Plankton Biol. Ecol. 48 (1): 52-58,2001 plankton biology & ecology © The Plankton Society of Japan 2001 Life history strategies of subarctic copepods Neocalanus flemingeriand N. plumchrus, especially concerning lipid accumulation patterns Atsushi Tsuda, Hiroaki Saito & Hiromi Kasai Hokkaido National Fishery Research Institute 116 Katsurakoi, Kushiro 085-0802, Japan Received 27 December 1999; accepted 21 August 2000 Abstract: Lipid accumulation patterns during development of Neocalanus flemingeri and N. plum chrus in the western subarctic Pacific were investigated as regards life-history strategies for overwin tering and survival in an environment with highly fluctuating food availability. Neocalanus plumchrus accumulates lipid mainly during the copepodite-5 stage; in contrast, N. fiemingeri starts to accumu late lipid as early as the copepodite-2 stage. The life history strategy of N. plumchrus, which is char acterized by fast growth without lipid storage and synchronized copepodite recruitment, might be an adaptation to the predictable timing and availability of food in their environment. In contrast, the de velopmental strategy of N. fiemingeri is characterized by slower growth, but with early and pro longed lipid storage, and prolonged copepodite recruitment. This strategy was regarded as an adap tation to the variable environment. The different strategies of N. plumchrus and N. flemingeri seem to be adapted for predictable food conditions in summer and for unpredictable conditions in winter- spring, respectively. Key words: copepod, Neocalanus, lipid storage, life history are sharply segregated in the timing of their seasonal uti Introduction lization of the surface mixed layer (Miller & Clemons "One of the key questions to be asked of Arctic zoo- 1988; Tsuda etal. 1999). plankton feeding at low trophic levels is how sympatric Lipid storage is a common adaptive strategy against pe species appropriate and maximally utilize the energy pro riods of restricted food supply for polar, subpolar and ba vided by intense pulses of phytoplankton production during thypelagic organisms (Lee et al. 1971; Sargent & Hender the sunlit summer months in order to survive the long win son 1986; Conover 1988). Copepods usually store neutral ter darkness period?" (Hopkins et al. 1984). The same lipids (wax esters and triglycerides) for survival and repro question can be extended to zooplankton in the subpolar duction (Lee et al. 1972). Neocalanus species in the subpo region. Three species of Neocalanus are dominant across lar oceans accumulate mainly wax esters (Lee et al. 1972; the subarctic Pacific and act as a trophic link between the Ohman 1987), which is a better class of compounds than primary production and higher trophic organisms such as triglycerides for the long-term storage of energy (Tande & pelagic fish (e.g. Mackas & Tsuda 1999). These copepods Henderson 1988). Euchaeta japonica (E. elongata), the are all ontogenetic vertical migrators, residing and growing dominant carnivorous copepod in the subarctic ocean, in the euphotic layer from winter to summer and descend shows high wax ester content throughout all developmental ing to the meso- and bathypelagic layers from summer to stages (Lee et al. 1974). However, Calanus spp. generally winter (or fall) for maturation and spawning (Miller et al. accumulate lipid only during older copepodite stages 1984; Miller & Clemons 1988; Tsuda et al. 1999). These (Hakanson 1984; Kattner & Krause 1987). copepods partition the habitat vertically and seasonally Although both N. plumchrus and N. flemingeri utilize the (Miller & Clemons 1988; Mackas et al. 1993). Neocalanus surface mixed layer during the growing season, N. flemin plumchrus and Ar. flemingeri have similar morphology, but geri grows from midwinter to May, while N. plumchrus grows after the descent of N. flemingeri in the western sub Corresponding author: Atsushi Tsuda; e-mail, [email protected] arctic gyre (Tsuda et al. 1999). The timing of the change in Lipid Accumulation in Neocalanus 53 dominance between the two species is roughly the peak sea 50°N son of the spring phytoplankton bloom (Kasai et al. 1997; Saito et al. 1998). Thus, quantity and quality of food avail ability are different for the two species. We will show that Okhotsk Sea the developmental timing of lipid storage as a survival strategy is also different and we will discuss the conse quences of these differences in terms of their life-history strategies. Oyashio Materials and Methods Seasonal sampling was carried out at stations located roughly in the first and second branches of the Oyashio cur rent by the FRV Hokkou Maru, Tankai Maru and Hokushin 40°N Maru, 6 to 10 times a year from July 1996 to July 1998 (Fig. 1). Copepods were collected by oblique tows with a bongo net (mouth diameter, 70cmX2; mesh aperture, North Pacific 330 /im) from about 500-m depth at night. These samplings covered the depth of overwintering Neocalanus flemingeri, but the overwintering iV. plumchrus mainly occurred in the deeper layers (Tsuda et al 1999). The net was equipped with a depth meter and flow meters. The samples were pre 140°E 150°E served with neutralized formalin seawater (10% v/v). Cope- Fig. 1. Sampling locations with schematic flow pattern of the podites-2 (C2) to 5 of N. flemingeri and N. plumchrus were Oyashio current. The stations sampled 1990-98 for annual varia identified according to Miller (1988) and Tsuda et al. tions are indicated by filled circles, and those sampled 1996-98 (1999) and were sorted from appropriate aliquots of the for seasonal variation are shown as hatched areas. seasonal samples. Ten to over 2000 individuals of each de velopmental stage from each sample were used. Cope- Results podite-1 individuals were not included in the following analysis because of uncertainty in their identification to Two populations were recognized in Neocalanus flemin species. However, the Cl individuals of either species geri based on body size (Tsuda et al. 1999). Small forms rarely have oil-sacs. Pale yellow or orange oil sacs in older (ca 3.6mm in prosome length as adult female) have a one- individuals were visible under a dissecting microscope. The year life cycle and occurred at the surface from winter to sizes of the oil sacs were roughly categorized by the lateral spring (Fig. 2). At least some individuals of the large form views into three classes: sparsely stored, 0-4%; medially (ca. 4.5 mm in prosome length as adult female) have a bien stored, 4-40%; and fully stored; >40% of the prosome area nial life cycle with winter dormancy as C4 and adult fe covered by the oil-sac. Only intact individuals were used for males. Neocalanus plumchrus have an annual life cycle; the analysis. they occur in the surface layer after the descent of N. Sampling for annual variations was carried out from flemingeri then grow to C5 by the end of summer and de 1990 to 1998 southeast of Hokkaido along a transect line scend to deeper layers for maturation and reproduction (Fig. which crossed the Oyashio current (Fig. 1). A small bongo 2). Sea surface temperature of the studied area increased net (mouth diameter, 30 cm; mesh aperture, 330 jum) was from March to August and the phytoplankton bloom took towed vertically from the base of the surface mixed layer. place between April and May (Fig. 3). Replacement of N. When the surface mixed layer was deeper than 50 m, the net flemingeri by N. plumchrus in the surface water took place was towed from 50-m depth. An aliquot of each sample was between mid-May and early June (Fig. 2). This season coin preserved with neutralized formalin seawater. The net tows cides with the peak or declining season of the spring phyto were conducted 4 to 6 times a year, but only samples col plankton bloom (Fig. 3). lected in May were used for the present study because both Lipid accumulation was observed in N. flemingeri as Neocalanus plumchrus and TV. flemingeri were distributed early as C2 and the fraction of C2 individuals with lipid in in the upper 50-m layer during this period. The data for creased later in the season of copepodite recruitment (Fig. each year contained 5 hauls, which roughly covered the first 4). Lipid accumulation increased with developmental stage: and second branches of the Oyashio current (Kono & about half of C3 were individuals with medially-stored lipid Kawasaki 1992). The sampling date varied by less than four and over 80% of CA throughout the year were individuals days interannually. All individuals of intact copepods were with medially or fully stored lipid (Fig. 4). C4 individuals used for the analysis. The oil-sacs of these samples were occurred throughout the year because of the presence of a also categorized based on the criteria mentioned above. biennial life cycle with diapause at both C4 and C6 female 54 A. Tsuda, H. Saito & H. Kasai female 500 1000 N. flemingeri (large form) Spawning 500 Q. 0) Q 1000 N. flemingeri (small form) 500 - C5 & female 1000 -. nauplii Winter Spring Summer Fall Winter Spring Summer Fall Season Fig. 2. Schematic illustrations of life cycles of Neocalanns flemingeri (large and small forms) and N. plumchrus in the western subarctic Pacific (modified from Tsuda et al. 1999). developmental stages (Fig. 2, Tsuda et al. 1999). Individu als of C4 with full lipid accumulation dominated during summer to fall and decreased in early spring. The spring decrease was caused by new recruitment of C4 with an an nual life cycle (Tsuda et al. 1999). Most C5 showed medial or full accumulation of lipid, and the percentage of fully- stored individuals increased later in the season (Fig. 4). The seasonal window for occurrence of young cope- podites of N. plumchrus was shorter than that for N. flemin geri because of more synchronized recruitment and faster growth.