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Copepod community succession during warm season in Lagoon Notoro-ko, northeastern Hokkaido, Japan
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ScienceDirect Polar Science 9 (2015) 249e257 http://ees.elsevier.com/polar/
Copepod community succession during warm season in Lagoon Notoro-ko, northeastern Hokkaido, Japan Yoshizumi Nakagawa a,b,*, Hideaki Ichikawa a, Mitsuaki Kitamura b, Yasuto Nishino a, Akira Taniguchi c b
a Faculty of Bioindustry, Tokyo University of Agriculture, 196 Yasaka, Abashiri, Hokkaido 099-2493, Japan Graduate School of Bioindustry, Tokyo University of Agriculture, 196 Yasaka, Abashiri, Hokkaido 099-2493, Japan c Sanyo Techno-Marine, Inc., 1-3-17 Nihombashi-Horidomecho, Chuoh-City, Tokyo 103-0012, Japan
Received 22 October 2014; revised 5 January 2015; accepted 16 February 2015 Available online 24 February 2015
Abstract Lagoon Notoro-ko, located on the northeastern coast of Hokkaido, Japan, and connected to the Okhotsk Sea by a humanmade channel, is strongly influenced by local hydrography, as water masses in the lagoon are seasonally influenced by the Soya Warm Current and the East Sakhalin Current. We here report on the succession of copepod communities during the warm season in relation to water mass exchange. Copepods were categorized into four seasonal communities (spring/early-summer, mid-summer, late-summer/fall, and early-winter) via a cluster analysis based on BrayeCurtis similarities. Spring/earlysummer and early-winter communities were characterized by the temperateeboreal calanoid Pseudocalanus newmani, comprising 34.9%e77.6% of the total abundance of copepods during times of low temperature/salinity, as influenced by the prevailing East Sakhalin Current. Late-summer/fall communities were characterized by the neritic warm-water calanoid Paracalanus parvus s.l., comprising 63.9%e96.3% of the total abundance, as influenced by the Soya Warm Current. Midsummer communities comprised approximately equal abundances of P. parvus, Eurytemora herdmani, Scolecithricella minor, and Centropages abdominalis (12.8%e28.2%); this community is transitional between those of the spring/earlysummer and late-summer/fall. Copepod community succession in Lagoon Notoro-ko can be largely explained by seasonal changes in water masses. © 2015 Elsevier B.V. and NIPR. All rights reserved.
Keywords: Lagoon Notoro-ko; Okhotsk Sea; Copepod community; Paracalanus parvus; Pseudocalanus newmani
1. Introduction
* Corresponding author. Faculty of Bioindustry, Tokyo University of Agriculture, 196 Yasaka, Abashiri, Hokkaido 099-2493, Japan. Tel.: þ81 152 48 3917; fax: þ81 152 48 3916. E-mail address: [email protected] (Y. Nakagawa). http://dx.doi.org/10.1016/j.polar.2015.02.001 1873-9652/© 2015 Elsevier B.V. and NIPR. All rights reserved.
Lagoon Notoro-ko (with a circumference of 35 km, a surface area of 58.4 km2, and a water volume of 0.5 km3) is located on the northeast coast of Hokkaido, Japan, and is connected to the southern Okhotsk Sea by a small human-made channel 324 m wide and 13 m deep (We unify the place name as “Lagoon Notoro-ko”
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afterwards). Along the northeast coast of Hokkaido, the Soya Warm Current, originating from the Tsushima Warm Current in the Sea of Japan, flows southward from the Soya Straits during the warm months (Aota, 1979). The Tsushima Current is a branch of the subtropical Kuroshio Current, and therefore in the Okhotsk Sea the Soya Current is characterized by high temperatures (7 Ce20 C) and salinities (33.6 psu) (Takizawa, 1982). In winter, the typical boreal East Sakhalin Current, with low temperatures (<7 C) and low salinities (<32.0 psu) (Takizawa, 1982), flows down southward from the northwestern Okhotsk Sea along the east coast of Sakhalin Island and occupies the entire coastal area off northeast Hokkaido (Aota, 1979). Consequently, water masses in Lagoon Notoro-ko change seasonally between warm subtropical water and cold boreal water (Asami et al., 1995; Imada et al., 1995; Kurata and Nishihama, 1987; Nishino et al., 2014). This paper focuses on the succession of the major copepod species in the copepod communities in the lagoon during the course of this water exchange. A number of previous studies have examined the copepod communities in Lagoon Notoro-ko (e.g., Kanno and Fukuda, 1993; Kitamura et al., 2014). Kitamura et al. (2014) reported that while cold-water species dominate in winter, numerous eurythermic species are alternately present in fluctuating numbers during the warm months (spring to fall). These fluctuations indicate that the properties of the water masses in the lagoon vary even during the warm months, probably on account of frequent inflow, outflow, and mixing of coastal waters of different origins. Thus, an understanding of copepod community dynamics depends on knowledge of species-level relationships and responses to hydrographic conditions. This study presents data on temporal changes in species abundances in the copepod communities of Lagoon Notoro-ko in relation to the hydrographic conditions during the warm season. 2. Materials and methods
Observations were conducted at a sampling site at the deepest part (21 m water depth) of Lagoon Notoroko (44 30 2.100 N, 144 90 38.800 E), once or twice a month during the warm months, from 14 April to 21 December 2011 (Fig. 1). Vertical profiles of temperature and salinity were recorded using a compact Conductivity-Temperature-Depth profiler (Model ASTD103; JFE Advantech, Japan). Water samples for determinations of chlorophyll a (Chl-a) were collected using a Van Dorn water sampler at five depths (0, 5, 10,
15, and 18 m). A 500-mL aliquot was filtered through a glass-fiber filter (Whatman), and plant pigments on the filter were extracted in 7 mL N,N-dimethylformamide. Concentrations of Chl-a were determined following Welschmeyer (1994) using a fluorometer (10-AU; Turner Designs). Zooplankton, collected by vertical haul from a depth of 15 m to the surface using a 45-cm diameter 335-mm mesh NORPAC net, were preserved in 5% (v/ v) buffered seawater formalin. The amount of water filtered by the net was estimated by assuming a filtering efficiency of 100%. All copepods, including copepodids and adults, were sorted under a dissecting microscope from 1/4 to 1/32 aliquots, and then classified to species level according to Ohtsuka and Ueda (1997); numbers of individuals were counted. However, as early copepodid stages could not be accurately identified to the species level, they were classified into generic groups. Lesser species, which did not exceed 10% of the total abundance in any sample, were categorized as “other copepods”. Similarities between samples were determined by a BrayeCurtis similarity analysis using the software package Plymouth Routines in Multivariate Ecological Research (PRIMER) v6 (Clarke, 1993; Clarke and Warwick, 2001). 3. Results 3.1. Hydrographic structures Seasonal changes in the vertical profiles of water temperature are apparent in Fig. 2. The temperature was <6 C in April and increased to a seasonal maximum of 21.5 C at the surface and 18.2 C just above the bottom in early September. A thermocline started to form in April, developed further until August, and then rapidly disappeared by the end of September. The temperature decreased thereafter to <3 C at the end of the survey period in December. Changes in salinity generally followed those of temperature (Fig. 3). In April, lower-salinity waters of <32 psu formed a 5-m layer on top of more saline water of >32.2 psu. During May and June, the lowsalinity water disappeared, and saline water of >32.2 psu formed the entire water column. From the end of June, more saline water of >33.0 psu intruded beneath the >32.2 psu water, resulting in vertical stratification. This stratification broke down in late September and a vertically uniform salinity was maintained until the end of the survey period. It should be noted, however, that the salinity gradually decreased to <32 psu during this period after late September.
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Fig. 1. Location of the sampling station (St. A) in Lagoon Notoro-ko, eastern Hokkaido, Japan, facing the Okhotsk Sea.
3.2. Chl-a concentrations Fig. 4 shows seasonal changes in Chl-a concentrations. The highest Chl-a level of >6 mg L1 was recorded near the lagoon bottom in April. While nearbottom values were uniformly high throughout the survey period, the subsurface maximum layer formed during July to September. Levels of Chl-a stabilized at ~3 mg L1 throughout the water column in October and November. The occurrence of low Chl-a levels in
subsurface layers in December is noteworthy; however, it should be noted that the seasonal minimum value of <2 mg L1 was recorded in June. 3.3. Seasonal changes in abundance and composition of the copepod community Copepods identified in the present study include 21 species in 15 genera belonging to 14 families in 3 orders (Table 1). The total abundance was
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Fig. 2. Relationship between temperature ( C) and depth during the warm months in Lagoon Notoro-ko in 2011.
1118e1120 ind. m3 in April, with levels increasing in May and exhibiting a sudden peak of 8602 ind. m3 on 30 May, followed by a rapid decrease to 483e496 ind. m3 in June and July (Fig. 5). After July, levels of abundance were relatively constant, with a small peak on 9 September (1385 ind. m3) and a minimum on 13 October (280 ind. m3). Numbers increased again to a winter peak of 801e902 ind. m3 in December (Fig. 5). Among the different copepod species, Pseudocalanus newmani was most abundant during the period from April to July (699e5273 ind. m3) (Fig. 5), comprising 60.6%e77.6% of total copepod abundance (Fig. 6). The peak abundance (5273 ind. me3) was recorded on 30 May and the second highest peak (1321 ind. m3) on 14 July (Fig. 5). The abundance of P. newmani was under the detection limit (13 ind. m3) during AugusteNovember, but then increased to 229e762 ind. m3 after 25 November and until 13 December. The levels of the dominant P. newmani during this period (84.5%) were higher than during other months (Fig. 6). The second most abundant copepod species, Acartia longiremis, also exhibited its highest abundance levels during AprileJuly (51e1906 ind. m3; 6.0%e22.2% of the total abundance) (Fig. 6). During AugusteDecember, its abundance was always below the detection limit (Fig. 5).
Fig. 4. Relationship between total chlorophyll a concentration (mg L1) and depth during the warm months in Lagoon Notoro-ko in 2011.
Eurytemora herdomani, although less abundant, was also common before September, having the highest levels on 30 May (407 ind. m3) and second highest on 19 August (Fig. 5), representing 25.6% of the total copepod abundance (Fig. 6). E. herdomani was also present in November and December, although in small numbers (13 ind. m3, respectively) (Fig. 5). Tortanus derjugini was present during the early half of the investigation period (April to August) and showed a seasonal peak of 191 ind. m3 on 28 July (Fig. 5), comprising 23.8% of the copepod population at that time (Fig. 6). Recorded occurrences of Centropages abdominalis and Scolecithricella minor were limited to August and September; C. abdominalis was present in two samples, on 19 August (with an abundance of 64 ind. m3 and dominance of 12.8%) and on 9 September (Figs. 5 and 6), while S. minor occurred only in August (with an abundance of ~76 ind. m3 and dominance of ~15.4%) (Figs. 5 and 6). Paracalanus parvus s.l. (hereafter P. parvus) was common throughout the investigation period, except for April and the 13 December sample (25e1334 ind. m3) (Fig. 5). The highest abundances of P. parvus, recorded on 9 September and 13 October (Fig. 5), represented 96.3% and 86.4% of the total copepod numbers, respectively (Fig. 6). Acartia hudsonica was first observed in June, and its abundance increased until winter, with peaks of 241 ind. m3 on 25 November and 21 December (Fig. 5); on 25 November, the dominance of A. hudsonica reached a peak of 38.0% of the total abundance (Fig. 6). 3.4. Similarities within the copepod communities
Fig. 3. Relationship between salinity (psu) and depth during the warm months in Lagoon Notoro-ko in 2011.
Cluster analyses of the copepod communities in Lagoon Notoro-ko were performed on the basis of
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Table 1 Copepod species identified in Lagoon Notoro-ko during warm season. Order
Family
Species
Apr
Mar Jun
14 29 30 Calanoida
Acartiidae
Acartia hudsonica Acartia longiremis Acartia omorii Acartia spp. Calanidae Calanus gracilis Calanus pacificus Neocalanus plumchrus Centropagidae Centropages abdominalis Clausocalanidae Clausocalanus pergens Eucalanidae Eucalanus bungi Metridiidae Metridia pacifica Paracalanidae Palacalanus parvus Pseudocalanidae Pseudocalanus minutus Pseudocalanus newmani Pseudocalanus spp. Pseudodiaptomidae Pseudodiatomus marinus Scolecitrichidae Scotecithricella minor Temoridae Eyurytemora affinis Eurytemora herdmani Eurytemora spp. Tortanidae Tortanus derjugini Tortanus discaudatus Tortanus spp. Cyclopoida Oithonidae Oithona atlantica Oithona similis Oithona spp. Harpacticodia Ectinosomatidae Microsetella sp. 1 Unidentified
þ þ þ
Jul
16 29 14
þ þþ þþþ þþ þþ þþ þ þ þ þ þ þ þ þ þ þ
þ þ þ þ þþ þ þ þþ þþ þþ þþþ þ þ þ þ þþ þ þ þ þ þ
þþ þþ þ þ þ þ
Aug
Sep
28 19 29 9 þ þ
þ
þ
þ
þ
þ
þ
þ þ
þ
Oct
Nov
Dec
30 13 25 11 25 13 21 þ þ þ þ
þ þ
þþ þþ þ
þþ
þ
þ
þ
þ þþ þþ þþ þ þþ þþ þþþ þþ þþ þþ þþ þþ þ þ þ þ þ þþ þþ þþþ þþ þ þ þþ þþ þþ
þ þ þ
þ
þ
þ þ
þ
þ þ
þ þ
þþ þ
þ þ
þ þ
þ þ
þ þ
þ þ
þ
þ
þþ
þ þ þ
þ þ
þ
þ
þ þ
þ
þ
þ: <100 ind. m3. þþ: <1000 ind. m3. þþþ: 0.1000 ind. m3.
BrayeCurtis similarities, which were calculated from data on the abundance and dominance values of copepod populations on each sampling date. Accordingly, three groups (A, B, and C) were recognized at a 39% similarity level, and two subgroups of Group B (B1 and B2) were identified at a 46% similarity level (Fig. 7). By referencing their seasonal patterns (Figs. 5 and 6), Group A was identified as a spring/early-summer group (14 Aprile14 July), Subgroup B1 as a midsummer group (19 August), Subgroup B2 as a latesummer/fall group (29 Auguste11 November), and Group C as an early-winter group (25 Novembere21 December) (Fig. 7). 4. Discussion In the present study, Groups A, B1, B2, and C, which were clearly defined by a cluster analysis based on BrayeCurtis similarities (Fig. 7), were recognized
as four seasonal communities present during the warm months in Lagoon Notoro-ko, i.e., in spring/earlysummer, mid-summer, late-summer/fall, and earlywinter. P. newmani was the predominant species in the spring/early-summer and early-winter communities, comprising 34.9%e77.6% of the total abundance (Fig. 6). P. newmani has been reported as a temperateeboreal species, distributed in coastal waters of Asia and North America (Frost, 1989). In eastern Asia, it is found in the northern Sea of Japan, in areas such as Toyama Bay (Yamaguchi et al., 1998), Ishikari Bay (Arima et al., 2014), the southwestern waters of Hokkaido (Yamaguchi and Shiga, 1997), and in the coastal waters off northeast Hokkaido (Asami et al., 2010). In the present study, P. newmani was especially abundant on 30 May, but numbers decreased sharply in June (Fig. 5). During this period, Chl-a concentrations below 10 m also decreased sharply, from >5 mg L1 in May to
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Fig. 5. Seasonal changes in abundance (ind. m3) of total and dominant species in the copepod communities during warm months in Lagoon Notoro-ko in 2011. Species accounting for 10% or more of the total abundance in any sample are considered “dominant”; otherwise the species are amalgamated as “other copepods”.
<2 mg L1 in June (Fig. 4). Because growth of P. newmani is reportedly limited under conditions of scarce food supply (McLaren et al., 1989; Yamaguchi and Shiga, 1997), levels of Chl-a in June (<2 mg L1) may not have been sufficient to support the large population size of this species. The decrease in Chl-a levels in June is observed regularly each year in Lagoon Notoro-ko (Nishino et al., 2014), and is attributed to active feeding of larvae of the Japanese scallop Patinopecten yessoensis, which is the most important commercially farmed species in the lagoon (Nishihama, 1994).
While Chl-a levels had rebounded quickly by July, the P. newmani population continued to decrease, probably owing to its preference for cold-water habitats (loc. cit.), and the population finally disappeared by 19 August (Fig. 5). Around Hokkaido, the upper temperature limit for P. newmani has been reported to be 15 C (Arima et al., 2014; Yamaguchi and Shiga, 1997; Yamaguchi et al., 1998); temperatures in Lagoon Notoro-ko had increased to over 15 C by 19 August (Fig. 2). This increase in temperature was largely a result of the intrusion of the Soya Warm Current into the lagoon, combined with seasonal
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Fig. 6. Seasonal succession in the dominance (%) of dominant copepods during the warm months in Lagoon Notoro-ko in 2011.
warming of lagoon waters (Aota, 1979). P. newmani was observed again in October, when temperatures had dropped to below 15 C, and its numbers continued to increase towards winter (Table 1; Fig. 5). This drop in temperature during October was caused by inflow of the East Sakhalin Current into the lagoon, which it occupies for the entire season of ice coverage until the following April (Nishino et al., 2014). The intrusion of the East Sakhalin Current is accompanied by low temperatures and salinities in the lagoon during November and December (Figs. 2 and 3) (Takizawa,
1982). The data suggest that P. newmani is introduced into the lagoon by the inflow of the East Sakhalin Current in early winter, and that it survives the winter under sea ice in the lagoon, before disappearing from the lagoon when the Soya Warm Current enters the lagoon in summer. During summer and fall, the lagoon is occupied by a late-summer/fall community dominated largely by P. parvus (Figs. 6 and 7). P. parvus is known as one of most widely distributed species in neritic waters in temperate and boreal seas (Brodskii, 1950; Mackas and
Fig. 7. Dendrogram of seasonal groups of copepods during the warm months in Lagoon Notoro-ko in 2011, classified via BrayeCurtis similarities: (A) spring/early-summer group; (B1) mid-summer group; (B2) late-summer/fall group; (C) early-winter group (before sea-ice formation).
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Tsuda, 1999; Vervoort, 1963). In the present study, P. parvus was found in samples from 30 May to 13 December, attaining its highest abundance of 1334 ind. L1 on 9 September (Fig. 5). Several surveys have reported that P. parvus is abundant in summer and fall in the coastal waters around northern Japan. Anraku (1954) reported that in waters near the present survey site, P. parvus is most abundant in August, under the influence of the Soya Warm Current. Hattori and Tsumura (1990) reported that in waters off northwestern Hokkaido, P. parvus is dominant from summer to late fall, when temperatures and salinities are elevated under the influence of the Tsushima Warm Current. Arima et al. (2014) conducted sampling in Ishikari Bay off western Hokkaido and recorded that P. parvus is abundant in JulyeSeptember, under the influence of the Tsushima Warm Current, but is absent in spring (April and May), when temperatures and salinities are low. In the present study, temperatures and salinities during the late summer to fall, when P. parvus was abundant, were as high as 11 Ce21 C and 33.0e33.3 psu, respectively (Figs. 2 and 3), indicating the influence of the Soya Warm Current. With reference to the mid-summer community, no single species displayed a dominance of >50%, with the abundances of P. parvus, Eurytemora herdmani, S. minor, and C. abdominalis being approximately equal, at 12.8%e28.2% of the total abundance (Fig. 6). Among these species, S. minor and C. abdominalis are commonly reported as cold water species (S. minor: Minoda, 1971; Mori, 1964; Morioka, 1976; Vervoort, 1965; Yamaguchi et al., 1999; C. abdominalis: Brodskii, 1950 as Centropages mcmurrichi; Hirakawa, 1986; Kas'yan, 2004; Liang et al., 1994, 1996; Mori, 1964). Our data and the data from these reports indicate that both species flourish in cold water and attain their maximum abundances at 15 C-18 C; neither species thrives in water warmer than 20 C. In this study, S. minor and C. abdominalis were found in August and September, when surface temperatures were higher than 20 C (Fig. 2). However, cold underlying water was present during this period, which had probably intruded from the outer lagoon, where temperatures were lower than 15 C and salinities were ~33.0 psu (Figs. 2 and 3). These two species likely survived the summer months in Lagoon Notoroko in the underlying water layer, and then re-populated lagoon waters during the transitional season between the dominance of the spring/early-summer community (dominantly P. newmani) and the early-winter community (dominantly P. parvus). Several studies have reported a similar increase in the abundance of another
cold-water brackish copepod E. herdmani (Brodskii, 1950; Heron, 1964; Mori, 1964); the data show a decrease from a peak in spring and into July during a time of increasing temperatures, and a temporary increase in abundances in August (Fig. 5). These observations indicate that niches occupied by dominant spring species become available in summer, until winter species become dominant. During this period, Chl-a concentrations are more or less constant throughout the water column; thus, food conditions for copepod populations remain suitable throughout the water column during this time. These varying temperature conditions may provide species with a variety of alternate niches. The present study showed that the copepod species succession in Lagoon Notoro-ko is basically controlled by variations in the conditions of water masses, which intrude from the outer lagoon. This is possibly the case in other areas of the southern Okhotsk Sea, which is the southern limit of seasonal sea-ice coverage in the Northern Hemisphere, and where seasonal fluctuations in the thermal regime are extremely large. Continuous monitoring of copepod communities, which are sensitive to changes in thermal conditions, is of critical importance under conditions of global warming. Acknowledgments We gratefully acknowledge the assistance of Kohichi Nishio, Tokyo University of Agriculture, and Toshifumi Kawajiri, West Abashiri Fishery Corporation, with field observations and samplings. References Anraku, M., 1954. Distribution of plankton copepods off Kitami, Hokkaido, in Okhotsk Sea in summer, 1949 and 1950. Bull. Fac. Fish. Hokkaido Univ. 4, 249e255. Aota, M., 1979. Variability of hydrography in coastal area along Hokkaido, the Sea of Okhotsk. Note Coast. Oceanogr. Study 17, 1e11 (In Japanese). Arima, D., Yamaguchi, A., Abe, Y., Matsuno, K., Saito, R., Asami, H., Shimada, H., Imai, I., 2014. Seasonal changes in body size and oil sac volume of three planktonic copepods, Paracalanus parvus (Claus, 1863), Pseudocalanus newmani Frost, 1989 and Oithona similis Claus, 1866, in a temperature embayment: what controls their seasonality? Crustaceana 87, 364e375. Asami, H., Imada, K., Yasutomi, R., Izawa, T., 1995. Seasonal cycles of phytoplankton and nutrients in Lake Notoro, Eastern Hokkaido. Jpn. Sci. Rep. Hokkaido Fish Hat. 49, 17e23 (in Japanese with English abstract). Asami, H., Shimada, H., Sawada, M., Miyakoshi, Y., Ando, D., Fujiwara, M., Nagata, M., 2010. Spatial and seasonal distributions of copepods from spring to summer in the Okhotsk Sea off eastern Hokkaido, Japan. PICES Sci. Rep. 36, 233e239.
Y. Nakagawa et al. / Polar Science 9 (2015) 249e257 Brodskii, K.A., 1950. Veslonogie rachki Calanoida Dal'nevostochnykh morei SSSR i Polyarnogo basseina. Akademia Nauk SSSR, Moscow/Leningrad (In Russian; English translation by Israel Program Sci. Transl., Jerusalem, 1967, under the title: Copepoda, Calanoida of the Far Eastern Seas of the USSR and the Polar Basin). Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18, 117e143. Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, second ed. PRIMER-E, Plymouth. Frost, B.W., 1989. A taxonomy of the marine calanoid copepod genus Pseudocalanus. Can. J. Zool. 67, 525e551. Hattori, H., Tsumura, K., 1990. Seasonal change in zooplankton distribution off Haboro, Japan Sea. Proc. Hokkaido Tokai Univ. Sci. Eng. 18, 115e128 (In Japanese with English abstract). Heron, G.A., 1964. Seven species of Eurytemora (Copepoda) from northwestern North America. Crustaceana 7, 199e211. Hirakawa, K., 1986. A new record of the planktonic copepod Centropages abdominalis (Copepoda, Calanoida) from Patagonian waters, southern Chile. Crustaceana 51, 296e299. Imada, K., Sakazaki, S., Kawajiri, T., Kobayashi, K., 1995. Lake basin and saline environments profiles of four brackish lakes in Abashiri, Northern Hokkaido. Sci. Rep. Hokkaido Fish Hat. 49, 17e23 (in Japanese with English abstract). Kanno, Y., Fukuda, K., 1993. Monthly occurrence of planktonic organisms and the feeding habits of inherent herring in Notoro Lake, Hokkaido. Bull. Fac. Fish. Hokkaido Univ. 44, 158e170 (in Japanese with English abstract). Kas'yan, V.V., 2004. Distribution and seasonal dynamics of the abundance of Centropages abdominalis Sato and C. tenuiremis Thompson et Scott (Copepoda) in Amursky Bay, Sea of Japan. Russ. J. Mar. Biol. 30, 87e95. Kitamura, M., Nakagawa, Y., Nishino, Y., Taniguchi, A., 2014. Effect of water mass replacement on seasonal variations in the copepod community in Lagoon Notoro-ko, Hokkaido, Japan. Eco-Engineering 26, 89e94 (in Japanese with English abstract). Kurata, N., Nishihama, Y., 1987. Seasonal change of the hydrographic condition in Lake Notoro, Hokkaido. Sci. Rep. Hokkaido Fish Res. Inst. 29, 17e24 (in Japanese with English abstract). Liang, D., Uye, S., Onbe, T., 1994. Production and loss of eggs in the calanoid copepod Centropages abdominalis Sato in Fukuyama Harbor, the Inland Sea of Japan. Bull. Plank. Soc. Jpn. 41, 131e142. Liang, D., Uye, S., Onbe, T., 1996. Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. I. Centropages abdominalis. Mar. Biol. 124, 527e536.
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Mackas, D.L., Tsuda, A., 1999. Mesozooplankton in the eastern and western subarctic Pacific: community structure, seasonal life histories, and interannual variability. Prog. Oceanogr. 43, 335e363. McLaren, I.A., Laberge, E., Corkett, C.J., Sevigny, J.M., 1989. Life cycles of four species of Pseudocalanus in Nova Scotia. Can. J. Zool. 67, 552e558. Minoda, T., 1971. Pelagic copepod in the Bering Sea and the northwestern North Pacific with special reference to their vertical distribution. Mem. Fac. Fish. Hokkaido Univ. 18, 1e74. Mori, T., 1964. The Pelagic Copepoda from the Neighbouring Waters of Japan. Soyo, Tokyo. Morioka, Y., 1976. Vertical invasion of boreal calanoid copepods into the shallow warm stratum. Bull. Jpn. Sea Reg. Fish. Res. Lab. 27, 91e101. Nishihama, Y., 1994. Fishery of the Japanese Scallop in Okhotsk Sea. Hokkaido University Press, Sapporo (in Japanese). Nishino, Y., Satoh, T., Taniguchi, A., 2014. Water condition in Lagoon Notoro-ko in the Eastern Hokkaido: seasonal changes of temperature, salinity, dissolved oxygen and nutrients. Eco-Engineering 26, 3e9 (in Japanese with English abstract). Ohtsuka, S., Ueda, H., 1997. Subclass Copepoda. In: Chimura, M., Murano, M. (Eds.), An Illustrated Guide to Marine Plankton in Japan. Tokai University Press, Tokyo, pp. 649e1004 (in Japanese). Takizawa, T., 1982. Characteristics of the soya warm current in the Okhotsk Sea. J. Oceanogr. Soc. Jpn. 38, 281e292. Vervoort, W., 1963. Pelagic Copepoda. Part I. Copepoda Calanoida of the families Calanidae up to and including Euchaetidae. Atlantide Rep. 7, 77e194. Vervoort, W., 1965. Pelagic Copepoda. Part II. Copepoda Calanoida of the families Phaennidae up to and including Acartiidae, containing the description of a new species of Aetideidae. Atlantide Rep. 8, 9e216. Welschmeyer, N.A., 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Oceanogr. 39, 1985e1992. Yamaguchi, A., Shiga, N., 1997. Vertical distributions and life cycles of Pseudocalanus minutus and P. newmani (Copepoda; Calanoida) off Cape Esan, southwestern Hokkaido. Bull. Plank. Soc. Jpn. 44, 11e20 (in Japanese with English abstract). Yamaguchi, A., Ikeda, T., Shiga, N., 1998. Population structure and life cycle of Pseudocalanus minutus and Pseudocalanus newmani (Copepoda: Calanoida) in Toyama Bay, southern Japan Sea. Plankton Biol. Ecol. 45, 183e193. Yamaguchi, A., Ikeda, T., Hirakawa, K., 1999. Diel vertical migration, population structure and life cycle of the copepod Scolecithricella minor (Calanoida: Scolecitrichidae) in Toyama Bay, southern Japan Sea. Plankton Biol. Ecol. 46, 54e61.
ScienceDirect Polar Science 9 (2015) 249e257 http://ees.elsevier.com/polar/
Copepod community succession during warm season in Lagoon Notoro-ko, northeastern Hokkaido, Japan Yoshizumi Nakagawa a,b,*, Hideaki Ichikawa a, Mitsuaki Kitamura b, Yasuto Nishino a, Akira Taniguchi c b
a Faculty of Bioindustry, Tokyo University of Agriculture, 196 Yasaka, Abashiri, Hokkaido 099-2493, Japan Graduate School of Bioindustry, Tokyo University of Agriculture, 196 Yasaka, Abashiri, Hokkaido 099-2493, Japan c Sanyo Techno-Marine, Inc., 1-3-17 Nihombashi-Horidomecho, Chuoh-City, Tokyo 103-0012, Japan
Received 22 October 2014; revised 5 January 2015; accepted 16 February 2015 Available online 24 February 2015
Abstract Lagoon Notoro-ko, located on the northeastern coast of Hokkaido, Japan, and connected to the Okhotsk Sea by a humanmade channel, is strongly influenced by local hydrography, as water masses in the lagoon are seasonally influenced by the Soya Warm Current and the East Sakhalin Current. We here report on the succession of copepod communities during the warm season in relation to water mass exchange. Copepods were categorized into four seasonal communities (spring/early-summer, mid-summer, late-summer/fall, and early-winter) via a cluster analysis based on BrayeCurtis similarities. Spring/earlysummer and early-winter communities were characterized by the temperateeboreal calanoid Pseudocalanus newmani, comprising 34.9%e77.6% of the total abundance of copepods during times of low temperature/salinity, as influenced by the prevailing East Sakhalin Current. Late-summer/fall communities were characterized by the neritic warm-water calanoid Paracalanus parvus s.l., comprising 63.9%e96.3% of the total abundance, as influenced by the Soya Warm Current. Midsummer communities comprised approximately equal abundances of P. parvus, Eurytemora herdmani, Scolecithricella minor, and Centropages abdominalis (12.8%e28.2%); this community is transitional between those of the spring/earlysummer and late-summer/fall. Copepod community succession in Lagoon Notoro-ko can be largely explained by seasonal changes in water masses. © 2015 Elsevier B.V. and NIPR. All rights reserved.
Keywords: Lagoon Notoro-ko; Okhotsk Sea; Copepod community; Paracalanus parvus; Pseudocalanus newmani
1. Introduction
* Corresponding author. Faculty of Bioindustry, Tokyo University of Agriculture, 196 Yasaka, Abashiri, Hokkaido 099-2493, Japan. Tel.: þ81 152 48 3917; fax: þ81 152 48 3916. E-mail address: [email protected] (Y. Nakagawa). http://dx.doi.org/10.1016/j.polar.2015.02.001 1873-9652/© 2015 Elsevier B.V. and NIPR. All rights reserved.
Lagoon Notoro-ko (with a circumference of 35 km, a surface area of 58.4 km2, and a water volume of 0.5 km3) is located on the northeast coast of Hokkaido, Japan, and is connected to the southern Okhotsk Sea by a small human-made channel 324 m wide and 13 m deep (We unify the place name as “Lagoon Notoro-ko”
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afterwards). Along the northeast coast of Hokkaido, the Soya Warm Current, originating from the Tsushima Warm Current in the Sea of Japan, flows southward from the Soya Straits during the warm months (Aota, 1979). The Tsushima Current is a branch of the subtropical Kuroshio Current, and therefore in the Okhotsk Sea the Soya Current is characterized by high temperatures (7 Ce20 C) and salinities (33.6 psu) (Takizawa, 1982). In winter, the typical boreal East Sakhalin Current, with low temperatures (<7 C) and low salinities (<32.0 psu) (Takizawa, 1982), flows down southward from the northwestern Okhotsk Sea along the east coast of Sakhalin Island and occupies the entire coastal area off northeast Hokkaido (Aota, 1979). Consequently, water masses in Lagoon Notoro-ko change seasonally between warm subtropical water and cold boreal water (Asami et al., 1995; Imada et al., 1995; Kurata and Nishihama, 1987; Nishino et al., 2014). This paper focuses on the succession of the major copepod species in the copepod communities in the lagoon during the course of this water exchange. A number of previous studies have examined the copepod communities in Lagoon Notoro-ko (e.g., Kanno and Fukuda, 1993; Kitamura et al., 2014). Kitamura et al. (2014) reported that while cold-water species dominate in winter, numerous eurythermic species are alternately present in fluctuating numbers during the warm months (spring to fall). These fluctuations indicate that the properties of the water masses in the lagoon vary even during the warm months, probably on account of frequent inflow, outflow, and mixing of coastal waters of different origins. Thus, an understanding of copepod community dynamics depends on knowledge of species-level relationships and responses to hydrographic conditions. This study presents data on temporal changes in species abundances in the copepod communities of Lagoon Notoro-ko in relation to the hydrographic conditions during the warm season. 2. Materials and methods
Observations were conducted at a sampling site at the deepest part (21 m water depth) of Lagoon Notoroko (44 30 2.100 N, 144 90 38.800 E), once or twice a month during the warm months, from 14 April to 21 December 2011 (Fig. 1). Vertical profiles of temperature and salinity were recorded using a compact Conductivity-Temperature-Depth profiler (Model ASTD103; JFE Advantech, Japan). Water samples for determinations of chlorophyll a (Chl-a) were collected using a Van Dorn water sampler at five depths (0, 5, 10,
15, and 18 m). A 500-mL aliquot was filtered through a glass-fiber filter (Whatman), and plant pigments on the filter were extracted in 7 mL N,N-dimethylformamide. Concentrations of Chl-a were determined following Welschmeyer (1994) using a fluorometer (10-AU; Turner Designs). Zooplankton, collected by vertical haul from a depth of 15 m to the surface using a 45-cm diameter 335-mm mesh NORPAC net, were preserved in 5% (v/ v) buffered seawater formalin. The amount of water filtered by the net was estimated by assuming a filtering efficiency of 100%. All copepods, including copepodids and adults, were sorted under a dissecting microscope from 1/4 to 1/32 aliquots, and then classified to species level according to Ohtsuka and Ueda (1997); numbers of individuals were counted. However, as early copepodid stages could not be accurately identified to the species level, they were classified into generic groups. Lesser species, which did not exceed 10% of the total abundance in any sample, were categorized as “other copepods”. Similarities between samples were determined by a BrayeCurtis similarity analysis using the software package Plymouth Routines in Multivariate Ecological Research (PRIMER) v6 (Clarke, 1993; Clarke and Warwick, 2001). 3. Results 3.1. Hydrographic structures Seasonal changes in the vertical profiles of water temperature are apparent in Fig. 2. The temperature was <6 C in April and increased to a seasonal maximum of 21.5 C at the surface and 18.2 C just above the bottom in early September. A thermocline started to form in April, developed further until August, and then rapidly disappeared by the end of September. The temperature decreased thereafter to <3 C at the end of the survey period in December. Changes in salinity generally followed those of temperature (Fig. 3). In April, lower-salinity waters of <32 psu formed a 5-m layer on top of more saline water of >32.2 psu. During May and June, the lowsalinity water disappeared, and saline water of >32.2 psu formed the entire water column. From the end of June, more saline water of >33.0 psu intruded beneath the >32.2 psu water, resulting in vertical stratification. This stratification broke down in late September and a vertically uniform salinity was maintained until the end of the survey period. It should be noted, however, that the salinity gradually decreased to <32 psu during this period after late September.
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Fig. 1. Location of the sampling station (St. A) in Lagoon Notoro-ko, eastern Hokkaido, Japan, facing the Okhotsk Sea.
3.2. Chl-a concentrations Fig. 4 shows seasonal changes in Chl-a concentrations. The highest Chl-a level of >6 mg L1 was recorded near the lagoon bottom in April. While nearbottom values were uniformly high throughout the survey period, the subsurface maximum layer formed during July to September. Levels of Chl-a stabilized at ~3 mg L1 throughout the water column in October and November. The occurrence of low Chl-a levels in
subsurface layers in December is noteworthy; however, it should be noted that the seasonal minimum value of <2 mg L1 was recorded in June. 3.3. Seasonal changes in abundance and composition of the copepod community Copepods identified in the present study include 21 species in 15 genera belonging to 14 families in 3 orders (Table 1). The total abundance was
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Fig. 2. Relationship between temperature ( C) and depth during the warm months in Lagoon Notoro-ko in 2011.
1118e1120 ind. m3 in April, with levels increasing in May and exhibiting a sudden peak of 8602 ind. m3 on 30 May, followed by a rapid decrease to 483e496 ind. m3 in June and July (Fig. 5). After July, levels of abundance were relatively constant, with a small peak on 9 September (1385 ind. m3) and a minimum on 13 October (280 ind. m3). Numbers increased again to a winter peak of 801e902 ind. m3 in December (Fig. 5). Among the different copepod species, Pseudocalanus newmani was most abundant during the period from April to July (699e5273 ind. m3) (Fig. 5), comprising 60.6%e77.6% of total copepod abundance (Fig. 6). The peak abundance (5273 ind. me3) was recorded on 30 May and the second highest peak (1321 ind. m3) on 14 July (Fig. 5). The abundance of P. newmani was under the detection limit (13 ind. m3) during AugusteNovember, but then increased to 229e762 ind. m3 after 25 November and until 13 December. The levels of the dominant P. newmani during this period (84.5%) were higher than during other months (Fig. 6). The second most abundant copepod species, Acartia longiremis, also exhibited its highest abundance levels during AprileJuly (51e1906 ind. m3; 6.0%e22.2% of the total abundance) (Fig. 6). During AugusteDecember, its abundance was always below the detection limit (Fig. 5).
Fig. 4. Relationship between total chlorophyll a concentration (mg L1) and depth during the warm months in Lagoon Notoro-ko in 2011.
Eurytemora herdomani, although less abundant, was also common before September, having the highest levels on 30 May (407 ind. m3) and second highest on 19 August (Fig. 5), representing 25.6% of the total copepod abundance (Fig. 6). E. herdomani was also present in November and December, although in small numbers (13 ind. m3, respectively) (Fig. 5). Tortanus derjugini was present during the early half of the investigation period (April to August) and showed a seasonal peak of 191 ind. m3 on 28 July (Fig. 5), comprising 23.8% of the copepod population at that time (Fig. 6). Recorded occurrences of Centropages abdominalis and Scolecithricella minor were limited to August and September; C. abdominalis was present in two samples, on 19 August (with an abundance of 64 ind. m3 and dominance of 12.8%) and on 9 September (Figs. 5 and 6), while S. minor occurred only in August (with an abundance of ~76 ind. m3 and dominance of ~15.4%) (Figs. 5 and 6). Paracalanus parvus s.l. (hereafter P. parvus) was common throughout the investigation period, except for April and the 13 December sample (25e1334 ind. m3) (Fig. 5). The highest abundances of P. parvus, recorded on 9 September and 13 October (Fig. 5), represented 96.3% and 86.4% of the total copepod numbers, respectively (Fig. 6). Acartia hudsonica was first observed in June, and its abundance increased until winter, with peaks of 241 ind. m3 on 25 November and 21 December (Fig. 5); on 25 November, the dominance of A. hudsonica reached a peak of 38.0% of the total abundance (Fig. 6). 3.4. Similarities within the copepod communities
Fig. 3. Relationship between salinity (psu) and depth during the warm months in Lagoon Notoro-ko in 2011.
Cluster analyses of the copepod communities in Lagoon Notoro-ko were performed on the basis of
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Table 1 Copepod species identified in Lagoon Notoro-ko during warm season. Order
Family
Species
Apr
Mar Jun
14 29 30 Calanoida
Acartiidae
Acartia hudsonica Acartia longiremis Acartia omorii Acartia spp. Calanidae Calanus gracilis Calanus pacificus Neocalanus plumchrus Centropagidae Centropages abdominalis Clausocalanidae Clausocalanus pergens Eucalanidae Eucalanus bungi Metridiidae Metridia pacifica Paracalanidae Palacalanus parvus Pseudocalanidae Pseudocalanus minutus Pseudocalanus newmani Pseudocalanus spp. Pseudodiaptomidae Pseudodiatomus marinus Scolecitrichidae Scotecithricella minor Temoridae Eyurytemora affinis Eurytemora herdmani Eurytemora spp. Tortanidae Tortanus derjugini Tortanus discaudatus Tortanus spp. Cyclopoida Oithonidae Oithona atlantica Oithona similis Oithona spp. Harpacticodia Ectinosomatidae Microsetella sp. 1 Unidentified
þ þ þ
Jul
16 29 14
þ þþ þþþ þþ þþ þþ þ þ þ þ þ þ þ þ þ þ
þ þ þ þ þþ þ þ þþ þþ þþ þþþ þ þ þ þ þþ þ þ þ þ þ
þþ þþ þ þ þ þ
Aug
Sep
28 19 29 9 þ þ
þ
þ
þ
þ
þ
þ
þ þ
þ
Oct
Nov
Dec
30 13 25 11 25 13 21 þ þ þ þ
þ þ
þþ þþ þ
þþ
þ
þ
þ
þ þþ þþ þþ þ þþ þþ þþþ þþ þþ þþ þþ þþ þ þ þ þ þ þþ þþ þþþ þþ þ þ þþ þþ þþ
þ þ þ
þ
þ
þ þ
þ
þ þ
þ þ
þþ þ
þ þ
þ þ
þ þ
þ þ
þ þ
þ
þ
þþ
þ þ þ
þ þ
þ
þ
þ þ
þ
þ
þ: <100 ind. m3. þþ: <1000 ind. m3. þþþ: 0.1000 ind. m3.
BrayeCurtis similarities, which were calculated from data on the abundance and dominance values of copepod populations on each sampling date. Accordingly, three groups (A, B, and C) were recognized at a 39% similarity level, and two subgroups of Group B (B1 and B2) were identified at a 46% similarity level (Fig. 7). By referencing their seasonal patterns (Figs. 5 and 6), Group A was identified as a spring/early-summer group (14 Aprile14 July), Subgroup B1 as a midsummer group (19 August), Subgroup B2 as a latesummer/fall group (29 Auguste11 November), and Group C as an early-winter group (25 Novembere21 December) (Fig. 7). 4. Discussion In the present study, Groups A, B1, B2, and C, which were clearly defined by a cluster analysis based on BrayeCurtis similarities (Fig. 7), were recognized
as four seasonal communities present during the warm months in Lagoon Notoro-ko, i.e., in spring/earlysummer, mid-summer, late-summer/fall, and earlywinter. P. newmani was the predominant species in the spring/early-summer and early-winter communities, comprising 34.9%e77.6% of the total abundance (Fig. 6). P. newmani has been reported as a temperateeboreal species, distributed in coastal waters of Asia and North America (Frost, 1989). In eastern Asia, it is found in the northern Sea of Japan, in areas such as Toyama Bay (Yamaguchi et al., 1998), Ishikari Bay (Arima et al., 2014), the southwestern waters of Hokkaido (Yamaguchi and Shiga, 1997), and in the coastal waters off northeast Hokkaido (Asami et al., 2010). In the present study, P. newmani was especially abundant on 30 May, but numbers decreased sharply in June (Fig. 5). During this period, Chl-a concentrations below 10 m also decreased sharply, from >5 mg L1 in May to
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Fig. 5. Seasonal changes in abundance (ind. m3) of total and dominant species in the copepod communities during warm months in Lagoon Notoro-ko in 2011. Species accounting for 10% or more of the total abundance in any sample are considered “dominant”; otherwise the species are amalgamated as “other copepods”.
<2 mg L1 in June (Fig. 4). Because growth of P. newmani is reportedly limited under conditions of scarce food supply (McLaren et al., 1989; Yamaguchi and Shiga, 1997), levels of Chl-a in June (<2 mg L1) may not have been sufficient to support the large population size of this species. The decrease in Chl-a levels in June is observed regularly each year in Lagoon Notoro-ko (Nishino et al., 2014), and is attributed to active feeding of larvae of the Japanese scallop Patinopecten yessoensis, which is the most important commercially farmed species in the lagoon (Nishihama, 1994).
While Chl-a levels had rebounded quickly by July, the P. newmani population continued to decrease, probably owing to its preference for cold-water habitats (loc. cit.), and the population finally disappeared by 19 August (Fig. 5). Around Hokkaido, the upper temperature limit for P. newmani has been reported to be 15 C (Arima et al., 2014; Yamaguchi and Shiga, 1997; Yamaguchi et al., 1998); temperatures in Lagoon Notoro-ko had increased to over 15 C by 19 August (Fig. 2). This increase in temperature was largely a result of the intrusion of the Soya Warm Current into the lagoon, combined with seasonal
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Fig. 6. Seasonal succession in the dominance (%) of dominant copepods during the warm months in Lagoon Notoro-ko in 2011.
warming of lagoon waters (Aota, 1979). P. newmani was observed again in October, when temperatures had dropped to below 15 C, and its numbers continued to increase towards winter (Table 1; Fig. 5). This drop in temperature during October was caused by inflow of the East Sakhalin Current into the lagoon, which it occupies for the entire season of ice coverage until the following April (Nishino et al., 2014). The intrusion of the East Sakhalin Current is accompanied by low temperatures and salinities in the lagoon during November and December (Figs. 2 and 3) (Takizawa,
1982). The data suggest that P. newmani is introduced into the lagoon by the inflow of the East Sakhalin Current in early winter, and that it survives the winter under sea ice in the lagoon, before disappearing from the lagoon when the Soya Warm Current enters the lagoon in summer. During summer and fall, the lagoon is occupied by a late-summer/fall community dominated largely by P. parvus (Figs. 6 and 7). P. parvus is known as one of most widely distributed species in neritic waters in temperate and boreal seas (Brodskii, 1950; Mackas and
Fig. 7. Dendrogram of seasonal groups of copepods during the warm months in Lagoon Notoro-ko in 2011, classified via BrayeCurtis similarities: (A) spring/early-summer group; (B1) mid-summer group; (B2) late-summer/fall group; (C) early-winter group (before sea-ice formation).
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Tsuda, 1999; Vervoort, 1963). In the present study, P. parvus was found in samples from 30 May to 13 December, attaining its highest abundance of 1334 ind. L1 on 9 September (Fig. 5). Several surveys have reported that P. parvus is abundant in summer and fall in the coastal waters around northern Japan. Anraku (1954) reported that in waters near the present survey site, P. parvus is most abundant in August, under the influence of the Soya Warm Current. Hattori and Tsumura (1990) reported that in waters off northwestern Hokkaido, P. parvus is dominant from summer to late fall, when temperatures and salinities are elevated under the influence of the Tsushima Warm Current. Arima et al. (2014) conducted sampling in Ishikari Bay off western Hokkaido and recorded that P. parvus is abundant in JulyeSeptember, under the influence of the Tsushima Warm Current, but is absent in spring (April and May), when temperatures and salinities are low. In the present study, temperatures and salinities during the late summer to fall, when P. parvus was abundant, were as high as 11 Ce21 C and 33.0e33.3 psu, respectively (Figs. 2 and 3), indicating the influence of the Soya Warm Current. With reference to the mid-summer community, no single species displayed a dominance of >50%, with the abundances of P. parvus, Eurytemora herdmani, S. minor, and C. abdominalis being approximately equal, at 12.8%e28.2% of the total abundance (Fig. 6). Among these species, S. minor and C. abdominalis are commonly reported as cold water species (S. minor: Minoda, 1971; Mori, 1964; Morioka, 1976; Vervoort, 1965; Yamaguchi et al., 1999; C. abdominalis: Brodskii, 1950 as Centropages mcmurrichi; Hirakawa, 1986; Kas'yan, 2004; Liang et al., 1994, 1996; Mori, 1964). Our data and the data from these reports indicate that both species flourish in cold water and attain their maximum abundances at 15 C-18 C; neither species thrives in water warmer than 20 C. In this study, S. minor and C. abdominalis were found in August and September, when surface temperatures were higher than 20 C (Fig. 2). However, cold underlying water was present during this period, which had probably intruded from the outer lagoon, where temperatures were lower than 15 C and salinities were ~33.0 psu (Figs. 2 and 3). These two species likely survived the summer months in Lagoon Notoroko in the underlying water layer, and then re-populated lagoon waters during the transitional season between the dominance of the spring/early-summer community (dominantly P. newmani) and the early-winter community (dominantly P. parvus). Several studies have reported a similar increase in the abundance of another
cold-water brackish copepod E. herdmani (Brodskii, 1950; Heron, 1964; Mori, 1964); the data show a decrease from a peak in spring and into July during a time of increasing temperatures, and a temporary increase in abundances in August (Fig. 5). These observations indicate that niches occupied by dominant spring species become available in summer, until winter species become dominant. During this period, Chl-a concentrations are more or less constant throughout the water column; thus, food conditions for copepod populations remain suitable throughout the water column during this time. These varying temperature conditions may provide species with a variety of alternate niches. The present study showed that the copepod species succession in Lagoon Notoro-ko is basically controlled by variations in the conditions of water masses, which intrude from the outer lagoon. This is possibly the case in other areas of the southern Okhotsk Sea, which is the southern limit of seasonal sea-ice coverage in the Northern Hemisphere, and where seasonal fluctuations in the thermal regime are extremely large. Continuous monitoring of copepod communities, which are sensitive to changes in thermal conditions, is of critical importance under conditions of global warming. Acknowledgments We gratefully acknowledge the assistance of Kohichi Nishio, Tokyo University of Agriculture, and Toshifumi Kawajiri, West Abashiri Fishery Corporation, with field observations and samplings. References Anraku, M., 1954. Distribution of plankton copepods off Kitami, Hokkaido, in Okhotsk Sea in summer, 1949 and 1950. Bull. Fac. Fish. Hokkaido Univ. 4, 249e255. Aota, M., 1979. Variability of hydrography in coastal area along Hokkaido, the Sea of Okhotsk. Note Coast. Oceanogr. Study 17, 1e11 (In Japanese). Arima, D., Yamaguchi, A., Abe, Y., Matsuno, K., Saito, R., Asami, H., Shimada, H., Imai, I., 2014. Seasonal changes in body size and oil sac volume of three planktonic copepods, Paracalanus parvus (Claus, 1863), Pseudocalanus newmani Frost, 1989 and Oithona similis Claus, 1866, in a temperature embayment: what controls their seasonality? Crustaceana 87, 364e375. Asami, H., Imada, K., Yasutomi, R., Izawa, T., 1995. Seasonal cycles of phytoplankton and nutrients in Lake Notoro, Eastern Hokkaido. Jpn. Sci. Rep. Hokkaido Fish Hat. 49, 17e23 (in Japanese with English abstract). Asami, H., Shimada, H., Sawada, M., Miyakoshi, Y., Ando, D., Fujiwara, M., Nagata, M., 2010. Spatial and seasonal distributions of copepods from spring to summer in the Okhotsk Sea off eastern Hokkaido, Japan. PICES Sci. Rep. 36, 233e239.
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