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Energy Sources for Recruitment of the Subantarctic Copepod Neocalanus Tonsus L M

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Energy Sources for Recruitment of the Subantarctic Copepod Neocalanus Tonsus L M Limnol. Oceanogr., 32(6), 1987, 13 17-1330 0 1987, by the American Society of Limnology and Oceanography, II-S. Energy sources for recruitment of the subantarctic copepod Neocalanus tonsus l M. D. Ohman Portobello Marine Laboratory, P.O. Box 8, Portobcllo, New Zealand, and New Zealand Oceanographic Institute, Division of Marine and Freshwater Science, D.S.I.R., Private Bag, Kilbirnie, Wellington Abstract Neocalanus tonsus Brady was collected in subantarctic waters off southeastern New Zealand to test experimentally the importance of storage lipids and particulate matter as energy sources for recruitment. Reproductive copepods occur in mesopelagic depths (1 ,OOO-500m) in austral winter and in epipelagic depths (150-O m) in spring. Winter copepods released up to 19 eggs female-’ d-l in filtered seawater; spring copepods required a particulate food source to release eggs. Winter females ingcstcd diatoms at half the rate of spring females. Winter CVs did not ingest diatoms, in contrast to spring and summer CVs. Winter females had 24 times the wax ester content, half the phospholipid, and half the nitrogen content of spring females. In contrast, the two groups did not differ in dry mass or carbon content. Application of a proposed method for estimating reproductive potential, combined with experimental results, suggests that stored lipids are the energy source for recruitment of mesopelagic winter animals but not epipelagic spring animals. Subantarctic N. tonsus is distinguished from subarctic Pacific Neocalanus plumchrus and Neo- Calanus cristatus by residence of adult females in surface waters, active suspension feeding, and the dcpcndence of egg production on particulate food in spring. Divergent life history traits may be observed for copepod species occupying parallel subpolar habitats in the southern and northern hemispheres. Subpolar zooplankton assemblages in the sumed under the designation N. plumchrus southern hemisphere, subantarctic ocean (C. B. Miller pers. comm.). and the northern hemisphere, subarctic Pa- A singular feature of recruitment of the cific are dominated by copepods currently North Pacific species is that mating and re- referred to the genus Neocalanus. Neocal- production occur exclusively in mesopelag- anus tonsus Brady is endemic to the oceanic ic depths (Beklemishev 1954; Heinrich subantarctic, bounded approximately by the 1962; Miller et al. 1984). Adult males and polar front to the south and the subtropical females do not occur in surface waters at convergence to the north (Vervoort 1957; any time ofyear (Vinogradov 1968; Minoda De Decker and Mombeck 1965; Brodskii 197 1; Miller et al. 1984). Adult females have 1964; Jillett 1968; Katiamura 1974). Neo- reduced, nonfunctional mouthparts (Camp- calanus plumchrus Marukawa and Neocal- bell 1934; Beklemishev 1954; Vyshkvartz- anus cristatus Kroyer are endemic to the eva 1977) and do not feed before releasing subarctic North Pacific, occurring princi- eggs at depth (Heinrich 1962; Fulton 1973). pally in the open ocean (Brodskii 1950; Mil- In the laboratory N. plumchrus females ler et al. 1984), some neighboring seas (Ma- maintained in filtered seawater release sev- rukawa 1921; Vidal and Smith 1986), and eral hundred eggs (Fulton 1973). Recruit- deep fjords (Fulton 1973; Mackie 1985). It ment is therefore decoupled from primary is now recognized that two species are sub- production in the euphotic zone. Rather, it depends on high concentrations of wax es- ters deposited by copepodid stage V, re- I Supported by a William Evans Visiting Fellowship, tained in females after the molt (cf. Gatten by the Department of Scientific and Industrial Re- et al. 1980) and subsequently used in egg search, and by NSF grant INT 84-10972. 2 Present address: Marine Life Rcscarch Group production (Lee et al. 1972). Although lip- A-027, Scripps Institution of Oceanography, UCSD, ids are commonly stored by copepod species La Jolla, Calif. 92093-0227. from higher latitudes (Lee et al. 197 1; Sar- 1317 1318 Ohman gent and Henderson 1986) the lack of vi- This method makes use of the observation able feeding appendages in adult females that storage lipids are the proximate energy and obligate dependence on stored lipids are sources for egg production of nonfecding unique characteristics of the subarctic Pa- adult copepods (Heinrich 1962; Conover cific calanids. 1967; Fulton 1973). This method, an ex- The distinctive life history characteristics tension of the approach of Gatten et al. of the subarctic species suggested compar- (1980), requires knowledge of adult lipid ison with the subantarctic N. tonsus. Jillett’s content., egg lipid content, and daily respi- (1968) study off the South Island of New ratory lipid oxidation. In addition, for com- Zealand indicated that males appeared first parison of N. tonsus with a species known and then females in deep water in austral to feed actively, parallel feeding experi- winter. Production of a first generation ap- ments were performed with Calanus aus- parently occurred at depth, followed by as- tralis Brodskii (cf. Drits 1985). cent of developing nauplii and copepodids The generic assignment Neocalanus is into surface waters. The occurrence of N. used herein, following Bradford and Jillett tonsus eggs in mesopelagic depths in Au- (1974), although the evolutionary relation- gust-September (pcrs. obs.) confirms that ships among calanid lineages are currently deep reproduction occurs in situ. Unlike N. under r’eview (Fleminger 1985). plumchrus and N. cristatus, however, once J. B. Jillett and J. M. Bradford shared the developing copepodids of N. tonsus at- ideas and expertise and were instrumental tained the CV stage in surface waters they in facilitating all aspects of this research. did not descend to deeper waters. Instead Numerous individuals at the Portobello development continued in surface waters to Marine Laboratory and the D.S.I.R. Divi- the adult stage followed by production of a sion of Marine and Freshwater Science and second generation (Jillett 1968). Lipid-rich Chemistry Division contributed to this ef- CVs arising from this second, surface gen- fort. Space for experimental work was made cration were then thought to descend into available at the University of Otago, De- mesopelagic depths. Occurrence of adult fe- partment of Microbiology. I thank M. R. males in surface waters in spring-summer Grigor, B. W. Frost, M. F. Barker, C. W. elsewhere in the subantarctic province (Ver- Burns, P. Jones, B. Chapman, and R. Bald- voort 1957; Bradford 1970; Kawamura win for their help. J. M. Bradford, C. B. 1974; Voronina 1975; Taw and Ritz 1979) Miller, and an anonymous referee provided supports Jillett’s interpretation of spring comments and criticisms of the manuscript. surface recruitment and suggests a signili- cant departure from the life history of the Met hods subarctic Pacific species. Collection - Live collections were made Because of the parallel subpolar habitats at a continental slope station (45”55’S, occupied, yet suggested differences in life 17 l”O6’E) 32 km southeast of Taiaroa history between N. tonsus and its congeners, Head, Otago Peninsula, New Zealand, or at the present study was designed to determine a shelf station 15 km offshore. Copepods the processes controlling recruitment of N. were collected in the upper 150 m in austral tonsus. This investigation compares the spring-summer (October 1984-January feeding behavior, fecundity, and organic 1985) and between 1,OOO-500 m in winter composition of deep winter and shallow (August 19 8 5). A 1-m-diameter, 3 3 3-pm- spring N. tonsus. The objective was to eval- mesh ring net or a 0.7-m, 202-pm-mesh uate the importance of particulate matter in closing net (Brown and Honegger 1978) was the water column as contrasted with storage used; cod ends were nonfiltering. Live ani- lipids as energy sources for recruitment of mals were transported to a shore laboratory the two apparent generations. One of the in thermally insulated containers. Cope- approaches is to estimate the reproductive pods intended for lipid, dry mass, carbon, potential of N. tonsus females under the as- and nitrogen analysis were quickly frozen sumption that only storage products pro- in liquid nitrogen aboard ship and trans- vide the energy source for egg production. ferred to a -70°C freezer ashore. Subantarctic copepod recruitment 1319 C, N, and lipid analysis- Dry mass was macerated in 90% acetone. Chlorophyll a determined with a Cahn G-2 clcctrobalance and pheopigments were assayed on a Turner after briefly rinsing in distilled water and model 111 fluorometer with a high-sensi- desiccating at 55°C. Nitrogen and carbon tivity door, and pigment content was com- were determined by combustion in a CN puted based on the equations of Strickland elemental analyzer (courtesy of M. Downcs). and Parsons (1972). Total pigment per co- Lipids of adults were extracted twice by ho- pepod is the sum of Chl a and pheopig- mogcnization (Bligh and Dyer 1959). Eggs ments resulting from these equations, with- released by N. tonsus females in the labo- out further correction (cf. Conover et al. ratory were extracted by sonication, fol- 19 8 6). No correction was made for apparent lowed by the Bligh and Dyer phase sepa- loss of Chl a, since Dagg and Walser (1987) ration. Lipids were analyzed by thin-layer reported that pigment losses averaged 11%. chromatography-flame ionization detection Background fluorescence was determined for with an Iatroscan TH- 10 Mark III (Parrish each developmental stage by starving ani- and Ackman 1985). Chromarods were de- mals in filtered seawater. Animals were col- veloped for 20 min in hexane : diethyl ether lected for experiments as follows: N. tonsus (95 : 5, vol/vol) followed by 20 min in hex- CIV (November and December), CV (No- ane : diethyl ether : formic acid (82 : 18 : 0.1, vember, December, January, August), males vol/vol/vol). Cetyl alcohol was the internal (August), females (November and August); standard, since copepod free alcohols were C.
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