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

RESEARCH ARTICLE

Vertical distribution, population structure and life cycles of four oncaeid 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 struc- T. borealis and O. parila copepodids, no clear seasonal ture of four dominant oncaeid copepods (Triconia succession was observed thus estimation of their gener- borealis, Triconia canadensis, grossa and ation time was uncertain. The present comprehensive Oncaea parila) were investigated in the Oyashio results of vertical distribution and life cycle features for region, western subarctic PaciWc. Seasonal samples T. borealis, T. canadensis, O. grossa and O. parila are were collected with 0.06 mm mesh nets from Wve dis- compared with the few published data on oncaeid spe- crete layers between the surface and 2,000 m depth at cies distributing in high latitude seas. seven occasions (March, May, June, August and Octo- ber 2002, December 2003 and February 2004). The depth of occurrence of major populations of each spe- Introduction cies diVered by ; the surface–250 m for T. bore- alis, 250–1,000 m for T. canadensis, 250–500 m for The family is a diverse group of O. grossa and 500–1,000 m for O. parila. The ontogenetic marine pelagic cyclopoids (Böttger-Schnack and Huys vertical migration characterized by deeper occurrence 1998; Boxshall and Halsey 2004). They inhabit all parts of early and late copepodid stages, and shallower of the world oceans, ranging from coastal to oceanic occurrence of middle copepodid stages was observed in waters, from tropical to polar regions (Malt 1983; T. canadensis and O. parila. Of the four oncaeid cope- PaVenhöfer 1993) and from epi- to bathypelagic zones pods, almost all copepodid stages occurred throughout (e.g. Boxshall 1977; Deevey and Brooks 1977; Böttger- the study period, suggesting that their reproduction Schnack 1994; Richter 1994; Nishibe and Ikeda 2004). continues throughout the year in the region. Neverthe- While oncaeid copepods are abundant also in coastal less, a clear developmental sequence of stage-to-stage waters (PaVenhöfer 1983; Uye et al. 1992; Noda et al. was traced for T. canadensis and O. grossa copepodids, 1998), their relative importance in the copepod com- implying their generation time to be 1 year. For munities becomes more evident in oceanic waters, especially in the meso- and bathypelagic zones (Bött- ger-Schnack 1995, 1996, 1997; Webber and RoV 1995; Satapoomin et al. 2004; Hopcroft et al. 2005). In these Communicated by S. Nishida, Tokyo depth layers, oncaeid copepods usually account for more than 50% and up to 90% of total copepod num- Y. Nishibe · T. Ikeda bers based on the sampling with Wne mesh nets (e.g. Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate 041-8611, Japan Böttger-Schnack 1994; KrniniT 1998; KrniniT and Grbec 2002; Yamaguchi et al. 2002). Present Address: Despite their ubiquitous distribution and high Y. Nishibe (&) abundances, our knowledge on the ecology of oncaeid Center for Marine Environmental Studies, Ehime University, W V 3 Bunkyo-cho, Matsuyama 790-8577, Japan copepods is still de cient (Pa enhöfer 1993; Böttger- e-mail: [email protected] Schnack et al. 2004; Turner 2004). In particular, there 123 610 Mar Biol (2007) 150:609–625 is little information available about the population referred to as Site H; Fig. 1), in 10 March, 30 May, 18 dynamics and life cycle strategies of oncaeid copepod June, 9 August and 9 October 2002 (Table 1). Addi- species. Metz (1996) examined the vertical distribution tional sampling was made aboard the T. S. ‘Oshoro and population structure of three dominant oncaeid Maru’ in 17 December 2003 and 9 February 2004 at species, Oncaea curvata, Oncaea parila and Triconia Site H, to complete the seasonal cycle. During the sur- antarctica, in the Bellingshausen Sea during two sea- vey in 2002, samples were collected with a sons and extrapolated their life cycle patterns. Some closing type net (60 cm mouth diameter, 0.06 mm mesh fragmentary information on the life cycles of Triconia size, Kawamura 1989) equipped with a Xowmeter (Rhi- borealis was provided by Pavshtiks (1975) and Richter gosha) inside the mouth of the net and a RMD depth (1994) from the Davis Strait and the Greenland Sea, meter (Rhigosha) on its suspension cable to read the respectively. Recently, Böttger-Schnack and Schnack depths the net reached. The net was hauled vertically (2005) studied the population structure and fecundity at speeds of 0.5–1.0 m s¡1 from Wve discrete layers: sur- of the warm-water species Oncaea bispinosa in the Red face to the bottom of the thermocline (Th), Th–250, Sea and discussed their reproduction traits. 250–500, 500–1,000 and 1,000–2,000 m (Table 1). For While a total of 40 oncaeid copepod species have the sampling on 17 December 2003 and 9 February been recorded in the Oyashio region, western subarctic 2004, a vertical multiple plankton sampler (VMPS; PaciWc, the four species T. borealis (Sars), Triconia 50 cm £ 50 cm mouth-opening, 0.06 mm mesh size; canadensis (Heron and Frost), Oncaea grossa Heron Terazaki and Tomatsu 1997) was employed. The and Frost, and O. parila Heron are most abundant in VMPS was hauled at a speed of 1.0 m s¡1 from the terms of both numbers and biomass (Nishibe and same depth stratum as described above. Average Wltra- Ikeda 2004; Nishibe 2005). T. borealis has been tion eYciencies for the closing type net and VMPS recorded from high latitude seas in the northern hemi- were 71 and 79%, respectively. Because the thermo- sphere such as the subarctic Atlantic (Malt 1983; cline was not recognized in 10 March 2002, the Th was Heron et al. 1984), the subarctic PaciWc (Heron and assumed arbitrarily as 100 m depth (Table 1). To inves- Frost 2000), and the Arctic Ocean (Heron et al. 1984), tigate the diel vertical migration pattern, day and night and thus is considered to be a genuine arctic/subarctic sampling was conducted on 9 October 2002 (Table 1). species. Conversely, O. parila occurs in high latitude After collection, samples were preserved immediately seas of both hemispheres such as the subarctic PaciWc on board ship in a 2% formaldehyde-seawater solution (Heron and Frost 2000), the Arctic Ocean (Heron buVered with borax. At each zooplankton sampling et al. 1984) and the Southern Ocean (Heron 1977). For date, vertical proWles of temperature and salinity were T. canadensis and O. grossa, previous records outside determined by using a CTD rosette system (SBE-9 the Oyashio region has been restricted to the eastern plus, Sea Bird Electronics). 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 W the Oyashio region, western subarctic Paci c by analy- Okhotsk Sea sing 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 44°N copepod species. Hokkaido 1000 m 3000 m 5000 m 7000 m Materials and methods Site H Field samplings Pacific Ocean 40°N Seasonal zooplankton samples were collected on board 140°E 144°E 148°E the T. S. ‘Oshoro Maru’ and R.V. ‘Ushio Maru’ at a Ј Ј Fig. 1 Location of sampling site (Site H; circled star) in the Oy- station (41°30 N; 145°47 E, 6,670 m deep) in the ashio region, western subarctic PaciWc. Bathymetric counters Oyashio region oV southeastern Hokkaido (here after (1,000, 3,000, 5,000 and 7,000 m) are also shown 123 Mar Biol (2007) 150:609–625 611

Table 1 Summary of zoo- Sampling date Time (local time) Ship Sampling depth (m) plankton sampling data at Site Ј Ј H (41°30 N; 145°47 E) 10 March 2002 09:16–12:18 Os 0–100, 100–250, 250–500, 500–1,000, 1,000–2,000 30 May 2002 13:26–15:38 Os 0–50, 50–250, 250–500, 500–1,000, 1,000–2,000 18 June 2002 02:24–06:17 Os 0–50, 50–250, 250–500, 500–1,000, 1,000–2,000 9 August 2002 19:30–22:31 Us 0–70, 70–250, 250–500, 500–1,000, 1,000–2,000 9 October 2002 09:10–12:19 (D), Us 0–70, 70–250, 250–500, 500–1,000, 1,000–2,000 19:00–22:09 (N) D Day sampling, N night sam- 17 December 2003 04:15–06:33 Os 0–100, 100–250, 250–500, 500–1,000, 1,000–2,000 pling, Os TS ‘Oshoro Maru, 9 February 2004 17:54–20:29 Os 0–180, 180–250, 250–500, 500–1,000, 1,000–2,000 Us RV ‘Ushio Maru’

IdentiWcation and enumeration all developmental stages were quantitatively retained for T. canadensis, O. grossa and O. parila. Copepodid stages of T. borealis, T. canadensis, O. grossa As an index of breeding activity, C6 females carrying and O. parila were sorted from the entire sample or egg sacs or having spermatophores attached to the geni- aliquots taken by using a box type splitter (Motoda tal double-somite were counted separately for the four 1959) and enumerated under a dissecting microscope. oncaeid copepod species. The egg sacs were removed Taxonomic identiWcations of C6 (adult) females from ovigerous females and dissected with a Wne needle and males of the four species were based on Heron to count the number of eggs per sac. The four oncaeid (1977), Heron et al. (1984) and Heron and Frost copepod species treated in this study have paired egg (2000), while the generic name of Triconia was adapted sacs, but more than half of the specimens examined had to Oncaea borealis Sars and O. canadensis Heron and lost one of sacs. Hence, clutch size of specimens with a Frost (cf. Böttger-Schnack 1999). At present, there is single egg sac was calculated by multiplying the egg uncertainty on the development sequences of the body numbers in a sac by two. Although many of the segmentation throughout the copepodid stages for the detached egg sacs found in the samples might have orig- family Oncaeidae. Malt (1982) described a C5 female inated from oncaeid copepods, those were not taken with a 4-segmented urosome, whereas Böttger-Sch- into account because of the diYculties in identifying the nack (2001) and Böttger-Schnack and Huys (2001) species of female from which the egg sacs were derived. deWned the C5 female as having a 5-segmented uro- some with no genital apertures. Our observations based on T. canadensis reared in the laboratory Results revealed that specimens with a 4-segmented urosome, the same as the C5 female in Malt (1982), molted to C6 Hydrography female with a 5-segmented urosome exhibiting well- developed genital apertures (cf. Nishibe 2005). In addi- The western boundary current of the subarctic circula- tion, no specimen of a C5 female such as described by tion in the North PaciWc is called the Oyashio. It Xows Böttger-Schnack (2001) was found throughout the southwestward along the Kuril Islands and Hokkaido present study. From our own observations, determina- and reaches the east coast of northern Honshu, Japan, tion of C5 female was made according to that of Malt where it turns east at about 40°N (Reid 1973). Site H of (1982). For the identiWcation of C1–C4 stages and C5 this study is near the southern end of the southwest- males, we referred to the descriptions by Malt (1982). ward alongshore Xow of the Oyashio Current. At Site Although Malt (1982) made a discrimination between H, surface temperatures ranged from 2.0°C (March) to females and males only from C5 stages, we were able 16.2°C (August) in 2002, and were 9.0 and 5.8°C on to distinguish both sexes from C4 stages for all four December 2003 and February 2004, respectively species by using body length, combined with propor- (Fig. 2). In March 2002, the Oyashio water, character- tional lengths of the second and third urosomites (cf. ized by a temperature of <3°C and a salinity of 33.0– Nishibe 2005). C1 stages of T. borealis were not quanti- 33.3 (Ohtani 1971), was seen in the upper 120 m, tatively collected by the 0.06 mm mesh size of the nets and the water column above that depth seemed to used (diagonal dimension: 0.085 mm), as mean body be well-mixed vertically. In June–October 2002, sur- width was 0.08 mm for this stage. Thus, the abundance face temperatures were above 10°C and the thermo- of C1 stages was probably underestimated to some cline was well established at 10–50 m in the water extent for this species in the present study. Otherwise, column. EVects of warm-core rings originating from 123 612 Mar Biol (2007) 150:609–625

Temperature (°C)

0 5 10 15 20 0 5 10 15 20 0 5 10 15 20 0 5 10 15 20 0 5 10 15 20 05101520 0 5 10 15 20 0

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10 Mar. 30 May 18 Jun. 9Aug. 9Oct. 17 Dec. 9 Feb. 2002 2003 2004 2000 32 33 34 35 32 33 34 35 32 33 34 35 32 33 34 35 32 33 34 35 32 33 34 35 32 33 34 35 Salinity

Fig. 2 Vertical proWles of temperature (solid line) and salinity (broken line) at Site H the Kuroshio Extension were observed in surface lay- abundance patterns of C3 and C4 males were almost ers in December 2003 and February 2004, as judged by similar to that of C2. C4 females exhibited a diVerent higher temperatures >5.5°C at 100 m depth and higher seasonal pattern, with high abundances in May–August salinities >33.5 in the water column of upper 100 m 2002. C5 males and females were most abundant in (December 2003) or 200 m depth (February 2004). May–June 2002, and the latter showed a conspicuous Below 200 m temperatures and salinities were nearly peak in May. C6 increased from March to June (males) constant at 2–3°C and 33.3–34.5, respectively, through- or August (females), and then decreased gradually out the study period. toward October. Both C6 males and females were very few in March 2002, December 2003 and February 2004. Triconia borealis In total, the rather irregular seasonal patterns of the occurrence of each copepodid stage make it diYcult to This species was distributed mainly in the top 500 m of trace their development sequence. the water column throughout the study period (Fig. 3). The sex ratios (the percentage of males in the total Day–night diVerences in vertical distribution patterns population) varied greatly with season, ranging from of the C1–C6 stages observed in October 2002 were not 28.7 to 90.2% (mean: 68.5%) for C4, 22.4 to 93.0% signiWcant statistically (Fig. 3; Kolmogorov–Smirnov (64.9%) for C5 and 55.7 to 74.0% (63.8%) for C6. C6 test, P > 0.05). Hence, the vertical distribution patterns females with spermatophores attached were found in of this copepod observed at diVerent times of the day May–June and December–February, but their propor- can be compared directly to examine its seasonal varia- tions to the total C6 females were low (<1.1%) tions. The C1–C5 stages were distributed almost exclu- (Fig. 4b). Throughout the study period, two C6 female sively in the top 250 m of the water column. C6 males specimens with egg sacs attached were observed; one concentrated largely in the upper 250 m of the water was in May and the other in June, which accounted for column, while C6 females showed a much more 0.43 and 0.25%, respectively, of the total numbers of extended vertical distribution throughout the upper C6 females (Fig. 4b). Clutch sizes were 56 and 62 eggs 500 m of the water column. Both sexes exhibited a per female in May and June, respectively. In addition, much deeper vertical distribution in late winter (March paired C6 females and males (the male grasping the 2002 and February 2004) as compared with other sea- female’s urosome with its maxillipeds) were also found sons. In August and October 2002, and December in May (0.30% of the total C6 individuals), June 2003, C6 females showed a marked bimodal vertical (0.30%) and August (0.39%). distribution pattern with peaks above Th and in 250– In terms of relative abundance of each copepodid 500 m depth, while C6 males exhibited a unimodal ver- stage, the structure of the T. borealis population consisted tical distribution with maximum concentrations above mainly of younger developmental stages (C1–C3) in the Th. March (73.6%), December (68.6%) and February All C1–C6 stages occurred throughout the study (85.5%) (Fig. 5a). The proportion of C4 was relatively periods (Fig. 4a). C1 individuals were abundant in stable throughout the study period, ranging from 7.6 to March–May and February. C2 showed their abundance 12.5%, while that of C5 varied seasonally (0.73– peaks in August 2002 and February 2004. The seasonal 20.5%), with a peak in May. Adults (C6 females and 123 Mar Biol (2007) 150:609–625 613

Abundance (inds. m -3)

0 200 400 0 200 400 0 100 200 0 200 400 0 100 200 0 100 200 0 100 200 0 200 400 0

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040800 150 300 040800 50 100 02040020400102004080 0

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05100 250 500 0306003060051005100120510 0 Depth (m) 500

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030600 300 600 0 200 400 0 200 400 0 200 400 0 200 400 0306001020 0

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1500 C6F C6M 2000 10 Mar. 30 May 18 Jun. 9 Aug. 9 Oct. 9 Oct. 17 Dec. 9 Feb. 2002 (D) (D) (N) (N) (D) (N)2003 (N)2004 (N)

Fig. 3 Triconia borealis. Vertical distribution of each developmental stage (C1–C6) at Site H. Female and male data are shown sepa- rately for C4–C6. Abbreviations are D day, N night males) consisted of 40.1–53.6% of the total population largely above the 500 m depth throughout all seasons. in May–October, but their contributions to the total It is noted that C4 and C5 stages migrated upward (Th– numbers were low in March, December and February 250 m layer) in May and/or October. Most C6 females (5.6–21.9%). and males exhibit broader distribution than C3–C5 stages did. Seasonally, both C6 females and males Triconia canadensis resided in shallower layers in May and June than in other months. The diVerences in vertical distribution This species was distributed below the Th to 2,000 m between sexes were not observed in C4 and C6, while depth (Fig. 6). While part of the C5 population seemed C5 females were distributed deeper than C5 males. to migrate to shallower depths (Th–250 m) at night in All copepodid stages (C1–C6) were found through- October 2002, day–night diVerences in vertical distri- out the study period, with the exception of C5 males bution patterns of all copepodid stages combined (C1– which were absent in March 2002 (Fig. 7a). The abun- C6) were not signiWcant (Fig. 6; Kolmogorov–Smirnov dances of C1–C5 stages showed a clear seasonal pat- test, P > 0.05). Throughout the study period, the C1 tern. C1 were abundant both in March 2002 and individuals were found between 500 and 2,000 m February 2004, but they are less abundant in May– depth. Compared with C1, C2 showed a shallower dis- October 2002 and December 2003. C2 and C3 were tribution (250–1,000 m depth). C3–C5 stages occurred most abundant in March–May, and in May–August, 123 614 Mar Biol (2007) 150:609–625

(a) 15 egg-carrying C6 females were found throughout the 10 study period, their proportion of the total females was 5 high in May–August (53.1–71.1%) and low in October, C1 December and February (5.8–15.4%), with an interme- 0 40 diate value in March (35.0%) (Fig. 7b). There were sig- C2 niWcant seasonal diVerences in clutch sizes (one-way 20 ANOVA: F =12.7, df =6, 71, P < 0.0001; Fig. 8); the numbers of eggs per female in October (mean: 39.2) 0 and December (37.6) were signiWcantly higher than 40 those in May (12.5), June (19.7) and February (16.0),

:0-2000m) with intermediate values in March (25.9) and August -2 20 C3 (33.8) (Tukey–Kramer test, P < 0.05). 0 Based on the abundance of each copepodid stage inds. m 3 10 T. canadensis Female (Fig. 7a), the population structure of was C4 reconstructed in terms of relative abundance (Fig. 5b). 5 Male Among the immature stages (C1–C5), C1 and C2 pre- 0 dominated in March–May 2002 and in February 2004, 30 C3 and C4 in June–August 2002, and C5 in October

Abundance ( x10 C5 2002. The proportions of adults (C6 female and male) 15 to the total population were high throughout the study period (34.3–71.0%), especially in winter (December 0 60 2003 and February 2004; 57.4–71.0%). C6 30 Oncaea grossa

0 This species occurred largely from Th to 1,000 m depth (Fig. 9). Day–night diVerences in the vertical distribu- (b) 2 tion patterns examined in October 2002 showed no sig- Egg-carrying niWcant diVerence (Fig. 9, Kolmogorov–Smirnov test, Spermatophores-attached 1 P > 0.1). C1–C5 stages were concentrated consistently between Th and 500 m depth throughout the study 0 MAMJJ A SO DJF period (Fig. 9). While C6 also showed abundance peak Frequency (%) 2002 2003 2004 in Th–500 m, C6 was diVerent from C1 to C5 in that the moderate number of individuals was also occurred Fig. 4 Triconia borealis. Seasonal changes in a abundance of each developmental stage and b incidence of spermatophores-at- from 500 to 1,000 m. Seasonally, C3–C6 migrated tached and egg-carrying specimens in the total C6 females (%) at upward (Th–250 m layer) in May. DiVerences between Site H. Female and male data are shown separately for C4–C6. x: the sexes in the vertical distribution patterns were not no occurrence evident for C4 through C6. All copepodid stages (C1–C6 stages) were observed respectively. The maximum abundance of C4 males throughout the entire study period (Fig. 10a). C1 stage was seen in June, while that of females occurred in was most abundant in August. Seasonal abundance August. The abundance of both C5 females and males patterns of C2 and C3 were similar each other, with a peaked in October, though the former also formed a marked peak in October. C4 was abundant in March– moderate peak in May. Seasonal variations in the May 2002 and February 2004, but was less abundant in abundance of C6 females and males were less marked, June–October 2002 and December 2003. C5 was most decreasing gradually from March to October 2002, abundant in May–June, and they decreased gradually with a further decrease (males) or stabilization from June onward. Abundance of C6 males and (female) from December 2003 to February 2004. females varied less markedly with season. For C4–C6, The sex ratios varied seasonally; the ranges were the abundance of males and females showed the simi- 14.3–66.2% (mean: 40.3%) for C4, 0–66.9% (35.2%) for lar seasonal pattern. C5 and 39.5–57.7% (51.1%) for C6. C6 females with While the sex ratios of C4 varied greatly with season attached spermatophores were found only in March, from 11.2 to 48.2% (mean: 36.0%), those of C5 [33.4– accounting for 2.9% of total females (Fig. 7b). While 51.8% (mean: 43.3%)] and C6 [44.9–56.8% (mean: 123 Mar Biol (2007) 150:609–625 615

Fig. 5 Triconia borealis (a), (a) 100 T. canadensis (b), O. grossa C6 female (c) and O. parila (d). Seasonal 80 C6 male changes in copepodid stage composition at Site H. Female 60 C5 and male data are shown sep- arately for C6 40 C4

Composition (%) 20 C3

0 C2 C1 (b) 100

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(c) 100

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50.2%)] were near constant throughout the study F =5.94, df = 5, 20, P = 0.0016; Fig. 8). Subsequent period. C6 females with attached spermatophores were analysis revealed that clutch sizes in October (mean: found throughout the study period, with higher inci- 28.0) were signiWcantly greater than those in May dence in May (55.1%) and June (41.0%) as compared (19.2) and June (20.5), with intermediate values in with other months (5.8–15.9%) (Fig. 10b). There were March (27.0), August (24.5) and December (24.4) no signiWcant relationships between the proportion of (Tukey–Kramer test, P < 0.05). males to the total C6 population and the frequency of In terms of stage composition, the copepodid popu- C6 females with spermatophores attached (Spearman’s lation of O. grossa consisted mainly of younger stages r = 0.643, P = 0.12). Egg-carrying C6 females were (C1–C3) in August and October 2002 (55.0–67.7% of found from March to October, and in December 2003, the total population) (Fig. 5c). On the other hand, C4 but their proportions of total C6 female abundance was and C5 were abundant in March, May and June (30.5– low, ranging from 0.42 to 3.1% (Fig. 10b). There were 34.6% of the total population). C6 male and female signiWcant diVerences in the clutch sizes of O. grossa were the most dominant stages in March toward Octo- depending on the sampling dates (one-way ANOVA: ber. During the winter (December 2003 and February 123 616 Mar Biol (2007) 150:609–625

Abundance (inds. m-3)

05100510051005100 0.5 1 01201200.51 0

500

1000 C3 1500 C2 C1 2000

012301230480480123012300.5100.51 0

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1500 C6F C6M 2000 10 Mar. 30 May 18 Jun. 9 Aug. 9 Oct. 9 Oct. 17 Dec. 9 Feb. 2002 (D) (D) (N) (N) (D) (N)2003 (N)2004 (N)

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

2004), C3, C4 and C6 males and females dominated in in 1,000–2,000 m was greater than those for C2–C5. the copepodid population. Male/female diVerences in vertical distribution pattern were not evident for C4 through C6. Oncaea parila All copepodid stages (C1–C6) of O. parila occurred throughout the study period (Fig. 12a). Seasonal This species inhabited a broad bathymetric range changes in abundance of C1, C2 and C3 paralleled each between 250 and 2,000 m depth (Fig. 11). Day–night other, with an abundance peak in August 2002. For C4 diVerences in vertical distribution patterns were not through C6 stages, abundance and seasonal patterns of signiWcant for the all copepodid stages (C1–C6) in males and females were nearly identical. While the sea- October 2002 (Fig. 11, Kolmogorov–Smirnov test, sonal abundance patterns of C4–C6 were irregular, P > 0.05). The C1 stage was found largely below 500 m they were numerous in March–August 2002 and less depth during all seasons (Fig. 11). The C2–C5 popula- numerous in December 2003 and February 2004. tions showed a broad vertical distribution from Th to The sex ratios were almost constant throughout the 2,000 m depth, but most of them were concentrated in study period, ranging from 43.1 to 62.4% (mean: 250–1,000 m depth throughout the year. While C6 51.0%) for C4, 40.0 to 60.5% (47.9%) for C5 and 45.7 females and males were also distributed mainly in 250– to 60.3% (51.1%) for C6. C6 females with attached 1,000 m depth, the proportion of the population found spermatophores were observed from March to 123 Mar Biol (2007) 150:609–625 617

(a) 15 50 Triconia canadensis 10 40 5 30 C1 ) -1 0 20 40 C2 10 20 0

30 0 30 C3 20

: 0-2000 m) 20 -2 10 Clutch size (eggs female 10 0 inds. m

2 Oncaea grossa 15 C4 Female 0 10 MAMJJ A SO DJF Male 2002 2003 2004 5 0 Fig. 8 Triconia canadensis and O. grossa. Seasonal changes in clutch size (eggs per female) at Site H. Vertical bars, which 10 C5

Abundance ( x10 indicate § SD, are shown when they exceed the size of symbol 5 female, thus indicating that more than half of the popu- 0 30 lation was comprised of the C6 stage. 20 10 C6 Discussion 0

(b) Vertical distribution 80 Egg-carrying Spermatophores- Among the four oncaeid copepod species studied, attached 40 information about vertical distribution from other seas

0 is available for T. borealis and O. parila. In the central MAMJJ A SO DJF Arctic Ocean, T. borealis showed a broad vertical dis- Frequency (%) 2002 2003 2004 tribution pattern from the surface to 1,500 m depth, Fig. 7 Triconia canadensis. Seasonal changes in a abundance of but more than one half of the population occurred in each developmental stage and b incidence of spermatophores-at- the upper 200 m (Auel and Hagen 2002). Similar verti- tached and egg-carrying specimens in the total C6 females (%) at cal distribution patterns of this species have also been Site H. Female and male data are shown separately for C4–C6. x: no occurrence reported by Groendahl and Hernroth (1984) from the Nansen Basin, Arctic Ocean. The present results in the Oyashio region, with T. borealis being mainly distrib- October 2002 and in December 2003, but not in Febru- uted in the top 500 m (Fig. 3), are in fair agreement ary 2004 (Fig. 12b). The proportion of C6 females with with the previous reports from the Arctic Ocean. Diel spermatophores attached ranged from 0.28 to 1.5% of vertical migration (DVM) of T. borealis has been the total population with its peak in May 2002. noted by Groendahl and Hernroth (1984) and Fortier Throughout this study, only three individuals of C6 et al. (2001) in Arctic waters; the former reported the female carrying egg sacs were found in October 2002 amplitudes of DVM of this species to be more than (1.1% of the total C6 females) (Fig. 12b). Clutch sizes 200 m, whereas the latter reported much lower ampli- of C6 females examined were 11–12 eggs per female. tudes of 10–30 m. In the present study, however, such The copepodid stage composition was relatively DVM behaviour of T. borealis could not be detected constant throughout the study period (Fig. 5d). The (Fig. 3), probably because the amplitudes of their ranges of proportion of each copepodid stage to the DVM, if any, could not be resolved by the broad sam- total copepodids were 2.8–13.6% for C1, 4.5–11.2% for pling intervals of the present study (see “Materials and C2, 5.3–8.1% for C3, 5.4–12.0% for C4, 7.2–17.4% for methods” section). According to Metz (1996), O. parila C5, 26.7–36.7% for C6 male and 24.2–35.5% for C6 was distributed over the entire water column between 123 618 Mar Biol (2007) 150:609–625

Abundance (inds. m-3)

0102002040020400 100 200 0 100 200 0 100 200 0102002040 0

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1500 C6F C6M 2000 10 Mar. 30 May 18 Jun. 9 Aug. 9 Oct. 9 Oct. 17 Dec. 9 Feb. 2002 (D) (D) (N) (N) (D) (N)2003 (N)2004 (N)

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 each copepodid stage (Fig. 13). An OVM pattern simi- Sea, but the majority of populations resided below lar to that for the Antarctic oncaeid species by Metz 200 m depth. In the Oyashio region, O. parila occurred (1996) was evident for T. canadensis and O. parila in below the thermocline to 2,000 m depth (Fig. 11), but the Oyashio region (Table 2). While the feeding habit most were concentrated in the 250–1,000 m depth of the meso- and bathypelagic oncaeid species is layer. The broad vertical distribution of O. parila poorly deWned at present, most of them are assumed to between 250 and 3,000 m depth has also been observed be detritivores (see Discussion below). Since the in the Arctic Ocean (Heron et al. 1984). amount of detrital material in terms of particulate Metz (1996) reported that two Antarctic oncaeid organic carbon decreases exponentially with increasing species, Oncaea curvata and Triconia antarctica, under- depths in the ocean (e.g. Suess 1980; Pace et al. 1987), went an extensive ontogenetic vertical migration upward migration during the development as seen in (OVM). As a common feature of both species, upward T. canadensis and O. parila can be interpreted as a result migration was seen during the development from early of life history traits toward maximizing feeding gain for to middle copepodid stages, whereas late copepodid their growth at middle copepodid stages, as also sug- and adult stages descended to deeper layers. From the gested by Metz (1996). In contrast to T. canadensis and present vertical distribution data for all stages (C1–C6) O. parila, the OVM was not clear for T. borealis and O. of T. borealis, T. canadensis, O. grossa and O. parila, grossa (Table 2), but their C6 females were distributed we calculated the depth above and below which 50% much deeper depth than immature copepodids (C1– of the population resided (D50%; cf. Pennak 1943) for C5) and/or C6 males (Fig. 13). For sac-spawning 123 Mar Biol (2007) 150:609–625 619

(a) 30 similar food sources (Auel 1999). For oncaeid cope- C1 V 20 pods, Böttger-Schnack et al. (2004) reported di erent depth distributions of two sibling species, Triconia 10 hawii and T. recta, in the Red Sea. Among the four 0 oncaeid species studied, O. grossa and O. parila are 20 C2 morphologically similar to each other (Heron 1977; 10 Heron and Frost 2000) and thus belong to the notopus- group of the family Oncaeidae (Böttger-Schnack and 0 Huys 1998). As is evident in Fig. 13, species-speciWc 10 C3 depth distributions (i.e. the D50%) of O. grossa (350–

: 0-2000 m) 470 m) and O. parila (590–940 m) were clearly sepa-

-2 5 rated vertically across all copepodid stages (see also 0 Table 2). Since body sizes of the corresponding inds. m

3 6 copepodid stages of these two oncaeid species are Female almost the same (cf. Nishibe 2005), they might be Male 3 exploiting similar food sources (e.g. prey size and C4 0 preference). Thus, the vertical separation of O. grossa– 6 O. parila found in the Oyashio region may also be C5 interpreted as an avoidance of food competition in Abundance ( x10 3 the resource-limited mesopelagic depth zone. While T. borealis and T. canadensis belong to same conifera- 0 group (Böttger-Schnack 1999, 2004), their diVerential 12 vertical distribution patterns at Site H would not be a 6 result of size-speciWc competition (Fig. 13, Table 2), C6 because their body sizes are much dissimilar to each 0 other (cf. Nishibe 2005). (b) 60 Life cycle Egg-carrying 40 Spermatophores-attached Triconia borealis 20 0 MAMJJ A SO DJF The occurrence of C1–C6 stages in all seasons indicates Frequency (%) 2002 2003 2004 the year-round reproduction of T. borealis at Site H in Fig. 10 Oncaea grossa. Seasonal changes in a abundance of each the Oyashio region (Fig. 4a). Seasonal data of inci- developmental stage and b incidence of spermatophores-at- dence of egg-carrying and spermatophores-attached tached and egg-carrying specimens in the total C6 females (%) at females of T. borealis are not suYcient enough to Site H. Female and male data are shown separately for C4–C6. x: deWne their major reproduction period (Fig. 4b), but no occurrence greater abundance and predominance of adults in late May–October would seem to suggest that the major copepods such as oncaeids, it has been demonstrated spawning season to be in summer–fall. From seasonal that egg-carrying females suVer higher mortality than sequences in stage composition (Fig. 5a), it may be males and juveniles due to higher susceptibility to thought that younger copepodids (C1–C3) dominating visual predators (Kiørboe and Sabatini 1994). Hence, in March developed rapidly to C4–C5 in late May, then the deeper distribution of C6 females of T. borealis reached C6 in June at Site H. However, the entire and O. grossa observed in this study may be regarded development sequence of the copepodids of T. borealis as a refuge from predator-abundant shallower layer, could not be traced clearly, so their generation time although almost nothing is known about the distribu- was left unresolved in this study. On the other hand, tion of potential predators of oncaeid copepods in the diVerent seasonal variation patterns in abundance Oyashio region at present. between males and females of C4–C6 stages may sug- Vertical partitioning of the water column between gest diVerential developmental times for them. closely related species is generally considered to be a Because of lower adult proportion to total population strategy for marine copepods to reduce inter-speciWc during winter (Fig. 5a), adults may have ended their competition, since these species are assumed to exploit life cycle within the year. 123 620 Mar Biol (2007) 150:609–625

Abundance (inds. m-3)

04804803601020036036036036 0

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2000 C1

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1500 C6F C6M 2000 10 Mar. 30 May18 Jun. 9 Aug. 9 Oct. 9 Oct. 17 Dec. 9 Feb. 2002 (D) (D) (N) (N) (D) (N)(2003 N)(2004 N)

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. reported to have a 1–2 year life cycle and year-round borealis is limited to the population in Arctic waters. reproduction with its peak in spring/summer in the By analysing seasonal data of the size–frequency dis- Bellingshausen Sea (Metz 1996). tributions of copepodid stages, Richter (1994) consid- ered that the major reproduction of T. borealis took Triconia canadensis place in early summer and fall in the Greenland Sea. He also suggested that both the summer and fall gen- The year-round occurrence of egg-carrying C6 females erations need 1 year to complete their life cycle, suggests continuous reproduction of T. canadensis at although the basis for this estimation was not Site H (Fig. 7). Unexpectedly, the incidence of egg- described. Pavshtiks (1975) brieXy noted that repro- carrying C6 females and clutch sizes showed diVerent duction of T. borealis occurred in summer in the seasonal patterns; the former was high in May–August, Davis Strait. This information from previous workers, whereas the latter was high in August–December combined with the present results, indicates that (Figs. 7b, 8). This discrepancy makes it diYcult to T. borealis has an extended reproductive period with deWne the major reproduction season of T. canadensis its peak during the warmer seasons (summer–fall) in from these data. Alternatively, the abundance peaks boreal waters. Regarding other epipelagic oncaeid of C1 seen in February–March (Fig. 7a) may suggest species in high-latitude seas, Oncaea curvata is that the major spawning season of T. canadensis is 123 Mar Biol (2007) 150:609–625 621

(a) 6 C1 December–February and March (Fig. 5b), C6 might overwinter and reproduce in the second year. 3 No comparable information is presently available about the life cycle of T. canadensis. According to 0 Metz (1996), T. antarctica, a closely-related species to 4 C2 T. canadensis (Heron 1977; Heron and Frost 2000), has 2 1 year life cycle in the northern Bellingshausen Sea. Despite the diVerences in the habitat temperature 0 between the Bellingshausen Sea (–1.8 to 2.5°C, cf. 4 C3 Metz 1996) and the Oyashio region (2.5–3.5°C, Fig. 2),

: 0-2000 m) the annual life cycle of T. antarctica is in good agree- -2 2 ment with the present estimates of that T. canadensis, 0 mentioned above. inds. m

3 3 C4 Female 2 Oncaea grossa Male 1 0 Nothing is known about the life cycle of O. grossa. The year-round occurrence of all copepodid stages and C6 3 C5

Abundance ( x10 2 females with spermatophores attached suggests that reproduction of O. grossa occurred in all seasons of the 1 year at Site H (Fig. 10). Judging from a marked increase 0 of C6 females with spermatophores attached in late 15 May–June (Fig. 10b), followed by high abundance of 10 C1 in August–October (Fig. 10a), the major reproduc- 5 C6 tion of this species is considered to occur in summer. 0 However, this scheme is not consistent with the lower (not higher) clutch size of this species in summer (b) 2 Egg-carrying (Fig. 8). By tracing the abundance peak of each copepo- Spermatophores-attached did stage, it can be estimated that C1 stage recruited in 1 August developed to C2–C3 in October (Fig. 10a). On the other hand, C4 that dominated in March developed 0 MAMJJ A SO DJF to C5 in May–June, and to C6 in August. Combining Frequency (%) 2002 2003 2004 these two segments of their development, the genera- tion time of O. grossa may be estimated as 1 year at Site Fig. 12 Oncaea parila. Seasonal changes in a abundance of each H. The high proportions of adults (C6 female and male) developmental stage and b incidence of spermatophores-at- tached and egg-carrying specimens in the total C6 females (%) at in the total population during winter–early spring Site H. Female and male data are shown separately for C4–C6. x: (December, February and March) (Fig. 5c), may indi- no occurrence cate that the adult population overwinters and repro- duces in the second year, if one assumes a repetition of the same annual cycle every year. fall–early winter, which coincides nearly with the season where higher clutch sizes were observed. Oncaea parila Laboratory observations showed that egg hatching of T. canadensis needs 70–85 days at the ambient temper- The occurrence of all copepodid stages (C1–C6) of ature (3°C) (Y. Nishibe, unpublished data), thus sup- O. parila throughout the study period (Fig. 12a), porting this scenario. By assuming the seasonal together with stable copepodid stage composition in all population structure is stable every year, it is possible seasons (Fig. 5d) suggests year-round reproduction and to trace the development sequence of the peak of C1 continuous recruitment to adult (C6) at Site H. The seen in February–March which reached C6 in Decem- lack of dominant cohorts throughout the year makes it ber (Fig. 5b). From this scenario, the generation time impossible to trace developmental sequences and esti- of T. canadensis is estimated to be approximately mation of the generation time of O. parila. Assuming 1 year at Site H. Because the proportions of C6 females constant mortality during each copepodid stage, pre- and males to the total population remained high in dominance of C6 individual in total copepodids would 123 622 Mar Biol (2007) 150:609–625

0

250

500

750 Triconia borealis Oncaea grossa 1000

Depth (m) 0

500

1000

1500 Triconia canadensis Oncaea parila 2000 C1 C2 C3 C4M C4F C5M C5F C6M C6F C1 C2 C3 C4M C4F C5M C5F C6M C6F

Fig. 13 Triconia borealis, T. canadensis, O. grossa and O. parila. Mean D50% for each copepodid stage at Site H. Vertical bars, which indicate § SD, are shown when they exceed the size of symbol. Note that depth scale of each panel is not necessarily the same

Table 2 Summary of life cycle data of four oncaeid copepods in the Oyashio region, western subarctic PaciWc Triconia borealis Triconia canadensis Oncaea grossa Oncaea parila

Body lengtha (C6 female/male: mm) 0.68/0.43 1.56/1.19 0.80/0.65 0.63/0.48 b Depth distribution (D50% of the whole 150 640 370 790 population: m) Ontogenetic vertical migration No Yes No Yes Reproductive pattern Year-round, with Year-round, with peak Year-round, with peak Year-round, with peak in summer–fall in fall–early winter around summer no seasonal peak Estimated generation time ? 1 year 1 year ? a Data from Nishibe (2005) b Calculated from the present vertical distibution data for each encaeid copepod suggest that stage duration of the C6 is very long as com- Food availability and reproduction pared with those of the preceding copepodid stages. On the basis of similar results as those found in the In the Oyashio region, it has been demonstrated that the present study, Metz (1996) could not resolve the life spring phytoplankton bloom, which usually occurs from cycle pattern of the O. parila population in the Bel- April to May (Kasai et al. 2001), plays an integral role, lingshausen Sea, though she also suggested a possibly directly or indirectly, in inducing spawning and facilitat- longer stage duration of adults and year-round con- ing rapid development of large grazing copepods such as stant reproduction of this species. Neocalanus spp., Metridia spp. and Eucalanus bungii In summary, it becomes evident that while the (e.g. Kobari and Ikeda 1999, 2001a, b; Padmavati et al. reproduction of T. borealis, T. canadensis, O. grossa 2004; Shoden et al. 2005). On the other hand, the major and O. parila continues throughout the year in the reproduction periods of T. borealis, T. canadensis and Oyashio region, the former three exhibit marked sea- O. grossa did not coincide with the phytoplankton bloom sonal peaks; summer–fall for T. borealis, fall–early period, although rapid development from early to late winter for T. canadensis and summer for O. grossa copepodid stage of T. borealis was seen in March–late (Table 2). In addition, we could estimate the genera- May (Fig. 5a). In general, oncaeid copepods are classi- tion time of T. canadensis and O. grossa as 1 year, Wed to omnivores, because various prey items (e.g. dia- but this was not the case for T. borealis and O. parila tom, dinoXagellate, copepods and other ) due to the diYculties in tracing the sequences of were found from their guts and faecal pellets (Pasternak cohorts. 1984; Turner 1986; Ohtsuka et al. 1996). Also, previous 123 Mar Biol (2007) 150:609–625 623 studies suggested that marine snow aggregates (includ- support for the data analysis and manuscript preparation. This ing discarded appendicularian houses), which are study was supported partly by JSPS KAKENHI 14209001. enriched by a variety of attached particles (e.g. bacteria, picophytoplankton, diatoms, protists and faecal pellets), are an important food source for oncaeid copepods (All- References dredge 1972; Ohtsuka and Kubo 1991; Lampitt et al. Alldredge AL (1972) Abandoned larvacean houses: a unique 1993; Ohtsuka et al. 1993, 1996; Steinberg et al. 1994). In food source in the pelagic environment. Science 177:885–887 our laboratory observations, T. canadensis feed well on Auel H (1999) The ecology of Arctic deep-sea copepods (Euchaeti- dead Artemia nauplii and weakened chaetognaths, sug- dae and Aetideidae). Aspects of their distribution, trophody- gesting their preference to dead or moribund namics and eVect on the carbon Xux. Ber Polarforsch 319:1–97 Auel H, Hagen W (2002) Mesozooplankton community struc- foods. Hopkins (1987) and Metz (1998) have reported ture, abundance and biomass in the central Arctic Ocean. carnivorous feeding of the sibling species T. antarctica. Mar Biol 140:1013–1021 Almost nothing is known about food for T. borealis and Böttger-Schnack R (1994) The microcopepod fauna in the East- O. grossa (and O. parila also), although Kattner et al. ern Mediterranean and Arabian Seas: a comparison with the Red Sea fauna. Hydrobiologia 292/293:271–282 (2003) suggested T. borealis to be detritivore and/or car- Böttger-Schnack R (1995) Summer distribution of micro- and nivore from analysis of fatty acid composition of its small mesozooplankton in the Red Sea and Gulf of Aden, body. O. curvata, which is as small as three of the with special reference to non-calanoid copepods. Mar Ecol oncaeid species in this study (T. borealis, O. grossa and Prog Ser 118:81–102 O parila Böttger-Schnack R (1996) Vertical structure of small metazoan . ), did not show carnivorous feeding and fed plankton, especially non-calanoid copepods I. Deep Arabian exclusively on large gelatinous aggregates of phyto- Sea. J Plankton Res 18:1073–1101 plankton (Metz 1998). From these results, it can be Böttger-Schnack R (1997) Vertical structure of small metazoan assumed that all T. borealis, T. canadensis, O. grossa and plankton, especially non-calanoid copepods. II. Deep Eastern Mediterranean (Levantine Sea). Oceanol Acta 20:399–419 O parila . utilize a wide spectrum of prey (e.g. phyto- Böttger-Schnack R (1999) of Oncaeidae (Copepoda, plankton, zooplankton and its carcasses, and marine ) from the Red Sea. I. 11 species of Trico- snow) in nature, but T. borealis and T. canadensis show a nia gen. nov. and a redescription of T similis (Sars) from Nor- more carnivorous feeding habit compared to the other wegian waters. Mitt Hamb Zool Mus Inst 96:37–128 Böttger-Schnack R (2001) Taxonomy of Oncaeidae (Copepoda, two species. In the Oyashio region, appendicularian bio- Poecilostomatoida) from the Red Sea. II. Seven species of mass and house production reaches its annual maximum Oncaea s str. Bull Br Mus Lond (Nat Hist) Zool 67:25–84 in July–October (Y. Shichinohe, unpublished data), Böttger-Schnack R (2004) Triconia parasimilis Böttger-Schnack, indicating that vertical Xux of marine snow originating 1999 (Copepoda, Oncaeidae), Wrst record from the NW Paci- Wc (Oyashio), with the description of the male. Mitt Hamb from discarded appendicularian houses may increase Zool Mus Inst 101:213–223 during this period. In addition, mesozooplankton bio- Böttger-Schnack R, Huys R (1998) Species groups within the ge- mass in the deeper layer (250–2,000 m depth) of the nus Oncaea Philippi 1843 (Copepoda, Poecilostomatoida). J region increases between July and December (cf. Mar Syst 15:369–371 Böttger-Schnack R, Huys R (2001) Taxonomy of Oncaeidae (Co- Kobari et al. 2003). These facts would seem to suggest pepoda, Poecilostomatoida) from the Red Sea. III. Morphol- that the main reproduction periods of T. borealis (sum- ogy and phylogenetic position of Oncaea subtilis Giesbrecht mer–fall), T. canadensis (fall–early winter) and O. grossa 1892. Hydrobiologia 453/454:467–481 (summer) are adjusted to the most abundant period of Böttger-Schnack R, Schnack D (2005) Population structure and fecundity of the microcopepod Oncaea bispinosa in the Red their potential foods in the Oyashio region. Clearly, Sea—a challenge to general concepts for the scaling of fecun- more precise evaluation of the feeding habits of the four dity. Mar Ecol Prog Ser 302:159–175 oncaeid copepod species studied here is an essential step Böttger-Schnack R, Lenz J, Weikert H (2004) Are taxonomic de- toward a better understanding of their life cycle patterns tails of relevance to ecologist? An example from oncaeid mi- crocopepods of the Red Sea. Mar Biol 144:1127–1140 and their roles in trophodynamics of copepods in the Boxshall GA (1977) The depth distributions and community Oyashio region. organization of the planktonic cyclopoids (Crustacea: Cope- poda) of the Cape Verde Islands region. J Mar biol Assoc Acknowledgments We greatly thank Dr. R. Böttger-Schnack UK 57:543–568 for reviewing an earlier draft of this paper; her constructive com- Boxshall GA, Halsey SH (2004) An introduction to copepod ments signiWcantly improved the manuscript. Dr. J. T. Turner diversity. The Ray Society, London provided editorial advice. Thanks are extended to the captains Deevey GB, Brooks AL (1977) Copepods of the Sargasso Sea oV and crews of T.S. ‘Oshoro Maru’ and R.V. ‘Ushio Maru’ (Hokka- Bermuda: species composition, and vertical and seasonal distri- ido University) for their help in Weld samplings. We thank Ms. Y. bution between the surface and 2000 m. Bull Mar Sci 27:256–291 Shichinohe who kindly provided unpublished data on appendicu- Fortier M, Fortier L, Hattori H, Saito H, Legendre L (2001) Vi- larians in the Oyashio region. Y. N. is grateful to the Division of sual predators and the diel vertical migration of copepods Aquatic Biology and Ecology, Center for Marine Environmental under Arctic sea ice during the midnight sun. J Plankton Res Studies, Ehime University, for providing logistical and Wnancial 23:1263–1278 123 624 Mar Biol (2007) 150:609–625

Groendahl F, Hernroth L (1984) Vertical distribution of cope- ida, Copepoda) in the Bellingshausen Sea (in German with pods in the Eurasian part of the Nansen basin, Arctic Ocean. English abstract). Ber Polarforsch 207:1–123 Syllogeus 58:311–320 Metz C (1998) Feeding of Oncaea curvata (Poecilostomatoida, Heron GA (1977) Twenty-six species of Oncaeidae (Copepoda: Copepoda). Mar Ecol Prog Ser 169:229–235 Cyclopoida) from the southwest PaciWc Antarctic area. In: Motoda S (1959) Devices of simple plankton apparatus. Mem Fac Pawson DL (ed) Biology of the Antarctic Seas, VI. Antarct Fish Hokkaido Univ 7:73–94 Res Ser, vol 26, pp 37–96 Nishibe Y (2005) The biology of oncaeid copepods (Poecilosto- Heron GA, Frost BW (2000) Copepods of the family Oncaeidae matoida) in the Oyashio region, western subarctic PaciWc: its (Crustacea: Poecilostomatoida) in the northeast PaciWc community structure, vertical distribution, life cycle and Ocean and inland coastal waters of Washington State. Proc metabolism. PhD Thesis, Hokkaido University Biol Soc Wash 113:1015–1063 Nishibe Y, Ikeda T (2004) Vertical distribution, abundance and Heron GA, English TS, Damkaer DM (1984) Arctic Ocean cope- community structure of oncaeid copepods in the Oyashio re- poda of the genera Lubbockia, Oncaea, and Epicalymma gion, western subarctic PaciWc. Mar Biol 145:931–941 (Poecilostomatoida: Oncaeidae), with remarks on distribu- Noda M, Ikeda I, Ueno S, Hashimoto H, Gushima K (1998) tions. J Crust Biol 4:448–490 Enrichment of coastal zooplankton communities by drifting Hopcroft RR, Clarke C, Nelson RJ, RaskoV KA (2005) Zoo- zooplankton patches from the Kuroshio front. Mar Ecol plankton communities of the Arctic’s Canada Basin: the con- Prog Ser 170:55–65 tribution by smaller taxa. Polar Biol 28:198–206 Ohtani K (1971) Studies on the changes of the hydrographic condi- Hopkins TL (1987) Midwater food web in McMurdo Sound, Ross tions in the Funka Bay. II. Characteristics of the waters occu- Sea, Antarctica. Mar Biol 96:93–106 pying the Funka Bay. Bull Fac Fish Hokkaido Univ 22:58–66 Kasai H, Saito H, Kashiwai M, Taneda T, Kusaka A, Kawasaki Y, Ohtsuka S, Kubo N (1991) Larvaceans and their houses as impor- Kono T, Taguchi S, Tsuda A (2001) Seasonal and interannu- tant food for some pelagic copepods. Bull Plankton Soc Jpn al variations in nutrients and plankton in the Oyashio region: Spec vol: 535–551 a summary of a 10-years observation along A-line. Bull Hok- Ohtsuka S, Kubo N, Okada M, Gushima K (1993) Attachment kaido Natl Fish Res Inst 65:55–65 and feeding of pelagic copepods on larvacean houses. J Oce- Kattner G, Albers C, Graeve M, Schnack-Schiel SB (2003) Fatty anogr Soc Jpn 49:115–120 acid and alcohol composition of the small polar copepods Ohtsuka S, Böttger-Schnack R, Okada M, Onbe T (1996) In situ Oithona and Oncaea: indication on feeding modes. Polar feeding habits of Oncaea (Copepoda: Poecilostomatoida) Biol 26:666–671 from the upper 250 m of the central Red Sea, with special ref- Kawamura A (1989) Fast sinking mouth ring for closing Norpac erence to consumption of appendicularian houses. Bull net. Nippon Suisan Gakk 55:1121 Plankton Soc Jpn 43:89–105 Kiørboe T, Sabatini M (1994) Reproductive and life cycle strate- Pace ML, Knauer GA, Karl DM, Martin JH (1987) Primary pro- gies in egg-carrying cyclopoid and free-spawning calanoid duction, new production and vertical Xux in the eastern Paci- copepods. J Plankton Res 16:1353–1366 Wc Ocean. Nature 325:803–804 Kobari T, Ikeda T (1999) Vertical distribution, population struc- Padmavati G, Ikeda T, Yamaguchi A (2004) Life cycle, popula- ture and life cycle of Neocalanus cristatus (Crustacea: Cope- tion structure and vertical distribution of Metridia spp. (Co- poda) in the Oyashio region, with notes on its regional pepoda: Calanoida) in the Oyashio region (NW PaciWc variations. Mar Biol 134:683–696 Ocean). Mar Ecol Prog Ser 270:181–198 Kobari T, Ikeda T (2001a) Life cycle of Neocalanus Xemingeri PaVenhöfer GA (1983) Vertical zooplankton distribution on the (Crustacea: Copepoda) in the Oyashio region, with notes on northeastern Florida shelf and its relation to temperature its regional variations. Mar Ecol Prog Ser 209:243–255 and food abundance. J Plankton Res 5:15–33 Kobari T, Ikeda T (2001b) Ontogenetic vertical migration and life PaVenhöfer GA (1993) On the ecology of marine cyclopoid cope- cycle of Neocalanus plumchrus (Crustacea: Copepoda) in the pods (Crustacea, Copepoda). J Plankton Res 15:37–55 Oyashio region, with notes on its regional variations in body Pasternak AF (1984) Feeding of copepods of the genus Oncaea size. J Plankton Res 23:287–302 (Cyclopoida) in the southeastern PaciWc Ocean. Oceanology Kobari T, Shinada A, Tsuda A (2003) Functional roles of inter- 24:609–612 zonal migrating mesozooplankton in the western subarctic Pavshtiks EA (1975) Biological seasons in the zooplankton of PaciWc. Prog Oceangr 57:279–298 Davis Strait. In: Zvereva ZhA (eds) Geographical and sea- KrniniT F (1998) Vertical distribution of protozoan and microco- sonal variability of marine plankton. Israel Program for Sci- pepod communities in the South Adriatic Pit. J Plankton Res entiWc Translations, Jerusalem, pp 200–247 20:1033–1060 Pennak RW (1943) An eVective method of diagramming diurnal KrniniT F, Grbec B (2002) Some distributional characteristics of movements of zooplankton organisms. Ecology 24:405–407 small zooplankton at two stations in the Otranto Strait (East- Reid JL (1973) North PaciWc Ocean waters in winter. The Johns ern Mediterranean). Hydrobiologia 482:119–136 Hopkins Oceanographic Studies No 5. The Johns Hopkins Lampitt RS, Wishner KF, Turley CM, Angel MV (1993) Marine Press, Baltimore, pp 1–9 snow studies in the Northeast Atlantic Ocean: distribution, Richter C (1994) Regional and seasonal variability in the vertical composition and roles as a food source for migrating plank- distribution of mesozooplankton in the Greenland Sea. Ber ton. Mar Biol 116:689–702 Polarforsch 154:1–90 Malt SJ (1982) Developmental stages of Oncaea media Giesbr- Satapoomin S, Nielsen TG, Hansen PJ (2004) Andaman Sea co- echt, 1891 and Oncaea subtilis Giesbrecht 1892. Bull Br Mus pepods: spatio-temporal variations in biomass and produc- Lond (Nat Hist) Zool 43:129–151 tion, and role in the pelagic food web. Mar Ecol Prog Ser Malt SJ (1983) Studies on the taxonomy and ecology of the ma- 274:99–122 rine copepod genus Oncaea Philippi. PhD Thesis, University Shoden S, Ikeda T, Yamaguchi A (2005) Vertical distribution, of London population structure and lifecycle of Eucalanus bungii (Co- Metz C (1996) Life strategies of dominant Antarctic Oithonidae pepoda: Calanoida) in the Oyashio region, with notes on its (Cyclopoida, Copepoda) and Oncaeidae (Poecilostomato- regional variations. Mar Biol 146:497–511

123 Mar Biol (2007) 150:609–625 625

Steinberg DK, Silver MW, Pilskaln CH, Coale SL, Paduan JB Uye S, Ayaki Y, Onbe T (1992) Seasonal geographical distribu- (1994) Midwater zooplankton communities on pelagic detri- tion of zooplankton in Hiroshima bay and its adjacent wa- tus (giant larvacean houses) in Monterey Bay, California. ters, the Inland Sea of Japan. J Fac Appl Biol Sci Hiroshima Limnol Oceanogr 39:1606–1620 Univ 31:99–119 Suess E (1980) Particulate organic carbon Xux in the oceans –sur- Webber MK, RoV JC (1995) Annual structure of the copepod face productivity and oxygen utilization. Nature 288:260–263 community and its associated pelagic environment oV Dis- Terazaki M, Tomatsu C (1997) A vertical multiple opening and clos- covery Bay, Jamaica. Mar Biol 123:467–479 ing plankton sampler. J Adv Mar Sci Technol Soc 3:127–132 Yamaguchi A, Watanabe Y, Ishida H, Harimoto T, Furusawa K, Turner JT (1986) Zooplankton feeding ecology: contents of fecal Suzuki S, Ishizaka J, Ikeda T, Takahashi MM (2002) Com- pellets of the cyclopoid copepods , Corycaeus munity and trophic structures of pelagic copepods down to amazonicus, Oithona plumifera and O simplex from the greater depths in the western subarctic PaciWc (WEST-COS- Northern Gulf of Mexico. Mar Ecol PSZNI 7:289–302 MIC). Deep-Sea Res I 49:1007–1025 Turner JT (2004) The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool Stud 43:255–266

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