Mar Biol (2007) 150:609–625 DOI 10.1007/s00227-006-0382-5

R E SEARCH ART I CLE

Vertical distribution, population structure and life cycles of four oncaeid copepods in the Oyashio region, western subarctic PaciWc Yuichiro Nishibe · Tsutomu Ikeda

Received: 5 April 2006 / Accepted: 7 June 2006 / Published online: 28 June 2006 © Springer-Verlag 2006

Abstract Vertical distribution and population structure of four dominant oncaeid copepods (Triconia borealis, Triconia canadensis, Oncaea grossa and Oncaea parila) were investigated in the Oyashio region, western subarctic PaciWc. Seasonal samples were collected with 0.06 mm mesh nets from Wve discrete layers between the surface and 2,000 m depth at seven occasions (March, May, June, August and October 2002, December 2003 and February 2004). The depth of occurrence of major populations of each species diVered by species; the surface–250 m for T. borealis, 250–1,000 m for T. canadensis, 250–500 m for O. grossa and 500–1,000 m for O. parila. The ontogenetic vertical migration characterized by deeper occurrence of early and late copepodid stages, and shallower occurrence of middle copepodid stages was observed in T. canadensis and O. parila. Of the four oncaeid copepods, almost all copepodid stages occurred throughout the study period, suggesting that their reproduction continues throughout the year in the region. Nevertheless, a clear developmental sequence of stage-to-stage was traced for T. canadensis and O. grossa copepodids, implying their generation time to be 1 year. For

Communicated by S. Nishida, Tokyo Y. Nishibe · T. Ikeda Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan Present Address: Y. Nishibe (&) Center for Marine Environmental Studies, Ehime University, 3 Bunkyo-cho, Matsuyama 790-8577, Japan e-mail: [email protected]

T. borealis and O. parila copepodids, no clear seasonal succession was observed thus estimation of their generation time was uncertain. The present comprehensive results of vertical distribution and life cycle features for T. borealis, T. canadensis, O. grossa and O. parila are compared with the few published data on oncaeid species distributing in high latitude seas.

Introduction The copepod family Oncaeidae is a diverse group of marine pelagic cyclopoids (Böttger-Schnack and Huys 1998; Boxshall and Halsey 2004). They inhabit all parts of the world oceans, ranging from coastal to oceanic waters, from tropical to polar regions (Malt 1983; PaVenhöfer 1993) and from epi- to bathypelagic zones (e.g. Boxshall 1977; Deevey and Brooks 1977; BöttgerSchnack 1994; Richter 1994; Nishibe and Ikeda 2004). While oncaeid copepods are abundant also in coastal waters (PaVenhöfer 1983; Uye et al. 1992; Noda et al. 1998), their relative importance in the copepod communities becomes more evident in oceanic waters, especially in the meso- and bathypelagic zones (Böttger-Schnack 1995, 1996, 1997; Webber and RoV 1995; Satapoomin et al. 2004; Hopcroft et al. 2005). In these depth layers, oncaeid copepods usually account for more than 50% and up to 90% of total copepod numbers based on the sampling with Wne mesh nets (e.g. Böttger-Schnack 1994; KrniniT 1998; KrniniT and Grbec 2002; Yamaguchi et al. 2002). Despite their ubiquitous distribution and high abundances, our knowledge on the ecology of oncaeid copepods is still deWcient (PaVenhöfer 1993; BöttgerSchnack et al. 2004; Turner 2004). In particular, there

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is little information available about the population dynamics and life cycle strategies of oncaeid copepod species. Metz (1996) examined the vertical distribution and population structure of three dominant oncaeid species, Oncaea curvata, Oncaea parila and Triconia antarctica, in the Bellingshausen Sea during two seasons and extrapolated their life cycle patterns. Some fragmentary information on the life cycles of Triconia borealis was provided by Pavshtiks (1975) and Richter (1994) from the Davis Strait and the Greenland Sea, respectively. Recently, Böttger-Schnack and Schnack (2005) studied the population structure and fecundity of the warm-water species Oncaea bispinosa in the Red Sea and discussed their reproduction traits. While a total of 40 oncaeid copepod species have been recorded in the Oyashio region, western subarctic PaciWc, the four species T. borealis (Sars), Triconia canadensis (Heron and Frost), Oncaea grossa Heron and Frost, and O. parila Heron are most abundant in terms of both numbers and biomass (Nishibe and Ikeda 2004; Nishibe 2005). T. borealis has been recorded from high latitude seas in the northern hemisphere such as the subarctic Atlantic (Malt 1983; Heron et al. 1984), the subarctic PaciWc (Heron and Frost 2000), and the Arctic Ocean (Heron et al. 1984), and thus is considered to be a genuine arctic/subarctic species. Conversely, O. parila occurs in high latitude seas of both hemispheres such as the subarctic PaciWc (Heron and Frost 2000), the Arctic Ocean (Heron et al. 1984) and the Southern Ocean (Heron 1977). For T. canadensis and O. grossa, previous records outside the Oyashio region has been restricted to the eastern subarctic PaciWc (Heron and Frost 2000). In the present study, we investigated the vertical distribution, abundance and population structure of T. borealis, T. canadensis, O. grossa and O. parila in the Oyashio region, western subarctic PaciWc by analysing seasonal samples collected from the surface to 2,000 m depth. We compare the present results with those from the other high latitude seas, and discuss life cycle features, such as ontogenetic vertical migration, generation time and reproduction of the four oncaeid copepod species.

Mar Biol (2007) 150:609–625

referred to as Site H; Fig. 1), in 10 March, 30 May, 18 June, 9 August and 9 October 2002 (Table 1). Additional sampling was made aboard the T. S. ‘Oshoro Maru’ in 17 December 2003 and 9 February 2004 at Site H, to complete the seasonal cycle. During the survey in 2002, zooplankton samples were collected with a closing type net (60 cm mouth diameter, 0.06 mm mesh size, Kawamura 1989) equipped with a Xowmeter (Rhigosha) inside the mouth of the net and a RMD depth meter (Rhigosha) on its suspension cable to read the depths the net reached. The net was hauled vertically at speeds of 0.5–1.0 m s¡1 from Wve discrete layers: surface to the bottom of the thermocline (Th), Th–250, 250–500, 500–1,000 and 1,000–2,000 m (Table 1). For the sampling on 17 December 2003 and 9 February 2004, a vertical multiple plankton sampler (VMPS; 50 cm £ 50 cm mouth-opening, 0.06 mm mesh size; Terazaki and Tomatsu 1997) was employed. The VMPS was hauled at a speed of 1.0 m s¡1 from the same depth stratum as described above. Average Wltration eYciencies for the closing type net and VMPS were 71 and 79%, respectively. Because the thermocline was not recognized in 10 March 2002, the Th was assumed arbitrarily as 100 m depth (Table 1). To investigate the diel vertical migration pattern, day and night sampling was conducted on 9 October 2002 (Table 1). After collection, samples were preserved immediately on board ship in a 2% formaldehyde-seawater solution buVered with borax. At each zooplankton sampling date, vertical proWles of temperature and salinity were determined by using a CTD rosette system (SBE-9 plus, Sea Bird Electronics).

Okhotsk Sea

44°N

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Materials and methods Site H

Field samplings

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40°N

Seasonal zooplankton samples were collected on board the T. S. ‘Oshoro Maru’ and R.V. ‘Ushio Maru’ at a station (41°30⬘N; 145°47⬘E, 6,670 m deep) in the Oyashio region oV southeastern Hokkaido (here after

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140°E

144°E

148°E

Fig. 1 Location of sampling site (Site H; circled star) in the Oyashio region, western subarctic PaciWc. Bathymetric counters (1,000, 3,000, 5,000 and 7,000 m) are also shown

Mar Biol (2007) 150:609–625 Table 1 Summary of zooplankton sampling data at Site H (41°30⬘N; 145°47⬘E)

D Day sampling, N night sampling, Os TS ‘Oshoro Maru, Us RV ‘Ushio Maru’

611

Sampling date

Time (local time)

Ship

Sampling depth (m)

10 March 2002 30 May 2002 18 June 2002 9 August 2002 9 October 2002

09:16–12:18 13:26–15:38 02:24–06:17 19:30–22:31 09:10–12:19 (D), 19:00–22:09 (N) 04:15–06:33 17:54–20:29

Os Os Os Us Us

0–100, 100–250, 250–500, 500–1,000, 1,000–2,000 0–50, 50–250, 250–500, 500–1,000, 1,000–2,000 0–50, 50–250, 250–500, 500–1,000, 1,000–2,000 0–70, 70–250, 250–500, 500–1,000, 1,000–2,000 0–70, 70–250, 250–500, 500–1,000, 1,000–2,000

Os Os

0–100, 100–250, 250–500, 500–1,000, 1,000–2,000 0–180, 180–250, 250–500, 500–1,000, 1,000–2,000

17 December 2003 9 February 2004

IdentiWcation and enumeration Copepodid stages of T. borealis, T. canadensis, O. grossa and O. parila were sorted from the entire sample or aliquots taken by using a box type splitter (Motoda 1959) and enumerated under a dissecting microscope. Taxonomic identiWcations of C6 (adult) females and males of the four species were based on Heron (1977), Heron et al. (1984) and Heron and Frost (2000), while the generic name of Triconia was adapted to Oncaea borealis Sars and O. canadensis Heron and Frost (cf. Böttger-Schnack 1999). At present, there is uncertainty on the development sequences of the body segmentation throughout the copepodid stages for the family Oncaeidae. Malt (1982) described a C5 female with a 4-segmented urosome, whereas Böttger-Schnack (2001) and Böttger-Schnack and Huys (2001) deWned the C5 female as having a 5-segmented urosome with no genital apertures. Our observations based on T. canadensis reared in the laboratory revealed that specimens with a 4-segmented urosome, the same as the C5 female in Malt (1982), molted to C6 female with a 5-segmented urosome exhibiting welldeveloped genital apertures (cf. Nishibe 2005). In addition, no specimen of a C5 female such as described by Böttger-Schnack (2001) was found throughout the present study. From our own observations, determination of C5 female was made according to that of Malt (1982). For the identiWcation of C1–C4 stages and C5 males, we referred to the descriptions by Malt (1982). Although Malt (1982) made a discrimination between females and males only from C5 stages, we were able to distinguish both sexes from C4 stages for all four species by using body length, combined with proportional lengths of the second and third urosomites (cf. Nishibe 2005). C1 stages of T. borealis were not quantitatively collected by the 0.06 mm mesh size of the nets used (diagonal dimension: 0.085 mm), as mean body width was 0.08 mm for this stage. Thus, the abundance of C1 stages was probably underestimated to some extent for this species in the present study. Otherwise,

all developmental stages were quantitatively retained for T. canadensis, O. grossa and O. parila. As an index of breeding activity, C6 females carrying egg sacs or having spermatophores attached to the genital double-somite were counted separately for the four oncaeid copepod species. The egg sacs were removed from ovigerous females and dissected with a Wne needle to count the number of eggs per sac. The four oncaeid copepod species treated in this study have paired egg sacs, but more than half of the specimens examined had lost one of sacs. Hence, clutch size of specimens with a single egg sac was calculated by multiplying the egg numbers in a sac by two. Although many of the detached egg sacs found in the samples might have originated from oncaeid copepods, those were not taken into account because of the diYculties in identifying the species of female from which the egg sacs were derived.

Results Hydrography The western boundary current of the subarctic circulation in the North PaciWc is called the Oyashio. It Xows southwestward along the Kuril Islands and Hokkaido and reaches the east coast of northern Honshu, Japan, where it turns east at about 40°N (Reid 1973). Site H of this study is near the southern end of the southwestward alongshore Xow of the Oyashio Current. At Site H, surface temperatures ranged from 2.0°C (March) to 16.2°C (August) in 2002, and were 9.0 and 5.8°C on December 2003 and February 2004, respectively (Fig. 2). In March 2002, the Oyashio water, characterized by a temperature of <3°C and a salinity of 33.0– 33.3 (Ohtani 1971), was seen in the upper 120 m, and the water column above that depth seemed to be well-mixed vertically. In June–October 2002, surface temperatures were above 10°C and the thermocline was well established at 10–50 m in the water column. EVects of warm-core rings originating from

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Mar Biol (2007) 150:609–625 Temperature (°C) 0

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Fig. 2 Vertical proWles of temperature (solid line) and salinity (broken line) at Site H

the Kuroshio Extension were observed in surface layers in December 2003 and February 2004, as judged by higher temperatures >5.5°C at 100 m depth and higher salinities >33.5 in the water column of upper 100 m (December 2003) or 200 m depth (February 2004). Below 200 m temperatures and salinities were nearly constant at 2–3°C and 33.3–34.5, respectively, throughout the study period. Triconia borealis This species was distributed mainly in the top 500 m of the water column throughout the study period (Fig. 3). Day–night diVerences in vertical distribution patterns of the C1–C6 stages observed in October 2002 were not signiWcant statistically (Fig. 3; Kolmogorov–Smirnov test, P > 0.05). Hence, the vertical distribution patterns of this copepod observed at diVerent times of the day can be compared directly to examine its seasonal variations. The C1–C5 stages were distributed almost exclusively in the top 250 m of the water column. C6 males concentrated largely in the upper 250 m of the water column, while C6 females showed a much more extended vertical distribution throughout the upper 500 m of the water column. Both sexes exhibited a much deeper vertical distribution in late winter (March 2002 and February 2004) as compared with other seasons. In August and October 2002, and December 2003, C6 females showed a marked bimodal vertical distribution pattern with peaks above Th and in 250– 500 m depth, while C6 males exhibited a unimodal vertical distribution with maximum concentrations above the Th. All C1–C6 stages occurred throughout the study periods (Fig. 4a). C1 individuals were abundant in March–May and February. C2 showed their abundance peaks in August 2002 and February 2004. The seasonal

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abundance patterns of C3 and C4 males were almost similar to that of C2. C4 females exhibited a diVerent seasonal pattern, with high abundances in May–August 2002. C5 males and females were most abundant in May–June 2002, and the latter showed a conspicuous peak in May. C6 increased from March to June (males) or August (females), and then decreased gradually toward October. Both C6 males and females were very few in March 2002, December 2003 and February 2004. In total, the rather irregular seasonal patterns of the occurrence of each copepodid stage make it diYcult to trace their development sequence. The sex ratios (the percentage of males in the total population) varied greatly with season, ranging from 28.7 to 90.2% (mean: 68.5%) for C4, 22.4 to 93.0% (64.9%) for C5 and 55.7 to 74.0% (63.8%) for C6. C6 females with spermatophores attached were found in May–June and December–February, but their proportions to the total C6 females were low (<1.1%) (Fig. 4b). Throughout the study period, two C6 female specimens with egg sacs attached were observed; one was in May and the other in June, which accounted for 0.43 and 0.25%, respectively, of the total numbers of C6 females (Fig. 4b). Clutch sizes were 56 and 62 eggs per female in May and June, respectively. In addition, paired C6 females and males (the male grasping the female’s urosome with its maxillipeds) were also found in May (0.30% of the total C6 individuals), June (0.30%) and August (0.39%). In terms of relative abundance of each copepodid stage, the structure of the T. borealis population consisted mainly of younger developmental stages (C1–C3) in March (73.6%), December (68.6%) and February (85.5%) (Fig. 5a). The proportion of C4 was relatively stable throughout the study period, ranging from 7.6 to 12.5%, while that of C5 varied seasonally (0.73– 20.5%), with a peak in May. Adults (C6 females and

Mar Biol (2007) 150:609–625

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Fig. 3 Triconia borealis. Vertical distribution of each developmental stage (C1–C6) at Site H. Female and male data are shown separately for C4–C6. Abbreviations are D day, N night

males) consisted of 40.1–53.6% of the total population in May–October, but their contributions to the total numbers were low in March, December and February (5.6–21.9%). Triconia canadensis This species was distributed below the Th to 2,000 m depth (Fig. 6). While part of the C5 population seemed to migrate to shallower depths (Th–250 m) at night in October 2002, day–night diVerences in vertical distribution patterns of all copepodid stages combined (C1– C6) were not signiWcant (Fig. 6; Kolmogorov–Smirnov test, P > 0.05). Throughout the study period, the C1 individuals were found between 500 and 2,000 m depth. Compared with C1, C2 showed a shallower distribution (250–1,000 m depth). C3–C5 stages occurred

largely above the 500 m depth throughout all seasons. It is noted that C4 and C5 stages migrated upward (Th– 250 m layer) in May and/or October. Most C6 females and males exhibit broader distribution than C3–C5 stages did. Seasonally, both C6 females and males resided in shallower layers in May and June than in other months. The diVerences in vertical distribution between sexes were not observed in C4 and C6, while C5 females were distributed deeper than C5 males. All copepodid stages (C1–C6) were found throughout the study period, with the exception of C5 males which were absent in March 2002 (Fig. 7a). The abundances of C1–C5 stages showed a clear seasonal pattern. C1 were abundant both in March 2002 and February 2004, but they are less abundant in May– October 2002 and December 2003. C2 and C3 were most abundant in March–May, and in May–August,

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Mar Biol (2007) 150:609–625 15 10 5

C1

0 40 C2

Abundance ( x103 inds. m-2: 0-2000 m)

20 0 40 20 C3 0 10 5 0 30

Female C4

Male

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15 0 60

egg-carrying C6 females were found throughout the study period, their proportion of the total females was high in May–August (53.1–71.1%) and low in October, December and February (5.8–15.4%), with an intermediate value in March (35.0%) (Fig. 7b). There were signiWcant seasonal diVerences in clutch sizes (one-way ANOVA: F = 12.7, df = 6, 71, P < 0.0001; Fig. 8); the numbers of eggs per female in October (mean: 39.2) and December (37.6) were signiWcantly higher than those in May (12.5), June (19.7) and February (16.0), with intermediate values in March (25.9) and August (33.8) (Tukey–Kramer test, P < 0.05). Based on the abundance of each copepodid stage (Fig. 7a), the population structure of T. canadensis was reconstructed in terms of relative abundance (Fig. 5b). Among the immature stages (C1–C5), C1 and C2 predominated in March–May 2002 and in February 2004, C3 and C4 in June–August 2002, and C5 in October 2002. The proportions of adults (C6 female and male) to the total population were high throughout the study period (34.3–71.0%), especially in winter (December 2003 and February 2004; 57.4–71.0%).

C6

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Fig. 4 Triconia borealis. Seasonal changes in a abundance of each developmental stage and b incidence of spermatophores-attached and egg-carrying specimens in the total C6 females (%) at Site H. Female and male data are shown separately for C4–C6. x: no occurrence

respectively. The maximum abundance of C4 males was seen in June, while that of females occurred in August. The abundance of both C5 females and males peaked in October, though the former also formed a moderate peak in May. Seasonal variations in the abundance of C6 females and males were less marked, decreasing gradually from March to October 2002, with a further decrease (males) or stabilization (female) from December 2003 to February 2004. The sex ratios varied seasonally; the ranges were 14.3–66.2% (mean: 40.3%) for C4, 0–66.9% (35.2%) for C5 and 39.5–57.7% (51.1%) for C6. C6 females with attached spermatophores were found only in March, accounting for 2.9% of total females (Fig. 7b). While

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This species occurred largely from Th to 1,000 m depth (Fig. 9). Day–night diVerences in the vertical distribution patterns examined in October 2002 showed no signiWcant diVerence (Fig. 9, Kolmogorov–Smirnov test, P > 0.1). C1–C5 stages were concentrated consistently between Th and 500 m depth throughout the study period (Fig. 9). While C6 also showed abundance peak in Th–500 m, C6 was diVerent from C1 to C5 in that the moderate number of individuals was also occurred from 500 to 1,000 m. Seasonally, C3–C6 migrated upward (Th–250 m layer) in May. DiVerences between the sexes in the vertical distribution patterns were not evident for C4 through C6. All copepodid stages (C1–C6 stages) were observed throughout the entire study period (Fig. 10a). C1 stage was most abundant in August. Seasonal abundance patterns of C2 and C3 were similar each other, with a marked peak in October. C4 was abundant in March– May 2002 and February 2004, but was less abundant in June–October 2002 and December 2003. C5 was most abundant in May–June, and they decreased gradually from June onward. Abundance of C6 males and females varied less markedly with season. For C4–C6, the abundance of males and females showed the similar seasonal pattern. While the sex ratios of C4 varied greatly with season from 11.2 to 48.2% (mean: 36.0%), those of C5 [33.4– 51.8% (mean: 43.3%)] and C6 [44.9–56.8% (mean:

Mar Biol (2007) 150:609–625 (a) 100

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Fig. 5 Triconia borealis (a), T. canadensis (b), O. grossa (c) and O. parila (d). Seasonal changes in copepodid stage composition at Site H. Female and male data are shown separately for C6

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50.2%)] were near constant throughout the study period. C6 females with attached spermatophores were found throughout the study period, with higher incidence in May (55.1%) and June (41.0%) as compared with other months (5.8–15.9%) (Fig. 10b). There were no signiWcant relationships between the proportion of males to the total C6 population and the frequency of C6 females with spermatophores attached (Spearman’s r = 0.643, P = 0.12). Egg-carrying C6 females were found from March to October, and in December 2003, but their proportions of total C6 female abundance was low, ranging from 0.42 to 3.1% (Fig. 10b). There were signiWcant diVerences in the clutch sizes of O. grossa depending on the sampling dates (one-way ANOVA:

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F = 5.94, df = 5, 20, P = 0.0016; Fig. 8). Subsequent analysis revealed that clutch sizes in October (mean: 28.0) were signiWcantly greater than those in May (19.2) and June (20.5), with intermediate values in March (27.0), August (24.5) and December (24.4) (Tukey–Kramer test, P < 0.05). In terms of stage composition, the copepodid population of O. grossa consisted mainly of younger stages (C1–C3) in August and October 2002 (55.0–67.7% of the total population) (Fig. 5c). On the other hand, C4 and C5 were abundant in March, May and June (30.5– 34.6% of the total population). C6 male and female were the most dominant stages in March toward October. During the winter (December 2003 and February

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Fig. 6 Triconia canadensis. Vertical distribution of each developmental stage (C1–C6) at Site H. Female and male data are shown separately for C4–C6. Abbreviations are D day, N night

2004), C3, C4 and C6 males and females dominated in the copepodid population. Oncaea parila This species inhabited a broad bathymetric range between 250 and 2,000 m depth (Fig. 11). Day–night diVerences in vertical distribution patterns were not signiWcant for the all copepodid stages (C1–C6) in October 2002 (Fig. 11, Kolmogorov–Smirnov test, P > 0.05). The C1 stage was found largely below 500 m depth during all seasons (Fig. 11). The C2–C5 populations showed a broad vertical distribution from Th to 2,000 m depth, but most of them were concentrated in 250–1,000 m depth throughout the year. While C6 females and males were also distributed mainly in 250– 1,000 m depth, the proportion of the population found

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in 1,000–2,000 m was greater than those for C2–C5. Male/female diVerences in vertical distribution pattern were not evident for C4 through C6. All copepodid stages (C1–C6) of O. parila occurred throughout the study period (Fig. 12a). Seasonal changes in abundance of C1, C2 and C3 paralleled each other, with an abundance peak in August 2002. For C4 through C6 stages, abundance and seasonal patterns of males and females were nearly identical. While the seasonal abundance patterns of C4–C6 were irregular, they were numerous in March–August 2002 and less numerous in December 2003 and February 2004. The sex ratios were almost constant throughout the study period, ranging from 43.1 to 62.4% (mean: 51.0%) for C4, 40.0 to 60.5% (47.9%) for C5 and 45.7 to 60.3% (51.1%) for C6. C6 females with attached spermatophores were observed from March to

Mar Biol (2007) 150:609–625 15

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Fig. 8 Triconia canadensis and O. grossa. Seasonal changes in clutch size (eggs per female) at Site H. Vertical bars, which indicate § SD, are shown when they exceed the size of symbol

0 10 C5 5

female, thus indicating that more than half of the population was comprised of the C6 stage.

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Fig. 7 Triconia canadensis. Seasonal changes in a abundance of each developmental stage and b incidence of spermatophores-attached and egg-carrying specimens in the total C6 females (%) at Site H. Female and male data are shown separately for C4–C6. x: no occurrence

October 2002 and in December 2003, but not in February 2004 (Fig. 12b). The proportion of C6 females with spermatophores attached ranged from 0.28 to 1.5% of the total population with its peak in May 2002. Throughout this study, only three individuals of C6 female carrying egg sacs were found in October 2002 (1.1% of the total C6 females) (Fig. 12b). Clutch sizes of C6 females examined were 11–12 eggs per female. The copepodid stage composition was relatively constant throughout the study period (Fig. 5d). The ranges of proportion of each copepodid stage to the total copepodids were 2.8–13.6% for C1, 4.5–11.2% for C2, 5.3–8.1% for C3, 5.4–12.0% for C4, 7.2–17.4% for C5, 26.7–36.7% for C6 male and 24.2–35.5% for C6

Among the four oncaeid copepod species studied, information about vertical distribution from other seas is available for T. borealis and O. parila. In the central Arctic Ocean, T. borealis showed a broad vertical distribution pattern from the surface to 1,500 m depth, but more than one half of the population occurred in the upper 200 m (Auel and Hagen 2002). Similar vertical distribution patterns of this species have also been reported by Groendahl and Hernroth (1984) from the Nansen Basin, Arctic Ocean. The present results in the Oyashio region, with T. borealis being mainly distributed in the top 500 m (Fig. 3), are in fair agreement with the previous reports from the Arctic Ocean. Diel vertical migration (DVM) of T. borealis has been noted by Groendahl and Hernroth (1984) and Fortier et al. (2001) in Arctic waters; the former reported the amplitudes of DVM of this species to be more than 200 m, whereas the latter reported much lower amplitudes of 10–30 m. In the present study, however, such DVM behaviour of T. borealis could not be detected (Fig. 3), probably because the amplitudes of their DVM, if any, could not be resolved by the broad sampling intervals of the present study (see “Materials and methods” section). According to Metz (1996), O. parila was distributed over the entire water column between

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Fig. 9 Oncaea grossa. Vertical distribution of each developmental stage (C1–C6) at Site H. Female and male data are shown separately for C4–C6. Abbreviations are D day, N night

the surface and 1,000 m depth in the Bellingshausen Sea, but the majority of populations resided below 200 m depth. In the Oyashio region, O. parila occurred below the thermocline to 2,000 m depth (Fig. 11), but most were concentrated in the 250–1,000 m depth layer. The broad vertical distribution of O. parila between 250 and 3,000 m depth has also been observed in the Arctic Ocean (Heron et al. 1984). Metz (1996) reported that two Antarctic oncaeid species, Oncaea curvata and Triconia antarctica, underwent an extensive ontogenetic vertical migration (OVM). As a common feature of both species, upward migration was seen during the development from early to middle copepodid stages, whereas late copepodid and adult stages descended to deeper layers. From the present vertical distribution data for all stages (C1–C6) of T. borealis, T. canadensis, O. grossa and O. parila, we calculated the depth above and below which 50% of the population resided (D50%; cf. Pennak 1943) for

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each copepodid stage (Fig. 13). An OVM pattern similar to that for the Antarctic oncaeid species by Metz (1996) was evident for T. canadensis and O. parila in the Oyashio region (Table 2). While the feeding habit of the meso- and bathypelagic oncaeid species is poorly deWned at present, most of them are assumed to be detritivores (see Discussion below). Since the amount of detrital material in terms of particulate organic carbon decreases exponentially with increasing depths in the ocean (e.g. Suess 1980; Pace et al. 1987), upward migration during the development as seen in T. canadensis and O. parila can be interpreted as a result of life history traits toward maximizing feeding gain for their growth at middle copepodid stages, as also suggested by Metz (1996). In contrast to T. canadensis and O. parila, the OVM was not clear for T. borealis and O. grossa (Table 2), but their C6 females were distributed much deeper depth than immature copepodids (C1– C5) and/or C6 males (Fig. 13). For sac-spawning

Mar Biol (2007) 150:609–625

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similar food sources (Auel 1999). For oncaeid copepods, Böttger-Schnack et al. (2004) reported diVerent depth distributions of two sibling species, Triconia hawii and T. recta, in the Red Sea. Among the four oncaeid species studied, O. grossa and O. parila are morphologically similar to each other (Heron 1977; Heron and Frost 2000) and thus belong to the notopusgroup of the family Oncaeidae (Böttger-Schnack and Huys 1998). As is evident in Fig. 13, species-speciWc depth distributions (i.e. the D50%) of O. grossa (350– 470 m) and O. parila (590–940 m) were clearly separated vertically across all copepodid stages (see also Table 2). Since body sizes of the corresponding copepodid stages of these two oncaeid species are almost the same (cf. Nishibe 2005), they might be exploiting similar food sources (e.g. prey size and preference). Thus, the vertical separation of O. grossa– O. parila found in the Oyashio region may also be interpreted as an avoidance of food competition in the resource-limited mesopelagic depth zone. While T. borealis and T. canadensis belong to same coniferagroup (Böttger-Schnack 1999, 2004), their diVerential vertical distribution patterns at Site H would not be a result of size-speciWc competition (Fig. 13, Table 2), because their body sizes are much dissimilar to each other (cf. Nishibe 2005). Life cycle

60 Egg-carrying Spermatophores-attached

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copepods such as oncaeids, it has been demonstrated that egg-carrying females suVer higher mortality than males and juveniles due to higher susceptibility to visual predators (Kiørboe and Sabatini 1994). Hence, the deeper distribution of C6 females of T. borealis and O. grossa observed in this study may be regarded as a refuge from predator-abundant shallower layer, although almost nothing is known about the distribution of potential predators of oncaeid copepods in the Oyashio region at present. Vertical partitioning of the water column between closely related species is generally considered to be a strategy for marine copepods to reduce inter-speciWc competition, since these species are assumed to exploit

Triconia borealis The occurrence of C1–C6 stages in all seasons indicates the year-round reproduction of T. borealis at Site H in the Oyashio region (Fig. 4a). Seasonal data of incidence of egg-carrying and spermatophores-attached females of T. borealis are not suYcient enough to deWne their major reproduction period (Fig. 4b), but greater abundance and predominance of adults in late May–October would seem to suggest that the major spawning season to be in summer–fall. From seasonal sequences in stage composition (Fig. 5a), it may be thought that younger copepodids (C1–C3) dominating in March developed rapidly to C4–C5 in late May, then reached C6 in June at Site H. However, the entire development sequence of the copepodids of T. borealis could not be traced clearly, so their generation time was left unresolved in this study. On the other hand, diVerent seasonal variation patterns in abundance between males and females of C4–C6 stages may suggest diVerential developmental times for them. Because of lower adult proportion to total population during winter (Fig. 5a), adults may have ended their life cycle within the year.

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Fig. 11 Oncaea parila. Vertical distribution of each developmental stage (C1–C6) at Site H. Female and male data are shown separately for C4–C6. Abbreviations are D day, N night

Comparable information about the life cycle of T. borealis is limited to the population in Arctic waters. By analysing seasonal data of the size–frequency distributions of copepodid stages, Richter (1994) considered that the major reproduction of T. borealis took place in early summer and fall in the Greenland Sea. He also suggested that both the summer and fall generations need 1 year to complete their life cycle, although the basis for this estimation was not described. Pavshtiks (1975) brieXy noted that reproduction of T. borealis occurred in summer in the Davis Strait. This information from previous workers, combined with the present results, indicates that T. borealis has an extended reproductive period with its peak during the warmer seasons (summer–fall) in boreal waters. Regarding other epipelagic oncaeid species in high-latitude seas, Oncaea curvata is

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reported to have a 1–2 year life cycle and year-round reproduction with its peak in spring/summer in the Bellingshausen Sea (Metz 1996). Triconia canadensis The year-round occurrence of egg-carrying C6 females suggests continuous reproduction of T. canadensis at Site H (Fig. 7). Unexpectedly, the incidence of eggcarrying C6 females and clutch sizes showed diVerent seasonal patterns; the former was high in May–August, whereas the latter was high in August–December (Figs. 7b, 8). This discrepancy makes it diYcult to deWne the major reproduction season of T. canadensis from these data. Alternatively, the abundance peaks of C1 seen in February–March (Fig. 7a) may suggest that the major spawning season of T. canadensis is

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(a)

621

December–February and March (Fig. 5b), C6 might overwinter and reproduce in the second year. No comparable information is presently available about the life cycle of T. canadensis. According to Metz (1996), T. antarctica, a closely-related species to T. canadensis (Heron 1977; Heron and Frost 2000), has 1 year life cycle in the northern Bellingshausen Sea. Despite the diVerences in the habitat temperature between the Bellingshausen Sea (–1.8 to 2.5°C, cf. Metz 1996) and the Oyashio region (2.5–3.5°C, Fig. 2), the annual life cycle of T. antarctica is in good agreement with the present estimates of that T. canadensis, mentioned above.

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fall–early winter, which coincides nearly with the season where higher clutch sizes were observed. Laboratory observations showed that egg hatching of T. canadensis needs 70–85 days at the ambient temperature (3°C) (Y. Nishibe, unpublished data), thus supporting this scenario. By assuming the seasonal population structure is stable every year, it is possible to trace the development sequence of the peak of C1 seen in February–March which reached C6 in December (Fig. 5b). From this scenario, the generation time of T. canadensis is estimated to be approximately 1 year at Site H. Because the proportions of C6 females and males to the total population remained high in

Nothing is known about the life cycle of O. grossa. The year-round occurrence of all copepodid stages and C6 females with spermatophores attached suggests that reproduction of O. grossa occurred in all seasons of the year at Site H (Fig. 10). Judging from a marked increase of C6 females with spermatophores attached in late May–June (Fig. 10b), followed by high abundance of C1 in August–October (Fig. 10a), the major reproduction of this species is considered to occur in summer. However, this scheme is not consistent with the lower (not higher) clutch size of this species in summer (Fig. 8). By tracing the abundance peak of each copepodid stage, it can be estimated that C1 stage recruited in August developed to C2–C3 in October (Fig. 10a). On the other hand, C4 that dominated in March developed to C5 in May–June, and to C6 in August. Combining these two segments of their development, the generation time of O. grossa may be estimated as 1 year at Site H. The high proportions of adults (C6 female and male) in the total population during winter–early spring (December, February and March) (Fig. 5c), may indicate that the adult population overwinters and reproduces in the second year, if one assumes a repetition of the same annual cycle every year. Oncaea parila The occurrence of all copepodid stages (C1–C6) of O. parila throughout the study period (Fig. 12a), together with stable copepodid stage composition in all seasons (Fig. 5d) suggests year-round reproduction and continuous recruitment to adult (C6) at Site H. The lack of dominant cohorts throughout the year makes it impossible to trace developmental sequences and estimation of the generation time of O. parila. Assuming constant mortality during each copepodid stage, predominance of C6 individual in total copepodids would

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Table 2 Summary of life cycle data of four oncaeid copepods in the Oyashio region, western subarctic PaciWc

Body lengtha (C6 female/male: mm) Depth distributionb (D50% of the whole population: m) Ontogenetic vertical migration Reproductive pattern Estimated generation time a b

Triconia borealis

Triconia canadensis

Oncaea grossa

Oncaea parila

0.68/0.43 150

1.56/1.19 640

0.80/0.65 370

0.63/0.48 790

No Yes No Year-round, with Year-round, with peak Year-round, with peak peak in summer–fall in fall–early winter around summer ? 1 year 1 year

Yes Year-round, with no seasonal peak ?

Data from Nishibe (2005) Calculated from the present vertical distibution data for each encaeid copepod

suggest that stage duration of the C6 is very long as compared with those of the preceding copepodid stages. On the basis of similar results as those found in the present study, Metz (1996) could not resolve the life cycle pattern of the O. parila population in the Bellingshausen Sea, though she also suggested a possibly longer stage duration of adults and year-round constant reproduction of this species. In summary, it becomes evident that while the reproduction of T. borealis, T. canadensis, O. grossa and O. parila continues throughout the year in the Oyashio region, the former three exhibit marked seasonal peaks; summer–fall for T. borealis, fall–early winter for T. canadensis and summer for O. grossa (Table 2). In addition, we could estimate the generation time of T. canadensis and O. grossa as 1 year, but this was not the case for T. borealis and O. parila due to the diYculties in tracing the sequences of cohorts.

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Food availability and reproduction In the Oyashio region, it has been demonstrated that the spring phytoplankton bloom, which usually occurs from April to May (Kasai et al. 2001), plays an integral role, directly or indirectly, in inducing spawning and facilitating rapid development of large grazing copepods such as Neocalanus spp., Metridia spp. and Eucalanus bungii (e.g. Kobari and Ikeda 1999, 2001a, b; Padmavati et al. 2004; Shoden et al. 2005). On the other hand, the major reproduction periods of T. borealis, T. canadensis and O. grossa did not coincide with the phytoplankton bloom period, although rapid development from early to late copepodid stage of T. borealis was seen in March–late May (Fig. 5a). In general, oncaeid copepods are classiWed to omnivores, because various prey items (e.g. diatom, dinoXagellate, copepods and other crustacean) were found from their guts and faecal pellets (Pasternak 1984; Turner 1986; Ohtsuka et al. 1996). Also, previous

Mar Biol (2007) 150:609–625

studies suggested that marine snow aggregates (including discarded appendicularian houses), which are enriched by a variety of attached particles (e.g. bacteria, picophytoplankton, diatoms, protists and faecal pellets), are an important food source for oncaeid copepods (Alldredge 1972; Ohtsuka and Kubo 1991; Lampitt et al. 1993; Ohtsuka et al. 1993, 1996; Steinberg et al. 1994). In our laboratory observations, T. canadensis feed well on dead Artemia nauplii and weakened chaetognaths, suggesting their preference to dead or moribund animal foods. Hopkins (1987) and Metz (1998) have reported carnivorous feeding of the sibling species T. antarctica. Almost nothing is known about food for T. borealis and O. grossa (and O. parila also), although Kattner et al. (2003) suggested T. borealis to be detritivore and/or carnivore from analysis of fatty acid composition of its body. O. curvata, which is as small as three of the oncaeid species in this study (T. borealis, O. grossa and O. parila), did not show carnivorous feeding and fed exclusively on large gelatinous aggregates of phytoplankton (Metz 1998). From these results, it can be assumed that all T. borealis, T. canadensis, O. grossa and O. parila utilize a wide spectrum of prey (e.g. phytoplankton, zooplankton and its carcasses, and marine snow) in nature, but T. borealis and T. canadensis show a more carnivorous feeding habit compared to the other two species. In the Oyashio region, appendicularian biomass and house production reaches its annual maximum in July–October (Y. Shichinohe, unpublished data), indicating that vertical Xux of marine snow originating from discarded appendicularian houses may increase during this period. In addition, mesozooplankton biomass in the deeper layer (250–2,000 m depth) of the region increases between July and December (cf. Kobari et al. 2003). These facts would seem to suggest that the main reproduction periods of T. borealis (summer–fall), T. canadensis (fall–early winter) and O. grossa (summer) are adjusted to the most abundant period of their potential foods in the Oyashio region. Clearly, more precise evaluation of the feeding habits of the four oncaeid copepod species studied here is an essential step toward a better understanding of their life cycle patterns and their roles in trophodynamics of copepods in the Oyashio region. Acknowledgments We greatly thank Dr. R. Böttger-Schnack for reviewing an earlier draft of this paper; her constructive comments signiWcantly improved the manuscript. Dr. J. T. Turner provided editorial advice. Thanks are extended to the captains and crews of T.S. ‘Oshoro Maru’ and R.V. ‘Ushio Maru’ (Hokkaido University) for their help in Weld samplings. We thank Ms. Y. Shichinohe who kindly provided unpublished data on appendicularians in the Oyashio region. Y. N. is grateful to the Division of Aquatic Biology and Ecology, Center for Marine Environmental Studies, Ehime University, for providing logistical and Wnancial

623 support for the data analysis and manuscript preparation. This study was supported partly by JSPS KAKENHI 14209001.

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