Marine Biology (2004) 145: 515–527 DOI 10.1007/s00227-004-1329-3

RESEARCH ARTICLE

Y. Yamada Æ T. Ikeda Æ A. Tsuda Comparative life-history study on sympatric hyperiid amphipods (Themisto pacifica and T. japonica) in the Oyashio region, western North Pacific

Received: 17 October 2003 / Accepted: 4 February 2004 / Published online: 26 March 2004 Springer-Verlag 2004

Abstract Life-history features of the sympatric amphi- specimens, the minimum and maximum generation pods Themisto pacifica and T. japonica in the western times of females at a temperature range of 2–12C were North Pacific were analyzed based on seasonal field computed as 32 days (12C) and 224 days (2C), samples collected from July 1996 through July 1998, and respectively, for T. pacifica, and 66 days (12C) and data from laboratory rearing experiments. T. pacifica 358 days (2C), respectively, for T. japonica. The num- occurred throughout the year, with populations peaking bers of eggs or juveniles in females’ marsupia increased from spring to summer. In contrast, T. japonica were with female body length and ranged from 23 to 64 for rare from autumn to early winter, but became abundant T. pacifica and from 152 to 601 for T. japonica. Taking in late winter to spring. Mature T. pacifica females and into account the number of mature female instars, life- juveniles occurred together throughout the year, indi- time fecundities were estimated as 342 eggs for T. cating year-round reproduction. Mature T. japonica pacifica and 1195 eggs for T. japonica. Possible mecha- females were observed only in spring, and juveniles nisms for the coexistence of these two amphipods in the occurred irregularly in small numbers, suggesting lim- Oyashio region are also discussed. ited, early-spring reproduction in this study area. Size composition analysis of T. pacifica identified a total of eight cohorts over the 2 years of the study. Due to the smaller sample size and rarity of mature females Introduction (>9.6 mm) and males (>7.1 mm), cohort analyses of T. japonica were not comparable. Laboratory rearing of Hyperiid amphipods are common components of marine specimens at 2C, 5C, 8C and 12C revealed that a zooplankton communities throughout the world. Among linear equation best expressed body length growth by hyperiid amphipods, those belonging to the genus T. pacifica, while a logistic equation best expressed body Themisto are numerous, both in abundance and biomass, length growth by T. japoncia. Combining these labora- in high-latitude seas worldwide. They are generally car- tory-derived growth patterns with maturity sizes of wild nivores, preying on other zooplankton. In turn, they form important prey components of fishes (Lambert 1960; LeBrasseur 1966; Lønne and Gulliksen 1989; Communicated by O. Kinne, Oldendorf/Luhe Dalpadado et al. 2000), sea birds (Ogi and Hamanaka Y. Yamada (&) Æ T. Ikeda 1982; Ogi et al. 1985; Pedersen and Falk 2000; Bocher Marine Biodiversity Laboratory, Graduate School of Fisheries et al. 2000), and marine mammals (Kawamura 1970; Sciences, Hokkaido University, 3-1-1 Minato-machi, Nemoto and Yoo 1970; Wathne et al. 2000). Themisto 041-8611 Hakodate, Hokkaido, Japan E-mail: [email protected] amphipods play an important intermediate role between Fax: +81-3-53516481 primary production and the production of higher trophic level animals in polar sea ecosystems (Pakhomov and A. Tsuda Hokkaido National Fisheries Research Institute, Perissinotto 1996; Froneman et al. 2000; Bocher et al. 116 Katsurakoi, 085-0802 Kushiro, Hokkaido, Japan 2001; Auel et al. 2002). In the western subarctic Pacific and its marginal seas, Present address: Y. Yamada Ocean Research Institute, University of Tokyo, Themisto pacifica and T. japonica are the most abundant 1-15-1 Minamidai, 164-8639 Nakano, Tokyo, Japan hyperiid amphipods (Bowman 1960). T. pacifica is dis- Present address: A. Tsuda tributed widely in the western through eastern North Ocean Research Institute, University of Tokyo, Pacific and Bering Sea, but not in the Japan Sea and 1-15-1 Minamidai, 164-8639 Nakano, Tokyo, Japan Okhotsk Sea. Compared with the wide geographical 516 distribution of T. pacifica, the distribution of T. japonica reason, only incidental information is currently available is limited to the Japan Sea and the Okhotsk Sea, off the on Themisto amphipods in the western subarctic Pacific. east coast of northern Japan and off the southern Kur- Studies on these amphipods have examined diel vertical iles (Bowman 1960). The trophic importance of these distribution for Themisto spp. (Yoo 1970; Sugisaki two amphipods is suggested by their frequent occurrence 1991), population growth for T. japonica (Sugisaki et al. in the stomach contents of the salmon Oncorhynchus 1990), and horizontal distribution patterns for T. pacif- gorbuscha, O. masou (Fukataki 1967, 1969) and O. keta ica (Bowman 1960; Vinogradov 1992). (Tadokoro et al. 1996), the walleye pollock Theragra As part of a research program to evaluate trophody- chalcogramma (Fujita et al. 1995; Kooka et al. 1997; namics in the pelagic ecosystem in the Oyashio region, Yamamura et al. 2002), the common squid Todarodes western North Pacific, we investigated seasonal changes pacificus (Okiyama 1965) and of mesopelagic fishes, such in abundance, biomass and population structure (size as Diaphus theta, Stenobrachisu leucopsarus and Gonos- and maturity) and brood size of T. pacifica and toma gracile (Beamish et al. 1999; Moku et al. 2000; T. japonica as a basis for evaluating their life-cycle pat- Uchikawa et al. 2001). terns. In conjunction with field population analyses, Numerous studies have examined various aspects of laboratory rearing experiments facilitated analyses of T. japonica living in the Japan Sea, including vertical growth and maturation patterns. From these combined distribution patterns (Semenova 1974; Ikeda et al. 1992), results, possible mechanisms that enable T. pacifica and life cycles (Ikeda et al. 1992), growth models (Ikeda T. japonica to coexist in the Oyashio region are discussed. 1990), lifetime carbon budgets (Ikeda 1991), and popu- lation production calculations (Ikeda and Shiga 1999). In contrast to the Japan Sea, the western North Pacific Materials and methods has two co-occurring Themisto amphipods (T. pacifica and T. japonica). T. pacifica and T. japonica are mor- Field sampling phologically similar and difficult to distinguish. For this Seasonal samples were collected at night using oblique tows of bongo nets (mouth opening: 70·2 cm, mesh size: 333 lm) from a Table 1 Sampling data of oblique tows of bongo nets in the depth of about 500 m (range: 386–900 m) to the surface (Tsuda Oyashio region from July 1996 to July 1998 (n.a. failed to record) et al. 1999). Samples were taken from July 1996 to July 1998 (Table 1) in the Oyashio region within the rectangle defined by Year Date Time of day Max. net depth (m) 4130¢–4230¢N and 14500¢–14600¢E (hereafter referred to as ‘‘site H’’; Fig. 1). The vessels used for sampling were the F.R.V. ‘‘Hokko Maru’’ and ‘‘Tankai Maru’’ of the Hokkaido National 1996 8 Jul 23:40–00:31 508 Fisheries Research Institute and the F.R.V. ‘‘Hokushin Maru’’ of 2 Aug 18:58–19:38 479 the Hokkaido Fisheries Experimental Station at Kushiro. Net 3 Oct 20:12–21:03 n.a. depth was measured with a depth-meter (Rigosha), and the volume 5 Dec 05:15–06:01 488 of water filtered through the nets was measured by a flow-meter 1997 13 Jan 23:05–23:58 851 (Rigosha). As mentioned below (see ‘‘Vertical distribution’’ sub- 13 Mar 22:13–00:07 574 section in ‘‘Results’’), the depth reached by the net is sufficient to 15 Apr 20:25–21:30 521 collect almost the entire populations of the two amphipods. Tem- 13 May 00:13–01:00 734 perature and salinity profiles were determined concurrently with a 4 Jul 01:35–02:26 435 CTD system during each sampling. 22 Aug 02:00–02:51 748 To evaluate day/night vertical distribution patterns, zooplank- 3 Oct 22:49–22:56 685 ton samples were collected from 15 depth horizons between the 1998 17 Jan 18:50–20:07 883 surface and a depth of 1100 m, using a set of MTD nets (mouth 14 Mar 23:06–00:01 386 opening: 56 cm; mesh opening: 0.33 mm; Motoda 1971) on 1 19 Apr 20:07–21:07 408 September 1992 aboard the T.S. ‘‘Oshoro Maru’’. The nets were 15 May 18:42–19:41 900 towed at a speed of 1.0–1.5 knots for 20 min, and the volume of 7 Jul 02:14–03:00 448 water that passed through each net was registered with flow-meters

Fig. 1 Location of sampling area (site H, shaded box) and station E-16 (dot) in the western North Pacific 517

(Rigosha) mounted in the center of the net mouth rings. All zoo- maintained at ca. 5C and transported to the laboratory on land. plankton samples collected with bongo nets and MTD nets were At each sampling, seawater was collected with Van Dorn or Niskin preserved immediately in 5% formalin-seawater buffered with water samplers from 100 m depth and kept in 20-l containers for borax. use in the experiments. Live specimens were placed individually in Zooplankton samples were weighed (wet biomass) at the labo- 50- to 1000-ml glass containers filled with seawater. The containers ratory on land. Themisto spp. were sorted from the zooplankton were placed in refrigerated incubators, where temperatures were samples for the following analyses. adjusted to 2C, 5C, 8C, or 12C. Specimens were reared in the dark. Cut whelk (Neptunes lyrata) meat was provided in excess as food. Seawater in the containers was changed every 5–10 days, with each new preparation of food. The containers were examined daily Body size, maturity stage and identification for molts. Molts, when found, were removed from the container, and the number of pleopod segments was determined. Body length (BL; mm) was measured under a dissecting microscope to the nearest 0.05 mm, as the maximum distance between the tip of the head and the distal end of the uropod of the straightened body. Brood size Amphipods have no larval stage. The sexual maturity of hyperiid amphipods can be determined from secondary sexual Some live female specimens collected for laboratory rearing characteristics, such as the development of oostegites in females experiments were sacrificed, and the eggs or larvae in their mar- and extended first or second antennae in males. We classified the supia were counted. To avoid possible losses during preservation, Themisto spp. specimens into the following three maturity stages eggs and larvae were removed from the female’s marsupia imme- using Kane’s (1963) criteria: ‘‘juveniles’’—no sexual characteristics diately after collection and preserved separately. evident; ‘‘immature adults’’—oostegites present but not fully developed beyond the gill (females), or segmented but not fully extended first and second antennae (males); and ‘‘adults’’—oos- tegites developed larger than the gills (females), or fully extended Results first and second antennal flagellae (males). Hydrography

Instar analysis In the western North Pacific, the current of the subarctic circulation called ‘‘Oyashio’’ flows to southwest along For amphipods that lack morphological development stages, the number of pleopod rami segments can be used as an instar number the Kuril Islands and Hokkaido, and reaches the east marker. Themisto amphipods (T. compressa and T. japonica) add coast of northern Honshu, Japan (cf. Reid 1973). Site H one new pleopod rami segment at each molting, although this is located just south of the main stream of the Oyashio regular pattern may stop near the end of their life span (Sheader current. Over the study period, surface temperatures 1981; Ikeda 1990). With this limitation in mind, the number of segments in the first pleopod rami was used as an indicator of the ranged from 2C (March and April 1997 and March instar number. 1998) to 16C (August 1996 and October 1997; Fig. 2). The Oyashio water, characterized by salinities from 33.0& to 33.3& and temperatures <3C (Ohtani 1971), Themisto pacifica versus T. japonica occurred in the upper 150 m from March to April 1997 and in March 1998. Surface temperatures >10C were Adult Themisto pacifica females and males can be distinguished observed from July to October 1996 and from June to from adult T. japonica males and females by the length of the first and second antennae, the number of setae on the inner margin of October 1997, when the thermocline was well established the propus of the sixth pereopod, and the number of exopod seg- at 20–50 m depth. Oyashio water is often modified as a ments of the first pleopod (Semura et al. 1991). However, until result of exchange with Okhotsk Sea water, Tsugaru Yamada and Ikeda’s (2004) study, no effective morphological warm current water and Kuroshio water during its flow characteristics had been identified to distinguish specimens of the two species smaller than 5 mm. According to Yamada and Ikeda (Kono 1996). Because of the meandering flow pattern, (2004), T. pacifica can be morphologically distinguished from isolated loops of the Kuroshio extension are often en- T. japonica at all developmental stages by the following criteria. trapped between the downstream and return flows of the ‘‘Adult females’’ have a body length <9 mm (T. pacifica)or Oyashio and are called ‘‘warm core rings’’ (Kobari and >9 mm (T. japonica). ‘‘Adult males’’ have a body length <7 mm Ikeda 1999). The effect of warm core rings, which have (T. pacifica)or>7mm(T. japonica). ‘‘Immature’’ females and males are determined by the number of setae on the inner margin of salinities >33.4& and temperatures >6C, was seen the carpus of pereopod 4: <5 (T. pacifica)or>6(T. japonica). near 50 m depth in October 1997. Both temperature and ‘‘Juveniles’’ are determined by the number of setae on the inner salinity below 200 m depth were nearly constant at margin of the carpus of pereopod 4 of equivalent instars; T. pacifica 2–4C and 33.5–34.2& throughout the study period. has a small number of setae, while T. japonica has many.

Laboratory rearing experiment Vertical distribution

Themisto japonica specimens used for the laboratory rearing On 1 September 1992, the surface temperature was experiment were those collected occasionally by vertical tows (0– >18C, and a sharp thermocline was located at 30 m 500 m) with a ring net (80 cm diameter; mesh opening: 333 lm), or oblique tows (wire length: 500 m) with a bongo net at E-16 (Fig. 1). depth (Fig. 3, right panel). Water temperatures below T. pacifica were caught in the same manner at stations located east 100 m depth were nearly identical, with a minimum of site H (44–41N; 155E). Live specimens were sorted on board, (1.8C) at 75 m depth. Salinities increased progressively 518

Fig. 2 Temperature (upper panel) and salinity (lower panel) profiles at the sampling station, site H. Sampling dates are indicated by solid triangles on the bottom abscissa

with increasing depth. The low salinities in the top depth), with a prominent peak at 200 m depth in day- 150 m (<33.3&) indicate the occupation of Oyashio time samples. At night, T. japonica were observed in the water (Ohtani 1971). top 200 m, and the bulk of the population was concen- Themisto pacifica occurred throughout a broad trated in the top 30 m. bathymetric range, from the surface to 900 m (Fig. 3, Weighted mean depth (WMD, cf. Frost and Bollens left panel). During the day, they were abundant over 1992) wasP calculatedP for each maturity stage as follows: broad depth strata (20–200 m). At night, the peak of WMD=( nidi)/ ni, where ni is the numerical abun- À3 abundance shifted to 20 m depth. T. japonica also oc- dance (number m ) at depth di. For Themisto pacifica, curred throughout a broad bathymetric layer (30–900 m the WMD of immature specimens (juveniles plus

Fig. 3 Themisto pacifica and T. japonica. Day and night vertical distribution at site H, western North Pacific in September 1992. Temperature and salinity profiles are given to the right 519 immature females and males) was 68 m during the (90.0%) and August 1997 (86.9%). The proportion of daytime and 15 m at night. The day and night WMD immature specimens (males plus females) ranged from values were 151 and 38 m, respectively, for mature fe- 0% (December 1996 and May 1997) to 51.1% (January males and 183 and 49 m, respectively, for mature males. 1998; grand mean: 20.3%), and the proportion of ma- From the calculated WMD, the magnitude of vertical ture specimens (males plus females) ranged from 6.7% migration distance was computed as 53 m for immature (August 1996 and 1997) to 72.7% (May 1997; grand specimens, 113 m for mature females and 134 m for mean: 35.2%). Female to male ratios of T. pacifica mature males. For T. japonica, the WMD of immature ranged from 1:0.2 to 1:1.2 (grand mean 1:0.8) for specimens was 187 m during the daytime and 18 m at immature specimens and from 1:0.2 to 1:2.7 (grand night. The WMD of mature females was 366 m during mean 1:1.2) for mature specimens. In contrast to the daytime and 12 m at night. For mature males, the T. pacifica, seasonal features of T. japonica maturity WMD was 89 m at night. Mature males were not found stage composition were characterized by the occasional in the daytime samples. The vertical migration distance absence of adult specimens (grand mean: 11.1%), espe- between day and night was computed as 175 m for cially adult females. Juvenile T. japonica were observed juveniles and 354 m for mature T. japonica females. throughout most seasons of the year, with peaks in January 1997 (77.8%) and October 1997 (68.1%; grand mean: 29.1%). Immature specimens (males plus females) Seasonal variations in abundance and population comprised 0–71.7% of the total population (grand structure mean: 46.2%). The female to male ratio of T. japonica was from 1:0.1 to 1:2.0 (grand mean; 1:0.66) for imma- Themisto pacifica occurred throughout the year, with a ture specimens and from 1:1 to 1:4.9 for mature speci- prominent numerical peak in August 1997 (875 indi- mens (grand mean; 1:2.96). viduals mÀ2) and moderate peaks in May 1998 The entire BL range was divided into 0.5-mm incre- (515 individuals mÀ2) and July 1997 (343 individuals ments. Seasonal sequences based on relative size (i.e. mÀ2) (Fig. 4). Two marked peaks of numerical abun- BL) compositions of T. pacifica and T. japonica popu- dance of T. japonica were seen in May 1998 (113 indi- lations were analyzed (Fig. 6). For Themisto pacifica, viduals mÀ2) and July 1997 (111 individuals mÀ2), and one or two size modes (i.e. cohorts) prevailed in most moderate peaks were seen from March to April 1997 seasonal samples. While the growth trajectory of each (40–30 individuals mÀ2) and in January 1998 (31 indi- cohort was not necessarily clear, a total of eight cohorts viduals mÀ2). T. japonica did not occur in December were identified over the 2-year survey, including clear 1997 (Fig. 4). Over the entire study period, the mean sequences (numbered as 2 and 1¢) and less clear se- abundance was 145.4 individuals mÀ2 for T. pacifica and quences (1, 3, 4, 2¢,3¢ and 4¢; see Fig. 6). These results 29.2 individuals mÀ2 for T. japonica. In terms of bio- suggest that T. pacifica produce four generations per mass, the contribution of T. pacifica and T. japonica to year. Considering that the minimum mature size of total zooplankton ranged seasonally from 0.005% to T. pacifica is 3.8 mm for males and 3.5 mm for females, 0.68% (grand mean: 0.21%) for the former and from their shortest generation length may be estimated 0% to 0.55% for the latter (0.30%) (Fig. 4). roughly as <2 months. With regard to T. japonica, All maturity stages occurred throughout the study small juveniles <3 mm and adults >10 mm were very period for Themisto pacifica (Fig. 5). Among the stages, rare, and these specimens occurred in limited numbers juveniles comprised a significant proportion of the only in early spring. The most dominant size was 3– population throughout the year (grand mean: 44.5%), 8 mm throughout the study period. However, develop- with peaks in August 1996 (88.9%), December 1996 mental sequences of 3- to 8-mm size-groups to >10 mm

Fig. 4 Themisto pacifica and T. japonica. Seasonal changes in numerical abundance (left abscissa) and the contribution to total zooplankton biomass (right abscissa) 520

Fig. 5 Themisto pacifica (upper panel) and T. japonica (lower panel). Seasonal changes in relative frequencies of maturity stages at site H from July 1996 to July 1998

size-groups were untraceable with the present data. value was substituted into the regression equation of Thus, seasonal population structure (i.e. size) data alone T. pacifica and T. japonica to calculate the intercept (b). are of limited (T. pacifica’s case) or no (T. japonica’s The relationship between b and T (temperature) was best case) use in evaluating the repetition of generations of expressed as b=À0.003T2À0.008T+1.128 (r=0.99, Themisto spp. n=4, P<0.01) for T. pacifica and b= 0.003T2 À0.083T+1.26 (r=0.99, n=4, P<0.01) for T. japonica (Fig. 7B). As a result, IP can be expressed as a function Intermolt periods as estimated from rearing experiments of BL and T as follows: log10IP= 0.056BLÀ0.033T2À0.008T+1.128 for T. pacifica 2 Due to the difficulty of accurately determining BL from and log10IP=0.037BL+0.003T À0.083T+1.26BL for molts, molt uropod length (UL) has commonly been T. japonica. used as a measure of BL for Themisto amphipods (Ikeda 1990). First, the relationship between body length (BL; mm) and uropod length (UL; mm) was established as Growth analysis BL=11.91UL+0.40 (r=0.99, n=27, P<0.01) for T. pacifica and BL=13.53UL+0.84 (r=0.99, n=25, The IP of each Themisto pacifica and T. japonica instar P<0.01) for T. japonica. Using these relationships, molt was calculated by substituting the mean BL data UL was converted to BL, and the intermolt periods (IP; (Table 3) of wild specimens into the IP–BL equation at days) recorded for the specimens reared at 2C, 5C, likely field temperatures (e.g. 2C, 5C, 8C and 12C). 8C, or 12C were plotted against the pre-molt BL for Cumulative IPs were then plotted against the BL of both species (Fig. 7A). No separation of males from each instar to yield each species’ growth pattern females was made. The shortest IP observed for (Fig. 8). T. pacifica was 3 days for a specimen with 1.55 mm pre- Regression analysis revealed that the growth in BL molt BL reared at 12C. The shortest IP for T. japonica (Y; mm) was linear with time (X; days) for Themisto was 6 days for a specimen with 3.0 mm pre-molt BL pacifica, i.e. Y=0.034X+1.32 at 2C, Y=0.039X+1.37 reared at 8C, and for those with 4.3 and 4.8 mm pre- at 5C, Y=0.048X+1.46 at 8C and Y=0.072X+1.75 molt BL reared at 12C. The longest IP recorded was at 12C (all r=0.99, P<0.01). Since juveniles are re- 24 days for a specimen with 6.55 mm pre-molt BL leased from females’ marsupia at instar 3, the estimated reared at 2C for T. pacifica, and 47 days for a specimen time required to complete one life cycle is 32 days with 12.0 mm pre-molt BL reared at 2C for T. japonica. (minimum mature size at 12C) to 224 days (maximum Table 2 summarizes the results of the regression analyses mature female size at 2C) for females and 33 days of log10IP on pre-molt BL for both species. Since the (minimum mature size at 12C) to 142 days (maximum 95% confidence intervals (CI) of the slopes (a) of the mature size at 2C) for males. regression lines overlapped each other for both species, a Preliminary plots of the data indicated that the common a (0.056 for T. pacifica and 0.037 for overall growth pattern of Themisto japonica was non- T. japonica) was calculated. The obtained common a linear, and thereby fitted to von Bertalanffy, Gompertz, 521

Fig. 6 Themisto pacifica (upper panel) and T. japonica (lower panel). Seasonal changes in size (body length; BL) composition at site H, in the western North Pacific. Numbers above the dates of samplings indicate the total number of specimens caught

and logistic growth curves (cf. Kaufman 1981). Adopt- Brood size ing Akaike’s information criterion (AIC; Sakamoto et al. 1986), the logistic curve in the form of BLt=BL¥/ Brood size (BS) ranged from 23 to 64 for Themisto [1+exp(bÀct)] (where BLt is BL at time t days, BL¥ is pacifica samples and from 152 to 601 for T. japonica the hypothetical asymptotic BL, and b and c are con- samples, and increased with increasing female BL for stants) was shown to be superior to the other two curves. both species. The relationship between BS and female Parameters were then estimated as BL¥=16.79 and BL was expressed as BS=14.98BLÀ51.35 (r=0.94, b=2.25 and c=0.013 at 2C, b=2.25 and c=0.019 at n=19, P<0.01) for T. pacifica and BS= 5C, b=2.25 and c=0.026 at 8Candb=2.25 and 52.12BLÀ428.41 (r=0.94, n=11, P<0.01) for c=0.032 at 12C. From these curves, the time to com- T. japonica (Fig. 9). Assuming that hyperiid amphipods plete one life cycle was estimated as 82 days (minimum of the genus Themisto have multiple broodings, each maturity size at 12C) to 358 days (maximum maturity separated by molting (Kane 1963; Sheader 1981), the size at 2C) for females and 66 days (minimum maturity lifetime fecundity of a female T. pacifica having seven size at 12C) to 234 days (maximum maturity size at adult instars and a female T. japonica having five adult 2C) for males. instars was estimated by combining the BS versus BL 522

Fig. 7A, B Themisto pacifica (upper panels) and T. japonica (lower panels). A The relationship between the intermold period (IP) and pre- molt body length (BL) determined at four temperatures. For details of the regression statistics, see Table 2. B The relationship between the intercept (b) and temperature (T; C)

Table 2 Themisto pacifica and T.japonica. Regression statistics Species T (C) Na(95% CI) r BL log10IP b of intermolt period (IP; days) on pre-molt body length T.pacifica 2 19 0.042 (0.030–0.053) 0.88 3.80 1.26 1.10 (BL; mm) at four different 5 16 0.046 (0.036–0.055) 0.94 3.86 1.19 1.01 temperatures (T ). Regression 8 17 0.057 (0.035–0.079) 0.82 3.64 1.06 0.85 model: log10IP=aBL+b. Note 12 13 0.078 (0.048–0.108) 0.86 3.30 0.86 0.57 that the calculation of intercept a=0.056 (b) is based on a common slope T.japonica 2 18 0.043 (0.035–0.051) 0.95 6.34 1.38 1.10 (a=0.056 for T. pacifica, 5 19 0.036 (0.030–0.043) 0.94 6.90 1.20 0.94 a=0.037 for T. japonica) 8 16 0.036 (0.028–0.044) 0.93 8.67 1.08 0.77 (N number of individuals) 12 15 0.033 (0.024–0.042) 0.91 8.45 0.97 0.70 a=0.037 relationship with the BLs of each adult instar (Table 3) coastal waters, where the annual range of surface tem- to be 342 and 1195 eggs, respectively. peratures is 2.5–14C. His results showed that during daylight hours immature and mature specimens of T. pacifica were consistently abundant in a 100–200 m Discussion depth stratum, while juveniles resided largely in the 0–100 m depth stratum. At night, all maturity stages Vertical distribution migrated upward and concentrated within a depth of 0–50 m. While our observations on day/night vertical Diel vertical migration (DVM) behavior, characterized distribution patterns of T. pacifica at site H were limited by ascending at night and descending during the day, to September only, the overall results (Fig. 3) obtained has been well documented for Themisto amphipods (cf. are nearly consistent with the patterns reported by Wing Ikeda et al. 1992). Wing (1976) studied the DVM of (1976). It should be noted that the surface temperature Themisto pacifica throughout the year in Alaskan recorded at site H during the day/night samplings was 523

Table 3 Themisto pacifica and T.japonica. Maturity stages, instar number and body length (BL; mm, means±SD) of T. pacifica and T. japonica collected from site H, western subarctic Pacific

Stage T.pacifica T.japonica

Instar (n) BL (mm) Instar (n) BL (mm)

Juveniles 3 (27) 1.62±0.14 3 (5) 1.59±0.12 4 (104) 1.90±0.16 4 (4) 2.40±0.17 5 (243) 2.39±0.20 5 (4) 2.68±0.16 6 (10) 2.86±0.17 Females Total 6(13) 2.94±0.16 7(15) 3.56±0.12 Immature 7 (37) 3.24±0.15 8 (70) 4.07±0.14 8 (190) 3.87±0.27 9 (73) 4.79±0.19 9 (122) 4.67±0.35 10 (112) 5.59±0.23 11 (92) 6.40±0.27 12 (50) 7.19±0.18 13 (33) 8.12±0.36 14 (13) 9.17±0.22 Mature 8 (47) 4.06±0.37 13 (3) 10.07±0.57 9 (86) 4.68±0.39 14 (3) 11.37±0.25 10 (152) 5.55±0.38 15 (5) 12.50±0.62 11 (125) 6.47±0.51 16 (2) 14.70±0.28 12 (118) 7.34±0.53 17 (6) 15.22±0.71 13 (27) 7.92±0.73 14 (2) 9.03±0.18 Males Total 5 (2) 2.65±0.01 7 (9) 3.55±0.23 Immature 6 (4) 2.98±0.10 8 (22) 3.86±0.28 7 (42) 3.33±0.29 9 (47) 4.68±0.39 Fig. 8 Themisto pacifica and T. japonica. Growth trajectories at 8 (109) 3.88±0.26 10 (46) 5.50±0.31 four temperatures estimated by combining laboratory-obtained 9 (73) 4.72±0.38 11 (5) 6.19±0.55 data on intermolt period (IP) (Fig. 7) with field data on mean body 12 (2) 7.60±0.85 length (BL) (Table 3) Mature 8 (21) 4.10±0.22 12 (10) 7.87±0.40 9 (99) 4.57±0.36 13 (36) 8.98±0.36 10 (259) 5.57±0.44 14 (29) 10.13±0.36 studies. Additionally, the high surface temperature 11 (162) 6.21±0.39 15 (4) 11.25±0.13 (18C) did not hamper the nighttime ascent to the sur- face layer of T. japonica at site H. The calculation of WMDs revealed that, while both 18C, which is much higher than the annual maximum Themisto pacifica and T. japonica reach the surface layer (14C) at Wing’s study site. Despite this warmer surface at night, the daytime distribution depth and the mag- temperature at site H, our results show that all maturity nitude of vertical migration distances of the former are stages of T. pacifica reached the surface layer at night. much less than those of the latter. These between-species Semenova (1974) and Ikeda et al. (1992) noted the differences may be explained primarily by the greater DVM behavior of Themisto japonica in the northwestern swimming abilities of T. japonica (observed during the and southern (Toyama Bay) Japan Sea, respectively. laboratory rearing experiments of this study), which are Semenova’s observations were made in July (estimated associated with its greater body size (cf. Table 3). surface temperature: 13C); immature and mature males and females were found at depths of 400–500 m during the daytime and migrated up to depths of 0–100 m at Life cycle night. Small juveniles (<5 mm) were distributed in the top 100 m and did not exhibit DVM. The investigations Despite the wide geographical distribution of Themisto by Ikeda et al. (1992) in Toyama Bay covered all seasons pacifica across the western to eastern subarctic Pacific of the year, yielding the same results as those reported (Bowman 1960), presently available information about by Semenova (1974), except for seasons when the surface T. pacifica’s life cycle is limited to Wing’s (1976) study of temperature rose beyond the limit of physiological tol- the waters of southeastern Alaska (eastern subarctic erance of T. japonica. For example, the upward migra- Pacific). Analyzing the population structure of T. paci- tion of juveniles and adults at night was hampered by fica throughout the year, Wing (1976) found reproduc- the 20C isotherm at 200 m depth in September, when tion throughout the year and an annual cycle starting in the surface temperature rose as high as 28C (Ikeda et al. May, with a first major brood release of juveniles, fol- 1992). As compared with these day/night vertical dis- lowed by successive but overlapping broods (maturing in tribution patterns of T. japonica reported in the Japan 6–8 weeks from summer to autumn). In winter, growth Sea, the pattern seen for the site H population in Sep- and maturation of successive broods decreased, and tember does not differ appreciably from these previous generation time appeared to be lengthened to 524

Fig. 9 Themisto pacifica and T. japonica. Relationship between brood size (BS) and body length (BL; mm) of gravid females

8–12 weeks. Given these results, Wing (1976) suggested peripheral region of the major T. pacifica habitat (cf. that T. pacifica can produce four or five generations per Bowman 1960) and that T. pacifica are not repeating year. normal life cycles at site H. Nevertheless, growth curves The annual range of surface temperatures in the established for T. japonica, based on laboratory-derived waters of southeastern Alaska is 2.5–14C (cf. Wing IP data in the present study, predict that the minimum 1976), which is narrower than the temperature range time required to reach maturity is 2–2.5 months at 12C (0.2–16C, cf. Fig. 2) at site H. Despite this difference in and that the maximum time to complete a life span is thermal regimes, the life-cycle patterns of Themisto 8.5–12 months at 2C (Table 4). pacifica at site H, evaluated from seasonal sequences of abundance and population structures, agree well with those of Wing (1976), in terms of major reproductive Reproduction seasons (summer) and the number of generations per year (four generations per year). These results suggest The brood sizes of many pelagic crustaceans are known that the positive effect of higher temperature (16C) and to be proportional to female size (Mauchline 1988). The the negative effect of lower temperature (0.2C) on the relationship between brood size and female size in the repetition of generations of T. pacifica at site H cancel genus Themisto has been examined for T. compressa each other out. (formerly T. gaudichaudii) in the North Sea (Sheader Information about Themisto japonica’s life cycle is 1977), T. japonica in the Japan Sea (Ikeda 1991) and currently available for the population in Toyama Bay T. libellula in Arctic waters (Percy 1993). The maximum in the southern Japan Sea (Ikeda et al. 1992). In brood size recorded for T. pacifica (64 eggs) in the Toyama Bay, all the developmental stages of present study is the least among all the Themisto am- T. japonica occur throughout the year. Thus, repro- phipods ever studied (200 eggs for T. compressa, duction continues year-round. Nevertheless, juveniles 525 eggs for T. japonica and 550 eggs for T. libellula). form a marked abundance peak in mid-summer, sug- From the brood size/female size relationship mentioned gesting reproduction is most prevalent in this season. above, the smallest brood size of T. pacifica may be due, Because of the complex size-frequency dataset, field in part, to the smaller maturity size of females (3.5– data alone cannot provide a straightforward identifi- 9.3 mm BL). The brood size (maximum: 601 eggs) of cation of cohorts nor a tracing of sequential growth. T. japonica at site H in this study was greater than that Ikeda et al. (1992), combining growth models of T. japonica derived from laboratory rearing experiments Table 4 Themisto pacifica and T.japonica. Estimated development (Ikeda 1990), determined that T. japonica can complete times to complete one life cycle at four different temperatures. The three generations per year in Toyama Bay. calculation is based on minimum and maximum sizes of both sexes The present results for life-cycle features of Themisto (Table 3) japonica at site H differ from those in Toyama Bay in Temperature (C) Development time (days) several respects. First, the annual maximum abundance was seen not in mid-summer but in early summer. T.pacifica T.japonica Second, T. japonica was much less abundant at site H Female Male Female Male (annual mean: 29.2 individuals mÀ2, as compared with 622 individuals mÀ2 in Toyama Bay; cf. Ikeda et al. 2 80–224 81–142 201–358 168–234 1992). Third, adult females occurred only in the spring 5 68–195 70–123 137–233 110–153 (Fig. 5), when the surface water temperature was <3C 8 55–159 56–100 101–172 81–113 12 32–101 33–62 82–139 66–91 (Fig. 2). All these results may imply that site H lies in a 525

(525 eggs) of the Japan Sea population (Ikeda 1991). For a coexistence mechanism for T. abyssorum and The diameter of eggs of T. pacifica (0.35 mm) was T. libellula in Arctic waters, Auel et al. (2002) demon- identical to that of T. japonica (0.35 mm), but much less strated that the former preys largely on Calanus than that of T. compressa (0.51 mm) and of T. libellula copepodites and the latter on ice-algae. Sheader and (0.54 mm). Batten (1995) noted that, while P. johnsoni and P. evansi The reproduction pattern of epipelagic crustaceans is have similar vertical migration patterns, as well as sim- characterized by larger brood sizes and higher lifetime ilar timing and sequence of reproductive events, possible fecundities as compared with their meso- and bathype- differences might exist in gelatinous zooplankters as prey lagic counterparts (Mauchline 1991). According to or as hosts in their juvenile stages. Species-specific rela- Mauchline (1991), the reduced fecundity of deeper living tionships of hyperiids with gelatinous zooplankters have species may reflect the exponential decrease in predatory been described by Madin and Harbison (1977), Harbi- pressure that occurs with increasing depth in the ocean. son et al. (1977) and Laval (1980). In recent studies, the The smallest brood size of T. pacifica living in the epi- lipid biomaker approach (including fatty acid and sterol pelagic zone at site H apparently violates this general- composition) has been used successfully to identify tro- ization. The lifetime fecundity of T. pacifica (342 eggs) is phic conditions of these animals (Phleger et al. 2000; less than that of T. japonica (1195 eggs). However, the Nelson et al. 2000, 2001). shorter life span (32 days at 12C, cf. Table 4) of T. pacifica could counteract the effect of their small Acknowledgements We are grateful to the captains, crews, and brood size. Compared with T. pacifica, T. japonica has a scientists aboard the F.R.V. ‘‘Hokkou Maru,’’ ‘‘Tankai Maru,’’ ‘‘Hokushin Maru’’ and ‘‘Oshoro Maru’’ for their help in field larger brood size and greater lifetime fecundity, but also sampling. Part of this study was supported by the Japan Society for a longer life span (82 days at 12C, cf. Table 4). the Promotion of Science and the ‘‘VEN-FISH’’ project of the Japanese Fishery Agency.

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