncaea media A total of 35 species, consisting of one species of Epica- and O. scottodicarloi, which comprised 16.6% in August lymma, six species and three forms of Oncaea, two species (N) and 12.4% in February (N), respectively, when they of Spinoncaea, 11 species of Triconia, and 13 species of were most abundant. ‘Oncaea’ were identified (Table 1). On each sampling occa- Community analysis sion, 24–33 species were collected, of which 24 species were found during all four seasons. The largest number of From a total of 64 samples collected in the present study, species (33) was found in August (N), whereas the smallest 63 samples could be allocated to one of three groups, de- number (24) occurred in February (N) because of the dis- fined as Communities A1, A2 and B, which were separated appearance of some mesopelagic species such as ‘Oncaea’ by a Bray-Curtis dissimilarity index of 0.43 (Fig. 4A). prendeli Shmeleva, 1966 and ‘O.’ tregoubovi Shmeleva, Only the sample from 125–150 m at night in February did 1968. Abundance of adult oncaeid copepods in the epipe- not cluster with any other sample. In the ordination by lagic zone (0–200 m depth) ranged from 47×103– NMDS, Communities A1 and A2 overlapped slightly with 141×103 ind. m－2, of which the maximum value was found each other, but were distinguishable from Community B, in August (N). A high abundance (>100×103 ind. m－2) was supporting the result of the cluster analysis (Fig. 4B). also found in February (D, N). Abundance was smallest in Community A1, consisting mainly of species of Oncaea November (<55×103 ind. m－2 in both D and N). There (especially O. media), had the lowest number of species were no remarkable seasonal or diel variations in species compared with the other communities (Table 2). Commu- compositions in the epipelagic zone. Species that ac- nity A2, which included Spinoncaea ivlevi, ‘Oncaea’ zer- counted for more than 5% of adult oncaeid copepods at novi with species of Oncaea (mostly O. scottodicarloi, O. least once in a sampling occasion were ‘Oncaea’ zernovi media and O. waldemari), had the highest abundance com- (maximum: 48.2%), Spinoncaea ivlevi (26.8%), Oncaea pared with the other communities. Community B was media Giesbrecht, 1891 (16.6%), O. scottodicarloi Heron & formed by small oncaeid copepods (<0.4 mm in body Bradford-Grieve, 1995 (12.4%), S. tenuis Böttger-Schnack, length) such as S. ivlevi, S. tenuis，‘O.’ vodjanitskii and ‘O.’ 2003 (12.0%), ‘O.’ vodjanitskii (9.9%), O. mediterranea zernovi with some mesopelagic species (e.g. ‘O.’ crypta and (Claus, 1863) (9.4%) and Triconia elongata Böttger- ‘O.’ parabathyalis). This community occupied numerically Schnack, 1999 (6.4%). Among them, ‘Oncaea’ zernovi and the highest proportion of the whole copepod community in Spinoncaea ivlevi were the most and the second most the lower epipelagic layer. abundant species on all sampling occasions, comprising The directions of the arrows in the NMDS plot indicate 6 H. Itoh et al. % 0.3 0.3 0.2 0.4 1.0 8.8 1.0 0.5 2.1 3.0 3.9 1.2 0.6 0.2 2.1 0.4 0.3 0.6 12.4 16.4 44.0 <0.1 <0.1 <0.1 <0.1 <0.1 Night 25 78 38 24 26 114 415 407 229 493 539 748 228 423 398 770 n 1184 1215 2566 3564 4601 1458 2565 10464 14765 19583 52569 119463 Feb. 2001 % 0.8 0.2 0.3 0.1 1.9 0.7 8.9 0.8 0.5 2.4 0.2 1.4 3.0 0.4 0.9 1.2 0.1 0.4 15.2 12.0 48.2 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 Day 13 51 62 69 67 67 25 919 205 366 141 865 941 619 216 492 126 468 n 2158 2761 1688 3513 1076 1353 10400 17758 13988 56141 116520 % 1.4 0.1 0.3 1.1 0.2 0.2 0.9 3.8 1.3 5.2 1.8 2.4 3.0 2.9 1.0 0.3 2.9 0.7 7.8 0.1 0.8 1.3 1.7 1.3 1.0 16.2 15.1 24.9 <0.1 <0.1 <0.1 Night 61 17 13 25 51 29 111 n 690 122 543 102 432 645 859 469 157 329 376 607 800 645 481 1137 1824 2468 1455 1370 7736 7234 1390 3750 11917 47814 Nov. 1998 Nov. % 2.4 0.2 0.8 0.1 2.0 6.5 1.6 5.4 0.9 2.6 4.4 3.9 3.3 0.7 0.5 1.5 0.3 9.9 0.6 2.1 1.9 0.5 0.7 26.8 20.0 <0.1 <0.1 <0.1 <0.1 <0.1 Day 37 74 35 44 13 43 28 n 120 430 891 505 389 284 829 158 275 384 337 1116 1156 1295 3575 2977 1421 2415 2159 1788 5398 1032 14656 10934 54767 % 4.0 0.2 0.2 1.2 0.1 0.6 3.7 5.7 0.2 1.5 0.6 1.3 2.0 1.2 0.3 0.2 0.2 0.3 5.4 0.1 2.0 1.7 0.5 1.1 0.5 3.1 16.6 22.7 22.5 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 Night 44 96 33 39 39 293 351 201 101 880 312 832 354 307 274 n 467 156 132 713 697 5680 1644 5231 8070 2077 1869 2789 1715 7623 2853 2390 4335 1514 23490 32092 31871 141534 Aug. 1998 % 6.4 0.2 1.2 0.2 9.4 7.9 0.2 1.3 0.6 1.5 2.4 1.3 0.3 0.2 0.3 0.1 8.1 0.2 0.1 2.6 1.5 0.2 1.0 0.2 1.4 0.2 10.5 20.4 20.0 <0.1 <0.1 <0.1 <0.1 Day 69 48 50 48 90 90 31 n 147 981 150 150 450 234 120 234 130 151 166 787 128 1175 1150 1141 5020 8303 7407 6241 1005 1890 1026 6357 2019 16057 15706 78722 % 0.6 0.1 1.2 0.2 6.7 1.9 9.9 0.3 2.7 1.7 1.0 6.8 0.6 1.7 0.2 0.1 0.2 0.1 4.2 0.3 2.2 0.9 0.5 1.5 1.8 16.2 36.2 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 Night 41 25 31 68 95 13 31 13 n 529 102 184 238 881 520 175 155 101 221 725 441 1012 1275 5662 1567 8306 2313 1464 5697 1393 3540 1854 1522 13625 30456 84243 Apr. 1998 Apr. % 1.7 0.1 0.4 0.7 0.2 5.5 1.3 9.5 0.3 4.0 2.3 1.1 9.1 0.6 0.6 0.1 0.4 0.2 0.9 6.3 0.6 2.0 1.0 2.2 0.3 15.5 32.9 <0.1 <0.1 <0.1 <0.1 Day 85 20 25 46 90 39 29 n 110 304 477 132 910 234 741 413 446 275 665 416 733 191 1167 4411 3848 6641 2814 1644 6415 1377 1558 10855 23097 70175 Sex F F, M F F F F F F F, M F, M F, M F, M F, M F, M F, M F, M F, M F, M F, M F F F, M F, M F, M F, M F, M F, M F, M F F, M M M F, M F, M M F, M F, M ) and numerical composition (%) of adult oncaeid copepods in the 0–200 m water column in the Kuroshio Extension. The abundances of small 2 － , ind. m may include those their of congeneric or sibling species text). (see * n * Species Heron & Bradford-Grieve, 1995 * Boxshall & Böttger, 1987 Boxshall & Böttger, Böttger-Schnack, 1999 Böttger-Schnack, Shmeleva, 1968 Gordejeva, 1972

Shmeleva, 1966 (Wi, Shin & Soh, 2011) (Wi, * Böttger-Schnack, 1999 Böttger-Schnack, +allied species Abundance( (Heron & Bradford-Grieve, 1995) Früchti, 1923 (Shmeleva, 1966) T. elongata T. (Farran, 1936) furcula T. giesbrechti T. minuta Giesbrecht, 1892 T. redacta T. similis (Sars, 1918) T. & Boxshall, 1990) umerus (Böttger-Schnack T. T. derivata (Heron & Bradford-Grieve, 1995) T. O. clevei O. media Giesbrecht, 1891 O. mediterranea (Claus, 1863) O. scottodicarloi form O. venusta Philippi, 1843 large O. venusta Philippi, 1843 medium form O. venusta Philippi, 1843 small form O. waldemari Bersano & Boxshall, 1994 S. ivlevi 2003 S. tenuis Böttger-Schnack, conifera (Giesbrecht, 1891) T. denticula T. dentipes (Giesbrecht, 1891) T. Böttger-Schnack, 2009 E. bulbosa Böttger-Schnack, ‘ O. ’ parila Heron, 1977 ‘ O. ’ prendeli ‘ O. ’ shmelevi Shmeleva, 1968 ‘ O. ’ tregoubovi ‘ O. ’ vodjanitskii ‘ O. ’ zernovi ‘ O. ’ sp. 1 ‘ O. ’ platysetosa T. elongata T. minuta +allied species T. 2005 ‘ O. ’ crypta Böttger-Schnack, ‘ O. ’ longipes Shmeleva, 1968 ‘ O. ’ longiseta 2005 ‘ O. ’ parabathyalis Böttger-Schnack, ‘ O. ’ minima Shmeleva, 1968 Oncaea s. str. Spinoncaea Triconia Epicalymma Total number of taxa number Total abundance Total ‘ Oncaea ’ species marked with an Table 1. 1. Table Vertical distribution of oncaeid copepods 7

Fig. 4. Cluster (A) and non-metric multidimensional scaling ordination (B) analyses for grouping of communities (samples) and vertical distributions of each community (C). Sample names in (A) were composed of month (Ap, April; Au, August; N, November; F, February), time (D, daytime; N, nighttime) and depth of sampling layer (m). Arrows in (B) indicate gradients of environmental parameters from low to high. that temperature, Chl a concentration and appendicularian cific differences of mean D50% throughout the four seasons abundance were more positively correlated with Commu- were statistically significant between some species/forms, nities A1 and A2, and that depth, salinity, and σt were more e.g. O. venusta large form was shallower than O. mediter- positively correlated with Community B (Fig. 4B). Among ranea, O. media was shallower than O. scottodicarloi and these factors, appendicularian abundance differed greatly O. venusta small form was shallower than O. meditteranea between the communities, i.e. their abundances in commu- etc. (p<0.05). The vertical distribution of each species/ nities A1 and A2 were about 10 times higher than in Com- form changed seasonally. The D50% in April (D, N) and in munity B (Table 2). Community A1 appeared only in April February (N) was shallower than 50 m in all species/forms

(D) and August (D, N) and was distributed in the upper- of Oncaea, whereas the D50% in the daytime was deeper most (0–30 or 0–50 m) layer. Community A2 was located than 50 m in November in O. clevei Früchtl, 1923 and O. above 50 m depth in April and 100–125 m depths in the venusta large form, and in August and November for all other seasons. Community B was always distributed below the other species/forms. Although the seasonal thermo- Community A2. The seasonal pattern of the community cline shifted downward by ca. 50 m from August to No- distribution was similar to that of the depth of the thermo- vember, D50% did not show a downward shift parallelling cline (Figs. 2, 4C). the thermocline, except for O. clevei, which apparently shifted downward in distribution from August to Novem- Vertical distribution of oncaeid copepods ber. For O. waldemari, O. venusta medium form, O. ve-

The layer between D25% and D75% (henceforth “D25–75% nusta small form, O. media, O. mediterranea and O. scot- layer”) of the species/forms of Oncaea were located in the todicarloi, the diel change of D50% in each season indicated thermocline and/or surface mixing zone and they usually an upward nocturnal migration as described for oncaeid overlapped with each other (Fig. 5). However, the interspe- copepods in previous investigations (e.g. Zalkina 1970, 8 H. Itoh et al.

Table 2. Mean abundance (ind. m－3) of adults of the analyzed species, total oncaeid copepods including immature copepodids, and ap- pendicularians in the three distinct communities. p is significance probability in one-way ANOVA for differences among the three com- munities (***: p<0.001, **: p<0.01, *: p<0.05). Underlines indicate maximum values and values with no difference (p>0.05) from maxi- mum values accoding to Tukey’s post-hoc test.

Community Species p A1 A2 B Oncaea clevei 4.1 1.8 0.0 *** O. media 67.3 30.3 0.8 *** O. mediterranea 3.2 9.2 2.4 *** O. scottodicarloi 6.6 45.5 8.2 *** O. venusta large form 4.2 1.8 0.0 *** O. venusta medium form 16.7 9.6 0.6 *** O. venusta small form 7.8 9.0 0.4 *** O. waldemari 1.0 15.1 0.6 *** Spinoncaea ivlevi 1.4 64.2 36.7 *** S. tenuis 2.4 1.0 22.2 *** Triconia conifera 0.7 2.3 1.8 T. denticula 0.0 0.1 2.2 *** T. elongata 0.6 4.4 2.9 T. furcula 0.4 0.7 0.2 * T. giesbrechti 0.0 1.3 0.0 *** T. minuta 0.5 3.2 2.1 * T. umerus 0.2 1.6 2.6 * ‘Oncaea’ crypta 0.0 0.0 1.5 *** ‘O.’ minima 0.0 0.1 2.6 *** ‘O.’ parabathyalis 0.0 0.0 7.4 *** ‘O.’ tregoubovi 0.0 0.1 0.6 * ‘O.’ vodjanitskii 0.0 9.2 25.1 *** ‘O.’ zernovi 18.0 119.1 105.4 ** Number of Species 11.4 15.2 14.7 * Abundance of oncaeid copepods (ind. m－3) 583.8 1310.5 644.5 *** Proportion of oncaeid copepods in whole 16.7 30.7 60.9 *** copepod community (%) Abundance of appendicularians (ind. m－3) 516.7 449.7 45.4 ***

1977, Boxshall 1977, Böttger-Schnack 1990a, b). D25–75% layers mostly in the surface mixed layer and in the Of the genus Spinoncaea, the D25–75% layer was found thermocline, respectively. The D25–75% layer of the latter above 150 m depth in S. ivlevi and below 150 m depth in S. species shifted downward with the thermocline from April tenuis. The D25–75% layer of the former species showed a to November and expanded in February. Regarding Trico- downward shift from April to August and no difference nia minuta Giesbrecht, 1892, T. umerus (Böttger-Schnack between August and November. It expanded in February & Boxshall, 1990) and T. denticula Wi et al., 2011 belong- and shifted considerably shallower at nighttime. The latter ing to the similis-subgroup (Böttger-Schnack 1999), the species exhibited no seasonal change in the depth of the D25–75% layer of the former two species was in or around D25–75% layer. the thermocline and showed a downward shift with the The D25–75% layer of Triconia conifera and T. furcula, be- thermocline from August to November. Triconia denticula longing to the conifer-subgroup (Böttger-Schnack 1999), was always distributed below the thermocline. Although was mostly below the thermocline in the daytime, but, con- the D25–75% layer of the former two species partially over- trastingly, was in the thermocline and/or the surface mixed lapped each other, the D50% of T. minuta was shallower layer in the nighttime. The D50% of the latter species was than that of T. umerus (p<0.05). The D25–75% layers ex- deeper than that of the former species (p<0.05) and the panded in February and shifted upward especially in the

D25–75% layer of the latter species expanded in the daytime. nighttime. Triconia conifera is well-known as a nocturnal upward mi- As for the species of ‘Oncaea’, the D25–75% layers of ‘O.’ grant (e.g. Zalkina 1970, 1977, Boxshall 1977, Böttger- zernovi and ‘O.’ vodjanitskii were found in or below the Schnack 1990a, b). Triconia giesbrechti Böttger-Schnack, thermocline and shifted downward from April to Novem- 1999 and T. elongata Böttger-Schnack, 1999, belonging to ber followed by an upward shift at nighttime in February. the dentipes-subgroup (Böttger-Schnack 1999), exhibited In the remaining four species, ‘O.’ tregoubovi, ‘O.’ minima Vertical distribution of oncaeid copepods 9

Fig. 5. Vertical distribution of oncaeid copepods in April (Ap), August (Au), November (N) 1998 and February (F) 2001.

Solid vertical bars indicate the layer between the depths of the 25th and 75th percentile population (D25–75%, layer in the text). Open and closed circles indicate depths of 50 th percentile population (D50% in the text) in the daytime and nighttime, respec- tively. Broken lines indicate range of thermocline (>0.1°C m－1).

Shmeleva, 1968, ‘O.’ parabathyalis Böttger-Schnack, 2005 tration and appendicularian abundance, but their densities and ‘O.’ crypta Böttger-Schnack, 2005, the D25–75% layer were significantly positively correlated to depth, salinity was deeper than in ‘O.’ zernovi and ‘O.’ vodjanitskii and ex- and σt. hibited a downward shift or entirely disappeared from the Body length of females of Oncaea and Triconia epipelagic zone in February. Mean body length of females of Oncaea spp. ranged Relationship between population density and environ- from 0.48 mm (O. waldemari) to 1.19 mm (O. venusta mental factors in oncaeid copepods large form) (Table 4). The interspecific differences in their Population densities of Oncaea spp. and Triconia gies- body length were significant (p<0.001) within the genus, brechti were significantly positively correlated (p<0.01) to except for the differences between O. clevei and O. scot- Chl a concentration and appendicularian abundance and, todicarloi and between O. venusta medium form and O. except for O. scottodicarloi, to water temperature (p<0.05) mediterranea (p>0.05). Mean body length of females of (Table 3). In contrast, population densities of Spinoncaea Triconia ranged from 0.45 mm (T. giesbrechti) to 1.14 mm tenuis, T. denticula and most species of ‘Oncaea’, excluding (T. conifera). The interspecific differences were significant ‘O.’ zernovi, were not positively correlated to Chl a concen- (p<0.001), except for the differences between T. gies- 10 H. Itoh et al.

Table 3. Spearman's rank correlation coefficients between abundance and evironmental parameters for the analyzed species. Significance probability: **, p<0.01; *, p<0.05.

Water Abundance of species Depth Salinity σ Chlorophyll-a temperature t appendicularians

Oncaea clevei －0.373** 0.567** －0.542** －0.362** 0.600** 0.539** O. media －0.705** 0.527** －0.450** －0.569** 0.653** 0.516** O. mediterranea －0.393** 0.305* 0.072 －0.320* 0.373** 0.433** O. scottodicarloi －0.463** 0.078 －0.028 －0.143 0.461** 0.680** O. venusta large form －0.396** 0.623** －0.388** －0.342** 0.647** 0.683** O. venusta medium form －0.754** 0.510** －0.443** －0.522** 0.727** 0.588** O. venusta small form －0.678** 0.577** －0.460** －0.572** 0.671** 0.780** O. waldemari －0.476** 0.278* －0.424** －0.307** 0.663** 0.666** Spinoncaea ivlevi 0.006 －0.068 0.246* 0.060 －0.047 0.257* S. tenuis 0.650** －0.529** 0.430** 0.608** －0.536** －0.594** Triconia conifera －0.012 0.131 0.317** －0.064 －0.087 0.114 T. denticula 0.701** －0.374** 0.522** 0.632** －0.466** －0.513** T. elongata 0.004 0.122 0.327** －0.110 0.014 0.205 T. furcula －0.048 0.150 0.018 0.098 0.275* 0.321** T. giesbrechti －0.157 0.274* －0.196 －0.105 0.550** 0.628** T. minuta －0.032 0.051 0.231 －0.064 0.023 0.208 T. umerus 0.271* －0.272* 0.421** 0.306* －0.228 －0.185* ‘Oncaea’ crypta 0.723** －0.082 0.503** 0.606** －0.193 －0.181 ‘O.’ minima 0.784** －0.281* 0.485** 0.518** －0.532** －0.524** ‘O.’ parabathyalis 0.824** －0.393** 0.459** 0.637** －0.556** －0.552** ‘O.’ tregoubovi 0.624** 0.178 0.527** 0.435** －0.045 －0.024 ‘O.’ vodjanitskii 0.473** －0.224 0.532** 0.285* －0.487** －0.322** ‘O.’ zernovi 0.034 －0.436** 0.115 0.394** 0.074 0.273*

Table 4. Body length of females of Oncaea and Triconia collected from the Kuroshio Extension in August 1998.

Body Length (mm) Species n Range Average SD

Oncaea waldemari 20 0.45–0.50 0.48 0.016 O. scottodicarloi 20 0.58–0.65 0.62 0.021 O. clevei 20 0.58–0.69 0.64 0.029 O. media 20 0.69–0.77 0.72 0.023 O. venusta small form 20 0.81–0.95 0.87 0.036 O. venusta medium form 20 0.90–1.09 0.98 0.054 O. mediterranea 20 0.92–1.12 0.98 0.041 O. venusta large form 20 1.09–1.33 1.19 0.065 Triconia giesbrechti 20 0.41–0.48 0.45 0.017 T. elongata 20 0.43–0.49 0.46 0.015 T. minuta 20 0.51–0.57 0.54 0.018 T. denticula 20 0.52–0.61 0.56 0.023 T. umerus 20 0.60–0.69 0.66 0.023 T. furcula 20 0.95–1.14 1.07 0.045 T. conifera 20 1.04–1.23 1.14 0.063 brechti and T. elongata, and between T. minuta and T. den- based on the data in August. The results showed that the ticula (p>0.05). These two exceptions belong to the same variation of D50% among the species/forms of Oncaea, ex- subgroups (dentipes-subgroup and similis-subgroup), re- cluding O. venusta large form, was greater in the nighttime spectively. than in the daytime (Fig. 6A). No correlation was found

The relationships between D50% and body length were between D50% and body length in these species/forms. examined for Oncaea and Triconia using scatter diagrams However, it is notable that two pairs of species/forms hav- Vertical distribution of oncaeid copepods 11

Fig. 6. Scatter diagrams of body length vs. depth of 50th percentile population of Oncaea (A) and Triconia (B) in August, 1998. Open circles and cross symbols represent daytime and nighttime samples, respectively. Abbreviations of the species/form names are the same as in Fig. 5. ing similar body lengths, viz. O. clevei and O. scottodicar- the present study was only 35 because of combining some loi of ca. 0.6 mm and O. venusta medium form and O. small species during the analysis and limitation of the mediterranea of ca. 1.0 mm, had very different nighttime sampling layer to the epipelagic zone, 33 of the species

D50%s, and that three pairs of species/forms with similar were common to Tosa Bay. Of the nine dominant species nighttime D50%s, viz. O. media and O. venusta medium in Tosa Bay (Nishibe et al. 2009), Oncaea media, O. scot- form with ca. 40 m D50%, O. waldemari and O. venusta todicarloi, Spinoncaea ivlevi, S. tenuis and ‘Oncaea’ zer- small form with ca. 60 m D50%, and O. scottodicarloi and novi were also the dominant oncaeid copepods in the Ku- O. mediterranea with ca. 75 m D50%, differed considerably roshio Extension. The three communities (A1, A2 and B) in body length within each pair. The differences in body detected in the present study were largely the same as the length between species/forms of these pairs were 1.4 times three communities reported in Tosa Bay, i.e. the upper epi- between O. media and O. venusta medium form, 1.8 times pelagic community predominated by O. venusta, O. media between O. waldemari and O. venusta small form, and 1.6 and O. waldemari, the lower epipelagic community domi- times between O. scottodicarloi and O. mediterranea. Al- nated by O. scottodicarloi, ‘O’. zernovi, ‘O’. bispinosa, Spi- though some pairs such as O. waldemari and O. scottodi- noncaea ivlevi and S. tenuis and the mesopelagic commu- carloi had similar body lengths and similar D50%s, the scat- nity dominated by ‘O’. crypta, ‘O’. parabathyalis, ‘O’. min- ter diagram of Oncaea indicates the trend that species/ ima and ‘O’. tregoubovi etc. The coincidence of oncaeid forms of Oncaea with similar sizes were distributed in dif- communities in the Kuroshio Extension region and up- ferent layers at night and those distributed in the same stream in Tosa Bay suggests that an oncaeid community layer at night had different sizes from each other. Regard- structure characterized by three communities inhabiting ing species of Triconia, body lengths were distinctly dif- different depth ranges is widespread in the epipelagic zone ferent among the subgroups but similar within a subgroup of temperate waters along the Kuroshio Current. (Fig. 6B). The diel migration patterns were different The present study revealed that there was a positive cor- among subgroups. Although D50%s were distinctly differ- relation between the population density and temperature in ent among species belonging to the same subgroup, the re- most species of Oncaea, which were the main component lationship between body length and D50% that was ob- of Communities A1 and A2, and a negative correlation in served for Oncaea was not apparent. Spinoncaea tenuis, Triconia denticula and three species of ‘Oncaea’, which were the main components characterizing Community B. This indicates that the vertical distribution Discussion of temperature is an important factor related to their verti- Although the vertical distribution of oncaeid copepods cal distribution. However, most Oncaea stayed in the sur- has been investigated in various places around the face mixed layer, despite the downward shift of the ther- world，studies focusing on their fine scale distribution in mocline from August to November. Utilization of appen- the epipelagic zone have been very limited. Nishibe et al. dicularian houses as a habitat and food by oncaeid cope- (2009) investigated the vertical distribution of oncaeid co- pods has been demonstrated by previous studies (All- pepods in the epipelagic and upper mesopelagic zone in dredge 1972, Ohtsuka & Kubo 1991, Ohtsuka et al. 1993, Tosa Bay on the Pacific coast of Japan in August and No- Steinberg et al. 1994, Ohtsuka et al. 1996). Enumeration of vember using a fine (63 μm) mesh net and reported 45 spe- appendicularians in the present study was not based on cies and three forms. Although the number of species in their houses but rather on their bodies. However, it is natu- 12 H. Itoh et al.

rally considered that the abundance of appendicularian roshio Extension and the D25–75% of the epipelagic species houses would be in high in waters where the abundance of were shallow in spring, shifted downward in summer or their bodies is high. Nishibe et al. (2009) observed that in autumn, and expanded (or shifted upward) in winter. The Tosa Bay the highest abundances of oncaeid copepods oc- seasonal change in vertical distribution resulted in fluctua- curred at the depths where appendicularians were abun- tions in their seasonal abundance in the surface layer shal- dant. They suggested that oncaeid copepods depend lower than 50 m, where the abundance of oncaeid cope- strongly on appendicularian houses. In the present study, pods was higher in spring and winter than in summer and highly significant positive correlations were observed par- autumn. Since larvae and juveniles of Japanese sardine, ticularly between the population densities of Oncaea, the Japanese anchovy and Pacific saury inhabit mainly the main component of Community A2, and the abundance of 0–50 m depth layer in spring (Tsukamoto et al. 2001, Yatsu appendicularians. This result mirrors that of Nishibe et al. et al. 2005), the abundance of small copepods, including (2009) in Tosa Bay, and suggests that dependence on ap- oncaeid copepods, in that layer is critically important for pendicularian houses is strong, especially in Oncaea. them as prey. Yamazi (1957) reported a nocturnally dense In the present study, six species and three forms of On- concentration of ‘Oncaea’ spp. at the sea surface in caea and 11 species of Triconia were recorded in the epipe- Wakayama Harbor on the Pacific coast of Japan. Extremely lagic zone of the Kuroshio Extension. Such coexistence of high abundance (ca. 150 ind. m－3) and high dominancy (ca. many congeneric species of oceanic copepods has also 40% of total copepods) of were observed been reported in the genera Euaugaptilus (Matsuura et al. in the surface layer (0–0.5 m) of Suruga Bay on the Pacific 2010) and Clausocalanus (Peralba & Mazzocchi 2004), the coast of Japan in September 1978 (Itoh unpublished). families Scolecitrichidae (Kuriyama & Nishida 2006) and These aggregations of oncaeid copepods, as well as the Oithonidae (Nishida & Marumo 1982), etc. Mechanisms seasonal pattern of their abundance in the surface layer allowing their coexistence in oceanic waters have been where they were abundant especially at night in winter and proposed to involve alleviation of interspecific competition spring, are probably important as food for fish larvae and by partition of niches represented by differences in distri- juveniles in the surface layer, especially for Pacific saury, bution layer, body size, morphs of mouthparts, etc. Some which have a neustonic ecology with nighttime feeding mechanisms for niche partitioning are considered with re- (Tsukamoto et al. 2001, Odate 1977) and occasionally have spect to the coexistence of species/forms of Oncaea in the high abundances of oncaeid copepods in their stomach present study. The relationship between their body length contents (Odate 1977). and D50%s in August showed the trend that in the night- time, species/forms with similar sizes were distributed in Acknowledgements different layers and those in the same layer had different sizes. According to Hutchinson (1959), a difference in the We thank Dr R. Böttger-Schnack for critical comments size of an by 1.3 times respective body lengths al- on an earlier draft of this paper. We also thank the editor lows alleviation of competition between two species in the and two anonymous referees for constructive comments on same guild. For the present case of Oncaea, the species/ the manuscript. We are grateful to the captain and crew of forms with similar D50%s had body lengths 1.4–1.8 times the R.V. Soyo-Maru, National Research Institute of Fisher- co-occurring species suggesting that competition between ies Science, for their help in sampling at sea. This work species/forms of each pair could be alleviated by size-de- was supported by the “Pacific Ocean Fishing resources pendent niche partitioning, perhaps signifying different (VENFISH)” and “study for the prediction and control of feeding habits. The present result that similar-sized spe- population outbreaks of marine life in relation to environ- cies/forms of Oncaea, such as O. clevei and O. scottodi- mental change (POML)” program from the Ministry of Ag- carloi, had very different D50%s from each other indicates riculture, Forestry, and Fisheries, Japan. another mechanism of coexistence, i.e. depth partitioning. Thus it is likely for Oncaea that the coexistence of species/ forms in the epipelagic zone is achieved by a combination References of body size and depth partitioning. On the other hand, the Alldredge AL (1972) Abandoned larvacean houses: A unique relationships between body size and D50% were not as ap- food source in the pelagic environment. 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